P Veysset

M Lherm

J P Boussemart

P Natier

Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?

Keywords: efficiency, farm economics, livestock farms, beef sector, surplus account Implications

Surplus accounting is a method for evaluating trends in how a firm's productivity factors (intermediate inputs, capital, land, labour) are performing and how the productivity gains are redistributed between agents in the economy. Here the surplus accounting method was applied on a database of 164 Charolais-area suckler cattle farms running from 1980 to 2015. Over this 36-year periodwith differences per sub-periodthe cumulative productivity surplus (PS) increased at a low rate of +0.17%/year (i.e. cumulative volume of outputs produced increased slightly more than cumulative volume of inputs used). This timid increase in PS is linked to the constant expansion in labour productivity whereas other factor productivities have shrunk. The observable period-wide macrotrends are that commercial farm businesses struggle to protect their revenues, we also observe a slight fall in input prices, land rent and financing costs, and a huge climb in direct support-policy payments. The bulk of the cumulative economic surplus has been captured downstream -64% downstream of the cattle value chain as a drop in prices, and 22% downstream of other value chains (chiefly cereals). It emerges that the productivity gains in beef cattle farming mostly benefit the downstream value chain (packers-processors, distributors and consumers), whereas it is mainly government money backing this drop in prices of agricultural output. Here we see the principal of the 1992 'MacSharry' reform at work, with a transfer from the taxpayer through direct supportpolicy payments through to the consumer via lower prices. The simple fact that farmers' incomes are stagnating is a clear indication that they are net losers in this distribution of productivity gains, despite the improvement in labour factor productivity.

Introduction

Factor (labour and/or capital and/or intermediate inputs) productivity has always been seen as the main driver of economic growth [START_REF] Kendrick | Factor prices, productivity and economic growth[END_REF] and competitiveness [START_REF] Ball | Productivity and international competitiveness of agriculture in the European Union and the United States[END_REF][START_REF] Latruffe | Competitiveness, productivity and efficiency in the agricultural and agri-food sectors[END_REF]. Productivity gains made by agriculture, which outstripped practically every other sector of the French economy over the last six decades, have enabled declining farm production costs and declining farm commodity prices [START_REF] Charroin | Labour productivity and economy in herbivore rearing: concepts, analysis and stakes[END_REF]. Up until the early 1990s, agriculture made substantial productivity gains in both Europe and the United States [START_REF] Ball | Levels of farm sector productivity: an international comparison[END_REF]. French agricultural output swelled 2.2-fold in volume between 1955 and 2010, driven by specialized farms, increased use of inputs, and increased capital intensity (equipment and buildings), while the share of the workingage population in agricultural work collapsed from 31% to 3.4% [START_REF] Charroin | Labour productivity and economy in herbivore rearing: concepts, analysis and stakes[END_REF]. Nevertheless, since the late 1990s, even though labour productivity on commercial farms continues to climb, French agriculture and the wider foodfarming industry have been losing competitiveness [START_REF] Butault | L'agriculture et l'agroalimentaire français à la recherche d'une compétitivité perdue[END_REF], as farmers struggle to hold onto their income and the productivity of all other resource factors (capital, land, intermediate inputs) is asphyxiating. Suckler beef production has counted among the sectors of agriculture most heavily subsidized by support-policy aids since the 1992 Common Agricultural Policy (CAP) reforms (Chatellier et al., 2003). Beef cattle farms in France have been continually restructuring, rebuilding, readapting and improving their labour productivity, and yet beef cattle farmers continue to register less income than practically any other sector of the French agriculture economy with no real signs of improvement on the horizon (Charroin et al., 2012; Veysset et al., 2014a). [START_REF] Veysset | Productivity and technical efficiency of suckler beef production systems: trends for the period 1990 to 2012[END_REF] have demonstrated and analysed the drop in variable-factor productivity for French suckler-cattle farms over 23 years (from 1990 to 2012). The aim of this study is to measure the evolution of the partial and TFP over the past 36 years for these French suckler-cattle farms, and to analyse the distribution between agents in the economy of these productivity gains. The generation and distribution of TFP gains are evaluated here by the surplus accounting method [START_REF] Burlaud | Global productivity surplus accounts[END_REF][START_REF] Boussemart | Generation and distribution of productivity gains in French agriculture. Who are the winners and the losers over the last fifty years?[END_REF].

After presenting the study sample of Charolais suckler beef farms, we start by detailing the methodology choices adopted. We then chart the macrotrends over a 36-year time series , by dividing this long period into three sub-periods (1980-92, 1993-2005 and 2006-15) and accounting for partial factor productivities, productivity surplus (PS) and how this surplus is redistributed between agents in the economy. We go on to discuss the macrotrends observed over three sub-periods.

Material and methods

The scholarship on productivity gain distribution addresses either a whole sector such as agriculture or a specific product sub-sector [START_REF] Christensen | Concepts and measurement of agricultural productivity[END_REF][START_REF] Ball | Agricultural productivity revisited[END_REF][START_REF] Boussemart | Generation and distribution of productivity gains in French agriculture. Who are the winners and the losers over the last fifty years?[END_REF], and either way, it is always entirely reliant on aggregated data from national or regional agriculture-sector accounts. However, the former employment, income and costs Council of France (CERC, 1980) underlines that it is better to work on individual data rather than aggregates, as the surplus calculations are affected by aggregation biases. Data on individual businesses is rarely available, often blurred (statistical secrecy), and already part-aggregated without the technical details on farm businesses' component commodity steams.

Here we adopt a novel approach that breaks from pre-existing studies by analysing the productivity gains of a network of suckler beef farms via a bottom-up approach. Accountancy data for this livestock farm network provides detailed structural, technical and econometric data on each individual farm. The productivity gains and price advantages (PA) of the farm products and factors of production are first calculated for each individual farm and then aggregated up to analyse the longrun trend trajectories of the whole-network data set.

Data from a Charolais suckler beef farms network

In order to conduct studies on the structural, technical and economic evolutions of French beef farms, since the 1970s the French National Institute for Agricultural Research (INRA) set up a Charolais-region farm network for long-term observations [START_REF] Veysset | Productivity and technical efficiency of suckler beef production systems: trends for the period 1990 to 2012[END_REF]. Each farm in the network is sample-surveyed every year. Data is collected on labour, structure, hectarage and land allocation scheme, herd, intermediate inputs, sales, aids and subsidies, investments, and borrowing. The set of technical-economic variables computed from these field surveys are geared to a technical-economic vision of farm management, which features a harmonized calculation on depreciation and depletion for each farm. As productivity gains measure year-onyear variation (see below), we filtered our database for the sub-sample of farms that had been surveyed at least two consecutive years after 1980 (the year marking the timeseries with zero missing data across all farms in our survey network). Our sub-sample thus counts 164 farms between 1980 and 2015, that is, 3127 farm-year observational datapoints over the 36-year series, with a mean of 87 observations per year (the network counts a maximum of 99 farms in 1985 and 1986 and a minimum of 60 farms in 2015). Our sample is relatively stable over the long-term, with a mean farm presence-in-series of 19 years.

These farms are big commercial beef cattle operations (Table 1). Between 1980 and 2015, at near-constant labour units, they have expanded in hectarage (+64%) and herd size (+75%), thus doubling their meat output in the process. Operating capital (excluding land) increased by 46%. The farms in this sample all run a grass-based feed systems with relatively non-intensive main forage area (MFA) management (stocking rate at 1.17 to 1.20 livestock units (LSU)/ha MFA). Demandside pressure (Italian market) has driven deep change in the type of cattle farmed, operating a switch from long grow-out cycles (fattened steers and heifers sold between 30 and 36 months) to young store cattle (weanling cattle sold between 10 and 12 months). These structural and productive system shifts, even coupled with huge increases in aid payments received under successive common agricultural policy (CAP) reforms, only managed to just about protect the income of livestock farmers (Veysset et al., 2014a). Both the structural trends (labour, hectarage, herd size) and economics trends (output, intermediate inputs, capital, income) observed on this INRA-Charolais-network sub-sample are wholly comparable to the trends observed on the commercial beef cattle farms in the Farm Accountancy Data Network (farming type 46 specialist cattle) statistically representative of French farm businesses (Veysset et al., 2015).

Gains in total factor productivity and surplus account Between two fiscal years (year t and year t + 1), the productivity gains measure changes in output volume net of variations in factor volumes (intermediate inputs, capital, land, labour). A variation in the partial productivity of a given factor is readily measurable, by ratioing output to that factor only (the output yield or partial productivity of one hectare of cereal crop, for instance), but this approach fails to coaccount all the factors used to produce output. In contrast, the more exhaustive measure of TFP is a calculation that models the aggregate value of all product (output) variations as a function of the aggregate value of all factor (input) variations. As explained by [START_REF] Christensen | Concepts and measurement of agricultural productivity[END_REF], and used by Ball et al. (1997), the measure of the TFP of the agricultural sector (or of a farm) has to include the intermediate inputs,

Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. (2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

as well as capital and labour. If Y jt and X it are the respective amounts of output j and input i at date-point t, dY j and dX i are their corresponding variations between the two datepoints t and t + 1, α j is the portion of output j in total output produced and β i is the portion of input i in total volume of inputs, then we get:

dTFP TFP t = X J j = 1 α j dY j Y j;t À X I i = 1 β i dX i X i;t dY j = Y j;t + 1 ÀY j;t dX i = X i;t + 1 ÀX i;t ð1Þ
This calculation has to proceed in two steps. The first step is to measure the volume change in each item. If the volumes of each item are unknown, they are computed from the annual mean econometric quantities observed and their specific price indexes [START_REF] Diewert | Index number concepts, measures and decomposition of productivity growth[END_REF]. By investigating in constant price terms, that is, by deflating the value of each income or expenditure by its respective price index, the observed yearon-year variation corresponds to the volume change of the item. Then, the second step is to weight the rate of input and output variation by the 2-year means of their respective shares in total all-output returns.

