Loyal Déborah

Anne-Laure Sutter

Rascle Nicole

Mothering Ideology and Work Involvement in Late Pregnancy: A Clustering Approach

Keywords: Intensive Mothering Ideology, Motherhood, Multiples Roles, Pregnancy, Psychological Distress, Work Family Balance

The aim of this study was to identify cognitive acrobatics performed by French women during late pregnancy (N = 139) to reconcile intensive mothering ideology (IMI) and work involvement. A hierarchical cluster analysis (Ward method, squared Euclidian distance) was performed to define different patterns and 4 clusters were retained: (1) women devoted to IMI (27%), (2) women devoted to IMI and worried about the consequences of maternal work (13%), (3) women not devoted to IMI (35%), (4) women not devoted to IMI and disengaged from work (25%). They exhibited differences regarding socio-demographic and psychological variables. Mainly, women devoted to IMI and worried about the consequences of maternal work (Cluster 2) showed more depressive symptoms (38.9%) and preoccupied attachment. They were also planning to go back to work later (50%) and not to breastfeed (39%) even if they had a highly positive opinion about breastfeeding (67%). These results are discussed in terms of socio-psychological resources and requirements regarding perinatal adjustment. Considering women's values and beliefs is a crucial aspect to understand better how mothering and working demands are experienced.

Owing to biological, psychological and social changes, new motherhood is a life transition that requires numerous adjustments (World Health Organization, 2009). Postpartum seems to have received much more attention than pregnancy [START_REF] Green | Postnatal depression or perinatal dysphoria ? Findings from a longitudinal community based study using the Edinburgh Postnatal Depression Scale[END_REF]. However, pregnant women might experience stressors such as the inability to perform daily tasks, physical symptoms and bodily changes, sleep disturbances, changes in intimate relationships, worries about delivery and child health and so forth [START_REF] Dipietro | Continuity in self-report measures of maternal anxiety, stress, and depressive symptoms from pregnancy through two years postpartum[END_REF].

Although it has long been assumed that pregnant women were protected against psychological distress [START_REF] Green | Postnatal depression or perinatal dysphoria ? Findings from a longitudinal community based study using the Edinburgh Postnatal Depression Scale[END_REF], it is now known that many women exhibit significant depressive and anxious symptoms during pregnancy (Bennett, Einarson, Taddio, Koren, & Einarson, 2004a;[START_REF] Grant | Maternal anxiety during the transition to parenthood: A prospective study[END_REF]. Indeed, in their systematic review, Bennett et al. (2004a) reported that depressive symptoms are as common during pregnancy (12.8% and 12% in the second and third trimester) as in the postpartum period (13%) [START_REF] O'hara | Rates and risk of postpartum depression: A meta-analysis[END_REF].

Anxiety symptoms also seem to be prevalent in pregnant women as in postpartum women (33% in both cases) [START_REF] Grant | Maternal anxiety during the transition to parenthood: A prospective study[END_REF]. Moreover, prenatal depression and anxiety has been found to be linked to postpartum depression in different meta-analysis [START_REF] O'hara | Postpartum depression: Current status and future directions[END_REF].

Many studies have explored the risk factors for prenatal and postpartum depression [START_REF] Lancaster | Risk factors for depressive symptoms during pregnancy: A systematic review[END_REF][START_REF] O'hara | Postpartum depression: Current status and future directions[END_REF]. However, whereas the normative aspects of motherhood are usually recognized to contribute to mental health in new mothers in the qualitative literature [START_REF] Arendell | Conceiving and investigating motherhood: The decade's scholarship[END_REF][START_REF] Tummala-Narra | Contemporary impingements on mothering[END_REF], it has received little attention in quantitative research. Mothering has been described as a role [START_REF] Ambert | An international perspective on parenting: Social change and social Constructs[END_REF][START_REF] Arendell | Conceiving and investigating motherhood: The decade's scholarship[END_REF][START_REF] Glenn | Social constructions of mothering: A thematic overview[END_REF] and as such, according to role theory [START_REF] Biddle | Role Theory: Expectations, Identities, and Behaviors[END_REF], is subjected to normative expectations rooted in specific social contexts. [START_REF] Hays | The cultural contradictions of motherhood[END_REF] argued that contemporary dominant discourse about motherhood in industrialized countries should be understood as an ideology, i.e. a system of interrelated representations that she labeled Intensive Mothering Ideology (IMI). According to Hays, parents who adhere to IMI more or less explicitly assume that mothers are inherently the essential and best caregivers for children. Although they mean well, fathers are depicted as incompetent or clumsy (essentialism). Childrearing is described as a demanding and consuming activity (challenge) that must be exclusively child-centered according to supposed child needs (child centrism). Parents must ensure that the child is adequately and kindly stimulated (stimulation). Parenting is seen as the hardest job in the world but also as the most rewarding and important one (fulfillment). The IMI concept, although originated in United States, has been successfully applied in French mothers and mothers-to-be [START_REF] Loyal | Idéologie du maternage intensif en France : Adaptation et validation de l'IPAQ (Intensive Parenting Attitudes Questionnaire)[END_REF].

Whereas adhesion to shared norms can be seen as an indicator of social inclusion and mental health [START_REF] Cialdini | Social influence: compliance and conformity[END_REF], through excessive and precise requirements and expectations that are difficult to meet [START_REF] Flykt | What explains violated expectations of parent-child relationship in transition to parenthood[END_REF][START_REF] Kalmuss | Parenting expectations, experiences, and adjustment to parenthood: A test of the violated expectations framework[END_REF]) IMI might represent a source of emotional disturbance in new mothers. Indeed, in a cross-sectional study of mothers of pre-schoolers controlling for social support, essentialism was linked to lower life satisfaction and challenge was linked to greater depression and stress [START_REF] Rizzo | Insight into the parenthood paradox: Mental health outcomes of intensive mothering[END_REF]. IMI might also be a threat to gender equality [START_REF] Arendell | Conceiving and investigating motherhood: The decade's scholarship[END_REF]Macdonald, 2009), notably through essentialism which places an undue burden on mothers. Indeed, women are still responsible for most household chores and childcare (Bauer, 2007;Brugeilles & Sebille, 2011).

Moreover, in her pioneering qualitative work, [START_REF] Villalobos | Motherload: Making It All Better in Insecure Times[END_REF] postulated that IMI might be linked to insecurity in intimate relationships. In other words, women who feel insecure might seek some kind of reassurance through an intense investment in motherhood. According to attachment theory [START_REF] Bowlby | Maternal care and mental health[END_REF] early interactions generate internal working models that guide, through the lifespan, the way that one perceives oneself and others [START_REF] Bartholomew | Attachment styles among young adults: A test of a four-category model[END_REF]. Of note, attachment style is one source of social support perception [START_REF] Collins | Working models of attachment shape perceptions of social support: Evidence from experimental and observational studies[END_REF]) and lack of social support have been found to be linked with perinatal depression [START_REF] Lancaster | Risk factors for depressive symptoms during pregnancy: A systematic review[END_REF][START_REF] O'hara | Postpartum depression: Current status and future directions[END_REF].

Beside, in most European countries, female employment rates have increased in recent decades [START_REF] Cipollone | Women's labour market performance in Europe trends and shaping factors[END_REF]. Although women long had to choose or shift between work and family responsibilities, most of them now undertake both simultaneously [START_REF] Maruani | Travail et emploi des femmes[END_REF]. Striving to combine work and family life harmoniously is still a woman's prerogative [START_REF] Meda | Le temps des femmes : pour un nouveau partage des rôles[END_REF][START_REF] Pailhe | Vie professionnelle et naissance : La charge de la conciliation repose essentiellement sur les femmes[END_REF] which translates into concrete arrangements (professional choices, extended parental leave, part-time job, teleworking…) and probably into cognitive patterns. Indeed, in their qualitative analyses, [START_REF] Johnston | Constructing the good mother : The experience of mothering ideologies by work status[END_REF][START_REF] Johnston | Cognitive acrobatics in the construction of worker-mother identity[END_REF] suggest that women, particularly working ones, need to perform cognitive acrobatics in order to "manage the tension between employment and the dominant mothering ideology" (Johnston & Swanson, 2007, p. 447). They identified different type of cognitive acrobatics: selection/selection through subjugation of worker identity, neutralization, separation and reframing. First, selection can be seen in most stay-at-home mothers who were devoted to IMI and had a low worker identity. In the same vein, it has been previously found that IMI was more highly endorsed by stay-at-home than by working mothers [START_REF] Liss | Development and validation of a quantitative measure of intensive parenting attitudes[END_REF][START_REF] Loyal | Idéologie du maternage intensif en France : Adaptation et validation de l'IPAQ (Intensive Parenting Attitudes Questionnaire)[END_REF] and was linked to the belief that maternal work is detrimental to children, separation anxiety in mothers and higher participation in childcare and household chores [START_REF] Liss | Development and validation of a quantitative measure of intensive parenting attitudes[END_REF].

Interestingly, [START_REF] Johnston | Cognitive acrobatics in the construction of worker-mother identity[END_REF] reported that certain stay-at-home mothers who had a strong worker identity reported that they had to struggle with work decisions and often ended up tempering their work investment and reinforcing their commitment to IMI (selection through subjugation of worker identity). This might be seen as an expression of the mommy track phenomenon [START_REF] Smith | A maze of metaphors around glass ceilings[END_REF], i.e. prioritizing mothering at the expense of work. They also reported that many working mothers feel torn between IMI and work requirements, trying in vain to meet the demands of both domains (neutralization). However, some women feel more detached from IMI, were primarily driven by their worker identity and thus experience fewer dilemmas in their work life (separation). Finally, some working women were reframing their work as a way to be a better mother and focused on the quality of time they spend with their children.

Lastly, it has been observed that, after the birth of child, family salience rises whereas work salience diminishes [START_REF] Katz-Wise | Gender-role attitudes and behavior across the transition to parenthood[END_REF]. However, some mechanisms might be put into effect earlier. For instance, in France 33% of women reported they changed their work organization during their pregnancy [START_REF] Penet | Le congé de maternité[END_REF]. Moreover, a lot of women who stopped working after the birth had made this decision during their pregnancy (around 50%) and even before it (around 20%) [START_REF] Meda | Pourquoi certaines femmes s'arrêtent-elles de travailler à la naissance d'un enfant ? Ministère de l'Emploi[END_REF]. Thus, pregnancy might be a pivotal period regarding work and family combination.

