Jay Ram Lamichhane

Leonardo Varvaro

Luciana Parisi

Jean-Marc Audergon

Cindy E Morris
email: cindy.morris@avignon.inra.fr

Disease and Frost Damage of Woody Plants Caused by Pseudomonas syringae: Seeing the Forest for the Trees

Pseudomonas syringae is a phytopathogenic bacterium that causes diseases of monocots, herbaceous dicots, and woody dicots, worldwide. On woody plants, reports of disease due to P. syringae have markedly increased in the last years and the diseases have been recognized as a major threat to the primary products of agroforestry practices. Detection

INTRODUCTION

The economic importance of a given plant species is an attribute of the quantity of services and products that it provides for humans. Edible components, firewood, and timber are usually considered to be the most important primary products obtained from plants. In addition, secondary products such as biofuels and plant-based medicines have a nonnegligible value for humans. Perennial plants are composed of the hard fibrous material consisting of secondary xylem tissue known as wood [START_REF] Hickey | The Cambridge Illustrated Glossary of Botanical Terms[END_REF][START_REF] Plomion | Wood formation in trees[END_REF]. Each year, most woody plants form new layers of woody tissue that are deposited on the inner side of the cambium, located immediately under the bark. However, in some monocotyledons, such as palms and dracaenas, the wood is formed in bundles scattered through the interior of the trunk [START_REF] Chase | Monocot relationships: an overview[END_REF]. A few herbaceous perennial species such as Uraria picta, some other species belonging to the Polygonaceae family and herbaceous perennials from alpine and dry environments, that have a thickened and short hard perennial stem known as caudex [START_REF] Welsh | New taxa of western plants in tribute[END_REF], develop wood-like stems. However, these species are not truly woody and they only develop hard densely packed stem tissue. Woody perennial plants, because of their long life cycle, ensure a regular income for growers and represent an important economic source for a large number of individuals. In addition to their primary products, the environmental services of trees are particularly significant to human life. Examples are prevention of soil erosion and land degradation [START_REF] Wilkinson | Poplars and willows for soil erosion control in New Zealand[END_REF], carbon sequestration [START_REF] Nowak | Carbon storage and sequestration by urban trees in the USA[END_REF], reduction of building energy consumption [START_REF] Akbari | Shade trees reduce building energy use and CO 2 emissions from power plants[END_REF], and of air pollution [START_REF] Nowak | Air pollution removal by urban trees and shrubs in the United States. Urban For[END_REF]. Among the numerous diseases of woody plants, those caused by Pseudomonas syringae have become markedly important in recent years. Since only the beginning of this century, 55 reports of disease outbreaks in 25 countries have been associated with P. syringae in 25 different woody hosts ( Advances in Agronomy, First Edition, 2014, 235-295 reports are also snapshots of recurring chronic problems, such as olive knot disease in Italy or apricot canker in France, that have been important over the past century. Hence, it can be assumed that this rate portents additional future outbreaks. To mitigate the consequences of such a disease emergence, it is important to understand the underlying causes. In this light, we have reviewed the literature in order to highlight the salient features of P. syringae as a pathogen of woody plant species and to underscore what remains unknown about the diseases it causes.

ECONOMIC IMPORTANCE

Reliable estimates of economic losses caused by plant pathogens are not only a prerequisite for optimal crop management at the farm level but also for basic decisions on broader issues such as research priorities and pesticide regulations. Although several methods have been proposed to evaluate economic losses caused by plant pathogens [START_REF] Heaton | Evaluating economic losses caused by pathogens of fruit and nut crops[END_REF][START_REF] James | Assessment of plant diseases and losses[END_REF], only few data are available in the literature. Insufficient information on the biological effects of the pathogens on their host is the major obstacle preventing more accurate crop-loss assessment in monetary terms. Crop-loss assessments have been made for major annual staple and cash crops [START_REF] Oerke | Crop losses to pests[END_REF][START_REF] Oerke | Crop Production and Crop Protection Estimated Losses in Major Food and Cash Crops[END_REF]. However, data inadequacies are particularly acute in the case of perennial crops, where intertemporal effects operate. For perennial plants, their health in any given season is likely to influence their health in future seasons [START_REF] Heaton | Evaluating economic losses caused by pathogens of fruit and nut crops[END_REF].

Bacterial cankers of perennial trees caused by P. syringae provoke serious economic losses around the world. Cankers are characterized by systemic wilting and dieback of twigs, branches or the entire tree resulting from systemic spread of the pathogen in the vessels. On hazelnut, bacterial canker was reported to be the most important factor limiting the cultivation and further expansion of hazelnut production in Greece [START_REF] Psallidas | Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana[END_REF] since its first outbreak [START_REF] Psallidas | A bacterial canker of hazelnut in Greece[END_REF]. In Italy, P. syringae destroyed thousands of hectares of hazelnut, with an annual loss of approximately US$ 1.5 million [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF][START_REF] Scortichini | Severe outbreak of Pseudomonas syringae pv. avellanae on hazelnut in Italy[END_REF]. Similarly, the recent bacterial canker epidemic of kiwifruit has decimated thousands of hectares around the world. In New Zealand alone, yield losses caused by the disease in 2012 were estimated to be 21% (90,820 ton less than in 2011) with economic losses of US$ 76 million (http://www.kvh.org.nz/newsroom). However, the most dramatic consequences of the disease can be seen for the long term. A risk analysis, performed in 2012, estimated that over the next five years bacterial Advances in Agronomy, First Edition, 2014, 235-295 canker of kiwifruit might cost between NZ$ 310 million to 410 million to the New Zealand kiwifruit industry [START_REF] Vanneste | Pseudomonas syringae pv. actinidiae (Psa): a threat to the New Zealand and global kiwifruit industry[END_REF]. It is estimated that over a 15-year period the cost might jump to NZ$ 885 million [START_REF] Greer | The Costs of Psa-V to the New Zealand Kiwifruit Industry and the Wider Community[END_REF]. In the Bay of Plenty area of New Zealand alone, 360 to 470 fulltime jobs might be lost between 2012 and 2016 due to the bacterial canker epidemic on kiwifruit [START_REF] Greer | The Costs of Psa-V to the New Zealand Kiwifruit Industry and the Wider Community[END_REF]. Although no estimation has been made for Italy, the situation in that country might be even worse, given the intensity and diffusion of the bacterial canker epidemics [START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF][START_REF] Vanneste | Pseudomonas syringae pv. actinidiae (Psa): a threat to the New Zealand and global kiwifruit industry[END_REF]. Due to the extent and serious impact of bacterial canker, it is thought that kiwifruit plantings in Italy will be significantly reduced over the next three to five years (http://www.kvh.org.nz/newsroom).

Bacterial canker also affects tree species in the genus Prunus (stone fruits and almond) [START_REF] English | Bacterial canker, an important decline disease of apricots and other stone fruits in California[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Vicente | Identification and discrimination of Pseudomonas syringae isolates from wild cherry in England[END_REF]. In South Africa, annual damage caused by bacterial canker of stone fruit crops is estimated to be over US$ 10 million [START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF]. Damage caused by P. syringae is not limited to field production but also occurs in nurseries where sudden wilting is a major problem. For example, annual losses in woody plant nurseries in Oregon are estimated at US$ 8 million [START_REF] Scheck | Copper and streptomycin resistance in strains of Pseudomonas syringae from Pacific Northwest nurseries[END_REF].

In Germany, bacterial canker causes annual tree mortality rates as high as 30% on plum [START_REF] Hinrichs-Berger | Epidemiology of Pseudomonas syringae pathovars associated with decline of plum trees in the southwest of Germany[END_REF]. In Oregon (the USA), bacterial canker is responsible for 17% annual tree deaths for sweet cherry [START_REF] Spotts | Incidence and control of cytospora canker and bacterial canker in a young sweet cherry orchard on Oregon[END_REF]. The incidence of bacterial canker is reported to be 50-100% on wild cherry in the UK [START_REF] Vicente | Identification and discrimination of Pseudomonas syringae isolates from wild cherry in England[END_REF], 50% on plum in the Netherlands [START_REF] Wenneker | Bacterial canker of plum caused by Pseudomonas syringae pathovars, as a serious threat for plum production in the Netherlands[END_REF], and 80% on apricot in Turkey [START_REF] Kotan | First record of bacterial canker caused by Pseudomonas syringae pv. syringae, on apricot trees in Turkey[END_REF]. In addition to stone fruits, P. syringae diseases are economically important also on pome fruits [START_REF] Mansvelt | Bacterial blister bark and blight of fruit spurs of apple in south Africa caused by Pseudomonas syringae pv. syringae[END_REF]. The disease results in economic losses in pear production around the world [START_REF] English | Bacterial canker, an important decline disease of apricots and other stone fruits in California[END_REF][START_REF] Fahy | Pseudomonas: the fluorescent pseudomonads[END_REF][START_REF] Manceau | Bacterial colonization of flowers and leaf surface of pear trees[END_REF][START_REF] Montesinos | Relationships among population-levels of Pseudomonas syringae, amount of ice nuclei, and incidence of blast of dormant flower buds in commercial pear orchards in Catalunya, Spain[END_REF]. Another very recent epidemic caused by P. syringae is bleeding canker of horse chestnut. The disease is widespread in many European countries [START_REF] Bultreys | Characterization of Pseudomonas syringae strains isolated from diseased horse chestnut trees in Belgium[END_REF][START_REF] Schmidt | Pseudomonas syringae pv. aesculi associated with horse chestnut bleeding canker in Germany[END_REF][START_REF] Webber | Isolation and identification of Pseudomonas syringae pv. aesculi causing bleeding canker of horse chestnut in the UK[END_REF]. However, no data are available on the potential losses.

TYPES OF DISEASES OF WOODY PLANTS CAUSED BY P. SYRINGAE AND THEIR IMPORTANCE

A broad range of crops is susceptible to diseases caused by the group of Gram-negative bacteria referred to as P. syringae [START_REF] Bull | Comprehensive list of names of plant pathogenic bacteria, 1980-2007[END_REF]. Concerning perennial plants, the literature suggests that a large number Advances in Agronomy, First Edition, 2014, 235-295 of woody tree species are attacked by this pathogen. An exhaustive list of diseases of perennial plants caused by P. syringae is reported in Table 4.2. Deciduous fruit and nut trees [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Mansvelt | Bacterial blister bark and blight of fruit spurs of apple in south Africa caused by Pseudomonas syringae pv. syringae[END_REF], ornamental trees and shrubs [START_REF] Garibaldi | First report of bacterial leaf spot caused by Pseudomonas syringae pv. viburnii on Viburnum sargentii in Italy[END_REF]Temsah et al., 2007a,b), deciduous forest tree species [START_REF] Ark | Bacterial leaf spot of maple[END_REF][START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF][START_REF] Menard | Pseudomonas syringae pv. avii (pv. nov.), the causal agent of bacterial canker of wild cherries (Prunus avium) in France[END_REF], and evergreen fruit trees [START_REF] Young | Olive knot and its pathogens[END_REF] are among the known hosts of P. syringae. Overall, phytopathogenic P. syringae causes two types of diseases on woody plants [START_REF] Agrios | Plant Pathology[END_REF], those whose symptoms are confined to parenchymatic tissue and those whose symptoms are manifested in vascular tissue.

Parenchymatic or Localized Diseases

One family of diseases of woody plants caused by P. syringae is characterized by the presence of localized symptoms affecting parenchymatic tissues. In this case, the pathogen does not move throughout the host vascular system. Typical symptoms are leaf spots [START_REF] Destéfano | Bacterial leaf spot of coffee caused by Pseudomonas syringae pv. tabaci in Brazil[END_REF]Goto, 1983aGoto, , 1983b;;Roberts, 1985a), fruit spots [START_REF] Bedford | Population dynamics of Pseudomonas syringae pv. papulans on Mutsu apple[END_REF][START_REF] Burr | Seasonal susceptibility of "Mutsu" apples to Pseudomonas syringae pv. papulans[END_REF], apical necrosis [START_REF] Cazorla | Bacterial apical necrosis of mango in southern Spain: a disease caused by Pseudomonas syringae pv. syringae[END_REF][START_REF] Golzar | First report of bacterial necrosis of mango caused by Pseudomonas syringae pv. syringae in Australia[END_REF], blossom and bud blasts [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Manceau | Bacterial colonization of flowers and leaf surface of pear trees[END_REF][START_REF] Mansvelt | Bacterial blister bark and blight of fruit spurs of apple in south Africa caused by Pseudomonas syringae pv. syringae[END_REF][START_REF] Young | Ice-nucleation on kiwifruit[END_REF], bud rot and necroses [START_REF] Cazorla | Bacterial apical necrosis of mango in southern Spain: a disease caused by Pseudomonas syringae pv. syringae[END_REF][START_REF] Conn | Bacterial blight of kiwifruit in California[END_REF], shoot tip dieback [START_REF] Mckeen | Pear blast in Vancouver Island[END_REF][START_REF] Polizzi | First report of bacterial blight of Strelitzia augusta caused by Pseudomonas syringae pv[END_REF][START_REF] Ramos | Seasonal periodicity and distribution of bacterial blight of coffee in Kenya[END_REF][START_REF] Tomihama | Environmental control in tea fields to reduce infection by Pseudomonas syringae pv[END_REF], and gall or outgrowth on stems, leaves, and trunks [START_REF] Kamiunten | Pseudomonas syringae pv. cerasicola pv. nov., the causal agent of bacterial gall of cherry tree[END_REF][START_REF] Ogimi | Studies on bacterial gall of chinaberry (Melia azedarach Lin.), caused by Pseudomonas meliae n. sp[END_REF][START_REF] Ogimi | Bacterial gall diseases of himeyuzuriha (Daphniphyllum teijsmanni Z.) caused by Pseudomonas syringae pv. daphniphylli pv[END_REF][START_REF] Ogimi | Bacterial gall disease of sharinbai (Rhaphiolepis umbellata Makino) caused by Pseudomonas syringae pv. rhaphiolepidis pv[END_REF]Temsah et al., 2007a,b). The resulting localized infections rarely kill the plants and losses are due mainly to damage to flowers and photosynthetic parts (leaves).