α j = 1 2 p j;t Y j;t P J j = 1 p j;t Y j;t + p j;t + 1 Y j;t + 1 P J j = 1 p j;t + 1 Y j;t + 1 0 B B B @ 1 C C C A β i = 1 2 w i;t X i;t P I i = 1 w i;t X i;t + w i;t + 1 X i;t + 1 P I i = 1 w i;t + 1 X i;t + 1 0 B B B @ 1 C C C A p j = unit price of productðoutputÞj w i = unit price of factorðinputÞi
The surplus accounts serve to single out how the economic surplus driven by productivity gains is distributed between agents in the economy. For each fiscal year at date t, considering that total value of different outputs J totally covers the value of different inputs I (balanced general profit/loss account; a general equilibrium that corresponds to the assumption of total income entirely dissolved in paying off total factor costs), we arrive at:

X J j = 1 p j;t Y j;t = X I i = 1 w i;t X i;t
Thus, between two periods t and t + 1, the variation in output values will be equal to the variation in input value:

X J j=1 p j;t+1 Y j;t+1 À X J j=1 p j;t Y j;t = X I i=1 w i;t+1 X i;t+1 À X I i=1 w i;t X i;t ð2Þ
After a re-arrangement of equation ( 2), it is easy to show that the period-to-period output and input value variations can be decomposed into volume and price variations.

X J j =1 p j;t dY j À X I i =1 w i;t dX i =À X J j =1 Y j;t +1 dp j + X I i =1 X i;t +1 dw i PS=PA ð3Þ
In equation (3), the left-hand side term becomes the difference, between periods t and t + 1, in volume variations between outputs and inputs at the initial-period price. This value gap tied to volume variations is called PS. Productivity surplus will be positive (between two periods) when output volumes grow faster than input volumes, and negative otherwise. The right-hand side term measures the sum of the Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

PA. For a given agent in the economy, their PA between two periods t and t + 1 equals the price variations weighted by the volumes of period t + 1. An input price increase is considered a PA for the input supplier (who gets paid more), while an output price decrease is considered a PA for the customer (as the output price becomes cheaper). Equation (3) expresses that PS equals sum of PA. This equality explicitly demonstrates that between two periods, a business cannot distribute as payment changes (or PA) more than it can generate from productivity gains. Net-negative PA can be considered as net provisions from stakeholders, and is cumulatable with a netpositive PS, which thus gives the total amount of resources that the beneficiaries of positive PA will share out. If the business registers a drop in productivity (PS < 0), it has to counterbalance by making certain stakeholders pay more for outputs or less for inputsand either way bear the brunt of price disadvantages, as the absolute (real) value of the PS becomes an added amount to finance. Here we can establish a uses/resources-balanced surplus account (Table 2). On aggregate, the price and quantity variations connect to either an 'origin' (resource) or a 'distribution' (use) of the total economic surplus, thus enabling us to analyse all the corresponding transfers (Figure 1) among customers, suppliers of intermediate inputs (feedingstuffs, fertilizers, fuels, services and so on), suppliers of primary factors (labour, land, fixed assets) and government subsidies and taxes (EU, national, regional, etc.).

Working up from equation ( 1), the relative (expressed in % terms) rate of TFP growth can likewise be calculated using the surplus rate by dividing PS by the total value of output (Boussemart et al., 2012).

dTFP TFP t = P J j = 1 p j;t dY j À P I i = 1 w i;t dX i P J j = 1 p j;t Y j;t
In equation ( 3), the volume variations between periods t and t + 1 were weighted by the initial-period prices (Laspeyres-type index) while the price variations were weighted by the final-period volumes (Paasche-type index). We could equally well have chosen a Paasche-type index for the volume variations and a Laspeyres-type index for the price variations. The choice of index used is not, therefore, a neutral choice. To ensure that the final result is not dependent on a random choice of index type, we use the Bennet approach which consists in computing the arithmetic mean of the Laspeyres and Paasche expressions [START_REF] Caves | Multilateral comparisons of output, input, and productivity using superlative index numbers[END_REF]:

X J j = 1 p j;t + p j;t + 1 2 dy j À X I i = 1 w i;t + w i;t + 1 2 dx i = À X J j = 1 y j;t + y j;t + 1 2 dp j + X I i = 1 x i;t + x i;t + 1 2 dw i

Empirical modelling

For each farm in our database of suckler cattle operations, we have the real volumes (quantities) for the following outputs:

• beef live weight produced;

• sheep live weight produced;

• cereal crops produced.

These three outputs together account for 90% to 95% of the gross value excluding aids of total farm output. With the value and volumes of these outputs for each farm and each year, we were able to compute the year-by-year unit prices of each of these outputs, and directly dissociate the volume and price values for a compact number of inputs farm-by-farm.

The labour factor. For waged labour, the net wages and payroll taxes are the values and the number of wage-earning annual work units (AWU) is taken as the volume. Net farm income, calculated as the balance between the farm's output returns and input expenditures (including social contributions), is considered as the profit made by the farmer, and this net income (or profit) thus corresponds to payment for non-waged labour, the volume of which is given by the number of AWU going unwaged. -PS (if < 0) economic loss tied to a bigger drop in input volumes used over the period than output volumes PS (if > 0) economic gain tied to a bigger rise in output volumes over the period than input volumes used -Y j,t + 1 dp j 1 drop in output tied to the drop in price of commodity j over the period Y j,t + 1 dp j 1 rise in output tied to the rise in price of commodity j over the period X i,t + 1 dw i 2 increase in expenditure tied to the rise in price of input i over the period -X i,t + 1 dw i 2 drop in expenditure tied to the drop in price of input i over the period … …

Total economic surplus

Total economic surplus PS = productivity surplus. The surplus accounts singles out how the economic surplus driven by productivity gains (quantities variations) is distributed between agents in the economy (prices variations). All the origins (Resources) of the balanced account are distributed (Uses).

1 Y j,t + 1 amounts of output j at date-point t + 1, dp j price variations of the output j between the two date-points t and t + 1. 2 X i,t + 1 amounts of input i at date-point t + 1, dw i price variations of the input i between the two date-points t and t + 1.

Veysset, Lherm, Boussemart and Natier

Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

The land factor. The cost of use of land is represented by land rent. To overcome the biases in system of land tenure, we considered that the all utilized agricultural area (UAA) of all the farms was under land-leasing arrangements. We thus applied a mean rental on ownership land. The volume of the 'land' factor is thus the UAA expressed in hectares.

The capital factor and financing costs. The capital addressed here only concerns fixed assets (farm buildings and fixed equipment, land improvements, machinery and equipment) and does not integrate the land and the herd-count. We distinguish two components of the account relating to the capital: (i) the physical capital (equipment, buildings), whose use in the production process causes equipment wear (consumption of fixed capital); this is measured by the depreciation; (ii) the immobilization in the holding of a financial capital provided by a supplier; these debts are remunerated by the interest paid. To respect the principle of the surplus accounts method, which is to assign a PA per partner identified for each entry of the farming accounts, we allocate the financial costs to the suppliers of the borrowed capital (mainly banks), and depreciation to the suppliers of equipment.

The volume (kg) of concentrate feedingstuffs purchased is known. This item accounts for 15% to 20% by value of total intermediate inputs.

As we only have the economic value for the other outputs and inputs, we use their respective prices indices to decompose the volume-price split. The index of producer prices of agricultural products (IPPAP) is designed as a metric of changes in prices paid to farmers (Eurostat, 2017). The annual values of output oilcrops, pigs and poultry for each farm in our farm network sample were deflated by their respective IPPAP.

Given the significance of aids and subsidies as important returns of livestock farm economics, the question arises as to their volume-price split. We worked to the assumption that these aids and subsidies did not change volume as they are broadly decoupled, and so price-effect of variation in subsidization thus corresponds to the observed variation in total price value. This means that we have year-to-year price movement but not year-to-year volume change.

The index of purchase prices of the means of agricultural production (IPPMAP) serves to track and trend the unit prices that farmers pay for goods and services needed for their farming activity (Eurostat, 2017). Just like for the output series, the annual mean values of each expenditureseed, fertilizer and soil amendments, veterinary, pest control products, energy, capital goods, consultancy and overheads of each farm in our network sample were deflated with their own respective annual IPPMAP.

All changes in volumes, prices (all nominal-value prices internalize currency depreciation using the national consumer price index as deflator), PS and PA are calculated at every year t + 1 as the differential with year t for each farm present in-sample at both years t and t + 1. The annual PS and PA results are averaged and then the averages are summed to get the cumulative PS and PA surplus figures, and thus establish the balanced surplus account over the period of study.

The 36-year period was stratified into three sub-periods charting the major CAP reform landmarks and the year these reforms came into full force. The core of the 1992 'MacSharry reforms', which were phased in from 1993, was to cut intervention prices for cereals and beef and compensate farmers through producer subsidies coupled to hectare of land and head of livestock

Results

Partial and total factor productivity and productivity surplus Over the 36-year period under study, mean farm area (UAA) has increased at a mean rate of 1.69% per year and volume of farm output has increased at a mean pace of 2.03% per year, whereas total labour input has remained practically unchanged, and is even tending to drop (-0.05%/year). We thus have contrasted trajectories of the partial factor productivity figures (Table 3). Labour-factor productivity has climbed steadily over the 36 years, whereas land-factor productivity has been in decline since 1992 (with an extensification of fodder area while cereal crop yields have stagnated). In global trend terms, there has been a net decline in the productivity growth of intermediate inputs. Heavy investment in buildings and equipment over the 1990s meant that farm equipment productivity plummeted between 1993 and 2005. In global trend terms, after a phase of growth from 1980-92 (+0.51%/year), TFP (or the cumulative trend in PS) shrank by 0.42%/year from 1993 to 2005 and 0.16%/year since 2006, that is, a net decline in TFP of 0.07%/year between 1993 and 2015 (Figure 2).