The aim of the present study was to explore quantitatively the cognitive acrobatics that pregnant women might perform to combine normative expectations about motherhood (i.e. IMI) and work involvement. In line with [START_REF] Johnston | Cognitive acrobatics in the construction of worker-mother identity[END_REF], we aimed at grouping women who share similar cognitive acrobatics, i.e. patterns of IMI endorsement and work involvement. To do so, a clustering approach was chosen to created groups "so that members of the resulting groups are as similar as possible to others within their group (high within-group homogeneity) and as different as possible to those in other groups (low between-group homogeneity)" (Clatworthy, Buick, Hankins, Weinman, & Horne, 2005, p. 330). This kind of approach can reconcile the nomothetic (variable-centered, "seeing the forest") and idiographic (person-centered, "seeing the tree") approaches [START_REF] Clatworthy | The use and reporting of cluster analysis in health psychology: A review[END_REF] and is particularly useful when considering interactionist framework and hypotheses [START_REF] Bergman | The person-oriented approach: A short theoretical and practical guide[END_REF]. Moreover, this approach has the advantage of resuming large quantities of multivariate information in simple and manageable units [START_REF] Bergman | The person-oriented approach: A short theoretical and practical guide[END_REF][START_REF] Clatworthy | The use and reporting of cluster analysis in health psychology: A review[END_REF]. Finally, this study was also meant to test the discriminant validity of the produced cluster classification [START_REF] Aldenderfer | Cluster analysis[END_REF][START_REF] Clatworthy | The use and reporting of cluster analysis in health psychology: A review[END_REF] by exploring how the different cognitive acrobatics performed by pregnant women might be linked to socio-economic and psychological characteristics.

In accordance with Johnston & Swanson's model (2007), it was hypothesized (Table 1) that different cluster would be identifiable in a pregnant women's sample: (1a, neutralization) women who endorse IMI and are involved in work, (1b, disengagement), women who do not endorse IMI and are disengaged from work, (1c, selection) women who endorse IMI and are disengaged from work, (1d, separation) women who do not endorse IMI and are involved in work. Secondly, it was hypothesized (Table 1) that cognitive acrobatics would be linked with distress: (2a) Neutralization and Disengagement would be linked to higher distress, (2b) whereas Selection and Separation would be linked to lower distress.

INSERT TABLE 1 AROUND HERE

Method

Pregnant women were recruited at the maternity ward of the local university hospital during a mandatory information reunion about childbirth pain relief (epidural anesthesia…) with an anesthesiologist. As this information reunion was strongly recommended for all women who planned to give birth in this maternity ward, one can guess that our invited population was, in some extent, representative of the maternity ward population. Participants had to be fluent in French (spoken and written), to be older than 18 years old. They had to have no multiple pregnancy, which is a known source of perinatal medical complications and emotional distress [START_REF] Blondel | Les naissances en 2010 et leur évolution en 2003[END_REF][START_REF] Fisher | Maternal perinatal mental health and multiple births: Implications for practice[END_REF], and no medically assisted procreation which might be risk factor for emotional distress [START_REF] Hammarberg | Psychological and social aspects of pregnancy, childbirth and early parenting after assisted conception: A systematic review[END_REF]. This study was approved by a national informatics right committee (https://www.cnil.fr/) and a regional ethic committee (http://www.cpp-soom3.u-bordeaux2.fr/).

Approximately 640 to 960 women were invited to participate and 144 were recruited (around 15-23% participation rate). Nevertheless, this quite low participation rate should be considered with caution because some women who were invited didn't participate because they couldn't be recruited (i.e. they were younger than 18 years, not fluent in French, had multiple pregnancy or medically assisted procreation). For instance, in France in 2010, 5-6% of births were resulting from a medically assisted procreation [START_REF] Blondel | Les naissances en 2010 et leur évolution en 2003[END_REF].

Moreover, one can reasonably assume that some women didn't participate because they delivery was impending.

Participants

Participants' (N = 144) age ranged from 21 to 41 years (M = 30.9 years, SD = 4.15). They were mostly married, in a civil solidarity pact (65.3%) or living as a couple (32.6%) and only 2.1% were single. They were well educated: 72.9% had at least 3 years of post-secondary education. They mainly had a high professional status: 41.1% were corporate executives, 39% were intermediate professionals and 19.9% were employees. Most of them were working women (80.6%), whereas some were unemployed (16.7%) or students (2.7%). Among the working women, the mean weekly work hours were 38.56 (SD = 7.39) and most of them were working 35 hours per week or more (90.5%). On average, they were 28.62 days away from the birth date (SD = 12.42). They were mainly primiparous (73.6%). Most multiparous women already had one child (86.8%) and some already had 2 or 3 children (13.2%). The youngest mean child age was about 3 years old (M = 35.32, SD = 13.47) ranging from 10 to 72 months (6 years).

Measures

Women were received individually in a quiet office of the maternity ward. They were given information regarding the study and signed an informed consent form. Socio-demographic information (age, number of children, educational level…) was gathered during the interview. Participants then completed a set of selfadministered questionnaires.

Intensive Mothering Ideology

The Mesure de L'ideologie du Maternage Intensif (MIMI) was administered. This scale is the French adaptation [START_REF] Loyal | Idéologie du maternage intensif en France : Adaptation et validation de l'IPAQ (Intensive Parenting Attitudes Questionnaire)[END_REF] of the Intensive Parenting Attitude Questionnaire (IPAQ) [START_REF] Liss | Development and validation of a quantitative measure of intensive parenting attitudes[END_REF], a tool designed to assess socio-normative constructions about motherhood, namely IMI. The MIMI contains 21 items assessing 6 dimensions of IMI: essentialism expresses the idea that mothers are the best caregivers for children (7 items); fulfillment expresses the idea that being a parent is a fulfilling, rewarding and consuming role (5 items); child-centrism conveys the idea that child-rearing should focus on the child's individual needs and rhythm (2 items); challenge expresses the idea that child-rearing is the hardest job in the world (2 items); sacrifice conveys the idea that parents should set aside many things, (3 items); and stimulation expresses the idea that children should be properly stimulated (2 items). Participants were asked to answer each item on a Likert scale ranging from 1 (disagree very strongly) to 6 (agree very strongly). A higher score is indicative of a stronger endorsement of the IMI component. Internal consistencies assessed with Cronbach's alpha were found to be satisfactory in two different samples comprising both mothers and mothers-to-be (N = 474 and N = 249) for essentialism (80-.83), fulfillment (.74-.81), child centrism (.70-.75), challenge (.60-.61), sacrifice (.61-.64) and stimulation (.56-.64) [START_REF] Loyal | Idéologie du maternage intensif en France : Adaptation et validation de l'IPAQ (Intensive Parenting Attitudes Questionnaire)[END_REF].

Breastfeeding Attitude and Intention

Participants were asked to rate their degree of accordance with the two following statements: "Breastfeeding one's child is a very good thing" and "I plan to breastfeed my child". Each item was offered with a Likert scale ranging from 1 (disagree very strongly) to 6 (agree very strongly).

Work Involvement

To assess work centrality, the method proposed by the Meaning of Work Team was used (Meaning of Work International Research Team, 1987). Participants were asked to share 100 points between 5 life domains (leisure, community, work, religion and family) according to how they mattered to them. Family (M = 45.84; SD = 11.9), work (M = 24.36; SD = 10.52) and leisure (M = 22.34, SD = 8.35) were the most important domains.

Community (M = 5.27; SD = 5.39) and religion (M = 2.46; SD = 5.46) were rarely considered as important. This ratio is referred to in the results and discussion as relative work centrality.

To assess work satisfaction, the Echelle de Satisfaction de Vie Professionnelle (ESVP) [START_REF] Fouquereau | Elaboration de l'Echelle de Satisfaction de Vie Professionnelle (ESVP) en langue française: Une démarche exploratoire[END_REF] was administered. This brief scale is composed of 5 items to be answered on a Likert scale ranging from 1 (strongly disagree) to 7 (strongly agree) with 4 being a middle point (neither agree nor disagree). A higher score is indicative of greater work life satisfaction.

The Beliefs about Consequences of Maternal Employment for Children (BACMEC) [START_REF] Greenberger | Beliefs about the consequences of maternal employment for children[END_REF][START_REF] Shibley Hyde | Beliefs about the consequences of maternal employment for children: Psychometric analyses[END_REF] was used. This scale was designed to assess perceptions of maternal employment as detrimental (cost, 11 items) or beneficial (reward, 13 items) to children. For the sake of brevity, only the cost dimension was retained because it was found to correlate more strongly with IMI than the benefit dimension [START_REF] Liss | Development and validation of a quantitative measure of intensive parenting attitudes[END_REF]. As this scale has never been used in French, an exploratory factor analysis (principal factor analysis) was performed on the translated version. All 11 items loaded on a single factor (loadings ranged from .66 to .82) explaining 55.15% of the variance. Cronbach's alpha was satisfactory (.92). Participants were asked to answer each item on a scale ranging from 1 (disagree very strongly) to 6 (agree very strongly). A higher score is indicative of the perception of maternal work as being detrimental to children.

Psychological Distress and Attachment

The French version of the Edinburgh Postnatal Depression Scale (EPDS) [START_REF] Cox | Detection of postnatal depression: Development of the 10-item Edinburgh Postnatal Depression Scale[END_REF][START_REF] Guedeney | Validation study of the French version of the Edinburgh Postnatal Depression Scale (EPDS): New results about use and psychometric properties[END_REF] was administered. This scale contains 10 items proposed with 4 possible responses rated from 0 to 3. A higher score is indicative of higher depressive symptoms. It is widely used in postpartum and pregnant women [START_REF] Boyd | Review of screening instruments for postpartum depression[END_REF][START_REF] Gibson | A systematic review of studies validating the Edinburgh Postnatal Depression Scale in antepartum and postpartum women[END_REF]. A cut-off of 11/12 is usually recommended in postpartum and pregnant women (Bennett, Einarson, Taddio, Koren, & Einarson, 2004b).

