A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus

[EN] Angiosperms are the most diverse and numerous group of plants, and it is generally accepted that this evolutionary success owes in part to the diversity found in fruits, key for protecting the developing seeds and ensuring seed dispersal. Although studies on the molecular basis of morphological innovations are few, they all illustrate the central role played by transcription factors acting as developmental regulators. Here, we show that a small change in the protein sequence of a MADS-box transcription factor correlates with the origin of a highly modified fruit morphology and the change in seed dispersal strategies that occurred in Medicago, a genus belonging to the large legume family. This protein sequence modification alters the functional properties of the protein, affecting the affinities for other protein partners involved in high-order complexes. Our work illustrates that variation in coding regions can generate evolutionary novelties not based on gene duplication/subfunctionalization but by interactions in complex networks, contributing also to the current debate on the relative importance of changes in regulatory or coding regions of master regulators in generating morphological novelties.This work was supported by the Spanish Ministerio de Ciencia e Innovacion (grant no. BIO2009-09920 to C.Fe.), the European Union (grant no. FP7-PEOPLE-PIRSES-2009-247589 to C.Fe. and A.C.d.O.), and a Fellowship for Foreign Young Postdocs from the Spanish Ministerio de Ciencia e Innovacion (to C.Fo.).Fourquin, C.; Del Cerro Fernández, C.; Victoria, FC.; Vialette-Guiraud, A.; De Oliveira, AC.; Ferrandiz Maestre, C. (2013). A change in SHATTERPROOF protein lies at the origin of a fruit morphological novelty and a new strategy for seed dispersal in Medicago genus. Plant Physiology. 162(2):907-917. https://doi.org/10.1104/pp.113.217570S907917162

Évolution et développement de la fleur

L’apparition de la fleur des angiospermes constitue une innovation morphologique importante dans l’évolution des plantes. À travers l’étude des bases moléculaires du développement de la fleur dans différentes espèces modèles, nous proposons un aperçu des réseaux génétiques qui sous-tendent la grande diversité de morphologie florale chez les angiospermes. L’évolution de la famille des facteurs de transcription à boîte MADS semble avoir joué un rôle central dans l’apparition de cette diversité

The evolutionary-developmental analysis of plant microRNAs

MicroRNAs (miRNAs) control many important aspects of plant development, suggesting these molecules may also have played key roles in the evolution of developmental processes in plants. However, evolutionary-developmental (evo-devo) studies of miRNAs have been held back by technical difficulties in gene identification. To help solve this problem, we have developed a two-step procedure for the efficient identification of miRNA genes in any plant species. As a test case, we have studied the evolution of the MIR164 family in the angiosperms. We have identified novel MIR164 genes in three species occupying key phylogenetic positions and used these, together with published sequence data, to partially reconstruct the evolution of the MIR164 family since the last common ancestor of the extant flowering plants. We use our evolutionary reconstruction to discuss potential roles for MIR164 genes in the evolution of leaf shape and carpel closure in the angiosperms. The techniques we describe may be applied to any miRNA family and should thus enable plant evo-devo to begin to investigate the contributions miRNAs have made to the evolution of plant development

A Conserved Role for the NAM/miR164 Developmental Module Reveals a Common Mechanism Underlying Carpel Margin Fusion in Monocarpous and Syncarpous Eurosids

International audienceThe majority of angiosperms are syncarpous- their gynoecium is composed of two or more fused carpels. In Arabidopsis thaliana, this fusion is regulated through the balance of expression between CUP SHAPED COTYLEDON (CUC) genes, which are orthologs of the Petunia hybrida transcription factor NO APICAL MERISTEM (NAM), and their post transcriptional regulator miR164. Accordingly, the expression of a miR164-insensitive form of A. thallana CUC2 causes a radical breakdown of carpel fusion. Here, we investigate the role of the NAM/miR164 genetic module in carpel closure in monocarpous plants. We show that the disruption of this module in monocarpous flowers of A. thaliana aux1-22 mutants causes a failure of carpel closure, similar to the failure of carpel fusion observed in the wild-type genetic background. This observation suggested that closely related mechanisms may bring about carpel closure and carpel fusion, at least in A. thaliana. We therefore tested whether these mechanisms were conserved in a eurosid species that is monocarpous in its wild type form. We observed that expression of MtNAM, the NAM ortholog in the monocarpous eurosid Medicago truncatula, decreases during carpel margin fusion, suggesting a role for the NAM/miR164 module in this process. We transformed M. truncatula with a miR164-resistant form of MtNAM and observed, among other phenotypes, incomplete carpel closure in the resulting transformants. These data confirm the underlying mechanistic similarity between carpel closure and carpel fusion which we observed in A. thaliana, Our observations suggest that the role of the NAM/miR164 module in the fusion of carpel margins has been conserved at least since the most recent common ancestor of the eurosid clade, and open the possibility that a similar mechanism may have been responsible for carpel closure at much earlier stages of angiosperm evolution. We combine our results with studies of early diverging angiosperms to speculate on the role of the NAM/miR164 module in the origin and further evolution of the angiosperm carpel