Surplus accounting: origin (resources) and distribution (use) of the cumulative economic surplus Over the end-to-end 36-year period, the cumulative surplus of TFP and absolute (real) value of negative PA, in constanteuro values and per-farm mean, comes to a total economic surplus of €84 584, that is, €2350/year (Table 4). This economic surplus essentially comes from government (69%) via aid support to livestock farmers, with only 14% coming from productivity gains. In global trend terms, over the period, there has been an observable drop in intermediate input prices and land leasing prices (which account for 3% and 5%, respectively, of economic surplus). Despite some productivity gains (PS > 0, Table 5) and all the government subsidies, farmer income has not moved and remains flat. 86% of these resources is captured downstream, as a drop in commodity prices. The downstream beef cattle value chain captures 64% of the resources generated. Farmers' payroll taxes have increased despite stagnating income capturing 4% of resources, cost of waged labour has only slightly increased, and suppliers of fixed assets and equipment have captured 4% of the surplus.

1980-92 period: gains in productivity and strong drops in commodity prices. Over this 13-year period, the origin of the total economic resources (€56 790, i.e. €4368/year, Table 6) was shared between gains TFP (24%), a drop in intermediate input prices (25%), and an increase in government money (29%). A 94% majority of these resources has been captured downstream -65% downstream of the cattle value chain as a drop in prices. The drop in intermediate input prices was essentially driven by the drop in petrol prices, which led to a drop in the cost of fertilizers, and by the drop in cost of animal feedingstuffs, which is itself linked to the drop in cereal prices. The rise in subsidizationand thus in government moneyin the origin of the economic surplus is linked to the introduction, in 1980, of the suckler cow premium as a mechanism to stop suckler beef herds being converted to more lucrative dairy cow herds, at a time when the EU already registered a milk surplus. In 1987, the special premium for male animal was also brought in to encourage fattening of bulls and steers. The drop in intermediate input prices, the technical efforts of the farmers to limit the volume of inputs used (PS >0, Table 5), and the stronger government subsidization support still failed to offset the PA captured downstream, and farmer incomes fell slightly. This drop in payment for the farmers' labour accounts for 7% of the resources in the economic surplus generated over this 13-year period. Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 ( 5), 1-11. , DOI : 10.1017/S1751731118002574

1993-2005: direct support-policy payments but declining total factor productivity. This 12-year-period's cumulative economic resources (€47 029, i.e. €3618 per year, Table 7) comes 94% from the increase in direct payments following the introduction of crop support mechanisms (cereals, highprotein oilseed and set-aside), the additional premium for extensive cattle systems (capped under a stocking-rate-perhectare threshold), the significant revaluation of existing scheme payments (suckler cow and male premium), and, later on, the regional farmland development contracts and sustainable farming contracts. The decline in commodity cereal prices, and thus animal feedingstuff prices, continued, while market-side demand shifted towards younger and heavier animals, thus leading to a sharp increase in volume of feedingstuffs. With support policy incentivizing extensive farming systems, livestock farmers decreased their fertilizer Table 5 Detail of the productivity surplus (volume effect): mean in constant-euro value cumulated over the period 1980-2015, and over the three sub-periods (1980-92, 1993-2005 and 2006-15), per Charolais suckler beef farms from the inra-network Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

input volumes, but at the same time investing in buildings and new fodder harvesting-storage-distribution machinery generating extra fuel-use and new needs for contract operations. In global trend terms, volume of inputs increased faster than volume of outputs (Table 5). Government money financed the entire drop in productivity, as well as the continuing drop in commodity prices and the increase in farmer incomes. These government support-policy aids, cumulated with a drop in interest rates, are distributed between the downstream sector supply chains (61%), farmers' income and payroll taxes (21% and 8%, respectively), and the drop in TFP (5%). Note that this period includes the heatwave year 2003, when the hottest summer on record led to a 50%-odd drop in grass growth. The heatwave brought about a tangible drop in quantities produced (livestock sold at lighter weight) and, crucially, an increase in animal feedingstuffs purchased. This climate episode caused a sharp decline in PS (Figure 1) and cancelled out the productivity gains made over the previous 23 years. Even if we exclude the year-2003 figures, cumulative PS over the 1993-2002 remains negative ( -€345). This does not undermine the observation made above: there was effectively a real downward trend in productivity over this period, but the 2003 climate episode accentuated the trend.

2006-15 period: rise in intermediate input prices, drop in government support aids and subsidies. This period has proven the most economically stable of the three, since the annualized mean resources amount to just €1720 per year. Highlighting the period is the rise in producer price for cattle. This price rise is at the origin of 20% of the 10year-period's cumulative economic surplus (Table 8). The cereal price spikes in 2007 and 2012 are at the origin of 30% of the 10-year-period's cumulative economic surplus. The rise in cereal prices, and thus animal feedingstuff prices, explains 50% of the rise in intermediate input prices, but it also prompted livestock farmers to distribute less to their animals. This declining use of purchased animal feedingstuffs, combined with the slowdown of investments in equipment and buildings, and thus a decrease in the use of capital assets, explains why PS swung back into the positive (Table 5), but it also accounts for just 3% of the origin of cumulative resources. The fact that the PS cumulated over this 10-year sub-period inched up into the positive is linked to the fact that the increase in UAA, fixed assets and intermediate inputs used is compensated for by the drop in number of AWU. However, the multi-factor (primarily labour) productivity gain and the rise in cereal crop and cattle outputs were still not enough to compensate for the rise in intermediate input prices and the scaleback of support policy (phase-out of regional farmland development contracts and 'modulation' of payments), all of which converged to decrease farmer income. This drop in payment for the farmers' labour accounts for 28% of surplus-account resources. Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

Discussion

The surplus accounting method, like most methods, is sensitive to the underlying assumptions. Decomposing economic value change into a volume effect and a price effect entails choices between indexes and between assumptions. Here, for instance, we chose to only consider a price effect on change in government subsidization, but as direct payments are allocated on the basis of headage or hectarage, we could equally well have chosen to consider a volume effect represented by change in number of premium-scheme cows or hectares. Calculations were repeated with this new assumption, and although the results were different in value terms, the trends of change were the same.

The bottom-up approach adopted here avoided the biases inherent to using aggregate national indexes that are not specific to a localized sector of activity. Working with real prices and volumes recorded every year for a significant set of items in the profit/loss account of each individual farm enables us to more accurately track and trend the changes in TFP established at domestic sub-sector and/or regional level.

Total factor productivity or labour productivity? The (very timid) productivity gains over this long 36-year time-series period manage to emerge. These gains are not continuous, and they vary significantly between periods. The key highlights are continuous growth in labour productivity, stagnation in farmer income and continuous decline in technical efficiency (productivity of intermediate inputs) of the production systems. These results counter most of the results found in literature. Many studies concluded that small family-farms, at a national level, are less efficient with a lower productivity than largest specialized farms that use improved technologies and economies of scale [START_REF] Gorton | Farm productivity and efficiency in the CEE applicant countries: a synthesis of results[END_REF][START_REF] Paul | Scale economies and efficiency in U.S. agriculture: are traditional farms history?[END_REF][START_REF] Latruffe | Technical and scale efficiency of crop and livestock farms in Poland: does specialization matter?[END_REF][START_REF] Mosheim | Scale economies and inefficiency[END_REF]. However, the ecoefficiency [START_REF] Keating | Eco-efficient agriculture: concepts, challenges, and opportunities[END_REF] of a livestock farm depends not only on its size, but also on its location or system management [START_REF] Soteriades | An approach to holistically assess (dairy) farm eco-efficiency by combining life cycle analysis with data envelopment analysis models and methodologies[END_REF]. We observe capital deepening with a work-for-assets/inputs switch. The upshot is that the only real productivity gains made in beef cattle farming over the past 36 years are labour productivity gains. It is legitimate to question whether this strategy holds relevancy, if it does not benefit the worker, if it completely masks (or even holds back) the expression of technical, genetic and knowledge-capital gains.

The downstream meat value chain captures the governmentfinanced economic surplus The cumulative economic surplus over the 36 years under study comes 69% from government aids and goes 86% to downstream value chains, with 64% captured by the downstream beef value chain. The downstream beef value chain stretches from the first link into market (livestock commodities market, at the slaughterhouse gate) through to the consumer end, including an array of actors in the economy (livestock trader, packers and processors, caterers, distributors, and more). Thus arises the question of how this surplus is distributed throughout the value chain downstream of the farm gate. Down at the very end of the chain, the meat consumer has failed to benefit from the drop in producer prices. On aggregate, over the past 36 years, in constant-euro values, the price of cattle paid to producers slumped by 40%, whereas the price of beef paid by consumers (consumer price index for beef) climbed 20%. The pattern of change in this index thus includes a quality effect, featuring a shift towards a more services-intensive product output (mincing, marketing, packaging, food safety guarantees) [START_REF] Verbeke | European citizen and consumer attitudes and preferences regarding beef and pork[END_REF][START_REF] Font-I-Furnols | Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?[END_REF] with all the allied costs involved, whereas back on the farm, the beef grade cattle have remained practically the same (mostly female cull cows and heifers aged 30 monthsplus). France has a food pricing and profit margins observatory that monitors how prices and margins are generated throughout the farmed food supply chains and on to retail. In its latest report (FranceAgriMer, 2016), the observatory notes that beef packers and processors are still registering paperthin pre-tax profits (0.4% to 2% of the value produced). This can be explained by the difficulties in improving raw material-to-final product conversion yields, difficulties compounded by the fact that yield gains cannot offset the tougher new environmental and food safety standards. The drop in producer price for cattle has thus been diluted through the downstream supply chain.