To assess anxiety symptoms, the Hospital Anxiety and Depression Scale or HADS [START_REF] Snaith | The Hospital Anxiety and Depression Scale[END_REF][START_REF] Zigmond | The Hospital Anxiety and Depression Scale[END_REF] was used. The HADS contains 7 items assessing depressive symptoms and 7 items assessing anxiety symptoms. Our goal was to assess anxiety symptoms so we used only the 5 items recommended by [START_REF] Straat | Methodological artifacts in dimensionality assessment of the Hospital Anxiety and Depression Scale (HADS)[END_REF]. A French adaptation of the HADS was made by [START_REF] Lepine | Evaluation of anxiety and depression among patients hospitalized on an internal medicine service[END_REF]. Each item has 4 possible responses rated from 0 to 3. A higher score is indicative of higher anxiety symptoms.

In order to assess attachment style, the Relationship Questionnaire [START_REF] Bartholomew | Attachment styles among young adults: A test of a four-category model[END_REF] was used. This 4-item scale is an adaptation of the measure designed by [START_REF] Hazan | Romantic love conceptualized as an attachment process[END_REF]. Participants were asked to assess their similarity on a Likert scale ranging from 1 (very much like me) to 7 (not at all like me), with 4 prototypes describing people with secure, dismissing, preoccupied or fearful attachment.

Social Desirability

Finally, in order to ensure that clusters would not be affected by a social desirability bias, Form A [START_REF] Reynolds | Development of reliable and valid short forms of the Marlowe-Crowne Social Desirability Scale[END_REF] of the Marlowe-Crowne Social Desirability Scale or MC-SDS [START_REF] Crowne | A new scale of social desirability independent of psychopathology[END_REF] was administered. This 11-item version of the MC-SDS is considered to be one of the best fitting versions of this scale [START_REF] Loo | Confirmatory factor analyses of the full and short versions of the Marlowe-Crowne Social Desirability Scale[END_REF]. A French adaptation was made by [START_REF] Blais | Validation of the French version of the Marlowe-Crowne measure of social desirability[END_REF]. Participants were asked to answer true or false to statements about themselves.

Statistical Analysis

Statistical analyses were conducted with SPSS version 20. Owing to the elimination of some outliers (Grubb's test), sample size was reduced to 139. A hierarchical cluster analysis was performed (Ward method, squared Euclidian distance) with 6 variables regarding IMI (essentialism, fulfillment, child-centrism, challenge, sacrifice and stimulation) and 3 variables regarding work (work-life satisfaction, relative work centrality and perceived costs of maternal employment). [START_REF] Aldenderfer | Cluster analysis[END_REF] delineated 5 principles that need to be respected when performing a cluster analysis. Authors should report the computer program, the similarity and the cluster method used. We have reported that information above. Authors should also explain the rationale used to determine the number of clusters and report evidence of their validity. The selection of the number of clusters was based on, in order of decreasing importance, the examination of the dendogram, the satisfactory sample size, the maximum number of differences provided on variables of interest, parsimony and clarity in interpretation. Finally, in order to assess the discriminant validity of clusters regarding external criteria (socio-demographic and psychological variables), mean comparison (Anova with Bonferroni post hoc comparison) and frequency comparisons (Fisher exact test (FET) with Bonferroni adjustment, p<.05) were performed. To avoid small expected frequency, we only used binomial variables in frequency comparisons (Appendix A). The major recommendations regarding cluster analysis and reporting were thus respected.

Results

Cluster Selection and Description

First, a hierarchical cluster analysis was carried out. Owing to the visual examination of the dendogram (Appendix B), classifications with 2, 3, 4, 5 and 6 clusters were initially retained. The classification with 6 clusters was dropped out because it contained one very small cluster (n = 8). Although the presence of a small cluster is not a problem in itself [START_REF] Clatworthy | The use and reporting of cluster analysis in health psychology: A review[END_REF] it might be a hindrance to performing the inferential analysis adequately to test cluster validity.

Mean comparison (Anova with Bonferroni post hoc comparison) were then conducted on the remaining classifications (2, 3, 4 and 5 clusters) and on the variables of interest (essentialism, fulfillment, child-centrism, challenge, sacrifice, stimulation, work life satisfaction, relative work centrality and perceived costs of maternal employment). The classifications with 2 and 3 clusters were not retained because they did not provide significant differences between clusters on relative work centrality and/or beliefs about the consequences of maternal employment on children. The 4 cluster and 5 cluster classifications provided significant differences on each variable of interest. After a careful examination, the 4 cluster classification was selected because it was more parsimonious and generated a clearer and more readable distinction between groups [START_REF] Bergman | The person-oriented approach: A short theoretical and practical guide[END_REF] (Table 2).

INSERT TABLE 2 AROUND HERE

Clusters 1 and 2 were marked by high endorsement of IMI, especially fulfillment and stimulation for Cluster 2. Nevertheless, they were different regarding beliefs in the negative effect of maternal employment on children: women in Cluster 2 held that belief whereas those in Cluster 1 did not. Clusters 3 and 4 were both marked by lower endorsement of IMI but they were different regarding work involvement (satisfaction and centrality). Women in Cluster 4 were dissatisfied with their work life and did not consider it as central whereas those in Cluster 3 considered it as more central and satisfactory (but no more than those in Clusters 1 and 2).

Participants are thus referred to hereafter as follows: "Devoted" i.e. women devoted to IMI (Cluster 1, 27%); "Devoted / worried" i.e. women devoted to IMI and worried about the consequences of maternal work on children (Cluster 2, 13%); "Non-devoted" i.e. women not devoted to IMI (Cluster 3, 35%); "Non-devoted / disengaged" i.e. women not devoted to IMI and disengaged (low satisfaction and centrality) from work (Cluster 4, 25%).

Cluster Validity

Mean comparison (Anova with Bonferroni post hoc comparison) were performed regarding clusters and socio-demographic variables (Table 3). Women in the various clusters did not differ regarding their age, spouse age, number of hours worked or days before term. Women in Cluster 2 (devoted/worried) reported their spouse worked fewer hours than did the women in Cluster 1 (devoted). Moreover, when they already had at least one child, women in Cluster 3 (non-devoted) had a significantly older last child than those in Cluster 1 (devoted).

Mean comparison (Anova with Bonferroni post hoc comparison) were also performed regarding clusters and psychological variables (Table 3). Women in the various clusters did not differ regarding, secure attachment, dismissing attachment, fearful attachment or social desirability. Nevertheless, women in Cluster 2 (devoted/worried) exhibited significantly more depressive symptoms than those in Cluster 3 (non-devoted) and more preoccupied attachment than those in Cluster 1 (devoted). Moreover, mean comparison regarding anxiety might be considered cautiously as nearly significant (p=.06) and the post hoc comparison was significant between Clusters 1 and 2 (p<.05) indicating that women in Cluster 2 might also exhibit more anxiety symptoms.

INSERT TABLE 3 AROUND HERE

Finally, frequency comparisons (Fisher exact test (FET) with Bonferroni adjustment p<.05) were performed. As stated previously, to avoid small expected frequency, we used only binomial variables in frequency comparisons (Appendix A). Significant differences between expected and observed frequencies and corresponding percentages are presented in Table 4. Women in Cluster 1 (devoted) more often than expected had a moderate level of education. Women in Cluster 2 (devoted/worried) were more often than expected planning on going back to work after a at least 6-month leave, not planning on breastfeeding their baby and exceeding cutoff of depression. Women in Cluster 3 (non-devoted) less often than expected had a very positive attitude towards breastfeeding (i.e. answering totally agree) and a negative reaction when discovering they were pregnant. Conversely, women in Cluster 4 (non-devoted/disengaged) more often than expected had a negative reaction when discovering their pregnancy. No differences were observed between clusters according to women's parity, pregnancy planning, employment status or professional level of themselves or their spouse (frequencies for those variables in the whole sample are reported in Appendix A)

INSERT TABLE 4 AROUND HERE

Discussion

Our hypotheses regarding cluster definition (Table 1) were partly confirmed. Clusters 1 (devoted) and Cluster 2 (devoted/worried) might be seen as an expression of neutralization cognitive acrobatic (hypothesis 1a): these women showed high endorsement to IMI and no lower work involvement, they want to meet the demands of both domains. Thus, hypothesis 1a is partly confirmed but results are more nuanced than expected due to differences in worries about consequences of maternal employment for children (low in Cluster 1 and high in Cluster 2). Moreover, Cluster 3 (non-devoted) might be seen as an expression of Separation cognitive acrobatic (hypothesis 1d): these women did not endorse IMI and didn't have a low work involvement; they were driven primarily by their worker identity. Thus Hypothesis 1d was confirmed. Cluster 4 (non-devoted/disengaged) might be seen as an expression of Disengagement cognitive acrobatic (hypothesis 1b), these women did not endorse IMI and had also a low work involvement. Thus hypothesis 1b is confirmed. Finally, the selection cognitive acrobatic (hypothesis 1c), i.e. women who endorsed IMI and were not involved in work, was not observed in our sample. Hypothesis 1c is not confirmed. Presumably, this might be because this kind of cognitive acrobatics (akin to the concept of mommy track [START_REF] Smith | A maze of metaphors around glass ceilings[END_REF]) was only observed in stay-athome mothers [START_REF] Johnston | Cognitive acrobatics in the construction of worker-mother identity[END_REF] and in our sample, most women were working (83%), working many hours (M = 38.53; SD = 7.43) and had mainly a high or intermediate professional level (78.7%) (Appendix A).

Our hypotheses about cognitive acrobatics and psychological distress were only partly confirmed. Hypothesis 2a stated that psychological distress would be more important for neutralization and disengagement cognitive acrobatics. Indeed, Psychological distress was found to be higher in Cluster 2 (devoted/worried, neutralization), i.e. they exhibited more depressive symptoms (and exceeded more than expected cut-off), preoccupied attachment and presumably anxiety symptoms. However, women in cluster 1 (devoted, neutralization) didn't show such distress. Women in Cluster 4 (non-devoted/disengaged, disengagement) didn't exhibit higher psychological distress per se but had frequently a negative reaction to pregnancy. Thus, hypothesis 2a is only partly confirmed. Hypothesis 2b stated that psychological distress would be less important for women who carry out selection and separation cognitive acrobatics. Indeed, women in Cluster 3 (non-devoted, separation) showed few depressive symptoms and negative reaction to pregnancy. Nevertheless, the Selection cognitive acrobatic remains unexplored as no such cluster was observed. Thus, hypothesis 2b is only partly confirmed.