Vascular or Systemic Diseases

Vascular diseases are characterized by the systemic movement of the disease throughout the plant and in particular the vessels (phloem and xylem). The vascular diseases caused by P. syringae are generally devastating. Sudden wilting and dieback [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF], presence of extended cankers on stems, branches, and main trunks [START_REF] Jones | Bacterial canker of sweet cherry in Michigan[END_REF]Latorre and Jones, 1979a;[START_REF] Little | Genetic characterization of Pseudomonas syringae pv. syringae strains from stone fruits in California[END_REF][START_REF] Sakamoto | Anatomy of bacterial canker on Maackia amurensis var. buergeri[END_REF]Young, 1988a), and production of exudates and gummosis [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF] are common symptoms.

To attack stems, branches, and trunks, P. syringae infects the woody tissue of the plant. Of all the plant tissues, woody tissue has the highest content of lignin, a complex phenolic polymer common to vascular plants. Plant lignin can be broadly divided into three classes, softwood (gymnosperm), hardwood (angiosperm), and grass (graminaceous) lignin [START_REF] Pearl | The Chemistry of Lignin[END_REF]. Lignin has a fundamental role in water transport, mechanical support, and biodefense [START_REF] Robinson | Lignin, land plants, and fungi: biological evolution affecting Phanerozoic oxygen balance[END_REF]. Within a plant, lignin content varies greatly in different tissues. For example, lignin content is very low in young shoots and high in woody tissues [START_REF] Novaes | Lignin and biomass: a negative correlation for wood formation and lignin content in trees[END_REF]. The lignin content of woody perennial plants can vary from 15% to 40% [START_REF] Sarkanen | Lignins: Occurrence, Formation, Structure and Reactions[END_REF] whereas in annual plants it represents only from 4% to 10% of the oven-dry weight [START_REF] Sullivan | Cellulose and lignin in forage grasses and their digestion coefficients[END_REF]. How P. syringae can overcome such a robust barrier and cause a collapse of woody tissues is not known. Interestingly, P. syringae-induced vascular diseases have been reported exclusively on deciduous trees [START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF][START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF] while only parenchymatic diseases are caused on evergreen woody plants [START_REF] Ramos | Seasonal periodicity and distribution of bacterial blight of coffee in Kenya[END_REF][START_REF] Young | Olive knot and its pathogens[END_REF]) (Table 4.2). Many aspects of the annual growth cycle differ significantly between deciduous and evergreen plants. Adaptation to a cold or dry season and to low nutrient levels has led to the differentiation of deciduous and evergreen woody plants [START_REF] Monk | An ecological significance of evergreenness[END_REF]. The annual phenology of deciduous trees is the process that begins with flower budbreak followed by leaf budbreak and sprouting in the spring and culminates in leaf fall in autumn followed by winter dormancy [START_REF] Arora | Induction and release of bud dormancy in woody perennials: a science comes of age[END_REF]. These characteristics differentiate a deciduous tree from evergreens where such phenomena do not occur in synchrony for the whole tree. Accordingly, the risk of P. syringae infection might be strikingly higher on deciduous trees given the synchronized abundance of tender tissues and natural openings into the vascular system. Succulent swelling buds and shoots are fragile and highly sensitive to frost damage, thereby predisposing deciduous trees to frost damage induced by P. syringae [START_REF] Gross | Ecotypes and pathogenicity of ice nucleation-active Pseudomonas syringae isolated from deciduous fruit tree orchards[END_REF][START_REF] Nejad | Pathogenic ice-nucleation active bacteria in willows for short rotation forestry[END_REF][START_REF] Ramstedt | Dieback of poplar and willow caused by Pseudomonas syringae in combination with freezing stress[END_REF]. On the other hand, complete leaf fall that creates an enormous availability of leaf scars for a long period of time perfectly coincides with climatic conditions that are ideal for the survival and multiplication of P. syringae [START_REF] Agrios | Plant Pathology[END_REF][START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF]. The presence of dormant buds, during the winter, represents an ideal overwintering site for P. syringae [START_REF] Crosse | Bacterial canker of stone fruits. II. Leaf scar infection of cherry[END_REF]Roos and Hattingh, 1986;[START_REF] Sundin | Overwintering and population dynamics of Pseudomonas syringae pv. syringae and P. s. pv. morsprunorum on sweet and sour cherry trees[END_REF]. On the contrary, evergreen species do not have autumn leaf shedding. However, leaf shed occurs very gradually over the years in evergreen plants [START_REF] Aerts | The advantages of being evergreen[END_REF]. Leaf spots caused by P. syringae are also almost exclusively reported on deciduous trees [START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. It is not known why a ubiquitous epiphyte such as P. syringae [START_REF] Hirano | Population biology and epidemiology of P. syringae[END_REF]) causes foliar diseases only on a Advances in Agronomy, First Edition, 2014, 235-295 very limited number of evergreen hosts, despite whole-year availability of leaf surfaces. In addition to the higher number of infection sites in deciduous trees, several studies have provided evidence of differences in protein content of bark between deciduous trees, including deciduous fruit trees [START_REF] Kang | Specific proteins may determine maximum cold resistance in apple shoots[END_REF][START_REF] Kuroda | Frost induces cold acclimation and peroxidasescavenging systems coupled with pentose phosphate cycle in apple twigs under natural conditions[END_REF][START_REF] Lang | Analysis of fruit bud proteins associated with plant dormancy[END_REF][START_REF] Mattheis | Changes in parameters of the plasmalemma ATPase during cold acclimation of apple (Malus domestica) bark tissues[END_REF], and evergreen woody plants [START_REF] Craker | Soluble proteins and cold hardiness of two woody species[END_REF][START_REF] Hummel | Protein comparisons of non-and coldacclimated Hibiscus syriacus and H. rosa-sinensis bark[END_REF]. For example, higher levels of polypeptide accumulation in bark tissues were observed in the deciduous peach compared with the evergreen one [START_REF] Arora | Cold acclimation in genetically related (sibling) deciduous and evergreen peach (Prunus persica [L.] Batsch): I. Seasonal changes in cold hardiness and polypeptides of bark and xylem tissues[END_REF]. Probably such polypeptides are involved in the process of vascularization of P. syringae. But this will need to be established by in-depth future studies. Species with both deciduous and evergreen traits, such as Viburnum spp., might provide some new insights in this regard.

EPIDEMIOLOGY

As for all plant diseases, biotic, abiotic and/or edaphic factors play an important role in epidemiology. Throughout the cultivation areas, these factors have been reported to weaken plant health and predispose them to pathogen attacks. In particular, soil texture, low soil pH, soil depth, tree nutrition, tree age, nematode parasitism, and environmental factors such as rain can influence P. syringae disease development [START_REF] English | Effect of certain soil treatments on the development of bacterial canker in peach trees (Abstract)[END_REF][START_REF] English | Bacterial canker, an important decline disease of apricots and other stone fruits in California[END_REF][START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF][START_REF] Scortichini | Epidemiology and predisposing factors of some major bacterial diseases of stone and nut fruit trees species[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF][START_REF] Vigouroux | Une action possible des sols sur la prédisposition des pêchers au dépérissement bactérien par modification de la teneur en eau hivernale des tiges[END_REF]. In addition, cultural practices such as rootstock selection, height of grafting and early fall pruning have been reported to affect P. syringae disease susceptibility of apricot and peach [START_REF] Dunquesne | L'inflience des porte-greffes sur la sensibilité de l'abricotier aux bactérioses[END_REF][START_REF] Fratantuono | Bactériose et choix du porte-greffe en Roussillon[END_REF][START_REF] Lownsbery | Influence of Nemaguard and Lovell rootstocks and Macroposthonia xenoplax on bacterial canker of peach[END_REF][START_REF] Prunier | Influence of rootstocks and height of grafting on the susceptibility of apricot cultivars to bacterial canker[END_REF][START_REF] Vigoroux | La sensibilité de pecher au dépérissement bactérien en France: incidence de certaines caractéristiques du sol et de l'irrigation[END_REF][START_REF] Vigoroux | Bactériose du pecher et de l'abricotier. Influene combinée du froid et du sol[END_REF]. Likewise, the correlation among tree water content, effect of exposure to freezing temperature, and necrosis caused by P. syringae has been reported for apricot [START_REF] Klement | Apoplexy of apricots. III. Relationship of winter frost and the bacterial canker dieback of apricots[END_REF][START_REF] Vigoroux | Ingress and spread of Pseudomonas in stems of peach and apricot promoted by frost-related water soaking tissue[END_REF], cherry [START_REF] Sobiczewski | Effect of exposure to freezing temperature on necrosis in sweet cherry shoots inoculated with Pseudomonas syringae pv. syringae or P. s. morsprunorum[END_REF], and peach [START_REF] Cao | Effect of leaf scar age, chilling and freezing-thawing on infection of Pseudomonas syringae pv. syringae through leaf scars and lenticels in stone fruits[END_REF][START_REF] Vigoroux | Bacterial Canker of Peach: Effect of Tree Winter Water Content on the Spread of Infection Through Frost!related Water Soaking in Stems[END_REF][START_REF] Weaver | Interaction of Pseudomonas syringae and freezing in bacterial canker on excised peach twigs[END_REF]. There are few generalities that can be made about the impact of abiotic factors and the production practices to which they are linked. On the other hand, biotic factors concerning both the plant and the pathogen have been received in the most intense study and offer the opportunity to identify key factors critical in disease development as illustrated below.

Sources of Inoculum

Overall, epiphytic populations, latent infection, overwintering sites on the infected hosts, the presence of orchard groundcovers, weeds, and detached Advances in Agronomy, First Edition, 2014, 235-295 plant parts (pollen and leaf litter) represent the inoculum reservoir of P. syringae. All these inoculum sources appear to be important in the epidemiology of diseases caused by P. syringae. Epiphytic populations of this pathogen on asymptomatic plants are the immediate source of inoculum for disease. Differences in epiphytic populations of P. syringae were observed on leaves of apple trees grown in two different orchards: one with a history of disease, the other where the disease had not been observed previously [START_REF] Bedford | Population dynamics of Pseudomonas syringae pv. papulans on Mutsu apple[END_REF]. Larger pathogen population sizes were found in association with greater disease incidence in the orchard with a prior history of the disease. Similarly, epiphytic populations of P. syringae as the source of inoculum for disease have been demonstrated on olive [START_REF] Young | Olive knot and its pathogens[END_REF], maple and pear trees [START_REF] Malvick | Population dynamics and diversity of Pseudomonas syringae on maple and pear trees and associated grasses[END_REF], and stone fruits (Roos and Hattingh, 1986). Monitoring of P. syringae epiphytic populations associated with nursery trees in Oregon showed that the population increased rapidly and peaked during the first 2-3 weeks after budbreak (Baca et al., 1987;[START_REF] Moore | Survival and dissemination of Pseudomonas syringae on maple trees and grasses[END_REF] increasing markedly the risk of bud infection.

Establishment of P. syringae populations inside symptomless tissues could represent a very important source of primary inoculum. For this reason, vegetative propagation of the apparently healthy but latently infected mother plants could be an important source of inoculum. Widespread disease dissemination with propagation material such as dormant cuttings or budwoods, and in vitro-propagated shoots can be therefore relevant. On hazelnut, a large-scale dissemination of P. syringae is thought to have occurred through distribution of latently infected suckers [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF]. In addition, infected nursery stock of olive has been reported as the main cause of P. syringae introduction into new regions [START_REF] Young | Olive knot and its pathogens[END_REF]. The isolation of pathogenic P. syringae from the vascular tissues of symptomless cherry [START_REF] Cameron | Pseudomonas content of cherry trees[END_REF] and pear trees [START_REF] Whitesides | Frequency, distribution, and characteristics of endophytic Pseudomonas syringae in pear trees[END_REF] clearly explains the latent presence of the pathogen also in deciduous woody hosts. Indeed, infected nursery materials have been reported as the main inoculum reservoir of P. syringae in Prunus spp. [START_REF] Dowler | Transmission of Pseudomonas syringae in peach trees by bud propagation[END_REF][START_REF] Lyskanowska | Bacterial canker of sweet cherry (Prunus avium) in Poland. I. Symptoms, disease development and economic importance[END_REF]Mansvelt and Hattingh, 1988).

Woody plants provide the unique overwintering sites compared to annual plants. The role of dormant buds in deciduous trees as an overwintering site for P. syringae has been demonstrated in South Africa (Roos and Hattingh, 1986a), in the United Kingdom [START_REF] Crosse | Bacterial canker of stone fruits. II. Leaf scar infection of cherry[END_REF], and in the USA [START_REF] Sundin | Overwintering and population dynamics of Pseudomonas syringae pv. syringae and P. s. pv. morsprunorum on sweet and sour cherry trees[END_REF]. On apple, a consistent population of P. syringae has been recovered from the innermost bud tissues and the population was larger than that found in the external tissues [START_REF] Bedford | Population dynamics of Pseudomonas syringae pv. papulans on Mutsu apple[END_REF]Burr and Katz,Advances in Agronomy,First Edition,2014,). Dormant buds in cherry are colonized via infection of leaf scars during autumn at leaf fall. Climatic conditions during leaf shedding typically include cooler temperatures and wind-driven rains during which P. syringae is transported from leaf surfaces to leaf scars where systemic colonization occurs [START_REF] Crosse | Bacterial canker of stone fruits. II. Leaf scar infection of cherry[END_REF]. Once P. syringae enters through leaf scars, it moves systematically throughout the plant and colonizes dormant buds where the pathogen overwinters. In the following spring, dormant and apparently healthy but infected buds provide the inoculum for blossom colonization.