Government has been the main driver behind of these changes. Prior to the 1992 MacSharry reforms, the indirect support-policy payments including in commodity selling prices did not prevent productivity gains generated by farmers getting transferred downstream the beef cattle value chain. Then, over the period during which policy aids were coupled to headage and hectarage, livestock farmers were able to benefit from upvaluation through the heavy aid-scheme premiums whereas the downstream supply chain continued to profit from declining prices. Lastly, since 2006, livestock farmers have not benefited from the (partial) decoupling and modulation of support payments. By modelling, [START_REF] Ash | Boosting the productivity and profitability of northern Australian beef enterprises: exploring innovation options using simulation modelling and systems analysis[END_REF] observed a positive impact of the factor productivity on beef farm profitability, but, in other hand, CAP subsidies could affect negatively the farm productivity [START_REF] Rizov | CAP subsidies and productivity of the EU farm[END_REF]. [START_REF] Bojnec | Farm size, agricultural subsidies and farm performance in Slovenia[END_REF] observed that mediumsize farms in Slovenia are the less profitable: large farms are technically efficient and small farms are highly subsidized and more allocatively efficient. Ultimately, French beef farmers' income is not correlated to farmer productivity gains, and government subsidies do not always benefit the professional branch they are partly intended for. Government subsidies to farming are designed to support a number of objectives (to support farming income, to support pricecompetitive agrifood supply chains, to curb food price inflation, etc.), yet in the case of the beef sector, producers have captured practically none of this support.

The constant increase in the farms and herds' size, encouraged by the non-capped subsidies, led to an increase in inputs and equipment used per unit of output. Thus, we Productivity gains in beef cattle farming Comment citer ce document : Veysset, P., Lherm, M., Boussemart, J. P., Natier, P. ( 2019). Generation and distribution of productivity gains in beef cattle farming: Who are the winners and losers between 1980 and 2015?.

Animal, 13 (5), 1-11. , DOI : 10.1017/S1751731118002574

observed an increase in the use of fossil-fuel energy and in greenhouse gas (GHG) emissions per kilogram live weight produced, and a negative correlation between the size of these Charolais suckler-cattle farms and these environmental performances (Veysset et al., 2014b). It also appeared that, through better technical performances and lower use of inputs, the less-GHG-emitting farms (that are smaller than the most-GHG-emitting farms) generated higher income per worker while consuming less fossil energy. The enlargement strategy runs counter to the clean energy challenge and the project of agroecology transition for green growth.

Conclusion

Analysis of how the Charolais beef cattle sector's productive resources have been redistributed over the course of the past 36 years finds that the sector's downstream customers have come out as the main winners via declining prices,. These declining prices have essentially been subsidized by government via CAP payments and other support-policy aids. There are TFP gains, but they tend to be modest, fluctuating between periods but tending to a downward curve, whereas the labour productivity of the livestock farmers shows constant steady growth. The gains in labour productivity made by the farmers mask the steady decline in all other factor productivity (land, intermediate inputs and equipment) leaving the beef cattle production systems increasingly inputs-and capital-dependent. The simple fact that farmers struggle to protect their income is a clear indication that they have been losers in this distribution of productivity gains. The strategy of continually re-adapting farm structure (up-scaling size and down-sizing labour, development of associative organization structures, investment in new infrastructure and new technologies) and farm systems (standardization of farmed animal output and feed management practices) to meet market requirements (basic commodity raw material) has not proven an entirely winning strategy for the farmers themselves. These macrotrends manifestly mask relatively significant interfarm and year-on-year variabilities that warrant further investigation in future studies. Livestock is more than just a sector of the economy producing market goodsit also plays a pivotal role in territorial land occupancy and rural development in less-favoured pasture-based zones where few if any viable alternatives exist. To stem the decline in value-added created by livestock farming and improve livestock farmer profits (without redistributing their share down to other agents in the economy), one solution could be to more actively couple farm outputs to territory, via localized bioregional farming practices (fattening livestock locally) and quality labels. In a context of beef consumption declining, consumers express preference and willingness to pay for country-of-origin-labelled beef and food safety enhancements. The challenge is for livestock farmers to capture a share of the fast-growing services value component of food consumption, for example, through new marketing chains or cooperatives. Public policies, and especially the laws, could have a role by inciting the bovine sector stakeholders to establish fair agreements.

Figure 1

 1 Figure 1 Distribution of the productivity gains and price advantages. Balanced economic surplus account.

Figure 2

 2 Figure 2 Productivity surplus as cumulative 1980-2015 figure and annual growth rate per sub-period for the Charolais suckler beef farms from the inra-network.

Table 1

 1 Main structural and economic characteristics of the sample of Charolais suckler beef farms from the inra-network for theyears 1980, 1992,

	2005 and 2015
		1980	1992	2005	2015
		91 farms	94 farms	84 farms	60 farms
		Mean (RSD) 1	Mean (RSD) 1	Mean (RSD) 1	Mean (RDS) 1
	Utilized agricultural area (UAA) (ha)	110 (40)	122 (44)	153 (44)	181 (41)
	Non-waged workers (AWU) (n)	1.5 (40)	1.8 (36)	1.7 (40)	1.6 (38)
	Waged workers (AWU) (n)	0.5 (120)	0.2 (205)	0.3 (147)	0.3 (154)
	Livestock units (LSU) (n)	9 7 ( 41)	127 (46)	151 (47)	170 (43)
	Cows (n)	4 7 ( 33)	69 (43)	85 (44)	100 (48)
	Stocking rate (LSU/ha main fodder area)	1.17 (24)	1.33 (18)	1.20 (14)	1.20 (18)
	Operating capital (k€ 2015)	333 (39)	347 (44)	434 (47)	485 (41)
	Beef production (kg live weight)	25 516 (40)	38 099 (49)	48 085 (53)	54 325 (47)
	Aids/subsidies received (€ 2015)	6266 (37)	24 920 (52)	72 402 (40)	71 249 (33)
	Profit (or net farm income) 2 (€ 2015)	43 312 (63)	39 734 (57)	48 025 (61)	35 547 (87)

AWU = annual work units. 1 RSD = Relative standard deviation = standard deviation mean % . 2 Profit (or net farm income) = gross farm product (including aids and subsidies)intermediate inputslabour costs (wages, payroll taxes and social contributions) land rent -financial costs.

Table 2

 2 Balanced economic surplus account of a holding

	Uses

Table 3

 3 Breakdown of partial and total factor productivity, average annual growth rate of the Charolais suckler beef farms from the inra-network, in %

	Period and sub-periods	1980-2015	1980-92	1993-2005	2006-15
	Labour	2.03	2.71	1.05	2.53
	Land	0.29	1.95	-0.26	-0.12
	Intermediate inputs	-0.37	-0.14	-1.40	0.13
	Fixed asset (farm equipment)	-0.85	1.10	-3.19	1.02
	Total factor productivity growth	0.17	0.51	-0.42	-0.16

Table 4

 4 Cumulative surplus account figures for the 1980-2015 period: mean distribution/uses and origin/resources in constant-euro values and % share, per Charolais suckler beef farms from the inra-network

	Distribution or uses	€uros	%	Origin or resources	€uros	%
	Downstream-cattle	54 323	64	Productivity surplus	11 544	14
	Downstream-other output	18 212	22	Suppliers of intermediate inputs	2386	3
	Farmer payroll taxes	3770	4	Landowners	4620	5
	Waged labour	4478	5	Banks (financing costs)	8002	9
	Materials and buildings	3605	4	Government	58 032	69
	Farmer	196	0
	Total-uses	84 584	100	Total-resources	84 584	100

Table 6

 6 Cumulative surplus account figures for the 1980-92 period: mean distribution/uses and origin/resources in constant-euro values and % share, per Charolais suckler beef farms from the inra-network

			1980-2015	1980-92	1993-2005		2006-15
	Total agricultural product		82 587	50 825	20 565		11 197
	Beef cattle product		69 666	39 039	21 791		8835
	Other product		12 921	11 786	-1226		2362
	Intermediate inputs		50 787	26 138	14 522		10 127
	Mineral fertilizers		2626	5059	-2457		25
	Other crop inputs		8967	4373	299		4295
	Purchased feedstuff		8703	7519	5203		-4020
	Veterinary		4064	2292	2016		-245
	Other livestock inputs		2823	1467	1490		-134
	Fuel		5100	225	2088		2788
	Equipment, building maintenance		6548	2519	2282		1747
	Contractor works		5664	1191	2188		2285
	Other intermediate inputs		6292	1493	1413		3386
	Equipment and building depreciation		16 823	5345	10 463		1104
	Land		9161	3266	3309		2586
	Total workforce		-5727	2648	-5319		-3056
	Productivity surplus		11 544	13 428	-2409		526
	Distribution or uses	€uros	%	Origin or resources		€uros	%
	Downstream-cattle	37 113	65	Productivity surplus		13 428	24
	Downstream-other output	16 480	29	Suppliers of intermediate inputs	14 251	25
	Farmer payroll taxes	1572	3	Landowners		5329	9
	Waged labour	1189	2	Banks (financing costs)		2871	5
	Materials and buildings	436	1	Government		16 688	29
				Farmers		4223	7
	Total-uses	56 790	100	Total-resources		56 790	100

Table 7

 7 Cumulative surplus account figures for the 1993-2005 period: mean distribution/uses and origin/resources in constant-euro values and % share, per Charolais suckler beef farms from the inra-network

	Distribution or uses	€uros	%	Origin or resources	€uros	%
	Downstream-cattle	20 588	46	Banks (financing costs)	2938	6
	Downstream-other output	6861	15	Government	44 091	94
	Suppliers of intermediate inputs	972	2
	Farmer payroll taxes	3430	8
	Waged labour	2015	5
	Landowners	379	1
	Materials and buildings	1218	3
	Farmer	9157	21
	Productivity surplus	2409	5
	Total-uses	47 029	100	Total-resources	47 029	100

Table 8

 8 Cumulative surplus account figures for the 2006-15 period: mean distribution/uses and origin/resources in constant-euro values and % share, per Charolais suckler beef farms from the inra-network

	Distribution or uses	€uros	%	Origin or resources	€uros	%
	Suppliers of intermediate inputs	10 893	63	Productivity surplus	526	3
	Waged labour	1275	7	Downstream-cattle	3378	20
	Landowners	330	2	Downstream-other output	5129	30
	Materials and buildings	1951	11	Banks (financing costs)	2193	13
	Government	2747	16	Farmer payroll taxes	1232	7
				Farmer	4738	28
	Total-uses	17 196	100	Total-resources	17 196	100

Acknowledgements

The authors thank the farmers who kindly provided the yearly data from their registers to complete this study.