Clusters characterized by IMI endorsement seemed to have a lower socioeconomic status: i.e lower educational level in Cluster 1 (devoted, neutralization) and few spouse work in Cluster 2 (devoted/worried, neutralization). This is in accordance with results showing that IMI might be endorsed more by women with lower educational level [START_REF] Loyal | Idéologie du maternage intensif en France : Adaptation et validation de l'IPAQ (Intensive Parenting Attitudes Questionnaire)[END_REF] as traditional gender ideology [START_REF] Davis | Gender ideology: components, predictors, and consequences[END_REF]. These results are also consistent with surveys from various European countries, showing that the cost of motherhood in women's professional lives varies depending on their professional status, social class, and more generally on the socio-economic context [START_REF] Romito | Studying work, motherhood and women's well-being: A few notes about the construction of knowledge[END_REF].

Regarding Cluster 2 (devoted/worried, neutralization) more than one third (38.9%) of women exceeded the cut-off score for depression. This is much higher than the prevalence observed in the whole sample (12.2%), in Clusters 1, 3 and 4 (respectively 7.9%, 6.1%, 11.8%), and in the literature on pregnant and postpartum women (Bennett et al., 2004a;[START_REF] O'hara | Rates and risk of postpartum depression: A meta-analysis[END_REF]. This high prevalence seems more congruent with that reported in pregnant women with low socio-economic status (Bennett et al., 2004a). They might also exhibit higher anxiety symptoms and this is of importance knowing how comorbid depression and anxiety is a severity indicator in the general population (Rivas-Vazquez, Saffa-Biller, Ruiz, [START_REF] Reynolds | Development of reliable and valid short forms of the Marlowe-Crowne Social Desirability Scale[END_REF]) and in postpartum women [START_REF] Farr | Postpartum anxiety and comorbid depression in a population-based sample of women[END_REF][START_REF] Matthey | Diagnosing postpartum depression in mothers and fathers: Whatever happened to anxiety[END_REF]. Moreover, women in Cluster 2 exhibited higher preoccupied attachment. This seems coherent with [START_REF] Villalobos | Motherload: Making It All Better in Insecure Times[END_REF] qualitative work regarding insecurity and intensity seeking in motherhood. Preoccupied attachment is characterized by positive model of others and negative model of oneself [START_REF] Bartholomew | Attachment styles among young adults: A test of a four-category model[END_REF]. For Bartholomew & Horowitz (1991, p. 227) "this combination of characteristics would lead the person to strive for self-acceptance by gaining the acceptance of valued others". This might be problematic if women do not receive much support and appreciation from their partner and other family members or if they face difficulties that might threaten their identity as "good" mothers (breastfeeding problems, difficulty to soothe baby's crying…). Women in Cluster 2 (devoted/worried, neutralization) were also more often than expected planning to go back to work more than 6 months after the birth. Nevertheless, they were less often than expected planning on breastfeeding their child. This result is in accordance with studies showing that women with higher depressive symptoms [START_REF] Figueiredo | Breastfeeding and postpartum depression: State of the art review[END_REF] and lower social status [START_REF] Kersuzan | Prévalence de l'allaitement à la maternité selon les caractéristiques des parents et les conditions de l'accouchement[END_REF] are less likely to initiate and maintain breastfeeding. One should note that 38.9% of women in Cluster 2 reported they might not breastfeed their baby (totally disagree, disagree, somewhat disagree) whereas in the whole sample, only 20.1% of women did so. Nevertheless, 66.7% of women in Cluster 2 had a highly positive attitude towards breastfeeding (totally agree). This might put them in an uncomfortable situation because they might not provide what they strongly consider as the best for their children [START_REF] Knaak | Contextualising risk, constructing choice: Breastfeeding and good mothering in risk society[END_REF][START_REF] Lee | Breastfeeding advocacy, risk society and health moralism: A decade's scholarship[END_REF].

Women in Cluster 1 (devoted, neutralization) were quite similar to women in Cluster 2 (devoted/worried, neutralization) but didn't exhibit psychological distress. Both clusters were characterized by neutralization cognitive acrobatics, i.e. high level of IMI endorsement and work involvement, but women in Cluster 1 didn't believe that maternal work have negative consequences for children as women in Cluster 2 did, so they might be protected from experiencing massive incongruence between their beliefs and their work status [START_REF] Kroska | Exploring the consequences of gender ideology -work discrepancies[END_REF][START_REF] Mchale | You can't always get what you want: Incongruence between sex-role attitudes and family work roles and its implications for marriage[END_REF], unlike women in Cluster 2.

Women in Cluster 3 (non-devoted, separation) appear to be protected from distress, (low level of depression and few negative reaction to pregnancy). Being detached from IMI and engaged in a pleasant and central work life might be regarded as a protective pattern for mothers/mothers-to-be. Interestingly, even if they did not plan on breastfeeding more or less than expected, most of them were not completely positive (61.2% not answering totally agree) about breastfeeding. This might be understood as a more relaxed attitude towards pressures to perform motherhood the "right way". Indeed, many scholars have observed that breastfeeding is increasingly considered as a measure of mothering quality [START_REF] Knaak | Contextualising risk, constructing choice: Breastfeeding and good mothering in risk society[END_REF][START_REF] Lee | Breastfeeding advocacy, risk society and health moralism: A decade's scholarship[END_REF] and as the "proper and 'moral' choice" (Knaak, 2010, p. 346). Moreover, when multiparous, they had an older child. Presumably, when a child grows up, women might feel freer to distance themselves from IMI. Moreover, women devoted to IMI might be more inclined to space pregnancies closer together. As taking care of a young child during pregnancy might be regarded as a source of stress [START_REF] Grant | Maternal anxiety during the transition to parenthood: A prospective study[END_REF], this might partly explained the lower distress exhibited by women in Cluster 3. Of note, even if women in Cluster 3 exhibited the lowest level of endorsement of IMI, an item-level analysis on the MIMI shows that they do not reject it per se. Among the 21 items of the MIMI, 14 (67%) were endorsed (somewhat agree, agree, agree very strongly) by more than 50% of the women.

For instance, most women in Cluster 3 were in agreement with "Children's needs should come before their parents." (73.4%, child-centrism) or with "Mothers are often more comfortable with babies than fathers." (71.3%, essentialism). This underlines the fact that IMI, as defined by [START_REF] Hays | The cultural contradictions of motherhood[END_REF], could be regarded as a dominant ideology that prevails even in women who endorse it at the lowest level.

Finally, women in Cluster 4 (non-devoted/disengaged, disengagement) were not at risk of distress per se but had often a negative reaction to pregnancy. They neither experience a central and satisfactory work life nor a normative commitment to motherhood, which might be a source of meaning and purpose. Conversely, one can argue that this disengagement from both domains might be a manifestation of distress.

Interestingly, the percentages of working women did not differ significantly between clusters.

Regarding work and family life, two competing hypothesis have been proposed [START_REF] Romito | Studying work, motherhood and women's well-being: A few notes about the construction of knowledge[END_REF]: the enhancement hypothesis, stating that positive commitment on one area provides women with the possibility to cope with dissatisfaction in the other area, and the scarcity hypothesis, stating that combination of different tasks and roles represents a source of stress that can generate distress [START_REF] Allen | Consequences associated with work-to-family conflict: a review and agenda for future research[END_REF]. Our results suggest, in accordance with previous work [START_REF] Barnett | Women and multiple roles: Myths and reality[END_REF][START_REF] Romito | Studying work, motherhood and women's well-being: A few notes about the construction of knowledge[END_REF], that both hypothesis might not be mutually exclusive. In other words, trying to explain working women's wellbeing should not be done without considering the degree of congruence between values, wishes and actual occupational status [START_REF] Romito | Studying work, motherhood and women's well-being: A few notes about the construction of knowledge[END_REF].

Indeed, it has previously been shown that the incongruence between gender ideology and work arrangements might be a source of distress [START_REF] Kroska | Exploring the consequences of gender ideology -work discrepancies[END_REF][START_REF] Mchale | You can't always get what you want: Incongruence between sex-role attitudes and family work roles and its implications for marriage[END_REF]. For instance, women who firmly adhere to the idea that childcare is the most important and fulfilling activity, that a child's needs are a priority and that mothers are the essential and best caregivers might feel reluctant or uncomfortable at the idea of going back to work. This might be especially true if they do not receive social support or if they perceive their child as temperamentally fragile or difficult.

This study has some limitations. First, since it is cross-sectional, one cannot draw conclusions regarding causality. Do worries about the effects of maternal work on children cause higher depressive symptoms? Do depressive symptoms impact the perception of maternal work in a negative way? Further research, with longitudinal design, is needed. Moreover, participation rate was rather low and sample size was moderate and led to the use of dichotomous variables in frequency comparisons in order to avoid small expected frequencies. In addition, the sample was mainly composed of rather privileged women, highly educated with skilled jobs. It would be interesting to conduct the same kind of analysis in a more disadvantaged population. Moreover, the selection cognitive acrobatic (high endorsement of IMI and low work involvement) could be studied in samples with more stay-at-home women. Nevertheless in France, most women are working regardless of whether they are childless (80.2%) have one child (79.7%) or two children (76.5%). Only women with 3 children or more are known to work less (55.5%) (Institut National de la Statistique et des Etudes Economiques, 2008) and family with 3 children or more are not frequent (9.9%) (Institut National de la Statistique et des Etudes Economiques, 2011). In sum, getting 83% of working women is presumably quite representative of the French feminine population. Nevertheless, in our sample, 90.5% of working women worked 35 hours a week or more (full time), whereas in France working women are often working part time (from 25% if they are childless to more than 50% if they have three child or more ) [START_REF] Pak | Le travail à temps partiel[END_REF]. Finally, using the complete BACMEC (i.e. the cost and benefit dimensions) would have been an interesting way to explore how women might reframe their work as positive for their children in a way that allows them both to work and to stick to the main discourse regarding mothering [START_REF] Johnston | Constructing the good mother : The experience of mothering ideologies by work status[END_REF][START_REF] Johnston | Cognitive acrobatics in the construction of worker-mother identity[END_REF]. For instance, working women may reframe their work as a way to ensure that their child receives a good environment (activities, leisure, education…).