The importance of groundcovers and weeds within and outside the orchard represent another potential source of inoculum reservoir of P. syringae. In particular, when no leaf surface is available on trees (autumn and winter) the pathogen can shift to the groundcovers where it multiplies thereby ensuring a constant source of inoculum. Work reported from California [START_REF] Davis | Factors related to the development of bacterial canker in peach[END_REF] was the first to implicate weeds as hosts for P. syringae. Successively, the association of P. syringae with stone fruit orchard weeds or grasses have been reported in the USA (Michigan (Latorre and Jones, 1979b), Oregon (Baca and Moore, 1987)), Poland [START_REF] Lyskanowska | Bacterial canker of sweet cherry (Prunus avium) in Poland. I. Symptoms, disease development and economic importance[END_REF], and South Africa (Roos and Hattingh, 1986b). Large populations of phytopathogenic P. syringae have been consistently isolated from perennial rye, red fescue, annual rye and broom grasses growing among ornamental trees in the maple nursery and on perennial rye grass in the pear orchard [START_REF] Malvick | Population dynamics and diversity of Pseudomonas syringae on maple and pear trees and associated grasses[END_REF].

In some cases, pollen can be an important inoculum source of the pathogen. On kiwifruit, P. syringae has been found in pollen samples (Vanneste et al., 2011a) and it is believed that pollen has been a source of P. syringae introduction in New Zealand. In addition, P. syringae is able to survive in detached kiwifruit organs, such as leaf litter and twigs, until 45 days post-leaf fall (http://www.kvh.org.nz). Leaf litter across the alpine environment has been reported as an important reservoir of P. syringae populations [START_REF] Monteil | Emigration of the plant pathogen Pseudomonas syringae from leaf litter contributes to its population dynamics in alpine snowpack[END_REF]. Finally, it is thought that P. syringae survives poorly in soil or host debris, mostly throughout the regions with warmer summer [START_REF] Mccarter | Survival of Pseudomonas syringae pathovar tomato in association with tomato lycopersicon esculentum seed, soil, host tissue and epiphytic hosts in Georgia[END_REF] although it is possible that the pathogen can survive for a long period in regions with cooler summer temperature, mostly under a constant soil moisture. Indeed, the ability of P. syringae to survive in the soil for a longer period has been demonstrated especially when the source of the inoculum was associated with plant debris and in the presence of constant soil moisture [START_REF] Kritzman | Survival of Pseudomonas syringae pv. lachrymans in soil, plant debris, and the rhizzosphere of no-host plants[END_REF]. It is also worth to noting that P. syringae has been isolated from the rhizosphere of crops and weeds [START_REF] Knoche | Root colonization by Pseudomonas syringae pv. tabaci[END_REF][START_REF] Valleu | Root infection of crop plants and weeds by tobacco leaf spot bacteria[END_REF]. The fact that P. syringae can't be

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Advances in Agronomy, First Edition, 2014, 235-295 found in agricultural soil all year round (mostly during the summer) might be because such lands are irrigated generally until the beginning of the summer and no water supply occurs afterward once the crops are harvested. Hence, warmer summer temperatures associated with a drastic reduction in soil moisture result in fatal conditions for the survival of P. syringae.

Snow is another important source of P. syringae inoculums, which may play an important role in a disease occurrence. An example is bacterial canker of blueberry [START_REF] Canfield | Isolation of Pseudomonas syringae from 40 cultivars of diseased woody plants with tip dieback in Pacific Northwest nurseries[END_REF]. This species grows naturally or in cultivated conditions across mountain areas where snowfall events are very common. At higher altitudes, spring frosts frequently occur where freezing and thawing are accentuated through the fluctuations in day/night temperatures. Such events cause lesions on plant parts exposing them to a high risk of infection. Snow per se can harbor populations of P. syringae as recently demonstrated [START_REF] Morris | Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand[END_REF]. Besides snow, other environmental reservoirs of P. syringae including headwaters and epilithic biofilm have been described [START_REF] Morris | Surprising niche for the plant pathogen Pseudomonas syringae[END_REF][START_REF] Morris | Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand[END_REF], and these eventually can come into contact with crops as irrigation water.

Ports of Entry for Infection of Plant Tissues

Unlike fungal pathogens, phytopathogenic bacteria are not able to make their own ports of entry [START_REF] Agrios | Plant Pathology[END_REF]. Woody plants present a wide range of entry ports for bacteria including natural openings and wounds caused by natural phenomena and man-made practices. Natural openings (lenticels, hydathodes, stomata, trichomes) that serve as water and gas pores, and the wounds made by biotic (humans, insects, animals) and abiotic factors (hailstones, frost), are the main ports of entry [START_REF] Agrios | Plant Pathology[END_REF]. For P. syringae pathogens of woody plants, the literature reports a large diversity of ports of entry as summarized in Figure 4.1. To gain access into plant tissues, the pathogen can use more than one port of entry. In general, foliar pathogens that cause localized symptoms enter mainly through the stomata, although some of them also enter via hydathodes and broken trichomes [START_REF] Agrios | Plant Pathology[END_REF][START_REF] Hirano | Population biology and epidemiology of P. syringae[END_REF]. Pathogens that cause woody parenchymatic diseases enter through wounds occurring on woody tissues (Garcia de los Rios, 1999; [START_REF] Kamiunten | Pseudomonas syringae pv. cerasicola pv. nov., the causal agent of bacterial gall of cherry tree[END_REF][START_REF] Ogimi | Bacterial gall diseases of himeyuzuriha (Daphniphyllum teijsmanni Z.) caused by Pseudomonas syringae pv. daphniphylli pv[END_REF][START_REF] Young | Olive knot and its pathogens[END_REF]. On the other hand, vascular pathogens use a vast number of ports including natural openings and lesions [START_REF] Crosse | Epidemiological relations of the pseudomonad pathogens of deciduous fruit trees[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF]. Lesions on woody tissues that allow a direct access to the vascular system are the most accessible port for vascular pathogens while natural openings are not always exploited by the different P. syringae pathogens of woody plants. There seems to be a Advances in Agronomy, First Edition, 2014, 235-295 relationship between the port of entry and the symptoms caused by vascular P. syringae pathogens. Interestingly, leaf symptoms do not occur on infected hazelnut [START_REF] Psallidas | Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana[END_REF][START_REF] Psallidas | A bacterial canker of hazelnut in Greece[END_REF] and horse chestnut [START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF] while they occur on infected kiwifruit [START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF][START_REF] Young | Pseudomonas syringae pv. actinidiae in New Zealand[END_REF] and Prunus spp. [START_REF] Bultreys | Bacterial cankers caused by Pseudomonas syringae on stone fruit species with special emphasis on the pathovars syringae and morsprunorum race 1 and race 2[END_REF][START_REF] Crosse | Epidemiological relations of the pseudomonad pathogens of deciduous fruit trees[END_REF][START_REF] Freigoun | Host relations and distribution of a physiological and pathological variant of Pseudomonas morsprunorum[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. On hazelnut, the only ports of entry used by P. syringae are leaf scars and lesions on woody tissues [START_REF] Psallidas | Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana[END_REF][START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF] giving the pathogen direct access to the vascular system. For horse chestnut, in addition to lesions, the role of lenticels as ports of entry has been demonstrated [START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF]. Indeed, lesions in proximity to lenticels appeared when stems of horse chestnut were spray-inoculated [START_REF] Green | Infection of horse chestnut (Aesculus hippocastanum) by Pseudomonas syringae pv. aesculi and its detection by quantitative real-time PCR[END_REF]. By contrast, Prunus spp. and in particular apricot and cherry, contain an impressive number of lenticels [START_REF] Guirguis | Leaf stomata and stem lenticels as a means of identification of some stone fruits stocks[END_REF] although no report is available about ingress of P. syringae through the lenticels on these hosts. It is worth exploring why an enormous availability of this port does not seem to be exploited by the pathogen. In Prunus spp. the role of infection seems to be quite different. For example, on cherry most canker symptoms are located on the branches since the pathogen enters through leaf scars while the main stem is affected on plum where the pathogen seems to gain access through small wounds, although of unknown origin [START_REF] Crosse | Pathogenicity of Pseudomonas morsprunorum in relation to host specificity[END_REF]. Although leaf scar is one of the main ports of entry for P. syringae that cause vascular disease, on cherry it is not always utilized as an avenue of infection at warmer temperatures in particular. In South Africa, it seems that P. syringae reaches buds through the systemic movement before the leaf fall [START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF]. Because P. syringae is a psychrophilic bacterium, it is possible that epiphytic populations of the pathogen do not survive in warmer temperatures, thereby favoring the organisms that colonize systemically. In Oregon, where mass destruction of dormant buds is the most conspicuous feature of the disease, attempts to infect cherry leaf scars with P. syringae failed [START_REF] Cameron | Mode of infection of sweet cherry by Pseudomonas syringae[END_REF]. Here, the author concluded that the infection was a result of direct bud infection, through the outer scales after the leaf-fall period. A recent study, based on the artificial inoculation experiments, showed that cherry is more susceptible to P. syringae infection through leaf scars than peach and "French" prune [START_REF] Cao | Effect of leaf scar age, chilling and freezing-thawing on infection of Pseudomonas syringae pv. syringae through leaf scars and lenticels in stone fruits[END_REF].

Means of Dissemination

Several natural and man-made phenomena favor the long-and short-distance dissemination of P. syringae. This pathogen can be carried in aerosols and thereby transported by wind-driven rain [START_REF] Crosse | Epidemiological relations of the pseudomonad pathogens of deciduous fruit trees[END_REF]. In addition, Advances in Agronomy, First Edition, 2014, 235-295 the discovery that the life history of P. syringae is linked to the water cycle [START_REF] Morris | The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle[END_REF] explains how easily the pathogen can be disseminated over a wide range of distances. P. syringae can also be transmitted through mechanical equipment and pruning tools although their role in pathogen dissemination is often overlooked. Furthermore, insects such as aphids have been demonstrated to be potential vectors of P. syringae [START_REF] Stavrinides | Pea aphid as both host and vector for the phytopathogenic bacterium Pseudomonas syringae[END_REF]. On stone fruits, the role of insects as a potential carrier of P. syringae inoculum has been demonstrated [START_REF] Wormland | Bacterial diseases of stone fruit trees in Britain. III. The symptoms of bacterial canker in plum trees[END_REF]. However, the most important dissemination source of P. syringae remains the transportation of infested nursery stock [START_REF] Dowler | Transmission of Pseudomonas syringae in peach trees by bud propagation[END_REF][START_REF] Lyskanowska | Bacterial canker of sweet cherry (Prunus avium) in Poland. I. Symptoms, disease development and economic importance[END_REF][START_REF] Mansvelt | Bacterial blister bark and blight of fruit spurs of apple in south Africa caused by Pseudomonas syringae pv. syringae[END_REF].

Variability in Host Genotype Susceptibility

The underlying genetic variability and intensity of production is also important in the epidemiology of diseases of woody plants caused by P. syringae. A recent example of kiwifruit bacterial canker epidemics reveals how the cultivation of a very narrow range of plant diversity threatens durability of plant resistance. The genus Actinidia consists of over 50 species native to China where all wild germplasm is naturally distributed [START_REF] Liang | On the distribution of Actinidia[END_REF]. However, the breeding of kiwifruit in New Zealand has been founded on imported planting materials where only two commercial varieties (cv. Hayward and Hort 16A, belonging to Actinidia deliciosa and Actinidia chinensis, respectively) have been developed and commercialized. For decades, the commercial kiwifruit industry was dominated by the sole cv. Hayward, grown in more than 80% of the world's kiwifruit production areas. It was not until 1999 that commercial marketing of cv. Hort16A was initiated [START_REF] Ferguson | Kiwifruit cultivars: breeding and selection[END_REF]. Suddenly, the kiwifruit industry has become vulnerable to P. syringae infection where the pathogen has jeopardized the entire kiwifruit industry [START_REF] Butler | Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in China[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF]. Intensive kiwifruit cultivation with very low genetic diversity in areas that are far from its center of origin has been detrimental for the long-term durability of the crop. Bacterial canker of European hazelnut (Corylus avellana L.) illustrates a marked contrast to the case of kiwifruit canker [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF]. Unlike kiwifruit, European hazelnut has a wide natural geographical distribution ranging from the Mediterranean coast of North Africa northward to the British Islands and the Scandinavian Peninsula, and eastward to the Ural Mountains of Russia, the Caucasus Mountains, Iran, and Lebanon [START_REF] Rushforth | Trees of Britain and Europe[END_REF] [START_REF] Mehlenbacher | Hazelnut genetic resources in temperate fruit and nut crops[END_REF]. A large number of European hazelnut varieties are grown around the globe. In Turkey, the world's most important hazelnut producer, an assorted number of varieties are grown together often in the same field. Bacterial canker has not been reported under these conditions. Indeed, the most extensive cultivated collection of hazelnut genetic resources resides in Turkey, which preserves 739 selections with over 700 genotypes of C. avellana [START_REF] Hummer | The mystical powers and culinary delights of the hazelnut: a globally important Mediterranean crop[END_REF][START_REF] Thompson | Hazelnuts[END_REF]. In contrast, in Greece where a hazelnut cultivar imported from Turkey (cv. Palaz) was intensively grown in monoculture, bacterial canker caused devastating losses making the cultivation impossible in some areas [START_REF] Psallidas | A bacterial canker of hazelnut in Greece[END_REF]. Similarly, bacterial canker of hazelnut is a serious problem in some areas of central Italy [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF] where only one cultivar (cv. Tonda Gentile Romana) is grown in more than 85% of the areas. By contrast, the disease is not reported from other Italian hazelnut growing areas such as Campania, Piedmont, Sardinia, and Sicily where several local varieties are grown [START_REF] Siscaro | Le principali avversita' del nocciolo in Sicilia[END_REF][START_REF] Virdis | Studio delle principali malattie del nocciolo in Sardegna[END_REF].