Declaration of interest

The authors declare no competiting interests regarding this publication.

Ethics statement

Section is irrelevant for this study.

Software and data repository resources

Data used are individual economic data protected by statistical confidentiality. They were not deposited in an official repository.


Abdellah Lakehal
email: abdellah.lakehal@umu.se

Catherine Bellini

Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions

Keywords: ABA, abscisic acid, ABCB19, ATP BINDING CASSETTE TYPE B 19, ACC, 1aminocyclopropane-1-carboxylic acid, AR, adventitious root, ARI, adventitious root initiation, ARF, AUXIN RESPONSE FACTOR, ASA1, ANTHRANILATE SYNTHASE ALPHA

HAL is

Introduction

Unlike most animals, plants have developed remarkable capacities of regeneration and propagation.

Inter alia, they can propagate both sexually and vegetatively due to their ability to develop adventitious roots (ARs) from aerial organs, which leads to the development of new genetically identical clonal plants. AR formation is a post-embryonic process, which is an intrinsic element of the normal development of monocots, while in both monocots and dicots it may occur in response to diverse environmental and physiological stimuli, such as darkness, flooding, mechanical wounding or nutrient deprivation (reviewed in Bellini et al. 2014, Steffens and[START_REF] Steffens | The physiology of adventitious roots[END_REF]. The process is a prime example of plants' evolution of sophisticated molecular machinery that precisely translates external cues and coordinates finely-tuned developmental responses that include de novo organogenesis (reviewed by [START_REF] Mauriat | Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport[END_REF][START_REF] Xu | De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition[END_REF].

This article is protected by copyright. All rights reserved. Vegetative or clonal propagation is exploited in horticulture and forest nurseries to produce large numbers of clones relatively quickly. However, some taxa (including economically important species) are difficult to root. For example, some Eucalyptus and Pinus species poorly develop AR without exogenous applications of phytohormones [START_REF] Fett-Neto | Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus[END_REF]. Reasons for the wide variety in plants' capacity to form ARs are not yet clear.

It is now evident that the internal cues regulating AR initiation (ARI) are mainly integrated by the interactive effects of phytohormones (reviewed by Pacurar et al. 2014b). Auxin is the central player, but it acts with an array of other phytohormones through very complex crosstalk, modulating each other's levels and actions at every level: biosynthesis, metabolism, transport and signalling. In this review we summarize the most recent advances in our understanding of hormonal regulation of AR formation, particularly the initiation steps.

Adventitious root initiation and patterning

AR formation is a tightly controlled developmental program, which generally involves three steps.

First, cell specification and reprogramming, in which differentiated cells acquire new cell fate programs leading to the specification of AR founder cells. Second, initiation, in which the AR founder cells undergo successive cell divisions leading to the formation of primordia. Third, primordia emergence and outgrowth. ARI may occur in various cell types, with distinct anatomical and molecular identities, depending on both the species and environmental stimuli involved (reviewed by [START_REF] Geiss | Adventitious root formation: new insights and perspective[END_REF]. In Arabidopsis thaliana (Arabidopsis), ARs may be initiated from xylem pole pericycle cells in both intact and de-rooted hypocotyls [START_REF] Sorin | Auxin and light control of adventitious rooting in Arabidopsis require ARGONAUTE1[END_REF][START_REF] Sukumar | Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis[END_REF]).

Alternatively, they may be initiated from procambium, and probably from the adjacent parenchyma cells of leaf explants kept in the dark on hormone-free B5 medium [START_REF] Liu | WOX11 and 12 are involved in the firststep cell fate transition during de novo root organogenesis in Arabidopsis[END_REF]). However, Bustillo-Avendaño et al. (2018) found that when a whole leaf including the petiole was used as a propagating system, ARs initiated from a pre-formed micro-callus. When the petiole is kept, vascular Regardless of the cell type from which AR arise, phytohormones in coordination with environmental stimuli guide every step of AR formation. They usually act in complex interactions that provide the robust spatio-temporal cues required for AR development (Fig. 1), as outlined in the following sections.

Auxin: the master player and hub of any crosstalk

Indole 3-acetic acid (IAA), the most abundant natural auxin, is a weak organic acid that is mainly derived from L-tryptophan. IAA controls a plethora of developmental programs in plants, including AR formation. It has long been established that different types of auxins promote AR formation in different species [START_REF] Mauriat | Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport[END_REF], Pacurar et al. 2014b). Indole-3-butyric acid (IBA) is the most frequently used natural auxin for clonal propagation in horticulture and forestry because of its stability and effectiveness in promoting AR from stem cuttings compared to other available auxins. IBA induces the auxin signalling machinery following conversion to IAA in planta [START_REF] Strader | Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin[END_REF].

Thus, the double mutant, ech2ibr10, in which IBA to IAA conversion is impaired, produces very few LRs and ARs compared to wild type counterparts [START_REF] Strader | Multiple facets of Arabidopsis seedling development require indole-3-butyric acid-derived auxin[END_REF], Fattorini et al. 2017). The conversion of IBA to IAA seems to be species and genotype dependent. This is significant, because (for example) the rooting capacity of elm (Ulmus americana) genotypes' stem cuttings is correlated with their ability to convert IBA to IAA [START_REF] Kreiser | Conversion of Indole-3-Butyric Acid to Indole-3-Acetic Acid in Shoot Tissue of Hazelnut (Corylus) and Elm (Ulmus)[END_REF]. IBA-derived IAA also controls many other developmental processes [START_REF] Frick | Roles for IBA-derived auxin in plant development[END_REF]. For example, root cap-derived IBA plays a prominent role in lateral root pre-branch site establishment in Arabidopsis [START_REF] Audenaert | Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root[END_REF].

In Arabidopsis, constitutively IAA-overproducing mutants such as superroot1 (sur1), superroot2

(sur2) and the activation tagged YUCCA1 (yuc1-D) spontaneously form AR in the hypocotyl (Boerjan et al. 1995, Delarue et al. 1998[START_REF] Zhao | A role for flavin monooxygenase -like enzymes in auxin biosynthesis[END_REF]). Very early steps in ARI and most organogenesis include formation of an IAA gradient and its accumulation in specific cell types, via processes that include polar auxin transport (PAT) and local auxin biosynthesis, conjugation and degradation.

IAA biosynthesis has been found to be crucial for the cell fate transition of procambium cells to AR founder cells in leaf explants grown on (hormone-free) B5 medium in darkness [START_REF] Liu | WOX11 and 12 are involved in the firststep cell fate transition during de novo root organogenesis in Arabidopsis[END_REF] It is well known that polar auxin transport (PAT) plays a key role in IAA distribution and gradient establishment. Ahkami et al. (2013) found that free IAA levels increased quickly in the stem base of petunia (Petunia hybrida) cuttings in a biphasic manner, with IAA peaking 2 and 24 h after cutting.

The second peak (24 h) was diminished when the plants were treated with naphthylphthalamic acid (NPA, an auxin transport inhibitor), confirming the importance of PAT in ARI (Ahkami et al. 2013).

The increase in IAA at the base of petunia stem cuttings triggered the IAA signalling machinery, leading to a dramatic increase in expression of GRETCHEN HAGEN3 (GH3) auxin-inducible genes as well as increases in cell wall and vacuolar invertases (Ahkami et al. 2013). GH3 enzymes play crucial roles in the regulation of levels of active forms of IAA, JA and SA [START_REF] Staswick | Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3acetic acid[END_REF][START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF][START_REF] Westfall | Arabidopsis thaliana GH3.5 acyl acid amido synthetase mediates metabolic crosstalk in auxin and salicylic acid homeostasis[END_REF]. Interestingly it has been demonstrated that JA is an inhibitor of ARI in Arabidopsis hypocotyls, and that auxin induces ARI by decreasing the pool of active JA through its conjugation to amino acids by GH3 enzymes [START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]. Therefore, we propose that the peaks of IAA that occur in petunia cuttings may prevent inhibition of ARI by wounding-induced accumulation of JA.

This article is protected by copyright. All rights reserved. regulators of ARI, and ARF17 as a negative regulator [START_REF] Gutierrez | Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance[END_REF][START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]. Interestingly, ARF6 and ARF8 genes were found to be specifically induced in the rooting-competent phloem parenchyma cells in stem cuttings of black walnut (Juglans nigra L.), while ARF17 expression decreased during the same developmental stage [START_REF] Stevens | Localized gene expression changes during adventitious root formation in black walnut (Juglans nigra L.)[END_REF]. This differential expression of the three ARF genes was observed before AR primordia formation [START_REF] Stevens | Localized gene expression changes during adventitious root formation in black walnut (Juglans nigra L.)[END_REF]. [START_REF] Ruedell | Concerted transcription of auxin and carbohydrate homeostasis-related genes underlies improved adventitious rooting of microcuttings derived from farred treated Eucalyptus globulus Labill mother plants[END_REF] found that expression of ARF6 and ARF8 was also induced in difficult-to-root Eucalyptus globulus donor plants treated with far-red enriched light, and after cutting. Moreover, this induction coincided with the promotion of AR formation under these conditions. These results suggest that ARF6 and ARF8, which were identified as positive regulators of AR formation in Arabidopsis, may be key elements of an ARI mechanism that has been conserved across diverse taxa.

