Diversité et évolution de la microsporogenèse chez les palmiers (Arecaceae) en relation avec la détermination du type apertural

Microsporogenesis or male meiosis in seed plants is the process leading to a tetrad of four haploid microspores separated by callose walls from a diploid mother cell, or microsporocyte. Each microspore then matures into a pollen grain, the male gametophyte of seed plants that produces the gametes necessary to achieve sexual reproduction. The aperture pattern of pollen grains, defined as the form, number and position of apertures on the pollen surface, is determined during microsporogenesis. The features of microsporogenesis vary among angiosperms and studying the evolution of these features would help to understand the evolution of aperture pattern in this group. We have chosen to examine the diversity and evolution of microsporogenesis in palms (Arecaceae), a family of angiosperms. A large diversity of pollen types is found in this family: a comparable diversity in microsporogenesis can therefore reasonably be expected. Well-supported phylogenies of the family have been recently published and provide the historical framework that is necessary to study the evolution of the characters examined. We have sampled palm species that present one major aperture type, the monosulcate type (a single aperture furrow-shaped and located at the distal pole of the pollen grain) but microsporogenesis was found unexpectedly variable: cytokinesis can be of the simultaneous or successive type or even mixed in some species; intersporal wall formation can be either centripetal or centrifugal; tetrads present a wide range of different forms varying in proportion among and within species. Different developmental pathways can then lead to the production of only one pollen type. We have reconstructed the evolution of the characteristics of microsporogenesis likely to play a role in aperture pattern determination using both Maximum Parsimony and Maximum Likelihood methods. In the case of the Maximum Likelihood method, two different models of evolution were tested: the symmetrical model (one transition rate) and the asymmetrical model (forward transition rate different from backward transition rate). Due to the high variability found in the characters examined, the inference at the ancestral nodes was often equivocal. However, we suggest that the ancestral type of microsporogenesis involved a cytokinesis of the successive type and resulted in tetragonal tetrads. Although it is commonly admitted in the literature that successive cytokinesis is associated with centrifugal cell wall formation whereas simultaneous cytokinesis is associated with centripetal wall formation, no such relationship was found in palms. The reasons underlying the remarkable diversity occurring in pollen morphology and pollen early development are still unclear. In Arecaceae, the relationship suggered by Ressayre et al. (2002a) between the aperture pattern and microsporogenesis could not be highlighted, in particular in consequence of the presence of irregular tetrahedral tetrads and of variable and asymmetrical additional callose deposits.La microsporogenèse ou méiose mâle des plantes à graines mène une cellule mère diploïde, appelée microsporocyte, à quatre microspores haploïdes disposées en tétrade et séparées par des parois de callose. Chacune de ces microspores devient ensuite un grain de pollen, le gamétophyte mâle des plantes à graines qui produit les gamètes indispensables à la reproduction sexuée. C'est au cours de la microsporogenèse qu'est déterminé le type apertural des grains de pollen, défini par la forme, le nombre et l'arrangement des apertures à la surface pollinique. Les caractéristiques de la microsporogenèse sont sujettes à variation chez les Angiospermes ; comprendre leur évolution permettrait de mieux appréhender l'évolution du type apertural au sein de ce groupe. Nous avons choisi d'étudier la diversité de la microsporogenèse ainsi que son évolution au sein de la famille des palmiers (Arecaceae). Cette famille d'Angiospermes présente une grande diversité de types polliniques, on s'attend donc à y rencontrer une diversité comparable de la microsporogenèse. Des phylogénies moléculaires récemment publiées et bien soutenues sont disponibles pour cette famille et fournissent le cadre historique nécessaire à l'étude de l'évolution des caractères choisis. Nous avons échantillonné des espèces de palmiers présentant un type pollinique très majoritaire, le pollen monosulqué (une aperture en forme de sillon et localisée au pôle distal du grain de pollen), mais la microsporogenèse s'est avérée très variable entre les espèces et même au sein d'une même espèce. En effet, la cytocinèse peut être successive ou simultanée, voire mixte chez certaines espèces, les parois intersporales se forment de manière centrifuge ou centripète et les tétrades adoptent une grande variété de formes, en proportions variables au niveau interspécifique comme intraspécifique. Ainsi, un même type de pollen peut être produit par diverses voies de développement. Nous avons reconstruit l'évolution de différents caractères de la microsporogenèse susceptibles d'intervenir dans la détermination du type apertural par la méthode du maximum de parcimonie et la méthode du maximum de vraisemblance. Pour cette dernière méthode, deux modèles d'évolution ont été utilisés, le modèle symétrique (taux de transition uniforme) et le modèle asymétrique (taux de transition ≠ taux de réversion). Les caractères de la microsporogenèse étant très variables, l'inférence des états de caractères aux noeuds les plus ancestraux est incertaine. Il semblerait tout de même que la cytocinèse ancestrale à l'ensemble des espèces de palmier échantillonnées soit successive et que les tétrades formées soient tétragonales. Aucune relation entre les différentes composantes de la microsporogenèse n'a pu être soulignée, bien qu'il soit couramment admis dans la littérature que la cytocinèse successive est généralement associée à une formation centrifuge des parois intersporales et à des tétrades tétragonales, tandis que la cytocinèse simultanée est associée à une formation centripète des parois et à des tétrades tétraédriques. Les causes de la remarquable diversité rencontrée chez les palmiers, tant au niveau de la morphologie pollinique que du développement pollinique précoce, restent à élucider. Chez les Arecaceae, la relation suggérée par Ressayre et al. (2002a) entre le type apertural et la microsporogenèse n'a pas pu être mise en évidence, en particulier en raison de l'existence de tétrades tétraédrique irrégulières et de dépôts additionnels de callose variables et asymétriques