Among other economically important woody crop species, grapevine (Vitis vinifera), Mango (Mangifera indica), and citrus (Citrus spp.) are the hosts of P. syringae, although attacks and economic losses on these species have been reported sporadically. A very large genetic diversity has been described in the cultivated grapevine Arroyo-Garcia et al., 2006). The genus Vitis is native to Transcaucasia (McGovern, 2003), which comprises about 60 interfertile wild Vitis species. The natural distribution of such species ranges from Asia to Europe and North America [START_REF] Terral | Evolution and history of grapevine (Vitis vinifera) under domestication: new morphometric perspectives to understand seed domestication syndrome and reveal origins of ancient European cultivars[END_REF]. Species native to North America, such as Vitis rupestris, Vitis riparia or Vitis berlandieri, are widely used in breeding programs against different fungal pathogens that cause economically important diseases on grapevine. Several wild species of Vitis were found to grow along the river banks, and in alluvial and colluvial deciduous and semideciduous forests [START_REF] Arnold | Situation de la vigne sauvage Vitis vinifera subsp. silvestris en Europe[END_REF]. The distribution in the wild of these species ranges from Western Europe to the Trans-Caucasian zone and around the Mediterranean Basin except the most southern infra-Mediterranean and non-Mediterranean zones [START_REF] Arnold | Situation de la vigne sauvage Vitis vinifera subsp. silvestris en Europe[END_REF]. In Mango, in addition to commercial varieties, a large number of local and wild germplasm is reported to form a vast genetic resource to the mango breeder [START_REF] Bally | Mango breeding[END_REF] [START_REF] Bally | Mango breeding[END_REF]. In Citrus spp., lower genetic diversity is reported among the cultivars of orange, grapefruit and lemon since they have originated from nucellar seedlings or budsports. Conversely, mandarins, pummelos, and citrons are reported to have a high level of genetic diversity since many of the cultivars have arisen through sexual hybridization (The Citrus and Date Crop Germplasm Committee, 2004). Only few reports of P. syringae disease on Citrus spp. seem to be linked with the high genetic diversity of this crop, throughout the range of cultivations, thereby enhancing its durability of resistance to the pathogen.

THE DIVERSITY OF P. SYRINGAE CAUSING DISEASE TO WOODY PLANT SPECIES

Pseudomonas syringae is a species complex that encompasses a wide variety of strains that are grouped into numerous phylogroups [START_REF] Parkinson | Rapid phylogenetic identification of members of the Pseudomonas syringae species complex using the rpoD locus[END_REF] based on phylogeny of housekeeping genes using the Multi Locus Sequence Typing method. Strains known to attack woody species are found in all phylogroups except phylogroup 6 that contains strains causing disease on papaya and on sunflower [START_REF] Parkinson | Rapid phylogenetic identification of members of the Pseudomonas syringae species complex using the rpoD locus[END_REF]). An exhaustive list of existing P. syringae pathogens of woody plants is presented in Table 4.2. The names of these pathogens were attributed after instauration of the pathovar nomenclature [START_REF] Dye | International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotypes[END_REF][START_REF] Young | A proposed nomenclature and classification for plant pathogenic bacteria[END_REF] and they were translated to pathovars according to this system for pathogens identified before 1978. Most of the taxonomic descriptions were performed at a time when it was impossible to classify bacteria precisely on the basis of phylogenetic analysis [START_REF] Cai | The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity[END_REF]. Furthermore, in only very few cases the attribution of a pathovar name was accomplished via host range tests (Table 4.3). It is a matter of debate whether the use of the so-called pathovar without thorough host-range description is justified. Among the P. syringae pathogens of woody plants, there are 14 existing pathovars, which were originally proposed as species novel on the basis of a few phenotypic tests (Table 4.3) and are still poorly circumscribed. Often, simply a few differences in biochemical traits in comparison to the lilac pathogen P. syringae pv. syringae were the basis of the proposal that the pathogen be considered as species novel. Such

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Advances in Agronomy, First Edition, 2014, 235-295 discriminate criteria for defining new pathovars are inconsistent with the common observation of high phenotypic and genetic diversity of P. syringae in a very restricted area and even in association with a single species of host plant (Table 4.4). Indeed, a high phenotypic and genetic variability is typical of P. syringae. For each disease, differences in phenotypes and genotypes among the strains incriminated in the disease have been reported in the literature (Table 4.4). In a very recent work, Cinelli et al. (2013c) demonstrated that even the disease symptoms caused by the strains isolated from the same woody plant markedly differ. Similarly, a high phenotypic variability has been reported among the P. syringae strains isolated from different plant organs of the same annual plant affected by the disease [START_REF] Morris | The relationship of host range, physiology, and genotype to virulence on cantaloupe in Pseudomonas syringae from cantaloupe blight epidemics in France[END_REF].

Although attempts to clarify the naming of pathovars were made after 1978, confusions still occur. According to the standards, in designating a novel pathovar, it is necessary to demonstrate, through a pathogenicity testing regime, that the pathogen has a distinct host range or causes a distinct disease when compared with previously described pathogens [START_REF] Young | A proposed nomenclature and classification for plant pathogenic bacteria[END_REF]. However, it seems that old habits persist. For example, P. syringae pv. avii is the name attributed to the causal agent of bacterial canker of wild cherry [START_REF] Menard | Pseudomonas syringae pv. avii (pv. nov.), the causal agent of bacterial canker of wild cherries (Prunus avium) in France[END_REF] without a host range test. Bacterial canker with identical symptoms is caused by P. syringae pv. syringae and P. syringae pv. morsprunorum races on wild cherry [START_REF] Vicente | Identification and discrimination of Pseudomonas syringae isolates from wild cherry in England[END_REF]. On Prunus spp., four distinct P. syringae pathovars (avii, morsprunorum race 1 and 2, persicae and syringae) have been described on the basis of some phenotypic differences. All of them cause bacterial canker on the same hosts and most of them are frequently associated with the same disease [START_REF] Hattingh | Infection and systemic invasion of deciduous fruit trees by Pseudomonas syringae in South Africa[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. Another important example concerns the pathogens of olive and oleander knots caused by Pseudomonas savastanoi pv. savastanoi and P. savastanoi pv. nerii, respectively. Previous studies demonstrated that there is an overlapping host range among these pathovars [START_REF] Alvarez | Phenotypic variability in different strains of Pseudomonas syringae subsp. savastanoi isolated from different hosts[END_REF][START_REF] Janse | Oleaceae and Neriurn oleander L[END_REF]. Recently, [START_REF] Young | An overview of bacterial nomenclature with special reference to plant pathogens[END_REF] questioned if they should be considered as separate pathovars (pv. savastanoi pathogenic to olive and pv. nerii pathogenic to oleander) or as a single pathovar. The debate about the naming of these pathovars can be set into the context of the studies of host range that have been conducted for single pathovars. In many cases, these pathovars infect hosts other than that of the original isolation. [START_REF] Dhanvantari | A taxonomic study of Pseudomonas papulans Rose 1917[END_REF] reported that P. syringae pv. papulans, previously described as species novel from apple [START_REF] Rose | Blister spot of apples and its relation to a disease of apple bark[END_REF], also infects peach. Similarly, [START_REF] Scortichini | Pseudomonas syringae pv. coryli, the causal agent of bacterial twig dieback of Corylus avellana[END_REF] reported a so-called novel pathovar from European hazelnut, P. syringae pv. coryli, which also causes mild disease symptoms on pear, apricot, and peach shoots.

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Advances in Agronomy, First Edition, 2014, 235-295

Without comparative host range testing, it is difficult to know if apple is also a host of strains from peach or if hazelnut is a host of strains from pear and apricot cankers or if these are reports of truly novel pathotypes.

It is difficult to assess if the abundance of reports of different pathovars of P. syringae of woody species reflects a real diversification in host specialization or if it is a reflection of the wide range and inconsistency of tests used to characterize these pathogens. The literature reveals a surprising heterogeneity in tests used for the characterization of P. syringae from woody plants. Firstly, in planta pathogenicity tests on the original host of isolation, for the completion of Koch's postulate, is lacking in some cases [START_REF] Gilbert | Genetic analyses of Pseudomonas syringae strains from Belgian fruit orchards reveal genetic variability and host preferences within pathovar syringae, and help identify both races of pathovar morsprunorum[END_REF][START_REF] Ivanovic | Molecular characterization of Pseudomonas syringae isolates from fruit trees and raspberry in Serbia[END_REF][START_REF] Kaluzna | Characterization and genetic diversity of Pseudomonas syringae from stone fruits and hazelnut using repetitive-PCR and MLST[END_REF]. Secondly, host range tests have been performed only in a limited number of studies and on a very low number of host species (1-5) [START_REF] Cirvilleri | Occurrence of Pseudomonas syringae pv. coryli on hazelnut orchards in sicily, Italy and characterization by fluorescent amplified fragment length polymorphism[END_REF][START_REF] Eltlbany | A new bacterial disease on Mandevilla sanderi, caused by Pseudomonas savastanoi: lessons learned for bacterial diversity studies[END_REF][START_REF] Golzar | First report of bacterial necrosis of mango caused by Pseudomonas syringae pv. syringae in Australia[END_REF][START_REF] Hall | First report of olive knot caused by Pseudomonas savastanoi pv. savastanoi on olives (Olea europea) in Australia[END_REF][START_REF] Psallidas | Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana[END_REF][START_REF] Samavatian | Identification and distribution of bacterial disease agent of almond. Tree canker in Isfahan province[END_REF][START_REF] Scortichini | Severe outbreak of Pseudomonas syringae pv. syringae on new apricot cultivars in central Italy[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. coryli, the causal agent of bacterial twig dieback of Corylus avellana[END_REF][START_REF] Taghavi | Occurrence of Pseudomonas savastanoi the causal agent of winter jasmine gall in Iran[END_REF][START_REF] Vicente | Identification and discrimination of Pseudomonas syringae isolates from wild cherry in England[END_REF] making it difficult to know if the described pathovar is really different from previously described pathovars. On Prunus spp., where different pathovars cause the disease, cross-infection tests within the genus are lacking. There is also inconsistency in tests of ice nucleation activity (INA) of strains. INA has often been reported as a virulence factor of plant pathogenic P. syringae [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Klement | The effect of cold on development of bacterial canker in apricot trees infected with Pseudomonas syringae pv. syringae[END_REF][START_REF] Sule | The role of ice formation in the infection of sour cherry leaves by Pseudomonas syringae pv. syringae[END_REF][START_REF] Weaver | Interaction of Pseudomonas syringae and freezing in bacterial canker on excised peach twigs[END_REF] and in particular those attacking woody plants because flowering, leaf bud formation and surges of succulent growth can occur during periods with risk of frost. However, tests of ice nucleation activity are missing in many of the descriptions of P. syringae that are pathogenic to woody plants [START_REF] Abbasi | Genetic variability of Iranian strains of Pseudomonas syringae pv. syringae causing bacterial canker disease of stone fruits[END_REF]Balestra et al., 2009c;[START_REF] Gilbert | Genetic analyses of Pseudomonas syringae strains from Belgian fruit orchards reveal genetic variability and host preferences within pathovar syringae, and help identify both races of pathovar morsprunorum[END_REF][START_REF] Ivanovic | Molecular characterization of Pseudomonas syringae isolates from fruit trees and raspberry in Serbia[END_REF][START_REF] Kaluzna | Characterization and genetic diversity of Pseudomonas syringae from stone fruits and hazelnut using repetitive-PCR and MLST[END_REF][START_REF] Kamiunten | Pseudomonas syringae pv. cerasicola pv. nov., the causal agent of bacterial gall of cherry tree[END_REF][START_REF] Mirik | First outbreak and occurrence of citrus blast disease, caused by Pseudomonas syringae pv. syringae, on orange and mandarin trees in Turkey[END_REF][START_REF] Vicente | Identification and discrimination of Pseudomonas syringae isolates from wild cherry in England[END_REF]. Biochemical tests, such as fluorescence on King's medium B, LOPAT (levan production, oxidase, potato rot, presence of arginine dihydrolase and induction of hypersensitivity on tobacco), GATTa (gelatin hydrolysis, aesculin hydrolysis, tyrosinase activity, and tartaric acid production), use of different carbohydrates as sole carbon sources, induction of lesions on detached plant organs, phytohormon production, resistance to copper compounds and antibiotics were among the most utilized for the characterization of strains (Table 4.4). While the identification of specific pathovars is the most common means for reporting new diseases, in some cases authors were reticent. Of the 55 outbreaks reported since 2000 (Table 4.1), 46 associated the causal agents to specific P. syringae pathovars, while only few reports described P. syringae "in sensu lato"

Advances in Agronomy, First Edition, 2014, 235-295 [START_REF] Bardoux | Le deperissement bacterien du marronnier[END_REF][START_REF] González | Disease of floral buds of kiwifruit in Spain caused by Pseudomonas syringae[END_REF][START_REF] Hall | First report of Pseudomonas syringae on olives (Olea europaea) in South Australia[END_REF][START_REF] Ivanova | First occurrence of apricot blast disease caused by Psеudomonas syringae in the north-eastern part of Bulgaria[END_REF][START_REF] Mahdavian | Isolation of Pseudomonas syringae from hazelnut trees in west part of Mazandaran province[END_REF][START_REF] Ozakatan | Information on peach bacterial canker in Aegean region of Turkey[END_REF]. [START_REF] Strange | Plant disease: a threat to global food security[END_REF] described three categories of methods for minimizing plant disease: (1) exclusion, elimination or reduction of pathogen inoculum, (2) promotion of genetic diversity in the crop and (3) inhibition of pathogen virulence mechanisms. These measures are pertinent to limiting diseases of woody plants caused by P. syringae. In practice, these methods should not be used in exclusion but rather they are combined together through an integrated management approach.