ARF6 and ARF8 genes regulate expression of the well-known auxin responsive genes GH3.3, GH3.5 and GH3.6 and the triple null mutant gh3.3gh3.5gh3.6 reportedly produces fewer ARs than wild-type counterparts, highlighting a paradox [START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]. The three corresponding GH3 proteins were initially described as auxin conjugating enzymes [START_REF] Staswick | Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3acetic acid[END_REF]), but knocking out gh3.3, gh3.5 and gh3.6 had no apparent effect on endogenous IAA contents, instead it resulted in higher production of free JA and its bioactive form (+)-7-iso-jasmonoyl-L-isoleucine (JA-Ile) [START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]). These findings prompted the conclusion that auxin acted through the GH3 proteins by controlling levels of active JA, which was demonstrated to be a negative regulator of AR formation (Fig. 1) [START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]).

This article is protected by copyright. All rights reserved. MeJA only had an ARI-promoting effect under these conditions, and it should be mentioned that exogenous application of phytohormones dramatically changes the balance of the internal signalling machinery. This is not surprising as regeneration and/or de novo organogenesis requires tight feedback systems and integration of multiple signalling cues (via complex interactions of endogenous phytohormones in natural conditions) that involve and affect multiple cell types and developmental stages.

JA is rapidly and transiently induced after cutting or mechanical wounding. ARs in petunia cuttings [START_REF] Lischweski | Jasmonates act positively in adventitious root formation in petunia cuttings[END_REF]. Nevertheless, the same authors showed that when leafy stem cuttings of petunia were continuously treated with exogenous JA, JA-Ile or OPDA they produced significantly fewer ARs than controls [START_REF] Lischweski | Jasmonates act positively in adventitious root formation in petunia cuttings[END_REF]. These results conflict with the hypothesis that JA could be a positive regulator of ARI, suggesting that long-term treatment with JA inhibits ARI. The latter hypothesis is strongly supported by the genetic characterization of Arabidopsis mutants with impairments in JA biosynthesis, perception and signalling, which prompted the conclusion that COI1-dependent JA signalling inhibits AR through MYC2, MYC3 and MYC4 transcription factors, downstream of IAA [START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF]). In conclusion, recent studies have shown that JA is a major regulator of AR formation, probably as an inhibitor of ARI, although its role could be more complex and species-dependent. JA strongly inhibits cell division and elongation [START_REF] Swiatek | Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells[END_REF], Pauwels et al. 2008), but we still have too little information about JA's mode of action in the specific phases of AR development. Future investigations of JA's effects on the formative cell divisions during ARI should be highly illuminating.

Ethylene: the gas that matters

Ethylene (ET) is a stress-related phytohormone that is rapidly induced in response to several environmental stimuli, inter alia mechanical wounding, darkness or flooding. The ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) seems to have species-dependent effects on AR and constitutive triple response1-1 (ctr1-1) mutants, which have constitutive ET signalling, produced more ARs, while ethylene insensitive2-1 (ein2-1) and ein3-1 mutants produced fewer ARs, than wild type controls. To the same end, Rasmussen et al. ( 2017) showed that at very low concentration (0.01 µM) ACC induced slightly higher AR densities, but higher concentrations (0.1-1 µM) had no significant effect. These results clearly indicate that ET biosynthesis and signalling promote AR formation. The effect of ET on ARI is likely independent of strigolactone (Rasmussen et al. 2017).

However, contrasting results were obtained in another study using the same system and concentration of ACC by [START_REF] Veloccia | Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana[END_REF], who found that treatment with 0.01 µM ACC had no significant effect and higher (0.1-1 µM) concentrations tended to suppress AR formation. These contrasting results might be due to differences in growth conditions and/or high concentrations of ACC affecting other physiological processes of the Arabidopsis seedlings, which might cause aberrant and pleiotropic developmental defects. [START_REF] Veloccia | Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana[END_REF] assumed that ET inhibits AR formation in Arabidopsis by repressing the transcription of WEI2, WEI7 and YUC6 genes by an unknown mechanism. This would be surprising because of previous findings that ET induces expression of WEI2 and WEI7, which leads to increases in IAA biosynthesis and signalling in the Arabidopsis root tip [START_REF] Stepanova | A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis[END_REF]. Because wei2 and wei7 mutations strongly suppressed the sur2-1 phenotype, Pacurar et al. In conclusion, several studies have provided indications that ET is involved in AR formation, but its mode of action is still far from clear. Identifying its downstream targets and acquiring direct evidence about its specific spatiotemporal regulatory role would be helpful for elucidating its mode of action.

Cytokinins: the required inhibitors

Like IAA, cytokinins (CKs) have been extensively studied and characterized. They are adeninederived phytohormones that were called cytokinins because of their ability to promote cell division

Strigolactones: the newcomers to the club

Strigolactones (SL) are carotenoid-derived phytohormones, which participate in regulation of many developmental programs, including root architecture development (reviewed by [START_REF] Waters | Strigolactone signaling and evolution[END_REF].

Their roles in the control of AR formation are not clearly understood, but they were recently shown to participate interactively in this process with other hormones in various species.

SLs promote crown root elongation in rice via effects on cell division in the meristematic zone (Arite et al. 2012). Recently, it has also been shown that SLs positively control crown root formation in rice.

In addition, [START_REF] Sun | Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions[END_REF] found that the SL-deficient rice mutant dawarf10 (d10), in which the key gene of SL biosynthesis is impaired, produced fewer ARs than wild type counterparts. AR production was also reduced in the SL-insensitive mutant d3, in which the F-box protein (a key component of the SCF complex involved in SL signalling) is affected. However, treating plants with GR24, a synthetic SL analogue, complemented the d10 phenotype but not the d3 phenotype [START_REF] Sun | Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions[END_REF]. SLs apparently promote AR formation in rice via the D4-dependent pathway, probably by modulating IAA transport [START_REF] Sun | Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions[END_REF]. However, they seem to inhibit AR formation in tomato (Solanum lycopersicum), pea (Pisum sativum) and Arabidopsis [START_REF] Kohlen | The tomato carotenoid cleavage dioxygenase8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis[END_REF], Rasmussen et al. 2012, 2017). [START_REF] Kohlen | The tomato carotenoid cleavage dioxygenase8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis[END_REF] Similarly, [START_REF] Mauriat | Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport[END_REF] showed that a treatment with GA4 inhibited AR formation in etiolated Arabidopsis hypocotyls and Populus stem cuttings, and that transgenic lines of both Arabidopsis and

Populus with enhanced GA biosynthesis or perception produced fewer ARs than wild type counterparts. In the cited study, GA inhibited AR formation independently of SL biosynthesis and JA signalling, but probably interfered with establishment of an IAA gradient at the base of the stem cuttings by perturbing expression of IAA auxin efflux carrier genes.

ABA, which is a stress-related hormone, has been shown to inhibit AR emergence in deepwater rice, possibly by interfering with ET and GA signalling pathways [START_REF] Steffens | Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice[END_REF]. Similarly, shootderived ABA inhibits LR and AR formation in tomato, likely via effects on ET and IAA pathways [START_REF] Mcadam | Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions[END_REF]).

Last, but not least, brassinosteroids (BRs) have been shown to stimulate ARI in Arabidopsis hypocotyls [START_REF] Maharjan | Arabidopsis gulliver1/superroot2-7 identifies a metabolic basis for auxin and brassinosteroid synergy[END_REF]). The cited authors showed that treating weakly IAA-overproducing

Conclusion and perspectives

AR formation is a developmental program that is controlled by complex hormonal crosstalk with strongly non-linear effects (Fig. 1). Numerous studies with model species such as Arabidopsis, rice and petunia, have provided information about the complex interactions involved. However, despite remarkable advances in molecular-level understanding of the process in the model species, little is still known about it in woody species such as Populus, Pinus, and Norway spruce. Checking whether the mechanisms identified in the model species are evolutionarily conserved is important, but challenging.

Fortunately, the availability of genome sequences of increasing numbers of species and rapid development of genome editing techniques such as TALEN and CRISPR-Cas9 will greatly facilitate elucidation of AR formation in diverse taxa (particularly ecologically and economically important species) and the evolution of associated developmental machinery.

While efforts have focused on elucidating this process in single linear hormonal pathways, advances in modelling and integrative system biology approaches, including hormonomics, should be exploited to acquire more insights into the complex hormonal interactions involved and their final outcomes. It This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.

PPL_12823_F1.tif

This article is protected by copyright. All rights reserved.

  Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823

  tissues including xylem and pericycle-like cells first undergo massive cell division, resulting in formation of a micro-callus, which subsequently undergoes a second step of reprogramming that specifies the AR founder cell (Bustillo-Avendaño et al. 2018). This process resembles the two-step mechanism during hormone-induced organogenesis (reviewed by Kareem et al. 2016). Histological studies of Populus and carnation (Dianthus caryophyllus L.) stem cuttings revealed that the first cell division leading to primordium formation occurs in cambial tissues (Rigal et al. 2012, Agulló-Antón et al. 2014). In monocots, serial cross sections in rice (Oryza sativa) have demonstrated that crown roots This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823initiate from the peripheral vascular cylinder. In conclusion, whatever the tissue or organ, ARs are initiated from cells with vascular associations.

  Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 The ATP-BINDING CASSETTE B19 (ABCB19) and PIN-formed 1 (PIN1) seem to be the main IAA efflux carriers involved in auxin accumulation at the base of excised Arabidopsis hypocotyls and, thus, contributors to AR formation. Accordingly, Sukumar et al. (2013) found that de-rooted abcb19-1 and pin1-1 loss-of-function mutant seedlings produced fewer ARs than wild type counterparts, and the ABCB19 gene was rapidly induced upon excision, especially in the hypocotyl epidermis and vascular tissues. PIN6 is also involved in AR formation, as demonstrated by phenotypes of loss-or gain-offunction lines reported by Simon et al. (2016). The pin6 knock-out mutant produced more ARs, whereas the over-expressing line 35:PIN6 produced very few ARs compared to wild type counterparts. These findings confirm the importance of rootward IAA transport during ARI. Many mutants with IAA perception or signalling impairments have been identified in the last decade and their functional analysis has illuminated some of the molecular mechanisms controlling ARI downstream of IAA. In intact Arabidopsis hypocotyls, IAA acts through transcription factors from the AUXIN RESPONSE FACTOR (ARF) family. ARF6 and ARF8 have been identified as positive

  Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 Additional components of the IAA signalling machinery were identified in a genetic screen for suppressors of the AR phenotype of the auxin-overproducing mutant sur2-1 (Pacurar et al. 2014a). For example, the COP9 SIGNALOSOME SUBUNIT 4 (CSN4), which controls de-neddylation of CULLIN1 in the SCF complex, acts on the ARF6/8 regulatory module and likely at the crossroads of IAA, JA and/or light signalling pathways involved in the control of both AR and LR formation (Pacurar et al. 2017). Intriguingly, phenotypic characterization of available viable csn mutants indicated a possible differential role of the COP9 signalosome in AR and LR formation (Pacurar et al. 2017). Moreover, the gain-of-function mutants crane-2 and solitary root-1 (slr-1), which harbour mutations in domain II of IAA18 and IAA14, respectively, that confer resistance to degradation by the proteasome, were also shown to be affected in ARI (Bustillo-Avendaño et al. 2018).Wounding-induced IAA accumulation at the base of leaf blades triggers expression of the homeobox genes WUSCHEL RELATED HOMEOBOX11 and 12 (WOX11 and WOX12), which are putatively key players in cell fate reprogramming during de novo organogenesis[START_REF] Liu | WOX11 and 12 are involved in the firststep cell fate transition during de novo root organogenesis in Arabidopsis[END_REF], Chen et al. 2016).WOX11, redundantly with WOX12, controls transition of competent cells into AR founder cells by activating BOUNDARY LATERAL DOMAIN16 and 29 (LBD16 and LBD29) genes in leaf cuttings[START_REF] Liu | WOX11 and 12 are involved in the firststep cell fate transition during de novo root organogenesis in Arabidopsis[END_REF]. Although expression of WOX11 was previously associated with ARI[START_REF] Liu | WOX11 and 12 are involved in the firststep cell fate transition during de novo root organogenesis in Arabidopsis[END_REF]), a more recent study of whole leaf explants, including the petiole, revealed that it was not expressed at the site of ARI but in the proliferating vascular tissues, suggesting it participates in callus formation (Bustillo-Avendaño et al. 2018). This indicates that WOX11 controls either very early events of cell reprogramming during ARI or callus formation, depending on the system. The OsWOX11 gene is specifically expressed in AR primordia and the corresponding protein interacts physically with ETHYLENE RESPONSE FACTOR (ERF3) in promotion of AR formation. The ERF3 gene is rapidly and transiently induced by exogenously applied synthetic auxin (2-4 D) and cytokinin (6-BA) (Zhao et al. 2015). Comparative analyses of transcripts in root tips of wox11 mutant and wild type plants revealed that OsWOX11 regulates the expression of many genes in the cytokinin and auxin signalling pathways, suggesting that OsWOX11-OsERF3 dimers mediate complex crosstalk between different hormones during ARI (Zhao et al. 2015, Jiang et al. 2017). The Populus (cultivar Nanline895') genome contains two WOX11 paralogs: PeWOX11a and PeWOX11b. Xu et al. (2015) found that constitutive overexpression of PeWOX11 in transgenic lines not only enhanced the rate of rooting, but also increased numbers of ARs per cutting. In conclusion, the closely-related homologs of AtWOX11 in rice and Populus are required for proper AR formation, suggesting that WOX11 likely This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823mediates a conserved evolutionary mechanism of adventitious rooting in monocots and dicots, including woody species[START_REF] Zhao | The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice[END_REF][START_REF] Xu | Two WUSCHEL-related HOMEOBOX genes, PeWOX11a and PeWOX11b, are involved in adventitious root formation of poplar[END_REF].Jasmonic acid: a positive or negative regulator of adventitious root initiation?Jasmonic acid (JA) is an oxylipin-derived phytohormone, usually associated with mechanical wounding and plant defence against pathogens. However, during the last decade it has attracted the attention of many researchers and shown to be a key hormonal player in normal plant growth and development. JA participates in diverse developmental processes, such as apical hook formation, hypocotyl elongation, flower development (inter alia its timing), primary root elongation, AR and LR formation (reviewed by[START_REF] Wasternack | Jasmonates: Biosynthesis, metabolism, and signaling by proteins activating and repressing transcription[END_REF].JA inhibits primary root elongation and promotes LR formation. In LR development, JA enhances IAA biosynthesis via transcriptional activation of ASA1, YUC2, YUC8 and YUC9 genes.[START_REF] Sun | Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation[END_REF] Cai et al. (2014) found that asa1, yuc2, yuc8 or yuc9 loss-of-function mutants produced far fewer LRs than wild type counterparts when treated with methyl jasmonate (MeJA). These resultssuggest that IAA biosynthesis is required for MeJA to promote LR formation.Cai et al. (2014) demonstrated that ERF109, which is highly induced by JA, binds directly to the promotor of ASA1 and YUC2 genes, activating their transcription and subsequently inducing IAA production, thereby providing the missing link between JA and IAA biosynthesis. MeJA has also been shown to be a positive regulator of AR formation in tobacco (Nicotiana tabacum) and Arabidopsis thin cell layers (TCLs) cultured on a root-inducing medium(Fattorini et al. 2009). However, this positive effect was not observed when the TCLs were cultured in hormone-free medium(Fattorini et al. 2009). The cited authors used a high concentration of IBA and low concentration of kinetin to induce AR formation.

  It accumulates at the site of wounds, where it induces responses that protect plants from pathogen attacks. Because JA rapidly and transiently accumulates at the base of petunia leafy stem cuttings, before ARs emerge, it was proposed to be a positive regulator of AR formation (Ahkami et al. 2009). This hypothesis was This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 corroborated by findings that downregulation of ALLENE OXIDE SYNTHASE (AOS), which catalyses a critical step leading to formation of cis-12-oxo-phytodienoic acid (OPDA), reduced formation of

  production. Etiolated tomato (Solanum lycopersicum) seedlings and petunia stem cuttings treated with ACC reportedly produce more ARs than controls(Negi et al. 2010, Druege et al. 2014) suggesting ET promotes AR formation. This is supported by findings that the ET-insensitive tomato mutant Never ripe (Nr), which has impaired ET perception, produced fewer ARs than wild type counterparts(Negi et al. 2010). Similarly, flooding-induced AR formation is mediated by ET biosynthesis and signalling in rice and tomato[START_REF] Lorbiecke | Adventitious root growth and cell-cycle induction in deepwater rice[END_REF] Sauter 1999, Vidoz et al. 2010).[START_REF] Vidoz | Hormonal interplay during adventitious root formation in flooded tomato plants[END_REF] found that treatment with the ET biosynthesis inhibitor aminoethoxyvinylglycine (AVG) suppressed floodinginduced AR formation in tomato hypocotyls and Nr mutants produced fewer ARs than wild type plants following flooding, confirming the positive role of ET in AR formation. Accordingly, darknessinduced AR emergence in rice stem cuttings is promoted by ET signalling because treatment with 1methylcyclopropene (1-MCP, an ET perception inhibitor) is sufficient to inhibit this process (Lin and Sauter 2018). It has been suggested that ET promotes ARI in de-rooted hypocotyls of Norway spruce This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 (Picea abies) by enhancing CK degradation (Bollmark and Eliasson 1990). ET also seems to have ARI-promoting effects on IAA transport (Negi et al. 2010). To obtain detailed insights into the key players involved in specific steps of AR formation in petunia stem cuttings, Druege et al. (2014) performed an extensive time course microarray analysis. This revealed that many ACC SYNTHASE (ACS) and ACC OXIDASE (ACO) genes were rapidly induced after cutting, suggesting that ET biosynthesis is required for ARI. In addition to ET biosynthesis genes, many APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) genes were differentially expressed at various stages during the process. Several AP2/ERF genes have been recently identified as potent players in regulation of tissue repair, de-novo organogenesis and regeneration (Heyman et al. 2017), indicating possible roles of the ET-induced AP2/ERF genes in AR formation. In attempts to elucidate ET's role in ARI, Rasmussen et al. (2017) analysed several Arabidopsis ET biosynthesis and signalling mutants. Both ethylene overproducing 2-1 (eto2-1) and eto3-1 mutants,

(

  2014a) proposed that ET might have a positive role in early stages of AR formation, by inducing IAA biosynthesis, but a negative role in later stages. This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823