Nevertheless, this study has several strengths. First, performing a cluster analysis is to provide results regarding patterns shared by sub-groups of women rather than variables themselves and to reconcile the nomothetic (variable-centered, "seeing the forest") and idiographic (person-centered, "seeing the tree") approaches [START_REF] Clatworthy | The use and reporting of cluster analysis in health psychology: A review[END_REF]. The five important principles for performing a cluster analysis adequately [START_REF] Aldenderfer | Cluster analysis[END_REF] were respected. To our knowledge, this is the first study to use this kind of research design and it gives interesting results regarding the balance between normative aspects of motherhood, a rather understudied field, and work involvement. Finally, since an assessment of social desirability was included, one can be reasonably sure that social desirability probably did not account for differences between clusters.

In conclusion, different cognitive acrobatics, i.e. patterns of endorsement of IMI and work involvement

  Family and work monopolized on average 2/3 of participants points (M = 70.20, SD = 11.08). A work/family ratio was obtained. A higher ratio (>1) is indicative of a high importance of work compared to family, whereas a lower ratio (<1) is indicative of a low importance of work compared to family. Values ranged from 0 to 1.43.

  Note. Cluster 1 (devoted, N = 38), Cluster 2 (devoted/worried, N = 18), Cluster 3 (non-devoted, N = 49) and Cluster 4 (non-devoted/disengaged N = 34) BACMEC = Beliefs About Consequences of Maternal Employment for Children. a, b,c,d : designate couple of groups which are significantly different at p<.05. Regarding Essentialism, Cluster 1 was different from Clusters 2, 3 and 4.

Table 1 .

 1 Hypotheses Summary.

	IMI Work Cognitive acrobatics Distress
	+	+	Neutralization 1a
			+ 2a
	-	-	Disengagement 1b
	+	-	Selection 1c
			-2b
	-	+	Separation 1d
	Note. IMI: Intensive Mothering Ideology

Table 2 .

 2 Mean comparison (Anova) with Post-hoc Comparisons (Bonferroni, p<.05) Regarding Clusters and

	Variables of Interest (N=139)
			Cluster 1	Cluster 2	Cluster 3	Cluster 4
		Anova
			M (SD)	M (SD)	M (SD)	M (SD)
	Ideology	Essentialism F(3)=15.93; p<.01 3.67 (0.57) abc 3.20 (0.56) a 2.78 (0.64) b 3.05 (0.62) c Fulfillment F(3)=28.03; p<.01 5.24 (0.51) ab 5.32 (0.46) cd 4.37 (0.51) ac 4.58 (0.57) bd
	Mothering	Child-Centrism F(3)=13.40; p<.01 4.84 (0.82) ab Challenge F(3)=15.77; p<.01 5.21 (0.64) abc 4.42 (1.12) a 4.19 (0.93)	3.61 (0.96) a 4.04 (0.98) b	4.06 (0.89) b 3.93 (0.92) c
	Intensive	Sacrifice F(3)=7.95; p<.01 3.20 (0.55) abc 2.59 (0.75) a Stimulation F(3)=6.89; p<.01 5.29 (0.66) a 5.58 (0.55) bc 4.71 (1.01) ab 4.96 (0.67) c 2.48 (0.73) b 2.67 (0.80) c
		Satisfaction F(3)=55.25; p<.01 5.00 (1.33) a	4.59 (0.80) b	5.33 (0.91) c 2.60 (0.78) abc
	Work	Centrality F(3)=4.80; p<.01	0.55 (0.21)	0.55(0.34)	0.63(0.28) a	0.41(0.21) a
		BACMEC F(3)=27.81; p<.01 1.47 (0.39) a 2.74 (0.69) abc 1.74 (0.58) b	1.50 (0.46) c

Table 3 .

 3 Mean comparison (Anova) with Post-hoc Comparisons (Bonferroni, p<.05) Regarding Clusters and Sociodemographic and Psychological Variables (N=139).

		Cluster 1	Cluster 2	Cluster 3	Cluster 4
	Anova	M (SD)	M (SD)	M (SD)	M (SD)

(3) = 3.42; p <.05 1.61 (1.59) a 3.22 (2.10) a

  designate couple of groups which are significantly different at p<.05.

					2.43 (1.79)	2.12 (2.04)
	Fearful Attachment	F(3) = 1.31; p = .28	1.58 (1.47)	2.61 (2.17)	2.06 (2.08)	2.24 (2.19)
	Social Desirability	F(3) = 1.80; p = .15	5.97 (2.24)	6.00 (2.22)	5.76 (2.38)	4.82 (2.49)
	Note. Cluster 1 (devoted, N = 38), Cluster 2 (devoted/worried, N = 18), Cluster 3 (non-devoted, N = 49) and
	Cluster 4 (non-devoted/disengaged N = 34)
	Significant mean differences are in bold.

a

Table 4 .

 4 Frequency Comparisons (Fisher exact test, FET) with Bonferroni adjustment (p<.05) (N = 139) Cluster 1 (devoted, N = 38), Cluster 2 (devoted/worried, N = 18), Cluster 3 (non-devoted, N = 49), Cluster 4 (non-devoted/disengaged, N = 34) and Total (N = 139) a Post-secondary Education ≤ 2 Years ; b ≥ 6 Months After Birth ; c Totally disagree, disagree, somewhat disagree ; d Totally agree, e EPDS (11/12) ; f Annoyed or ambivalentSignificant differences (p<.05) between observed and expected differences are in bold ;(+) More than expected ;

		FET	Cluster 1 Cluster 2 Cluster 3 Cluster 4	Total
	Lower Educational Level a	F = 7.89; p<.05	42.1% (+)	33.3%	18.4%	17.6%	26.6%
	Delayed Back to Work b	F = 7.51; p<.06	19.4%	50% (+)	20.4%	16.1%	23.1%
	Not Planning to Breastfeed c	F = 6.47; p<.09	21.1%	38.9% (+)	20.4%	8.8%	20.1%
	Breastfeeding Positive Attitude d	F = 7.47; p<.06	63.2%	66.7%	38.8% (-)	44.1%	50.4%
	Exceed Depression Cut-off e	F = 10.94; p<.01	7.9%	38.9.% (+)	6.1%	11.8%	12.2%
	Negative Reaction to Pregnancy f F = 11.63.; p<.01	23.7%	16.7%	4.1% (-)	29.4% (+) 17.3%
	Note. (-) Less than expected.

Appendix B. Hierarchical Cluster Analysis (Ward Method, Squared Euclidian Distance)

can be observed in pregnant women. Those different patterns seem to be linked with socioeconomic factors and emotional distress. Attention should be paid to the values and beliefs women hold when trying to understand how they cope with work and family life demands.

Compliance with Ethical Standards

The authors declare that they have no conflict of interest.

This study was approved by a national informatics right committee (https://www.cnil.fr/) and a regional ethic committee (http://www.cpp-soom3.u-bordeaux2.fr/). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent was obtained from all individual participants included in the study.


Libert Brice Tonfack

Hanane Moummou

Alain Latché

Emmanuel Youmbi

Mohamed Benichou

Jean-Claude Pech

Benoît Van Der Rest

The plant SDR superfamily: involvement in primary and secondary metabolism

Keywords: Short-Chain Dehydrogenase -Oxidoreductase -Multigenic Family -Primary and Secondary Metabolism -Plant -Arabidopsis thaliana Abscisic Acid, ACP: Acyl Carrier Protein, BKR: Beta-Keto (Acyl Carrier Protein) Reductase, CCR: Cinnamoyl Coenzyme A Reductase

Short-chain dehydrogenases/reductases (SDRs) comprise a large family of NAD(P)(H)-dependent oxidoreductases represented in plant kingdom by around 190 members in Arabidopsis. Here we will focus on the so-called 'classical' SDRs that account for about half of the SDRs and are characterized by a core structure of 250 amino acids and the conservations of specific motifs (cofactor binding site, catalytical residues). Although the 'classical' SDR family is highly divergent, an inventory of SDR from the model plant Arabidopsis thaliana genome reveals that it contains both large subfamilies with numerous members that share significant homologies (e.g. tropinone reductase, menthone/salutaridine reductase, NAD-dependent dehydrogenase) and small subfamilies with a limited number of members (e.g. protochlorophyllide reductase, β-ketoacyl-acyl carrier protein reductase and enoyl-reductase). The involvement of SDRs in plant metabolism illustrates the large functional diversity of the SDR superfamily's members. Functions of SDR encompass many aspects of primary (lipid synthesis, chlorophyll biosynthesis or degradation) and secondary (terpenoids, steroids, phenolics and alkaloids) metabolism. The present paper aims at reviewing the metabolic functions where the role of SDR has been documented and at discussing their phylogenetic diversification and structural features.

INTRODUCTION

Short-chain dehydrogenases/reductases (SDRs) perform NAD(P)(H)-dependent oxidoreduction reactions together with mediumchain alcohol dehydrogenases and aldo-keto reductases. It has been estimated that 25% of the identified dehydrogenases belong to the SDR superfamily with 47000 primary structures [1]. This ancient family, found in all domains of life (Archea, Eukaryotes, Prokaryotes) is characterized by a low sequence conservation, but several common properties [2,3]: (i) a conserved 3D structure with a common α/β folding pattern characterized by a 'Rossman-fold' β-sheet with helices on either sides, (ii) an N-terminal dinucleotide cofactor binding motif, (iii) an active site with a catalytical residue motif YxxxK, and (iv) a variable substrate binding region at the C-terminal region of the protein. With the release of the genome sequences of a number of living organisms, the availability of around 300 crystal structures and the identification of many enzymatic functions, much attention was given to classify the members of the superfamily on the base of the primary sequences, structures and functions [1,3,[4][5][6][7][8]. These efforts have led to the discrimination of five types of SDR: the 'classical' type, consisting of approximately 250 amino acids, the 'extended' type that has an additional 100residue domain in the C-terminal region, the 'intermediary' and 'divergent' types, which harbour modifications on the cofactor and active sites motifs and the 'complex' SDR which are usually a part of large multi-domain enzymes, such as mammalian fatty acid synthases or bacterial polyketide synthases. It has become obvious that SDRs participate in many aspects of primary and secondary metabolism and are not only restricted to carbonyl-alcohol oxidoreduction, but comprise also isomerase, epimerase, dehydratase and decarboxylase activities. However, in all cases, the overall enzymatic reaction requires an oxidoreductive step. Among higher eukaryotes, the SDRs (either extended or classical) are highly represented in the plant kingdom. In Arabidopsis thaliana, Kavanagh et al. [3] listed 149 'nonredundant' SDR enzymes (all families included), in contrast with animals (46 in rat, 71 in human or 82 in fruit fly) or yeast (25 SDRs).