CONTROL OF DISEASES OF WOODY PLANTS CAUSED BY P. SYRINGAE

Exclusion, Elimination, or Reduction of Pathogen Inoculum

In theory, hygiene and quarantine are effective control methods and they are currently being put to test for bacterial canker of kiwifruit. In 2012, P. syringae pv. actinidiae was declared a quarantine pathogen in the southern part of the EPPO region (http://www.eppo.int/QUARANTINE/ recent_additions.htm). Similarly, P. syringae pv. persicae, the causal agent of bacterial dieback of peach, is another EPPO quarantine pathogen (OEPP/ [START_REF] Eppo | Pseudomonas syringae pv. persicae[END_REF]. Whether the quarantine regulation applied to a specific pathovar can be effective in controlling the introduction of the pathogen into new areas is a matter of debate. In some cases, the pathogen can be latently present in plant tissues for long periods of time without causing diseases as those reported from Prunus spp. [START_REF] Dowler | Transmission of Pseudomonas syringae in peach trees by bud propagation[END_REF][START_REF] Lyskanowska | Bacterial canker of sweet cherry (Prunus avium) in Poland. I. Symptoms, disease development and economic importance[END_REF][START_REF] Mansvelt | Bacterial blister bark and blight of fruit spurs of apple in south Africa caused by Pseudomonas syringae pv. syringae[END_REF]. The development of early detection methods should be the first step to avoid the introduction of latently infected nursery materials to a given area. Several detection methods have been developed with the aim of early detection of P. syringae from asymptomatic plant parts [START_REF] Bertolini | Highly sensitive detection of Pseudomonas savastanoi pv. savastanoi in asymptomatic olive plants by nested-PCR in a single closed tube[END_REF][START_REF] Biondi | Pseudomonas syringae pv. actinidiae detection in kiwifruit plant tissue and bleeding sap[END_REF][START_REF] Gallelli | Detection of Pseudomonas syringae pv. actinidiae, causal agent of bacterial canker of kiwifruit, from symptomless fruits, and twigs, and from pollen[END_REF]. However, the limit of such methods is based on the fact that they can detect only a narrow range of the diversity of the P. syringae population, usually targeting the so-called pathovar level. Only detection methods that are able to identify a broader P. syringae diversity can be effective in order to promptly detect the emerging pathogens from asymptomatic propagation materials, given the high phenotypic and genetic diversity of this pathogen.

Advances in Agronomy, First Edition, 2014, 235-295 Freedom from pathogens in planting material is not a static event and requires constant monitoring and maintenance during all stages of production, storage, and distribution [START_REF] Janse | Possibilities of avoidance and control of bacterial plant diseases when using pathogen-tested ( certified ) or -treated planting material[END_REF]. Hence, a clear understanding of the causal agent of a given disease might be a good starting point to develop sensitive and effective detection methods from asymptomatic propagation materials. Besides propagation materials, the pathogen can spread for long distance also through migrating birds, insects (honey bees), wind-driven slime and undetected infections on wild hosts as those reported for the quarantine pathogen Erwinia amylovora, which led to a complete failure of the eradication campaign of fire blight disease [START_REF] Calzolari | Fire blight: prevention and control in the Emilia-Romagna region[END_REF][START_REF] Vanneste | The Disease and its Causative Agent, Erwinia amylovora[END_REF]. There are several examples in the literature on the reintroduction of an eradicated bacterial disease of woody plants that clearly indicate the difficulty of effective application of quarantine measures. Citrus canker, caused by Xanthomonas axonopodis pv. citri on citrus, in Florida [START_REF] Graham | Research perspectives on eradication of citrus bacterial diseases in Florida[END_REF][START_REF] Schubert | Bacterial citrus canker[END_REF][START_REF] Schubert | Meeting the challenge of eradicating citrus canker in Florida again[END_REF] and fire blight of pome fruits, caused by E. amylovora, in many countries [START_REF] Calzolari | Fire blight: prevention and control in the Emilia-Romagna region[END_REF][START_REF] Vanneste | The Disease and its Causative Agent, Erwinia amylovora[END_REF] are examples. Overall, a complete eradication of plants is rarely accomplished and often the common practice in the field is to eliminate only heavily damaged plants that are no longer productive. Current epidemics of kiwifruit bacterial canker fully reflects this scenario in which no reports on plant eradication exist, except those reported from some areas of Spain [START_REF] Abelleira | First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Spain[END_REF]. Furthermore, an accurate definition of the pathovar responsible for the disease is essential for quarantine. As mentioned earlier, it is possible that these definitions are too narrow at present, thereby limiting the scope of quarantine actions to a range of strains that is narrower than the full diversity truely responsible for disease.

The only way to reduce P. syringae pathogen inoculum is effective cultural practices [START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF][START_REF] Young | Olive knot and its pathogens[END_REF][START_REF] Young | Pseudomonas syringae pv. actinidiae in New Zealand[END_REF]. Treatments of propagative materials in nurseries with bactericides might be an effective solution but no efficient product is commercially available (see below). In fields, infected plants or plant parts may be either completely uprooted or pruned and burned. The nature of P. syringae, in that it lives, multiplies and overwinters on plant surfaces, makes its management extremely difficult compared to soil pathogens, for example. The reduction of inoculum of the latter is often successful through crop rotation and plowing [START_REF] Summerell | Factors influencing survival of Pyrenophora tritici repentis-stubble management[END_REF], soil solarization [START_REF] Katan | Solar heating (solarization) of soil for control of soilborne pests[END_REF], the addition of amendments [START_REF] Lazarovits | Management of soilborne plant pathogens with organic soil amendments: a disease control strategy salvaged from the past[END_REF], and in some instances, by flooding [START_REF] Thurston | Plant-disease management-practices of traditional farmers[END_REF].

Overall, chemical control has been exclusively used for decades in the plant disease management. However, only a few effective and economical Advances in Agronomy, First Edition, 2014, 235-295 bactericides have been developed to control bacterial pathogens. Plant pathogenic bacteria have been more recalcitrant to chemical treatments than their fungal counterparts [START_REF] Jones | Considerations for using bacteriophages for plant disease control[END_REF]. Unlike several products available for the control of phytopathogenic fungi [START_REF] Oerke | Crop losses to pests[END_REF] (many of them systemic), only a limited number of products is commercially available for the control of phytopathogenic P. syringae [START_REF] Agrios | Plant Pathology[END_REF]. The use of antibiotics is strictly forbidden in many countries including those in the European Union [START_REF] Casewell | The European ban on growth-promoting antibiotics and emerging consequences for human and animal health[END_REF], because of their implication for human health and the risk of resistance that the pathogen develops under selective pressure [START_REF] Khachatourians | Agricultural use of antibiotics and the evolution and transfer of antibiotic-resistant bacteria[END_REF][START_REF] Lipsitch | Antibiotics in agriculture: when is it time to close the barn door[END_REF]. Growers have to settle for only few commercially available chemicals. Among them, copper compounds are the standard bactericides, almost exclusively used, for the control of bacterial diseases [START_REF] Agrios | Plant Pathology[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. Although these compounds often give satisfactory results on herbaceous plants, where P. syringae does not cause systemic disease, the success is limited on woody plants because they do not penetrate inside plant tissues to where the pathogen has invaded the vascular tissues [START_REF] Alvarez | Integrated approaches for detection of plant pathogenic bacteria and diagnosis of bacterial diseases[END_REF][START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. The only way to have success in controlling vascular pathogens is to intervene at the time of infection, by coinciding with periods when the host is susceptible, when the pathogen is accessible, and when conditions are favorable for disease [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF]. Previously, a predictive system for timing of chemical applications has been reported to improve chemical spray control of P. syringae [START_REF] Jardine | A predictive system for timing chemical applications to control Pseudomonas syringae pv. tomato, causal agent of bacterial speck[END_REF]. The authors used stagewise multiple linear regression techniques to identify meteorological and biological variables useful in predicting P. syringae disease development. However, it is worth noting that different hosts react differently to the same treatment. Stone fruits are examples of this differential reaction where preventive treatments, with copper-based compounds following leaf shedding, are effective to control P. syringae infection of peach and cherry but not of apricot. Knowledge of infection ports is useful for this reason. However, the phytotoxic effect of copper compounds on some species can be incompatible with such timings. For example, treatment during flower bloom is not possible for some species because flowers are highly sensitive to copper compounds [START_REF] Lalancette | Phytotoxicity of copper-based bactericides to peach and nectarine[END_REF]. Copper is one of the most used bactericides in agriculture, leading to the development of copperresistant lines of P. syringae [START_REF] Masami | Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. actinidiae[END_REF][START_REF] Scheck | Copper and streptomycin resistance in strains of Pseudomonas syringae from Pacific Northwest nurseries[END_REF][START_REF] Sundin | Ecological and genetic analysis of copper and streptomycin resistance in Pseudomonas syringae pv. syringae[END_REF]. Whatever the utility of copper, the environmental concerns provoked by its heavy use are leading to increasing restrictions in the European Union [START_REF] Pietrzak | Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia[END_REF].

Advances in Agronomy, First Edition, 2014, 235-295 New directions in chemical control emerged recently to overcome the limitations of the common bactericides. Examples are elicitors such as harpins that activate plant defense and induce resistance, and polysaccharides such as chitosan [START_REF] Dong | Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene[END_REF][START_REF] Reglinski | Short Report on Commercially Available Elicitors, Natural Products and Microbes for Evaluation against Pseudomonas syringae pv. actinidiae[END_REF]. Chitosan has attracted concern because of its strong antimicrobial activity toward a broad spectrum of pathogens, including common plant pathogenic bacteria and fungi. The major advantage of chitosan over conventional chemicals is its biocompatibility and biodegradability [START_REF] Badawy | A biopolymer chitosan and its derivatives as promising antimicrobial agents against plant pathogens and their applications in crop protection[END_REF]. In addition to chitosan, other compounds that have shown in vitro inhibitory effects on P. syringae include terpens [START_REF] Ferrante | Molecular and phenotypic features of Pseudomonas syringae pv. actinidiae isolated during recent epidemics of bacterial canker on yellow kiwifruit (Actinidia chinensis) in central Italy[END_REF] and antimicrobial peptides [START_REF] Cameron | Pseudomonas syringae pv. actinidiae: chemical control, resistance mechanisms and possible alternatives[END_REF]. The latter are reported also to inhibit biofilms [START_REF] De Zoysa | The undiscovered potential of dehydroproline as a fire blight control option[END_REF], commonly formed by P. syringae. However, the use of these compounds has been limited to controlled environments and no information is available for open conditions. Other chemicals used in fields are Acibenzolar-S-methyl (ASM, BTH, Bion or Actigard), an inducer of systemic acquired resistance (SAR) [START_REF] Scortichini | Integrated management of bacterial decline of hazelnut, by using Bion as an activator of systemic acquired resistance (SAR)[END_REF] and prohexadione calcium [START_REF] Costa | Prohexadione-Ca (Apogee): growth regulation and reduced fire blight incidence in pear[END_REF][START_REF] Norelli | Effect of prohexadione-calcium dose level on shoot growth and fire blight in young apple trees[END_REF], a growth regulator that has been tested on several species. While inducers of SAR can be effective under controlled conditions, the host response can be highly variable in the field, raising questions about their potential for disease management. Although SAR inducers may reduce disease to a certain extent in some species such as apple and hazelnut [START_REF] Maxson-Stein | Effect of treating apple trees with acibenzolar-S-methyl on fire blight and expression of pathogenesis-related protein genes[END_REF][START_REF] Scortichini | Integrated management of bacterial decline of hazelnut, by using Bion as an activator of systemic acquired resistance (SAR)[END_REF], in fields they may also have deleterious effects on certain other plant species and/or affect yield [START_REF] Gent | Management of Xanthomonas leaf blight of onion with a plant activator, biological control agents, and copper bactericides[END_REF][START_REF] Romero | Resistance to bacterial spot in bell pepper induced by acibenzolar-S-methyl[END_REF]. Furthermore, it has been reported that plant inducers did not result in any effective disease control in some pathosystems such as citrus canker [START_REF] Graham | Lack of control of citrus canker by induced systemic resistance compounds[END_REF]. Studies carried out in Italy and New Zealand showed that in glasshouse conditions SAR can reduce the disease incidence on young kiwifruit seedlings [START_REF] Vanneste | Reducing susceptibility of kiwifruit plant to Pseudomonas syringae pv. actinidiae by manipulating the plant metabolism using elicitors and hormones. In: A Snapshot of Psa (Pseudomonas syringae pv. actinidiae)[END_REF] although no information is available from the field. Since a large number of similarities have been reported among P. syringae diseases of woody plants (such as bacterial cankers of stone fruit and kiwifruit) and citrus canker (http://www.kvh.org.nz/vdb/document/91507), the effect of SAR on P. syringae disease control might not be effective in natural field conditions. However, in-depth future investigations are needed before making a conclusion.