Diversité et évolution de la microsporogenèse chez les palmiers (Arecaceae) en relation avec la détermination du type apertural

La microsporogenèse ou méiose mâle des plantes à graines mène une cellule mère diploïde, le microsporocyte, à quatre microspores haploïdes disposées en tétrade et séparées par des parois de callose. Chacune d entre elles devient ensuite un grain de pollen (gamétophyte mâle). C est au cours de la microsporogenèse qu est déterminé le type apertural des grains de pollen, défini par la forme, le nombre et l arrangement des apertures à la surface pollinique. Nous avons choisi d étudier la diversité et l évolution de la microsporogenèse chez les palmiers (Arecaceae). Malgré la production d un seul type pollinique majoritaire, le pollen monosulqué (une aperture en forme de sillon localisée au pôle distal), la microsporogenèse s est avérée très variable. En effet, la cytocinèse peut être successive, simultanée ou mixte, les parois intersporales se forment de manière centrifuge ou centripète et les tétrades adoptent une grande variété de formes, en proportions variables. Ainsi, un même type de pollen peut être produit par diverses voies de développement. Nous avons reconstruit l évolution des caractères précédents chez les palmiers par la méthode du maximum de parcimonie et celle du maximum de vraisemblance. Les caractères de la microsporogenèse étant très variables, l inférence des états de caractères aux nœuds les plus ancestraux est incertaine. Il semblerait tout de même que la cytocinèse ancestrale à l ensemble des espèces de palmier échantillonnées soit successive et que les tétrades formées soient tétragonales. Chez les Arecaceae, la relation suggérée par Ressayre et al. (2002) entre le type apertural et la microsporogenèse n a pas pu être mise en évidence.Microsporogenesis or male meiosis in seed plants is the process leading to a tetrad of four haploïd microspores separated by callose walls from a diploid mother cell, or microsporocyte. Each of them then matures into a pollen grain (male gametophyte). The aperture pattern of pollen grains, defined as the form, number and position of apertures on the pollen surface, is determined during microsporogenesis. We have chosen to examine the diversity and evolution of microsporogenesis in palms (Arecaceae). In spite of the production of only one major pollen type, the monosulcate pollen (a single aperture furrow-shaped located at the distal pole), microsporogenesis was found unexpectedly variable. Indeed, cytokinesis can be of the simultaneous or successive type or even mixed, intersporal wall formation can be either centripetal or centrifugal and tetrads present a wide range of different forms varying in proportion. Different developmental pathways can then lead to the production of only one pollen type. We have reconstructed the evolution of the previous characters using both Maximum Parsimony and Maximum Likelihood methods. Due to the high variability found in the characters examined, the inference at the ancestral nodes was often equivocal. However, we suggest that the ancestral type of cytokinesis involved a cytokinesis of the successive type and resulted in tetragonal tetrads. In Arecaceae, the relationship suggered by Ressayre et al. (2002) between the aperture pattern and microsporogenesis could not be highlighted.ORSAY-PARIS 11-BU Sciences (914712101) / SudocSudocFranceF

Combining phylogenetic and syntenic analyses for understanding the evolution of TCP ECE genes in eudicots

TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the gamma event. Genomic comparisons in Arabidopsis thaliana and Solanum lycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegia coerulea and Nelumbo nucifera suggests that the two TCP ECE paralogs in these species are also derived from large-scale duplications. TCP ECE loci from basal eudicots share many features with the three main core eudicot loci, and allow us to infer the makeup of the ancestral eudicot locus

Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots

International audienceThis paper presents the first broad overview of three main features of microsporogenesis (male meiosis) in angiosperms: cytokinesis (cell division), intersporal wall formation, and tetrad form. A phylogenetic comparative approach was used to test for correlated evolution among these characters and to make hypotheses about evolutionary trends in microsporogenesis. The link between features of microsporogenesis and pollen aperture type was examined. We show that the pathway associated with successive cytokinesis (cytoplasm is partitioned after each meiotic division) is restricted to wall formation mediated by centrifugally developing cell plates, and tetragonal (or decussate, T-shaped, linear) tetrads. Conversely, much more flexibility is observed when cytokinesis is simultaneous (two meiotic divisions completed before cytoplasmic partitioning). We suggest that the ancestral type of microsporogenesis for angiosperms, and perhaps for all seed plants, associated simultaneous cytokinesis with centripetal wall formation, resulting in a large diversity in tetrad forms, ranging from regular tetrahedral to tetragonal tetrads, including rhomboidal tetrads. From this ancestral pathway, switches toward successive cytokinesis occurred among basal angiosperms and monocots, generally associated with a switch toward centrifugal intersporal wall formation, whereas eudicots evolved toward an almost exclusive production of regular tetrahedral tetrads. No straightforward link is found between the type of microsporogenesis and pollen aperture type

TCP ECE gene phylogeny in eudicots, rooted on monocot sequences.

<p>Phylogeny was inferred by ML analysis of the nucleotide sequences of the TCP, ECE and R domains (249 characters). Clades with ≥75% Shimodaira-Hasegawa (SH)-like support are shown; SH values are given below each branch; posterior probabilities (PPs) from the Bayesian analysis of the same dataset are given after. Sequence names of basal eudicots are in blue, and of <i>Gunnera</i><i>tinctoria</i> in red.</p

Results of the tests of molecular evolution in each sublineage of <i>RanaCyL1</i> and <i>RanaCyL2</i>.

<p>Results of the tests of molecular evolution in each sublineage of <i>RanaCyL1</i> and <i>RanaCyL2</i>.</p

Main types of perianth organization in the tribe Delphinieae.

<p>The four sketches are not at the same scale. (A) <i>Aconitum</i> type (applicable to groups 7, 8, and 9 from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0095727#pone-0095727-g001" target="_blank">Figure 1</a>). (B) <i>Delphinium</i> type (applicable to groups 1, 5, 6, and 10 from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0095727#pone-0095727-g001" target="_blank">Figure 1</a>). (C) <i>Consolida</i> type (applicable to groups 3 and 4 from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0095727#pone-0095727-g001" target="_blank">Figure 1</a>). (D) <i>Aconitella</i> type (applicable to group 2 from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0095727#pone-0095727-g001" target="_blank">Figure 1</a>). Sepals, dorsal petals, and lateral petals (or lateral lobes of the single petal in <i>Consolida</i> and <i>Aconitella</i>) are delineated by black, blue, and purple lines, respectively. The organs responsible for covering-protecting the nectar and the sexual organs are colored in light blue and purple, respectively. Nectar is shown in orange; it is secreted and concealed in the spur of the dorsal petal(s). Androecium and gynoecium are presented as a beige disk. The limb of the single petal has three lobes (two lateral lobes, in purple, and one upper lobe, in blue) in <i>Consolida</i>, and five (two lower lobes, in purple, and three lateral and upper lobes, in blue) in <i>Aconitella</i>. The expression level of each of the four <i>RanaCyL</i> paralogs is shown in the grids for <i>Aconitum carmichaelii</i> and <i>Consolida regalis</i>, in the following perianth compartments: petals (results were available only for <i>C. regalis</i>), dorsal (D), lateral (L), and ventral (V) sepals. Increasing expression level is shown with increasing levels of red. White: no expression detected. Grey: the paralog could not be amplified. The expression profiles are schematized based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0095727#pone-0095727-g003" target="_blank">Figure 3</a>.</p

Phylogeny of <i>Cyc</i>-like sequences in Ranunculaceae.

<p>The phylogeny is inferred using Bayesian and maximum likelihood analysis, rooted in order to group together all the <i>RanaCyL1</i> sequences in one clade, and all the <i>RanaCyL2</i> sequences in another clade. The tree topology obtained by Bayesian inference is shown. Bayesian posterior probability ≥70 and bootstrap support from maximum likelihood analysis ≥50 are given (hyphen if inferior to those thresholds). The 381-position alignment was generated from 109 <i>RanaCyL</i> (from 48 species including 27 Delphinieae) and five other Ranunculales <i>Cyc</i>-like sequences (from three species). Portions of the tree are highlighted with colors according to the subfamilies of Ranunculaceae. The species sequenced for <i>RanaCyL</i> belong to: pink: Ranunculoideae, green: Thalictroideae, purple: Coptidoideae, and orange: Glaucidioideae. A: <i>Aconitum</i>, D: <i>Delphinium</i>, G: <i>Gymnaconitum</i>, S: <i>Staphisagria</i>. The <i>RanaCyL</i> branches tested in the molecular evolution analyses are 1a and 1b in <i>RanaCyL1</i>, and 2a and 2b in <i>RanaCyL2</i>.</p