The present paper is aimed at providing an overview of the diversity of the SDR super-family with main focus on 'classical' SDRs and at reviewing the different metabolic pathways where they are involved. The question will be addressed of how SDR diversification has participated in the development of the large repertoire of chemical compounds encountered in plants.

OVERVIEW OF PLANT 'CLASSICAL' SDR 1.1 CLUSTERING ARABIDOPSIS THALIANA SDRS

The genome sequencing and the annotation data available for the model plant Arabidopsis thaliana [9,10] provide a reliable set of data useful for a global inventory of a multigenic family in a plant species. Contrary to 'extended' or 'divergent' SDR, the classical SDR are defined by a single Pfam (PF00106) or INTERPRO (IPR002196). Hence, Arabidopsis genes coding for the classical SDRs were sorted and presented in a global clustering tree (Fig. 1). In order to give a better functional overview of plant SDRs, functionally-characterized SDRs of other plant species have been integrated together with the Arabidopsis genes. Since SDRs are a very ancient superfamily (probably polyphyletic) and the homologies between subfamilies are limited, the clustering tree does not necessarily reflect the overall phylogenetic relationships. However, within subfamilies, the tree clearly illustrates the existence of several clades: a large cluster of NAD-dependent dehydrogenase (Fig. 1B), which counts up to 11 genes in Arabidopsis genome, a cluster called HSD (Hydroxysteroid Dehydrogenase, Fig. 1C) with 8 different genes in Arabidopsis, the tropinone reductase cluster with 15 Arabidopsis genes (Fig. 1D), the Menthone/Salutaridine Reductase cluster, with 6 Arabidopsis genes (Fig. 1E), and the Protochlorophyllide Reductase (POR) cluster (Fig. 1F), with 3 Arabidopsis genes.

FUNCTIONAL DIVERSITY OF PLANT SDR

Traditionally, an opposition is made between primary and secondary metabolites. Primary metabolites are encountered in all plants and are involved in essential metabolic pathways such as lipid, sugar, nucleic acid and amino acid biosynthesis or degradation pathways, and also all the metabolic functions linked to photosynthesis. Secondary metabolites are perceived as compounds involved in environmental interactions such as defence against biotic agents (fungi, viruses, herbivores, insects), competition between plants (allelopathic agents), attraction of pollinators and seed-dispersing agents and adaptation to abiotic stresses [START_REF] Croteau | Biochemistry & Molecular Biology of Plants[END_REF].

Figure 1 shows that most of the enzymes involved in primary metabolism (β-ketoacyl-ACPreductase or enoyl-ACP-reductase in lipid biosynthesis, chlorophyll degradation, folate salvage) exist as a single copy gene. On the contrary, the four subfamilies detached from the main phylogenic tree (Fig. 1B, C, D andE) which are involved in the main routes of secondary metabolism (phenolics, isoprenoids and alkaloids) are largely diversified and the genes annotated have very precise functions (Datura stramonium or Solanum tuberosum tropinone reductase, Papaver somniferum salutaridine reductase, Forsythia x intermedia secoisolariciresinol dehydrogenase, Mentha piperita isopiperitenol dehydrogenase, menthone reductase, (-)-isopiperitenol/(-)-carveol dehydrogenase). Besides, several genes in Arabidopsis are located in adjacent positions, suggesting that these multigenic families may have evolved by duplication events. The significance of the multigenic families may be analysed in two ways: either there are cases of functional redundancy, but the genes are differentially expressed; or the emergence of multigenic families served as a template for chemical diversification: random mutations and selection leading to the emergence of new metabolic pathways.

FUNCTIONS OF SDR

2.1.1.1.Fatty acid synthase

The overall pathway of fatty acid biosynthesis is roughly identical in all living organisms. However, in plants, fatty acid synthase (named FAS II) is composed of separate soluble enzymes carrying single enzymatic reaction which are localized in the plastids, while in animal and yeast fatty acid synthase (FAS I) is composed of one or two multifunctional polypeptides. In the synthesis of lipids there are two reduction steps catalysed by two SDRs, a β ketoacyl-ACP reductase (BKR) with a function similar to bacterial FAB G (AT1G24360.1 in Arabidopsis) and an enoyl-ACP reductase (ENR) with a function similar to bacterial FAB I (AT2G05990.1 in Arabidopsis). BKR is NADPH-dependent while ENR is NADH-dependent [START_REF] Ohlrogge | [END_REF]14]. The fine crystal structure of the two reductases of Brassica napus has been determined. It reveals that the two enzymes are homotetramers with each subunit having a dinucleotide-binding fold. BKR harbours a triad of Sr154, Tyr167 and Lys171 residues in the active site characteristic of the SDR family [15] while ENR does not have the catalytic triad but is believed to utilize conserved tyrosine and lysine residues for catalysis [16]. Primary sequences analyses reveal that this function is probably conserved in all plant kingdom, a conserved orthologue being found in one or two copies in every sequenced genomes (Os08g23810.1 and Os09g10600.1 in Oryza sativa; Pp1s29252V2.1 and Pp1s9954V2.1 in Physcomitrella patens). In the case of BKR, the sequence displays also a high homology with the cyanobacteria Synechocystis (55% identity between At1g24360.1 and P73574), in agreement with the endosymbiotic origin of the plastids.

Fatty acid elongase

Very long chain fatty acids are biosynthesized by an endoplasmic reticulumlocalized enzyme complex, named fatty acid elongase comprising a β-ketoacyl reduction as observed for de novo fatty acid synthesis [17]. Two β-ketoacyl reductase genes (GL8a and GL8b) belonging to the SDR family have been isolated and characterized in maize [18] and one in Brassica napus [19]. There are two potential Arabidopsis BKRs in the fatty acid elongase cluster, AtKCR1 (At1g67730) and AtKCR2, (At1g24470) but functional characterization indicated that only AtKCR1 was involved in microsomal fatty acid elongation [20]. Even if the reticulum β-ketoacyl reductase catalyses reactions similar to fatty acid synthase BKR, its sequences remain distant, suggesting that these two mechanisms emerged independently during evolution. This 'independent' evolution is even more obvious in the case of the enoyl-reductase reaction, catalysed in the reticulum by CER10 (At3g55360, [21]) which does not harbour any signature (PF00106, PF01073 or PF01370) of typical SDR. At last, the high similarity between yeast and plant fatty acid elongase complexes support the hypothesis of an ancestral eukaryotic elongation system, contrary to FAS-II which probably emerged as a result of plastid endosymbiosis.

Chlorophyll biosynthesis

SDR members are involved in the biosynthesis of chlorophyll by participating in the conversion of protochlorophyllide a into chlorophyllide a. This conversion is performed by a plastid-targeted NADPH:protochloropyllide oxidoreductase A (POR). Several isoforms of the protein are present in the POR clade (Fig. 1F). There are three genes encoding POR proteins in Arabidopsis, PORA, B and C that share 84-89% identity and that exhibit functional redundancy [22].

In addition an enzyme belonging to the extended SDRs, 3,8-divinyl protochlorophyllide a 8-vinyl reductase (DVR) participates in the synthesis of monovinyl derivatives of chlorophyll by performing reduction of the 8-vinyl group to an ethyl group on the tetrapyrrole ring [23]. DVR is a single-copy gene having sequence similarity to isoflavone reductases. As observed with plant FAS-II (BKR), all POR proteins are also closely related to cyanobacterial POR (Synechocystis Q59987.2, 55% identity with Arabidopsis POR A). In the case of DVR, an orthologue copy is also found in cyanobacteria (Synechococcus), but only in certain classes which produce monovinyl chlorophyll [23].

Chlorophyll degradation

Chlorophyll b is the major pigment of Light-Harvesting Complexes LHCII. The conversion of chlorophyll b to 7-hydroxymethylchlorophyll a is the first step of chlorophyll degradation and is catalysed by the chlorophyll b reductases Non Yellow Coloring (NYC1) and NYC1-like (NOL), two SDR-type enzymes [24][25]. Both proteins exhibit Chlorophyll b reductase activity in rice (Q5N800.1 and Q84ST4.1) and in Arabidopsis (At4g13250.1 and At5g04900.1). The two proteins interact in vitro, which suggests that they may form a complex that acts as Chl b reductase.

Folate synthesis

Folates are a group of essential dietary compounds referring to all derivatives of tetrahydrofolic acid, a water-soluble vitamin B (B9). They are acting as co-factors in one-carbon metabolism. Folates undergo oxidative cleavage, releasing a pterin aldehyde moiety which is re-used in folate biosynthesis after reduction of the aldehyde group. The reduction can be performed by several NADPH-dependent aldehyde reductases having broad-specificity towards diverse aromatic and aliphatic aldehydes. A gene of Arabidopsis (At1g10310) has been identified whose corresponding recombinant protein exhibited non specific pterin aldehyde reductase (PterAR) activity [26]. Interestingly, the recombinant protein encoded by a gene located in a neighbour cluster (At4g20760) proved to be inactive towards pterin aldehydes.

Protein associated with plastid import translocon (Tic32)

A member of the SDR family, Tic32 is a component of the protein import translocon of the inner envelope of chloroplast (Tic). The protein interacts with other members of the translocon and could function as a redox sensor, but its molecular substrate is unknown [27]. Originally described in pea (Pisum sativum), Tic32 is very similar to a cluster of 5 Arabidopsis SDRs (At4g23420, At4g23430, At4g11410, At5g02540, At2g37540, Fig. 1). Only At4g23430 encodes a protein with a predicted chloroplastic peptide signal at the Nterminal extremity, but none of these genes have been characterised yet.