During the last decades, there is a growing interest in adopting biological control measures. At present, only inundative methods of biological control have been developed for diseases of woody species whereby Advances in Agronomy, First Edition, 2014, 235-295 nonpathogenic microorganisms are applied to foliar or root tissues resulting in disease suppression. Such strategies include the use of nonpathogenic or pathogenically attenuated strains of the pathogen species [START_REF] Frey | Hrpmutants of Pseudomonas solanacearum as potential biocontrol agents of tomato bacterial wilt[END_REF][START_REF] Liu | Biological Control with Tomato Bacterial Spot with hrp-Mutants of Xanthomonas campestris pv[END_REF][START_REF] Hert | Evaluation of Bacteriocins in Xanthomonas perforans for Use in Biological Control of Xanthomonas euvesicatoria[END_REF], saprophytic bacteria [START_REF] Ji | Integrated biological control of bacterial speck and spot of tomato under field conditions using foliar biological control agents and plant growth-promoting rhizobacteria[END_REF], nonpathogenic bacteriocin-producing Agrobacterium radiobacter strains that inhibit closely related pathogenic strains [START_REF] Kerr | Soil microbiological studies on Agrobacterium radiobacter and biological control of crown gall[END_REF][START_REF] Kerr | Biological control of crown gall through bacteriocin production[END_REF], and plant growth-promoting rhizobacteria [START_REF] Ji | Integrated biological control of bacterial speck and spot of tomato under field conditions using foliar biological control agents and plant growth-promoting rhizobacteria[END_REF]. These strategies aim to suppress pathogen populations or induce SAR or a similar response in the plant that reduces the ability of the pathogen to colonize the plant and cause disease. Biological control approaches have been used to control bacterial pathogens of several woody plants such as fire blight diseases of pome fruits [START_REF] Boulé | Isolation and characterization of eight bacteriophages infecting Erwinia amylovora and their potential as biological control agents in British Columbia, Canada[END_REF][START_REF] Vanneste | Role of antibiotic production by Erwinia herbicola Eh252 in biological control of Erwinia amylovora[END_REF], caused by E. amylovora and bacterial spot of peach [START_REF] Biondi | Use of a bacterial antagonist for the biological control of bacterial leaf/fruit spot of stone fruits[END_REF] caused by Xanthomonas arboricola pv. pruni. However, throughout the literature, there is only an example on the biocontrol of P. syringae, which involved in vitro efficacy of aqueous plants extracts [START_REF] Bhardwaj | Potential use of some plant extracts against Pseudomonas syringae pv. syringae[END_REF].

The use of bacteriophages is another form of biological control and has been successful for managing several annual plant diseases [START_REF] Jackson | Bacteriophage prevention and control of harmful plant bacteria[END_REF]. Phages have been under evaluation for controlling several woody plantpathogenic bacteria. Examples are fire blight on apple and pear [START_REF] Schnabel | Isolation and characterization of five Erwinia amylovora bacteriophages and assessment of phage resistance in strains of Erwinia amylovora[END_REF] and bacterial canker and bacterial spot of citrus [START_REF] Balogh | Characterization and Use of Bacteriophages Associated with Citrus Bacterial Pathogens for Disease Control[END_REF][START_REF] Balogh | Control of citrus canker and citrus bacterial spot with bacteriophages[END_REF]. To date, all the successful application of phages concerns foliar pathogens and there are virtually no reports for woody tissues. Only one study has shown a preventative and beneficial effect with phage treatment, on vascular disease system on citrus, caused by X. axonopodis pv. citri [START_REF] Balogh | Control of citrus canker and citrus bacterial spot with bacteriophages[END_REF]. The disease symptoms and location of infection within or on the plant can pose challenges for phage biocontrol. For example, most of the economically important diseases on trees are caused by vascular P. syringae pathogens [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF]. The latter spend some of the disease cycle inside the host plant following infection through plant openings or wounds [START_REF] Kennelly | Pseudomonas syringae diseases of fruit trees: progress toward understanding and control[END_REF][START_REF] Scortichini | Bacterial canker and decline of European hazelnut[END_REF][START_REF] Scortichini | Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen[END_REF]. High numbers of bacteria can accumulate within cankers in the plant and are protected from any control agent applied to the outside of the plant that cannot penetrate to deeper tissues. However, the ability of phage to act as a curative agent of cankers was not directly assessed. In a recent report, use of bacteriophages has been indicated among the biocontrol agents with potential to control or suppress bacterial canker of kiwifruit, caused by P. syringae pv. actinidiae [START_REF] Stewart | Desktop Evaluation on Commercially Available Microbial-Based Products for Control or Suppression of Pseudomonas syringae pv[END_REF]. In addition, there are some ongoing studies on the

Author's personal copy

Advances in Agronomy, First Edition, 2014, 235-295 bacteriophage of this pathogen [START_REF] Qing | Primary study of bacteriophage of Pseudomonas syringae pv. actinidiae[END_REF]. Despite several attempts to use of bacteriophage to control different phytopathogenic bacteria, little is known on the possibility of control of P. syringae pathogens of woody plants.

Enhancing Crop Genetic Diversity

As mentioned above, the diversity of the woody crop can have a marked impact on epidemics as illustrated by the contrasting cases of the cankers of kiwifruit and hazelnut. In the case of bacterial canker of kiwifruit, there has been a call to try to increase the diversity of the crop in an attempt to reduce disease pressure [START_REF] Mccann | Genomic analysis of the kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease[END_REF]. This needs to be done with foresight, in order to not enhance the abundance of disease sensitive plants as in the case of yellow-fleshed kiwifruit, A. chinensis. A thorough knowledge of crop genetic resources and their diversity is a prerequisite for their preservation and further use in breeding programs. The centers of origin and diversification of the most important woody hosts of P. syringae are listed in Table 4.5. Wild genetic resources of most of the woody crops are present in more than one country and they have been domesticated for centuries or even millennia. However, their origins and the natural distribution of their progenitor species are usually matters of debate [START_REF] Frankel | Genetic Resources in Plants, Their Exploration and Conservation[END_REF] mostly for Citrus spp., Prunus spp. and Vitis spp. By contrast, the domestication of kiwifruit has occurred only a century ago and almost all the diversity of the genus Actinidia is present in China [START_REF] Ferguson | Genetic resources of kiwifruit: domestication and breeding[END_REF]. Aside from Prunus spp., almost all woody fruit crop species have Asia as the center of origin and domestication and this occurred several centuries ago. Domestication is reported as the main cause of reduction of genetic diversity in crops relative to their wild progenitors, due to human selection and genetic drift through bottleneck effects [START_REF] Tanksley | Seed banks and molecular maps: unlooked genetic potential from the wild[END_REF].

For woody plant species characterized by a high genetic diversity, spontaneous variation in disease resistance can be selected and used in breeding programs. In Prunus spp., some successful control of P. syringae has been reported using plant germplasm resistant to this pathogen. Example is the rootstock F12-1 used in Oregon, which is found to be quite resistant to the pathogen [START_REF] Moore | Pseudomonas syringae disease and ice nucleation activity[END_REF]. Similarly, some cultivars of sour cherry in Germany were resistant to bacterial canker caused by P. syringae [START_REF] Schmidle | Zur resistaenz von sauerkirschosorten gegen den bakteienbrand Pseudomonas syringae van Hall[END_REF].

Plantation of mixtures of varieties or cultivars versus only one variety within the same field might be useful to improve the efficacy of control methods. Because different plant genotypes present different resistance to pathogen, the overall yield loss in this way may be significantly reduced. An example is rice blast control in China [START_REF] Zhu | Genetic diversity and disease control in rice[END_REF] where a significant Advances in Agronomy, First Edition, 2014, 235-295 limit our understanding of the full host range of P. syringae pathovars and make it difficult to predict the efficiency of intercropping as a means of disease control.

Inhibition of P. syringae Virulence Mechanisms

Exploitation of a pathogen's dependence on certain virulence mechanisms might be useful for their control. Table 4.6 presents a list of P. syringae virulence factors. It is well known that most of the virulence factors are induced by plant signal molecules [START_REF] Ausubel | Areinnate immune signaling pathways in plants and animals conserved?[END_REF][START_REF] Tör | Receptor mediated signalling in plants: molecular patterns and programmes[END_REF]. For example, the Type-Three Secretion System (TTSS) is the system in which bacteria can inject effector (virulence) proteins into the host cells [START_REF] Alfano | Type III secretion system effector proteins: double agents in bacterial disease and plant defense[END_REF]. These proteins, as well as the apparatus for the syringae, are coded by genes located in the exchangeable effector loci (EEL), hrp/hrc and conserved effector loci (CEL) [START_REF] Block | Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys?[END_REF]. Type-III effectors are believed to contribute to pathogenesis in two ways: by eliciting the release of water and/or nutrients from the host cell in the apoplastic space; and by suppressing and/or evading plant host defense responses [START_REF] Block | Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys?[END_REF][START_REF] Tampakaki | Playing the "Harp": evolution of our understanding of hrp/hrc genes[END_REF]. Recent studies have firmly established the concept that the suppression of various plant defenses, including basal defense, genefor-gene resistance, and nonhost resistance (NHR), is a major virulence function of intracellular TTSS effectors [START_REF] Nomura | Suppression of host defense in compatible plant-Pseudomonas syringae interactions[END_REF][START_REF] Tampakaki | Playing the "Harp": evolution of our understanding of hrp/hrc genes[END_REF]. In particular, NHR is the most important form of resistance since it provides immunity to all members of plant species against all pathogens that cause disease to other plant species. Different plant genes have been reported to show NHR against plant pathogens. In arabidopsis, NONHOST1 was the first gene to confer NHR against P. syringae pv. phaseolicola [START_REF] Kang | Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence[END_REF]. In tomato, host resistance to P. syringae disease is conferred by the Pto protein kinase, which acts in concert with the Prf nucleotide-binding lucine-rich repeat protein to recognize the pathogen expressing the TTSS effector genes AvrPto or AvrPtoB [START_REF] Pedley | Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato[END_REF]. In tobacco and tomato, the successful use of a pattern recognition receptor gene, EFR, from Arabidopsis reduced the growth of P. syringae pv. tabaci and pv. tomato, respectively [START_REF] Lacombe | Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance[END_REF]. In tomato, the R gene from pepper, Bs2, has been shown to impart resistance to bacterial pathogen Xanthomonas campestris pv. vesicatoria [START_REF] Tai | Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato[END_REF]. The same pepper gene Bs2 confers resistance to lemon against the bacterial pathogen X. axonopodis pv. citri. In barley, penetration deficient genes (PEN) 1, 2 and 3 provide NHR against the pathogen Blumeria graminis f. sp. hordei at the prehaustorial level [START_REF] Lipka | Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis[END_REF]. In addition, NHR Arabidopsis gene PSS1 confers immunity Advances in Agronomy, First Edition, 2014, 235-295 against Phytopthora sojae and Fusarium virguliformae [START_REF] Sumit | Arabidopsis nonhost resistance gene PSS1 confers immunity against an oomycete and a fungal pathogen but not a bacterial pathogen that cause diseases in soybean[END_REF]. Recognition of pathogen-associated molecular patterns (PAMPs) of nonadapted pathogens by PAMP recognition receptors (PRRs) triggers the PAMP-triggered immunity (PTI) in nonhost species [START_REF] Dangl | Plant pathogens and integrated defence responses to infection[END_REF]. PTI has been demonstrated to play a major role in NHR [START_REF] Schwessinger | News from the frontline: recent insights into PAMPtriggered immunity in plants[END_REF]. Both physical (callose deposition at the infection sites, waxy coating on leaves) and chemical (deposition of various reactive oxygen species such as H 2 O 2 and phenolic compounds at the infection sites) barriers induced by PTI restrict nonadapted pathogens from invading nonhost species [START_REF] Bittel | Microbe-associated molecular patterns (MAMPs) probe plant immunity[END_REF][START_REF] Mittler | Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection[END_REF]. Hence, identification, characterization, and the use of different NHR genes from various plants may be a good strategy to develop P. syringae disease resistant woody crops, through breeding. The virulence of numerous phytopathogenic bacteria has been correlated with their ability to produce exopolysaccharide polymers in planta [START_REF] Denny | Involvement of bacterial polysaccharide in plant pathogenesis[END_REF][START_REF] Kao | Extracellular polysaccharide is required for wildtype virulence of Pseudomonas solanacearum[END_REF][START_REF] Katzen | Xanthomonas campestris pv. campestris gum mutants: effects on xanthan biosynthesis and plant virulence[END_REF]. Studies on the exopolysaccharide molecules produced by P. syringae in planta indicated that alginate was the major exopolysaccharide produced in water-soaked lesions [START_REF] Fett | Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts[END_REF][START_REF] Rudolph | Extracellular polysaccharides as determinants of leaf spot diseases caused by pseudomonads and xanthomonads[END_REF]. Alginate production by P. syringae has been associated with increased epiphytic fitness, resistance to desiccation and toxic molecules, and the induction of water-soaked lesions on infected leaves [START_REF] Fett | Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts[END_REF][START_REF] Yu | Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae[END_REF]. Furthermore, a positive correlation between the virulence of P. syringae and the quantity of alginate produced in planta has been demonstrated [START_REF] Osman | Exopolysaccharides of the phytopathogen Pseudomonas syringae pv. glycinea[END_REF][START_REF] Gross | Demonstration of levan and alginate in bean plants (Phaseolus vulgaris) infected by Pseudomonas syringae pv. phaseolicola[END_REF][START_REF] Yu | Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae[END_REF]. A recent study demonstrated the presence of phase variation in P. syringae where the same clonal line can give rise to two phenotypes, a mucoid and a transparent [START_REF] Bartoli | The Pseudomonas viridiflava phylogroups in the P. syringae species complex are characterized by genetic variability and phenotypic plasticity of pathogenicity-related traits[END_REF]. Only the mucoid phenotype, where the production of exopolysaccharide occurs, is reported to have pectolytic activity and to induce tobacco hypersensitivity. In addition, the two phases of the pathogen can be fixed in vitro and are not revertible. In addition, the disease is caused only by the mucoid phase in planta. Hence, targeting the molecular switch between these different phases could be a means to manipulate the pathogen.