(

  cytokinesis). In hormone-induced de novo organogenesis systems, the balance between CK and IAA is the main determinant of cell fate reprogramming mechanisms. High concentrations of CKs promote shoot formation but inhibit root formation. Thus, CKs have long-known roles in AR and LR formation (reviewed by[START_REF] Kareem | De novo assembly of plant body plan: a step ahead of Deadpool[END_REF].Ramirez-Carvajal et al. (2009) found that upregulating CK signalling by overexpressing an active version of the RESPONSE REGULATOR type B transcription factor PtRR13 in Populus reduced numbers of ARs formed at the base of stem cuttings, and formation of callus. In rice, CKs inhibit crown root formation downstream of the IAA-induced CROWN ROOTLESS 5 transcription factor[START_REF] Kitomi | The auxin responsive AP2/ERF transcription factor CROWN ROOTLESS5 is involved in crown root initiation in rice through the induction of OsRR1, a type-A response regulator of cytokinin signaling[END_REF].Very recently,Bustillo-Avendaño et al. (2018) suggested that in hormone-free medium de novo ARI at the base of petioles of detached leaves, involves a two-step mechanism in which CK synthesis and signalling play crucial roles. In this system, ARI involves two distinct reprogramming events. First, vascular-associated cells in the petiole proliferate, forming a micro-callus. Subsequently, a few cells in the micro-callus undergo another reprogramming event leading to AR founder cell specification and subsequently ARI. This mechanism has previously been proposed as an indirect ARI in difficult-toroot species such as of Pinus and Eucalyptus (Rasmussen et al. 2009). To confirm this interesting observation, cell lineage tracing and single cell transcriptomic analyses are needed to confirm that the proliferating cells have lost their original vascular identity and shifted towards callus identity. CKs seem to promote the first step i.e. cell proliferation but inhibit the second step i.e. cell reprogramming leading to specification of AR founder cells from the pre-formed micro-callus. Several indications of CKs' roles in AR formation have been obtained from analyses of CK perception and signalling mutants, including wol (wooden leg), which carries a mutation of the CK receptor ARABIDOPSIS HISTIDINE KINASE4 (AHK4) and arr1arr10arr12, a triple loss-of-function of ARABIDOPSIS RESPONSE ELEMENT type B genes mutant. Bustillo-Avendaño et al. (2018) found that vasculature proliferation or micro-callus formation was reduced in these mutants but, This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 interestingly, the petioles that developed a micro-callus generated higher numbers of ARs. Accordingly, downregulation of arr1arr10arr12, using oestradiol-inducible artificial microRNA, reportedly resulted in production of ARs rather than shoots by root explants incubated in CK-rich shoot induction medium (CIM) (Meng et al. 2017). ARR1, ARR10 and ARR12 directly bind to the promoter of YUC4 and inhibit its transcriptional activity, suggesting that CKs likely inhibit ARI by repressing YUC-mediated IAA biosynthesis (Meng et al. 2017). Knowledge of the role of CKs in callus and shoot formation has provided important steps towards understanding their mechanistic mode of action, but accounts of their role in ARI are still descriptive and fragmentary. Mechanical wounding appears to locally enhance CK biosynthesis and signalling in Arabidopsis (Bustillo-Avendaño et al. 2018, Ikeuchi et al. 2017), thus it would be interesting to check whether there is a link between CKs and other wounding-induced hormones, such as JA because both hormones seem to be negative regulators of ARI.

  found that AR numbers were significantly increased in CAROTENOID CLEAVAGE DIOXYGENASE 8 (SlCCD8) RNAi transgenic lines, suggesting that SL-mediated AR formation is species-dependent. Moreover, SLs inhibit AR formation independently from the IAA, CK and ET pathways (Rasmussen et al. 2012, 2017). The contrasting effects of SL in AR formation This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 between monocots (rice) and dicots (pea, tomato, Arabidopsis) raise intriguing questions that remain to be answered. Abscisic acid (ABA), gibberellic acid (GA) and brassinosteroids (BRs): the least investigated hormones in adventitious rooting Roles of ABA, GA and BRs in AR formation are largely unclear, but there are interesting indications that they participate. For example, GA stimulates AR formation in deepwater rice via a mechanism that requires the presence of ET (Steffens et al. 2006). Treatment with GA3 alone was reportedly ineffective, but in combination with ET it significantly stimulated AR emergence (Steffens et al. 2006). In contrast, Busov et al. (2006) found that treatment with GA3 inhibited AR formation in Populus stem cuttings. This negative effect was corroborated by the finding that constitutive overexpression of RGL1 (REPRESSOR OF GA1-3-LIKE 1) or GAI (GIBERELLIC ACID INSENSITIVE) genes without the DELLA domain, making them resistant to GA, increased numbers of ARs, indicating that GA is a negative regulator of AR formation in Populus (Busov et al. 2006).

  gulliver1/sur2-7 mutants with exogenous brassinolide induced them to form ARs from light-grown hypocotyls, which they do not normally do, likely by enhancing IAA biosynthesis. BR and IAA synergistically promote cell elongation in Arabidopsis hypocotyls through a mechanism that involves BRASSINAZOLE-RESISTANT 1 (BZR1), ARF6, ARF8 and PHYTOCHROME INTERACTING FACTOR (PIF4). These transcription factors interact with each other physically and genetically in regulation of common targets including GH3.3 and GH3.6 (Oh et al. 2014). It is possible that BR This article is protected by copyright. All rights reserved. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823signalling acts synergistically with the ARF6/ARF8 signalling module identified by[START_REF] Gutierrez | Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis[END_REF] in ARI promotion.

  would also be interesting to discover how plants couple the intrinsic and extrinsic stimuli that guide and shape AR architecture. Further knowledge is required of how the external stimuli are perceived, transmitted and translated into tight internal signalling cues, as well as how specific subsets of cell types are targeted by these cues and transformed into AR founder cells.•Author contributions • A.L. wrote the manuscript, A.L. and C.B. edited it. Comment citer ce document : Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823 Meng W, Cheng ZJ, Sang YL, Zhang MM, Rong XF, Wang ZW, Tang YY, Zhang XS (2017) Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell Online 29: 1357-1372 Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61: 3-15 Oh E, Zhu JY, Bai MY, Arenhart RA ugust., Sun Y, Wang ZY (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. Elife 3: 1-19 Pacurar DI, Pacurar ML, Bussell JD, Schwambach J, Pop TI, Kowalczyk M, Gutierrez L, Cavel E, Chaabouni S, Ljung K, Fett-Neto AG, Pamfil D, Bellini C (2014a) Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J Exp Bot 65: 1605-1618 Pacurar DI, Pacurar ML, Lakehal A, Pacurar AM, Ranjan A, Bellini C (2017) The Arabidopsis Cop9 signalosome subunit 4 (CNS4) is involved in adventitious root formation. Sci Rep 7: 1-12 Pacurar DI, Perrone I, Bellini C (2014b) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant 151: 83-96 Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, Inze D, Goossens A (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci 105: 1380-1385 Ramirez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 is a negative regulator of adventitious root development in Populus. Plant Physiol 150: 759-771 Rasmussen A, Hu Y, Depaepe T, Vandenbussche F, Boyer FD, Van Der Straeten D, Geelen D (2017) Ethylene controls adventitious root initiation sites in Arabidopsis hypocotyls independently of strigolactones. J Plant Growth Regul 36: 897-911 Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158: 1976-1987 Rasmussen A, Smith TE, Hunt MA (2009) Cellular stages of root formation, root system quality and survival of Pinus elliottii var. elliottii × P. caribaea var. hondurensis cuttings in different temperature environments. New For 38: 285-294

Figure legend Fig. 1 .

 legend1 Figure legendFig. 1. Overview of hormonal crosstalk during adventitious root initiation (ARI): Auxin (IAA) is the central modulator. Besides IAA, ethylene (ET) and brassinosteroids (BRs) promote ARI, while cytokinins (CKs), jasmonic acid (JA), gibberellic acid (GA), strigolactone (SL) and abscisic acid (ABA) are negative regulators. Continuous and dashed lines indicate proven and possible links, respectively. Blue and red colors indicate positive and negative regulators, respectively.

  . (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165 (1), 90-100. , DOI : 10.1111/ppl.12823

  , Chen et al. 2016). The cited authors showed that induction of YUC genes' expression in detached Arabidopsis leaves rapidly mediated increases in free IAA levels. Expression of YUC1 and YUC4 ubiquitously increased in the mesophyll after leaf detachment. The quadruple mutant yuc1,2,4,6 was This article is protected by copyright. All rights reserved. ARs and blocking the activity of YUC enzymes with the chemical yucasin severely affected adventitious rooting in leaf explants. In both cases, exposure to 0.1 µM of IAA could restore AR formation. These results clearly indicate that YUC-mediated auxin biosynthesis is required to trigger cell reprogramming and/or cell fate transition in leaf explants (Chen et al. 2016). Therefore, a link between wounding-induced YUCs and de novo AR initiation has been proposed (Chen et al.

	unable to develop 2016, Xu 2018). However, whether wounding induces expression of YUC genes directly or indirectly
	via jasmonate (JA) and/or ethylene (ET) remains to be resolved. Both JA and ET are highly induced
	during mechanical wounding and they may trigger expression of YUCs and possibly other IAA
	biosynthesis genes such as ANTHRANILATE SYNTHASE ALPHA 1/WEAK ETHYLENE INSENSITIVE
	2 (ASA1/WEI2) (Stepanova 2005, Sun et al. 2009, Cai et al. 2014). As Chen et al. (2016) found that
	dark-grown leaf explants produced more ARs than light-grown counterparts, it would be interesting to
	elucidate the molecular link between darkness and wounding in promotion of IAA-induced de novo
	organogenesis. Several IAA biosynthesis genes have been identified in a suppressor screen of sur2-1
	AR phenotype, such as ASA1/WEI2, ASB1/WEI7, and TRYPTOPHAN SYNTHASE BETA 1 (TSB1)
	(Pacurar et al. 2014a). Loss of function of any of these genes reduced numbers of ARs produced by
	sur2-1 mutants, confirming the pivotal role of IAA biosynthesis in AR formation (Pacurar et al.
	2014a).
	Comment citer ce document :
	Lakehal, A. (Auteur de correspondance), Bellini, C. (2019). Control of adventitious root
	formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum,
	165 (1), 90-100. , DOI : 10.1111/ppl.12823

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Acknowledgements -We apologize to all colleagues whose work could not be cited due to space limitations. Research by our group is supported by the Swedish Research Council for Research and Innovation for Sustainable Growth (VINNOVA), the Swedish Research Council (VR), and the Carl Kempe Foundation.

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