SECONDARY METABOLISM

Steroids

In animals, the diversity of SDR partly relies on hydroxysteroid metabolism. On the SDR classification proposed by Kallberg et al. [1], enzymes involved in hydroxysteroids metabolism are found in 15 distinct subfamilies (SDR9C, SDR11E, SDR12C, SDR13C, SDR16C, SDR26C, SDR28C, SDR30C, SDR31E, SDR37C, SDR47C, SDR60E, SDR75U, SDR119C, SDR133E). In plants, only three (SDR31E, SDR75E, SDR119C) comprise genes encoding SDRs putatively involved steroids metabolism.

3-β-hydroxysteroid dehydrogenase-decarboxylase (3β-HSD/D)

Sterols are commonly found in all eukaryotic cell membranes. Sterol biosynthesis implies the removal of two methyl groups at the C-4 position. In plants, this removal is carried out by the successive action of a sterol C-4 methyl oxidase, a 4-α-carboxysterol-3β-hydroxysteroid dehydrogenase/C-4 decarboxylase (3β-HSD/D) and a NADPH-dependent 3-oxosteroid reductase. Rahier et al. [28,29] recently characterized two NADdependent Arabidopsis 3β-HSD/D (At1g47290 and At2g26260) and demonstrated, by yeast functional complementation and by VIGS-mediated silencing, their involvement in sterol biosynthesis. Both isoforms are classified as extended SDR (SDR31E family, in the Kallberg et al. [1] nomenclature).

11β-and 17β-hydroxysteroid dehydrogenase

The level of active glucocorticoids in animals is regulated by an 11β-hydroxysteroid dehydrogenase (HSD). Although these compounds have not been identified in plants, 8 genes coding for 11β-HSD-like proteins were found in the Arabidopsis genome (SDR119C family, Fig. 1C). These proteins, also named steroleosin, belong to the SDR family and possess 11β-and 17 β-HDS activity, but the actual substrates in vivo are unknown [30]. AtHSD1 is thought to regulate plant growth and development by promoting or mediating the effects of brassinosteroids [31]. The protein, located at the surface of oil bodies, is highly similar to Sop2 from sesame [32].

Progesterone 5β-Reductase

Digitalis species comprise plants of medical interest for their capacity to accumulate cardenolides, a class of steroids with cardiotonic properties that are efficient for treating cardiac insufficiencies. The reduction of progesterone by progesterone 5β-reductase constitutes a central step in cardenolides biosynthesis. This reaction is catalyzed by a stereospecific NADPH-dependent 'extended'-SDR (belonging to the SDR75E family defined by Kallberg et al. [1]) which has been also crystallized [33]. Herl et al. [34] recently characterized an Arabidopsis orthologue, VEP1 (At4g24220) of Digitalis progesterone 5β-reductase and confirmed, by heterologous expression, its Δ 4,5steroid 5β-reductase activity.

Alkaloids biosynthesis

Plant alkaloids are pharmacologically active nitrogen-containing compounds originating from amino acids, polyamines or purines. SDRs were found to be involved in the biosynthesis of at least two major classes of alkaloids: benzylisiquinoline alkaloids (morphine, codeine) and tropane-derived alkaloids (scopalamine, atropine, cocaine).

Benzylisiquinoline pathway

By comparative transcripts and metabolites profiling in different Papaver (Poppy) species, Ziegler et al. [35] identified a stereospecific NADPH-dependent salutaridine reductase (SalR) belonging to the same cluster as menthone reductase or neomenthol reductase (Fig. 1E). Contrary to most SDRs, SalR-SDR is active as a monomer and contains an additional 40 amino acids sequence upstream of the catalytic YxxxK motif. Several molecular modelling studies supported by sitedirected mutagenesis enabled the characterisation of the substrate binding pocket. Amino acids of the binding sites are located on three areas which are poorly conserved in other proteins belonging to the Salutaridine/menthone reductase clade (Fig. 1E). Interestingly, several mutations of these amino acids led to the formation of enzymes with lower affinity but higher turnover than the native enzyme [36,37].

Tropane pathway

Tropane alkaloids (scopolamine, hyoscamine, atropine, cocaine) have received much attention given their interest as drugs. Tropinone reduction, either into tropine or into pseudotropine is considered as a branching point of alkaloids metabolism. In Solanaceous species, where both tropine stereoisomers-derived compounds are found, two stereospecific NADPH dependent-SDRs were identified: tropinone reductase I (TR-I), yielding tropine and tropinone reductase II (TR-II), yielding pseudotropine [START_REF] Nakajima | Proc. Natl. Acad. Sci[END_REF]. The crystal structures of both TR-I and TR-II were described [START_REF] Nakajima | Proc. Natl. Acad. Sci. USA[END_REF][START_REF] Yamashita | [END_REF]; interestingly, the stereospecificity appeared to be controlled by few charged amino acids which control the binding orientation of tropinone within the substrate binding site. In TR-II, a glutamate (E156), absent in TR-I direclty interacts with the positively-charged tropinone nitrogen while the orientation of tropinone in TR-I is controlled by electrostatic repulsion between the substrate and a histidine (H112).

Yet, in all sequenced plant species, several 'tropinone reductases' are predicted that show high similarity to either TR-I or TR-II (Fig. 1D). In rice or Arabidopsis, the adjacent positions of various TR on different chromosome segments suggest that, in higher plants, the tropinone reductase family was diversified by several independent duplication events. To understand the significance of this diversification, Brock et al. [41] characterized tropinone reductase from the Brassicaceae Cochlearia officinalis and Arabidopsis and after mutagenesis, evaluated the importance of certain amino acids in substrate specificity and stereospecificity. Both enzymes show broad substrate specificity but only Cochlearia TR-I can reduce tropinone in tropine and pseudotropine. As observed with Solanaceous TR, the enzyme specificity can be altered by few amino acids mutations. Thus, the authors suggested a scenario for the emergence of TR among the SDR superfamily. From a TR prototype (probably with relaxed specificity and low turnover), the family first diversified into two major families (TR-I and TR-II) and subsequent gene duplication has generated a wide spectrum of non-specific isoforms. Some of these isoforms (as in Solanaceae) were selected for specialization and acquired higher specificities. The high number of duplications in the alkaloid pathway highlights the importance of co-evolution of the secondary metabolism in response to various biotic stresses or interactions (detoxification of xenobiotics, defence against pests and herbivores).

SDRs involved in alkaloids biosynthesis may not be restricted to the tropinone reductase or salutaridine reductase clusters. Indeed, FgaDH, an NAD-chanoclavine-I dehydrogenase involved ergot alkaloid biosynthesis was recently characterized in Aspergillus fumigatus and Claviceps purpurea [42]. Interestingly, this protein harbours motifs similar to the conserved motifs of plant NAD-dependent dehydrogenase cluster (Fig. 1B), which is involved in several metabolic pathways (phenolics, isoprenoids, hormones).

Phenolics

Two SDR families play a central role in phenylpropanoid metabolism: the dehydroflavonol-4-reductase (DFR) family (classified SDR108E by Kallberg et al. [1]) and the 'isoflavone-reductase' family (reviewed by Ferrer et al. [43]). However, none of them are classified as 'classical' SDRs.

Besides DFR, its representative member, which converts flavanones into flavanols [44], the DFR family includes cinnamoyl-CoA reductases, the first reaction of the monolignol biosynthesis pathway [45] and anthocyanidin reductase encoded by the BANYULS genes [46]. Like tropinone reductase, this subfamily shows a high diversification pattern. In Arabidopsis, 24 proteins belong to this SDR-subfamily, most of them still awaiting functional characterization. Yet, the characterization and further annotation of some CCR-like proteins may be puzzling. A CCR-like NADPH-reductase (which is present as two close isoforms in Arabidopsis, tobacco and tomato) was investigated in Eucalyptus gunnii [47], Mungbean (Vigna radiata, [48]), grapevine [49], tobacco [50] and tomato [51]. Depending on the publications, the authors focused on the reduction of either cinnamaldehyde [47,50], phenylacetaldehyde [51] or the fungal toxin eutypine [48,49]. Although the enzymatic constants (K m , V max ) are variable between the different substrates, these CCR-like proteins can reduce a broad range of aldehydes. However, it can be hypothesized that these NADPH-reductases play specific roles in plant-micro-organisms interaction. In grapevine, this hypothesis is supported by the high affinity of NADPH-reductase towards eutypine, a xenobiotic toxin emitted by the pathogen Eutypa lata, and by the fact that over-expression of mungbean eutypine reductase in grapevine increases the detoxification capacity against eutypine [52]. In other species, the level of NADPH-reductase activity may control the release of pollinator-attractive aroma volatiles. The selection and evolution of enzymes may then be controlled by very specific ecological niche interactions.

The second family (enzymes related to isoflavone-reductase) comprises only 9 members in Arabidopsis thaliana. Several functions have already been described in various plant species: pinoresinol reductase in Forsythia x intermedia [53], eugenol synthase in sweet basil (Ocimum basilicum) [START_REF] Koeduka | Proc. Natl. Acad. Sci. USA[END_REF], vestitone reductase in alfalfa (Medicago sativa), phenylcoumaran benzylic ether reductase in Pinus taeda and Populus trichocarpa [START_REF] Min | [END_REF], leucoanthocyanidin reductase in Arabidopsis [56]. Many of these enzymes have been crystallized recently [43].

In addition to these two 'extended' SDR subfamilies, a secoisolariciresinol dehydrogenase (SDH) was purified and identified in Forsythia x intermedia and Podophyllum peltatum [57], the latter being crystallized [58]. This 'classical' NADdependent homotetrameric SDR catalyzes the two step lactonization (oxidation) of secoisolariciresinol into matairesinol. Interestingly, this enzyme is closely related to xanthoxine reductase ABA2 (52% identity, Fig. 1B), involved in ABA biosynthesis and also performing a two-steps oxidation as mentioned below.