Phytotoxins are products of plant pathogens or of the host-pathogen interaction that directly injure plant cells and influence the course of disease development or symptoms [START_REF] Bender | Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases[END_REF]. Although phytotoxins are not required for pathogenicity in P. syringae, they generally function as factors that enhance aggressiveness of the pathogen leading to increased disease severity. For example, P. syringae phytotoxins can contribute to systemic movement of bacteria in planta [START_REF] Patil | An ultraviolet-induced nontoxigenic mutant of Pseudomonas phaseolicola of altered pathogenicity[END_REF], to lesion size [START_REF] Bender | Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn mutants defective in coronatine production[END_REF][START_REF] Xu | Evaluation of the role of syringomycin in plant pathogenesis by using Tn5 mutants of Pseudomonas syringae pv. syringae defective in syringomycin production[END_REF], and to multiplication of the pathogen in the host [START_REF] Bender | Reduced pathogen fitness of Pseudomonas syringae pv. tomato Tn mutants defective in coronatine production[END_REF][START_REF] Feys | Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen[END_REF][START_REF] Mittal | Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato[END_REF]. In nature, other microorganisms resistant to the toxins produced by P. syringae may exist thereby allowing their use as biocontrol agents, to detoxify the effect of P. syringae produced toxins in plant. An example is the use of a strain of Pantoea dispersa as a biocontrol agent [START_REF] Zhang | The gene for albicidin detoxification from Pantoea dispersa encodes an esterase and attenuates pathogenicity of Xanthomonas albilineans to sugarcane[END_REF] which is resistant to the toxin albicidin produced by Xanthomonas albilineans, the causal agent of sugarcane leaf scald.

THE CASE OF FROST DAMAGE DUE TO ICE NUCLEATION-ACTIVE P. SYRINGAE

In addition to its pathogenicity sensu stricto, P. syringae causes significant crop losses through frost damage. The frost sensitivity of plants is augmented Advances in Agronomy, First Edition, 2014, 235-295 when they harbor large population of INA bacteria [START_REF] Hirano | Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte[END_REF]. The amount of frost damage at a given temperature increases directly with increasing numbers of INA bacteria on that plant [START_REF] Hirano | Population biology and epidemiology of P. syringae[END_REF][START_REF] Lindow | New method of frost control through control of epiphytic ice nucleation-active bacteria[END_REF]. In the presence of INA populations of P. syringae, the freezing point of plant tissue is raised compared to when INA bacteria are absent. Overall, plants can resist temperatures below freezing by supercooling. At temperatures below 0 °C, a process known as ice nucleation can occur whereby a solid particle (dust, bacteria etc.) serves as a catalyst for ice formation. As discussed previously, P. syringae can survive and multiply both as an endophyte and epiphyte, even in association to symptomless plants thereby increasing the risk of frost injury.

Frost injury in association to P. syringae has been reported as a predisposing factor for blossom blight, bud and twig diebacks in numerous woody plants. Blossom blights are reported on kiwifruit (Balestra et al., 2009c;[START_REF] Young | Ice-nucleation on kiwifruit[END_REF]Young, , 1988b)), pear [START_REF] Panagopoulos | Frost injury as a predisposing factor in blossom blight of pear caused by Pseudomonas syringae van Hall[END_REF], magnolia [START_REF] Goto | A taxonomic study on ice nucleation-active bacteria isolated from gemmisphere of tea (Thea sinensis L.), phyllosphere of vegetables, and flowers of Magnolia denudata[END_REF], pistachio [START_REF] Rostami | Isolation and identification of ice-nucleating -active bacteria and their antagonistic bacteria from pistachio trees in Rafsanjan region[END_REF], and rhododendron (Baca et al., 1987). Similarly, twig dieback has been reported in tea [START_REF] Goto | A taxonomic study on ice nucleation-active bacteria isolated from gemmisphere of tea (Thea sinensis L.), phyllosphere of vegetables, and flowers of Magnolia denudata[END_REF] and coffee [START_REF] Ramos | Seasonal periodicity and distribution of bacterial blight of coffee in Kenya[END_REF]. P. syringae is reported to affect ice nucleation of grapevine buds [START_REF] Luisetti | Pseudomonas syringae pv. syringae as one of the factors affecting the ice nucleation of grapevine buds in controlled conditions[END_REF]. In addition, the predisposition of plants to P. syringae leaf infection was increased in the presence of readily available inoculum, within 20 min of thawing. However, after 30 min, no effect of thawing has been observed in the formation of leaf lesions [START_REF] Sule | The role of ice formation in the infection of sour cherry leaves by Pseudomonas syringae pv. syringae[END_REF].

In contrast to its effect on tender and succulent plant parts, the contribution of P. syringae INA population to frost injury of lignified tissues is limited as demonstrated previously [START_REF] Gross | Distribution, population dynamics, and characteristics of ice nucleation active bacteria in deciduous fruit tree orchards[END_REF]. Indeed, the woody stem tissue of these plants has a source of INA material that by itself can promote ice formation at -2 to -4 °C [START_REF] Andrews | Differential thermal analysis and freezing injury of deacclimating peach and sweet cherry reproductive organs[END_REF][START_REF] Ashworth | Properties of ice nuclei associated with peach trees[END_REF][START_REF] Proebsting | Supercooling young developing fruit and floral buds in deciduous orchards[END_REF]. Freezing and thawing events, irrespective of INA bacteria, have been reported to predispose woody plants to infection by phytopathogenic bacteria in orchards [START_REF] Ferrante | Frost promotes the pathogenicity of Pseudomonas syringae pv. actinidiae in Actinidia chinensis and A. deliciosa plants[END_REF][START_REF] Lamichhane | Epidemiological study of hazelnut bacterial blight in central Italy by using laboratory analysis and geostatistics[END_REF]. In nurseries, frost damage is reported to predispose a large number of woody plants to P. syringae infection (Baca et al., 1987). Moreover, in short-rotation forestry, twig dieback of poplar [START_REF] Ramstedt | Dieback of poplar and willow caused by Pseudomonas syringae in combination with freezing stress[END_REF] willow [START_REF] Nejad | Pathogenic ice-nucleation active bacteria in willows for short rotation forestry[END_REF][START_REF] Ramstedt | Dieback of poplar and willow caused by Pseudomonas syringae in combination with freezing stress[END_REF] and black alder [START_REF] Scortichini | Leaf necrosis and sucker and twig dieback of Alnus glutinosa incited by Pseudomonas syringae pv. syringae[END_REF] has been attributed to P. syringae in combination with freezing stress.

Preventive measures can be applied to reduce the propensity of ice nucleation. Prediction of critical conditions that favor frost damage is the basis to avoid crop losses. More specifically, prediction of INA P. syringae population sizes maybe compared to weather forecasting. Classical Advances in Agronomy, First Edition, 2014, 235-295 methods of preventing frost damage include sprinkler irrigation and heating of orchards (Lindow, 1983a). In addition, bacterial ice nucleation can be inhibited by agents that kill whole cells such as bactericides [START_REF] Kawahara | Identification of a compound in Chamaecyparis taiwanensis inhibiting the ice-nucleating activity of Pseudomonas fluorescens KUIN-1[END_REF][START_REF] Menkissoglu-Spiroudi | Hypervalent iodine compounds as potent antibacterial agents against ice nucleation active (INA) Pseudomonas syringae[END_REF], antibiotics [START_REF] Hirano | Ice nucleation temperature of individual leaves in relation to population sizes of ice nucleation active bacteria and frost injury[END_REF]Lindow, 1983aLindow, , 1983b)), various heavy metal ions in a soluble state [START_REF] Hirano | Ice nucleation temperature of individual leaves in relation to population sizes of ice nucleation active bacteria and frost injury[END_REF]Lindow, 1983aLindow, , 1983b;;[START_REF] Menkissoglu | Chemical form of copper on leaves in relation to the bactericidal activity of cupric hydroxide deposits on leaves[END_REF], surfactants [START_REF] Himelrick | Cryoprotectants influence freezing resistance of grapevine bud and leaf tissue[END_REF], organic solvents [START_REF] Turner | Three separate classes of bacterial ice nucleation structures[END_REF], and phospholipases [START_REF] Govindarajan | Phospholipid requirement for expression of ice nuclei in Pseudomonas syringae and in vitro[END_REF][START_REF] Turner | Components of ice nucleation structures of bacteria[END_REF]. These compounds inactivate the nucleus produced by the INA bacteria. Copper compounds were used successfully to reduce frost injury induced by INA P. syringae (Lindow, 1983b). A combination of copper-streptomycin sprays was also used to control pear blossom blast in California [START_REF] Bethell | Copper-streptomycin sprays control pear blossom blast[END_REF].

Efforts at biological control have been directed almost entirely at frost control using bacterial antagonists to prevent buildup of P. syringae INA populations [START_REF] Lindemann | Competition between ice nucleation-active wild type and ice nucleation-deficient deletion mutant strains of Pseudomonas syringae and P. fluorescens biovar I and biological control of frost injury on strawberry blossoms[END_REF]Lindow, 1983b). [START_REF] Lindow | Isolation of ice nucleation deficient mutants of Pseudomonas syringae and Erwinia herbicola and their transformation with plasmid DNA[END_REF], by using recombinant DNA technology, used an INA positive P. syringae strain from which the gene responsible for ice nucleation had been removed. Other tests for biocontrol of frost damage concerned the use of chemically mutated P. syringae INA -strains and of naturally occurring INA -bacterial antagonists, which reduced significantly the population sizes of naturally occurring INA + P. syringae [START_REF] Lindow | Design and results of field tests of recombinant Ice-Pseudomonas syringae strains[END_REF][START_REF] Lindow | Control of epiphytic ice nucleation-active bacteria for management of plant frost injury[END_REF]. Application of these antagonists prior to budbreak (woody plants) or at seedling (annual plants) allowed the antagonist to obtain a dominant competitive position in the phylloplane. Examples are reduction of frost injury to strawberry [START_REF] Lindemann | Competition between ice nucleation-active wild type and ice nucleation-deficient deletion mutant strains of Pseudomonas syringae and P. fluorescens biovar I and biological control of frost injury on strawberry blossoms[END_REF], almond [START_REF] Lindow | Reduction of frost injury to almond by control of ice nucleation active bacteria[END_REF], and potato (Lindow and Panagopoulous, 1988). The use of bacterial ice nucleation inhibitors appears to offer a "day-before" type of immediate prevention of INA-bacteria-induced frost, which is not provided by bactericides or antagonistic bacteria [START_REF] Lindow | New method of frost control through control of epiphytic ice nucleation-active bacteria[END_REF] and hence is reliant on accurate prediction of frost events. However, frost control was not achieved by using such antagonists or chemical bactericides in field trials on apple and pear in Washington [START_REF] Gross | Ecotypes and pathogenicity of ice nucleation-active Pseudomonas syringae isolated from deciduous fruit tree orchards[END_REF]. It is believed that, in these hosts, there are intrinsic INA molecules within plant tissue independent from the P. syringae INA populations.

CONCLUSIONS AND PERSPECTIVES

Within P. syringae, the designation of the so-called pathovars has complicated the understanding of disease epidemiology and the establishment of management practices. Such pathovar definitions are too narrow at present Advances in Agronomy, First Edition, 2014, 235-295 thereby strongly limiting the objective of quarantine actions to a range of strains that is narrower than the full diversity involved in disease development. Do the pathovar names truly suggest that the strains within a pathovar are specialized to a host exclusive from other pathovars? If so how can we then explain the variability that can be observed among the strains of the same pathovar? Without comparative host range testing, it is difficult to know whether peach is also a host of strains from kiwifruit or if hazelnut is a host of strains from apricot canker or if these are reports of truly novel pathotypes. Such aspects are critical and should be addressed for the management of inoculum reservoirs, breeding for resistance and control targets.

Other criteria for grouping hosts, beyond that of shared sensitivity to P. syringae, might be informative. Groupings based on the availability of ports of entry may provide a clear picture on the gradient of sensitivity to P. syringae infection. To this aim, two major groups of woody plants (deciduous and evergreen) can be classified in different groups. For example, plants with a very high, moderate and low stomatal and lenticellular density on leaves and lignified tissues, respectively. Likewise, on the basis of the time required for suberization of leaf scar followed by leaf fall, a further subgrouping in plants with a high, moderate, and low rate of suberization is needed. Such groupings of woody plants might allow us to investigate whether there is a correlation between the ports of entry and the rate of infection thereby allowing breeders to find further solutions.

Genetic diversity can be deployed at spatial scales down to the level of orchards. In the field, large-scale intensive cultivation of vegetatively propagated clonal plants leads to an increased vulnerability of plants to pathogen attacks. Only the promotion of genetic mixtures within a field can ensure a greater stability of plant resistance in the long term. With this mind, the introduction of either different plant cultivars of the same species or different species within the same field (intercropping) may significantly reduce the risk of severe infection. The cultivation of different landraces of the same species might present some disadvantages such as unsynchronized phenological phases among the genotypes with different flowering, fruiting, and ripening time. However, this technique may be economically advantageous in the long term if it reduces the severity of infections that could otherwise lead to drastic yield losses.