A Conserved Role for the NAM/miR164 Developmental Module Reveals a Common Mechanism Underlying Carpel Margin Fusion in Monocarpous and Syncarpous Eurosids

International audienceThe majority of angiosperms are syncarpous- their gynoecium is composed of two or more fused carpels. In Arabidopsis thaliana, this fusion is regulated through the balance of expression between CUP SHAPED COTYLEDON (CUC) genes, which are orthologs of the Petunia hybrida transcription factor NO APICAL MERISTEM (NAM), and their post transcriptional regulator miR164. Accordingly, the expression of a miR164-insensitive form of A. thallana CUC2 causes a radical breakdown of carpel fusion. Here, we investigate the role of the NAM/miR164 genetic module in carpel closure in monocarpous plants. We show that the disruption of this module in monocarpous flowers of A. thaliana aux1-22 mutants causes a failure of carpel closure, similar to the failure of carpel fusion observed in the wild-type genetic background. This observation suggested that closely related mechanisms may bring about carpel closure and carpel fusion, at least in A. thaliana. We therefore tested whether these mechanisms were conserved in a eurosid species that is monocarpous in its wild type form. We observed that expression of MtNAM, the NAM ortholog in the monocarpous eurosid Medicago truncatula, decreases during carpel margin fusion, suggesting a role for the NAM/miR164 module in this process. We transformed M. truncatula with a miR164-resistant form of MtNAM and observed, among other phenotypes, incomplete carpel closure in the resulting transformants. These data confirm the underlying mechanistic similarity between carpel closure and carpel fusion which we observed in A. thaliana, Our observations suggest that the role of the NAM/miR164 module in the fusion of carpel margins has been conserved at least since the most recent common ancestor of the eurosid clade, and open the possibility that a similar mechanism may have been responsible for carpel closure at much earlier stages of angiosperm evolution. We combine our results with studies of early diverging angiosperms to speculate on the role of the NAM/miR164 module in the origin and further evolution of the angiosperm carpel

Carpel development

International audienceThe carpel is the female reproductive organ that encloses the ovules in the flowering plants or angiosperms. The origin of the carpel and its subsequent morphological modifications were probably of vital importance to the evolution of the angiosperms, and the carpel is also very important as the precursor organ to the fruit. Here we describe the general attributes of the angiosperm carpel and several hypotheses for its evolutionary origin. As carpels share many developmental processes with leaves, we describe these processes in the leaf, and then detail the regulation of carpel and fruit development in the model angiosperm Arabidopsis thaliana. We also describe the relationship between carpel formation and the arrest of organ proliferation which occurs at the centre of the Arabidopsis floral meristem. We then provide a brief overview of carpel development in angiosperms occupying important phylogenetic positions, including ANA grade angiosperms, monocots, basal eudicots and core eudicots, focussing on the probable ancestral state of the carpel in each case, and on the available molecular and genetic data. We end with a brief discussion of future research directions relating to carpel and fruit development

Des modèles pour comprendre le développement des eucaryotes

International audienceBien qu’extrêmement diversifiés, il est clairement admis que les êtres vivants ont tous un seul ancêtre commun. Pour reconstituer un scénario évolutif robuste à l’origine de la biodiversité il est essentiel de développer des espèces modèles judicieusement placées et suffisamment dispersées dans " l'arbre de vie "

Divergence of the floral a-function between an asterid and a rosid species

The ABC model is widely used as a genetic framework for understanding floral development and evolution. In this model, the A-function is required for the development of sepals and petals and to antagonize the C-function in the outer floral whorls. In the rosid species Arabidopsis thaliana, the AP2-type AP2 transcription factor represents a major A-function protein, but how the A-function is encoded in other species is not well understood. Here, we show that in the asterid species petunia (Petunia hybrida), AP2B/BLIND ENHANCER (BEN) confines the C-function to the inner petunia floral whorls, in parallel with the microRNA BLIND. BEN belongs to the TOE-type AP2 gene family, members of which control flowering time in Arabidopsis. In turn, we demonstrate that the petunia AP2-type REPRESSOR OF B-FUNCTION (ROB) genes repress the B-function (but not the C-function) in the first floral whorl, together with BEN. We propose a combinatorial model for patterning the B-and C-functions, leading to the homeotic conversion of sepals into petals, carpels, or stamens, depending on the genetic context. Combined with earlier results, our findings suggest that the molecular mechanisms controlling the spatial restriction of the floral organ identity genes are more diverse than the well-conserved B and C floral organ identity functions