Terpenoids metabolism

Menthol biosynthetic pathway

Monoterpenes represent the major components of essential oils. The monoterpene (-)menthol and its derivatives are particularly abundant in peppermint (Mentha x piperita) and spearmint (Mentha spicata). The biosynthetic pathways of menthol and menthol isomers comprise several reduction steps that are catalysed by monomeric reductases of the SDR family (Fig. 1E). Two double-bond NADPH-dependent reductases, (-)isopiperitenone reductase and (+)-pulegone reductase represent important steps in the biosynthesis of (-)-menthone. The corresponding genes have been isolated and characterized in peppermint [59]. Thereafter, (-)-menthone is reduced into (-)-menthol and (+)-neomenthol by two types of stereospecific and NADPH-dependent menthone reductases: (-)-menthone:(-)-(3R)-menthol reductase (MMR) and (-)-menthone:(-)-(3S)-neomenthol reductase (MNR). The MMR and MNR genes of peppermint have been isolated and functionally characterized [60]. Both belong to the SDR superfamily. MNR genes have later been characterized in pepper (Capsicum annuum, CaMNR1) and Arabidopsis (AtSDR1, At3g61220). They share 59% and 54% sequence identity with the peppermint MNR gene and increased plant resistance against a broad spectrum of pathogens [61]. Interestingly, MNR are closely related to Papaver salutaridine reductase (SalR), involved in benzylisiquinoline alkaloids biosynthesis (Fig. 1E). Ziegler et al. [37] formulated a scenario where MNR and SalR evolved from a common ancestor potentially involved in pathogen defence. Speciation (after duplication events) of this gene in poppy and peppermint would have led to specific salutaridine or (-)-menthol producing reductases. Spearmint and peppermint monoterpene pathway involves also, in the early step, the NAD-dependent oxidation of isopiperitenone (in peppermint) or carveol (in spearmint). Contrary to the reductions described above, this enzymatic steps involves an (-)isopiperitenol/(-)-carveol dehydrogenase belonging to the NAD-dependent dehydrogenase cluster (Fig. 1B, [62]). This example illustrates that metabolic diversification may arise from independent enzymatic families.

Phytoalexins

When plants are attacked by pathogens, they produce secondary metabolites called phytoalexins which are generally diterpenoids. A gene cluster for the synthesis of momilactones, one type of diterpenoid phytoalexins, has been characterized in rice. The cluster harbours a SDR gene encoding a reductase capable of converting 3βhydroxy-9βH-primara-7,15-dien-19,6β-olide into momilactone A [63].

Plant aromas

Given its chemical diversity and its importance in ecological interactions between plants and animals, volatile compounds must be considered as an important class of secondary metabolites. Several independent pathways are involved in aroma formation: terpenoid and phenolic metabolism, lipids and amino acids degradation [64,[START_REF] Pech | Fruit and Vegetable Flavour[END_REF]. However, the diversity of aroma compounds is also linked to the presence of large multigenic families such as acyl-transferases, O-methyl-transferases, or Cytochrome P450 mono-oxygenases [START_REF] Gang | [END_REF]. In that view, the involvement and diversification of SDR in the monoteprene-derived menthol pathway gives credit to the idea that SDR evolution played a major role in metabolic diversification. Similarly, extended SDR have been described either in the formation of eugenol [START_REF] Koeduka | Proc. Natl. Acad. Sci. USA[END_REF] or in the interconversion of phenylacetaldehyde into 2-phenylethanol [51].

At last, expression analyses in various fruits (melon, strawberries, banana, apricot, [67,68]) report the expression of a well conserved SDR during ripening, its expression being enhanced along other genes involved in aroma biosynthesis (acyltransferases, medium-chain alcohol dehydrogenase). Conversely, in Arabidopsis, GENEVESTIGATOR microarray database reveals that the orthologue (At3g01980) is highly expressed in flowers [69]. This SDR, original by its weakly conserved cofactor binding sites or by its 'divergent' catalytic site displays the other features of classical SDR, yet, it still awaits full characterization.

Plant hormones

Plants hormones are synthesized through independent metabolic pathways (steroids, terpenoids, phenolics, lipids catabolism, decarboxylation of tryptophan). In analogy with animal SDRs largely involved in steroids or prostaglandins synthesis, modifications, or catabolism [3], it may be rational to assume that several plant SDRs play a major role regarding hormone metabolism.

ABA biosynthesis

Abscisic Acid (ABA) is a sesquiterpenoid plant hormone involved in the control of many physiological processes such as seed development and germination and in the response to various stresses. The biosynthesis pathway comprises an NAD-dependent conversion of xanthoxin into ABA aldehyde. The enzyme responsible for this conversion is short-chain alcohol dehydrogenase (At1g52340) named ABA2 in Arabidopsis [70,71]. Although ABA2 belongs to the 'diversified' NADdehydrogenase cluster (Fig. 1B), the ABA2 sequence is well conserved among higher plants (55 % identity between rice and Arabidopsis) but is absent in the Physcomitrella patens moss. This suggests that ABA biosynthesis emerged as a consequence of higher plant metabolism diversification and was probably selected and conserved when it acquired a major physiological function.

Auxin

Indole-3-butyric acid (IBA) and 2,4dichlorophenoxybutyric acid (2,4-DB) are synthetic auxins that mimic auxin effects in plants. In fact their activity is due to the metabolisation by βoxidation into indole-3-acetic acid (IAA) and 2,4dichlorophenoxyacetic acid (2,4-D) respectively [72]. Arabidopsis mutants have been identified that are resistant to IBA and 2,4-DB. One of these mutants has been characterized and the encoding protein, identified simultaneously by two separate groups of researchers, was named IBR1 by Zolman et al. [73] and SDRa by Wiszniewski et al. [72]. IBR1/SDRa (At4g055630.1) protein is a NADP(H)dependent classical SDR member very distant from other classical SDRs (Fig. 1) but close (49% identity) to the human DHRS4 peroxysomal protein, an SDR thought to be involved either in 3βhydroxysteroid reduction or in xenobiotic detoxification [74]. The IBR1/SRDa mutant phenotype does not show any alteration of fatty acid metabolism, indicating that the primary role of the encoded protein is in hormone metabolism. The protein possesses a C-terminal peroxisomaltargeting signal and has been localized in the peroxisome by the GFP fusion method [72] or proteomics [75].

Role of SDRs in developmental processes via the putative interference in the synthesis or action of hormones

Contrary to ABA2, where a metabolic role has clearly been assigned to a SDR in ABA biosynthesis, several papers describe spectacular developmental perturbations induced by alteration of SDR-encoding genes expression [76][77][78]. These papers suggest that SDRs may interfere with the biosynthesis, catabolism or action of some hormones. The TASSELSEED2 gene (TS2), originally described in maize as involved in feminization of the flower [78] is representative of this situation. TS2 belongs to the NAD-dependent dehydrogenase clade (Fig. 1B). Phylogenetic studies in grass lineages [79] have shown that the TS2-like family has undergone a large diversification in Monocots. However, the identity of the reaction catalyzed by TS2 remains enigmatic. Wu et al. [80] showed that TS2 could bind a broad spectrum of substrates, with a probable preference towards steroids. However, the recent positional cloning of ts1 gene suggests alternative role for TS2 [81]. Indeed, TS1 encodes a 13-lipoxygenase involved in jasmonic acid synthesis and application of exogenous jasmonic acid can rescue feminization either in ts1 or ts2 mutant rice. The authors proposed that TS2 could be involved in jasmonic acid (JA) biosynthesis (in the peroxysomal β-oxidation steps), but the activity has not been demonstrated. The elucidation of the accurate function of TS2 will be of great interest, especially if it highlights the cross-talk between different hormones (GA, JA or steroids for example).

A second example is the TDF511 potato gene involved in several aspects of plant development including tuber morphology, early sprouting and stolon elongation. The gene shows homology to steroid dehydrogenases but the activity of the encoded protein has not been determined. Nevertheless, it was shown that TDF51-inhibited transgenic potatoes had elevated levels of biologically active GAs and their respective precursors [77]. However the direct involvement in GA catabolism has not been demonstrated. Rather, TDF511 could play an indirect role via the synthesis or breakdown of other hormones.

CONCLUDING REMARKS

The present review shows the diversity of the plant short chain dehydrogenase superfamily. This diversity is first illustrated by the size of the family: in Arabidopsis, 92 genes code for 'classical'-SDRs and 98 genes code for 'intermediary', 'extended', 'divergent', 'complex' or 'unknown' SDR. Plants contain SDRs with both prokaryote and eukaryote origins. Some plastid SDRs (POR, FASII) clearly emerged from cyanobacteria as a consequence of the plastidial endosymbiosis, while other SDRs (hydroxysteroid dehydrogenase, progesterone reductase, fatty acid elongase) are common to all eukaryotes. However, the most striking diversity concerns the functions of the enzymes. While some SDRs are involved in primary metabolism pathways (lipid biosynthesis, chlorophyll synthesis and degradation, folate salvage), a large number of SDRs intervene in all the secondary metabolism routes (steroids, terpenoids, alkaloids, phenolics). In primary metabolism, the enzymes show a clear relationship with other eukaryotes or prokaryotes (for plastid enzymes) homologues, suggesting that these essential functions were conserved during evolution. By contrast, SDRs involved in secondary metabolism often belong to large subfamilies that probably have arisen by several duplication events. Moreover, the observation that stereo-or substrate specificity relies on a small number of amino acids and the coexistence of 'broad' or 'specialised' SDRs among the different subfamilies suggests that during evolution, SDR diversification enabled the development of an enzymatic 'repertoire', some of its members being selected and specialised as they acquired major functions (hormone synthesis, synthesis of abundant metabolite). In that view, the emergence of complex family such as SDR, but also acyltransferase, glucosyltransferase or cytochrome P450-dependent monooxygenases can be considered as a prerequisite to plant chemical diversification.

IN PLANT METABOLISM 2.1. PRIMARY METABOLISM 2.1.1. Fatty acid biosynthesis.

Acknowledgements-Libert Brice Tonfack has received a doctoral fellowship from the "Service de Coopération et d'Action Culturelle" of the French Embassy (Cameroon) and Hanane Moummou from EGIDE within the frame of a French-Morocco Volubilis project (MA-06-155). This work was financially supported by the Midi-Pyrénées Regional Council.

Hydroxysteroid Dehydrogenase; 3β-HSD/D: 3-Beta-Hydroxysteroid Dehydrogenase-Decarboxylase; IsplDH: Isopiperitenol Dehydrogenase; IspR: (-)-Isopiperitenone Reductase; JA: Jasmonic Acid; MMR: (-)-Menthone:(-)-(3R)-Menthol Reductase; MNR: (-)-Menthone:(-)-(3S)-Neomenthol Reductase; POR