Figure 4 . 1

 41 Figure 4.1 Schematic representation of infection ports of phytopathogenic Pseudomonas syringae. Clockwise from lower left: tissue damage caused by frost, branch breaking due to wind or mechanical damage, lenticels, broken trichomes, stomata, wounds caused by hailstones, leaf scars and wounds caused by pruning.

  Advances in Agronomy, FirstEdition, 2014, 235-295

  Table 4.1). These

	Europe	Belgium	2007	Horse chestnut	NR	Psaes	Bultreys et al. (2008)
		Bulgaria	2004-2005	Firethorn	NR	Pss	Bobev et al. (2008)
			2004-2006	Apricot	85	Ps	Ivanova (2009)
		Czech
	Advances in Agronomy, First Edition, 2014, 235-295

Table 4 .2

 4 Pathogens from the Pseudomonas syringae Complex Reported to be Virulent on Woody Plants

	Organism	Phylogroup a	Disease	Host(s)	Plant Type	Refereces b
	P. syringae pv.
	actinidiae f,h		Bacterial canker	Kiwifruit	Tree	Scortichini et al.
						(2012)
	avellanae f,h		Bacterial canker	European hazelnut	Tree	Scortichini (2002)
	avii f,h		Bacterial canker	Wild cherry	Tree	Menard et al. (2003)
	berberidis g		Bacterial leaf spot	Berberis spp.	Woody shrub	Roberts (1985b)
	lachrymans g		Bacterial blight	White bird of paradise	Tree	Polizzi et al. (2005)
	morsprunorum f,h		Bacterial canker	Stone fruit	Tree	Crosse (1966)
	persicae f,h		Bacterial dieback	Peach	Tree	Young (1988a)
	theae g		Bacterial shoot blight	Tea	Tree	Tomihama et al.
						(2009)
	viburni g		Bacterial blight	Viburnum spp.	Woody shrub	Thornberry and
						Anderson (1931a)
	aceris g		Bacterial leaf spot	Maple	Tree	Ark (1939)
	dysoxyli g		Bacterial leaf diseases	Kohekohe	Tree	Hutchinson (1949)
	papulans g		Blister spot	Apple	Tree	Bedford et al.
						(1988)

Continued

Author's personal copy

Table 4 .2

 4 Pathogens from the Pseudomonas syringae Complex Reported to be Virulent on Woody Plants-cont'd

			Author's personal copy
	Organism	Phylogroup a	Disease	Host(s)	Plant Type	Refereces b

Continued

Author's personal copy P. syringae pv.

Table 4 .2 Pathogens from the Pseudomonas syringae Complex

 4 Reported to be Virulent on Woody Plants-cont'd

Organism Phylogroup a Disease Host(s) Plant Type Refereces b Author's personal copy

	garcae g	4	Bacterial blight	Coffee	Woody shrub	Ramos and Kamidi
						(1981)
	philadelphi g	5	Bacterial blight	Sweet mock-orange	Woody shrub	Roberts (1985a)
	ribicola g	7	Leaf spot and defolia-	Golden currant	Woody shrub	Bohn and Maloit
			tion			(1946)
	P. viridiflava g	7	Blossom blight	Kiwifruit	Tree	Young (1988b)
			Tree apoplaxy	Peach	Tree	Scortichini and
						Morone (1997)
	coryli e,f	ND	Twig dieback and
			canker
		Advances in Agronomy, First Edition, 2014, 235-295

  . Moreover, there are other wild Corylus species native to North American (Corylus americana, Corylus cornuta), European and western Asian countries (Corylus Advances in Agronomy, First Edition, 2014, 235-295 maxima, C. colurna), China (Corylus chinensis, Corylus fargesii, Corylus yunnanensis, Corylus wangii, Corylus tibetica), Japan (Corylus sieboldiana), and Siberia (Corylus heterophylla)

  ). In-depth lists of mango accessions in collections are also available (http://www.ipgri.cgiar.org/germplasm/dbintro.htm). Concerning Citrus spp., they originated in Southeast Asian countries. For Advances in Agronomy, First Edition, 2014, 235-295 example, Key lime (Corylus aurantifolia) and citron (Corylus medica) are native to India while pomelo (C. maxima) is native to Malay Archipelago. Similarly, Mandarin orange (Corylus reticulata) is native to China while trifoliate orange (Corylus trifoliate) is native to Korea and adjacent China. Finger lime (Corylus australasica), Australian round lime (Corylus australis), and desert lime (Citrus glauca) are native to Australia

Table 4 .3

 4 Tests and Number of Strains Used to Describe Novel Pseudomonas syringae Pathovars

Pathovar No. of Strains Used Tests Used for Characterization Host Range and Species Used Original References pv. Designation

				Author's personal copy
		eriobotryae b	a	Takimoto (1931)	Young et al. (1978)
	Advances in Agronomy, First Edition, 2014, 235-295	aceris b garcae b actinidiae aesculi lachrymans b avellanae mori b avii c berberidis b castaneae cerasicola ciccaronei b coryli d morspruno-rum b myricae papulans e persicae b philadelphi photiniae rhaphiolepidis a 1 a a a 3 18 a 9 1 a 4 7 38 1 a 9 57 20 a ribicola b 3 syringae a theae b a ulmi b a daphniphylli a viburni b 1	Biochemical and pathogenicity Biochemical, copper resistance, pathogenicity Biochemmical, serological, bacte-riocin, phage typing, antibiotic resistance, pathogenicity and lesion tests Biochemical tests, DNA-DNA hybridization, rep-PCR, cluster analysis, pathogenicity tests on different Prunus spp. Biochemical and pathogenicity Biochemical and pathogenicity tests Yes (66 species) Kamiunten et al. No Ark (1939) Do Amaral et al. (1956) Takikawa et al. (1989) Takikawa et al. (1989) Young et al. (1978) Young et al. (1978) Durgapal and Singh (1980) No Smith and Bryan Young et al. (1978) Durgapal and Singh (1915) (1980) Yes (12 differ-ent species) Psallidas (1993) Boyer and Lambert Young et al. (1978) Psallidas (1993) No Menard et al. (2003) Menard et al. (2003) No Thornberry and Anderson (1931b) Young et al. (1978) Takanashi and Shimizu (1989) Takanashi and Shimizu (1989) (2000) Kamiunten et al. (2000) Biochemical and pathogenicity tests No Ercolani and Caldarola (1972) Young et al. (1978) Fatty acid analysis, rep-PCR and genomic fingerprinting, 16S Yes (7 different species) Scortichini et al. (2005) (1993) Biocheical and pathogenicity No Wormland (1931) Young et al. (1978) Ogimi and Higuchi (1981) Ogimi and Higuchi (1981) Biochemical, serological and patho-genicity Yes (2 species) Rose (1917) Dhanvantari (1977) Biochemical tests No Prunier et al. (1970) Young et al. (1978) Biochemical, phage typing and pathogenicity tests Yes (plants of 10 different genera) Roberts (1985a) Roberts (1985a) Goto (1983a) Goto (1983a) Ogimi et al. (1992) Ogimi et al. (1992) Biochemical and pathogenicity No Bohn and Maloit (1946) Young et al. (1978) Van Hall (1902) Young (1992) Scortichini et al. Hori (1915) Young et al. (1978) (2005) Sutic and Tesic (1958) Young et al. (1978) rDNA, hrpL gene, pathogenic-Ogimi et al. (1990) Ogimi et al. (1990) Anderson (1931a) ity test Biochemical and pathogenicity No Thornberry and Young et al. (1978)
		dysoxyli b	NA	Hutchinson (1949)	Young et al. (1978)
		dendropanacis a	Ogimi et al. (1988b) Ogimi et al. (1988b)

a Published in different language than English and in local journal, NA: not available. b Pathogen, originally described as a novel species, not included in the approved list, successively translated to pathovar without any description. c In pathogenicity tests the strains caused symptoms also on sweet cherry. d In host range test the strains caused mild symptoms also on some other hosts. e In host range test the strains caused symptoms also on peach.

Table 4 .4

 4 Phenotypic and Genetic Diversity Observed among Strains of Pseudomonas syringae Pathovars Pathogenic on Woody Plants

			No. of
	Pathogen(s) Isolated Host	Strains Used Analysis	Haplotypes References
	Genetic diversity
	Pss	Stone fruits	91	ERIC PCR	11	Little et al. (1998)
	Psa	Kiwifruit	44	MLST	4	Chapman et al. (2012)
	Pss	Stone fruit and almond	78	ERIC, REP, BOXA1R, IS50	9	Abbasi et al. (2012)
	Pss, Psm	Stone fruit and hazelnut	33	MLST	5,3	Kaluzna et al. (2010)
	Pss	Pome and stone fruits	280	BOX PCR	4	Gilbert et al. (2009)
	Pss	Cherry and plum	87	rep-PCR	10	Vicente and Roberts (2007)
	Pss	Pome and stone fruits	101	rep-PCR	17	Scortichini et al. (2003)
	Pss	Pear	90	BOX PCR	4	Natalini et al. (2006)
	Psm1	Cherry and plum	19	Phage typing	6	Crosse and Garrett (1970)
	Phenotypic diversity			Phenotypic patterns
	Pss	Apple	60	F, LOPAT, GATTa, INA,	16	Mansvelt and Hattingh
				syringomycin		(1986)
	Pss	Mixed hosts		LOPAT, syringomycin, other		Young (1991)
				biochemical tests
	Psa	Kiwifruit	46	F, LOPAT, INA, syringomycin	3	Vanneste et al. (2013)
				production, resistance to
				streptomycin and copper
	Psav	Olive	26	F, LOPAT	2	Marchi et al. (2005)
	Psav	Myrtle	34	Pathogenicity	4	Cinelli et al. (2013b)
	Pss	Pear	90	F, INA, LOPAT, GATTa, viru-	4	Natalini et al. (2006)
				lence tests on lemon fruits,
				pear and lilac leaves
	Pss	Pome and stone fruits	70	F, LOPAT, GATTa, virulence tests 3	Gilbert et al. (2010)
	Pss	Cherry and plum	54	Pathogenicity	4	Vicente et al. (2004)

Note: Pss, Pseudomonas syringae pv. syringae; Psav, P. savastanoi; Pssav, P. savastanoi pv. savastanoi; Psm1, P. syringae pv. morsprunorum race 1; Psa, P. syringae pv. actinidiae; Pav, Pseudomonas avellanae; F, fluorecence on KB, LOPAT, levan, oxidase, potato rot, arginine dihydrolase and tobacco hypersensitivity, respectively; GATTa, Gelatin hydrolysis, aesculin hydrolysis, tyrosinase activity and tartaric acid utilization, respectively; INA, ice nucleation activity.

Table 4 .6

 4 Virulence Factor of Pseudomonas syringae Pathogen of Woody Plants

	Virulence Factor	Pathogen	References
	Functional T3SS	All	Cunnac et al. (2009), Jin et al.
			(2003)
	Ice nucleation activity Pss	Klement et al. (1984), Sule and
			Seemuller (1987), Weaver
			(1978)
	Exopolysaccarides	All	Corsaro et al. (2001), Denny
			(1995), Yu et al. (1999)
	Coronatin	Psa; Psm	Bender et al. (1999), Gross (1991),
			Han et al. (2003), Liang and
			Jones (1995)
	Mangotoxin	Pss, Pav	Arrebola et al. (2003), Carrión
			et al. (2013)
	Persicomycin	Psp	Barzic and Guittet (1996)
	Phaseolotoxin	Psa	Bender et al. (1999), Gross (1991)
	Tabtoxin	Psg	Bender et al. (1999), Gross (1991),
			Mitchell (1984)
	Tagetotoxin	Pst	Mitchell and Hart (1983)
	Syringomycin	Pss	Bender et al. (1999), Gross (1991)
	Yersiniabactin	Psm	Bender et al. (1999), Kaluzna
			et al. (2010)
	Phytohormones	Pss, Psc, Psac, Psmy,	Bultreys et al. (2008), Glickmann
		Psph, Psav, Pa,	et al. (1998), MacDonald et al.
		Psr, Psac	(1986), Young (2004)

Note: T3SS, Effectors and type-three secretion system; Pss, Pseudomonas syringae pv. syringae; Psc, P. syringae pv. ciccaronei; Psa, P. syringae pv. actiidiae; Psm, P. syringae pv. morsprunorum; Psp, P. syringae pv. persicae; Pav, P. syringae pv. avellanae; Psav, P. savastanoi pathovars; Psg, P. syringae pv. garcae; Pst, P. syringae pv. tagetis; Psmy, P. syringae pv. myricae; Psph, P. syringae pv. photinae; Psr, P. syringae pv. ribicola; Psac, P. syringae pv. aceris; Pa, P. amygdali.

Author's personal copy

Advances in Agronomy, First

Edition, 2014, 235-295

Advances in Agronomy, FirstEdition, 2014, 235-295

ACKNOWLEDGMENTS

The authors wish to thank Dr Enrico Scarici of the University of Tuscia, Viterbo for providing us a hand drawing of P. syringae entry ports of an imaginary tree. Many thanks to Drs Claudia Bartoli and Odile Berge for their constructive suggestions during the preparation of the manuscript.

Advances in Agronomy, First Edition, 2014, 235-295

reduction of the disease has been observed through the interspaced cultivation of two rice cultivars, one resistant and the another susceptible to rice blast disease. Even more effective results might be obtained through intercropping whereby a mixture of different plant species is grown in close proximity. However, prior to intercropping, it is necessary to know whether two or more crop species that constitute the mixture are susceptible to the same pathogen. To date, the lack of comparative host range tests

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