Unraveling the Developmental and Genetic Mechanisms Underpinning Floral Architecture in Proteaceae.

Catherine Damerval,Yannick Staedler,Yves Deveaux,Sophie Nadot,Natalia Conde E Silva,Franck Simonnet,Etienne Delannoy,Hélène Citerne,Hervé Sauquet,Johann Joets,Jürg Schönenberger,Jennifer Yansouni,Martine Le Guilloux

doi:10.3389/fpls.2019.00018

Abstract

Proteaceae are a basal eudicot family with a highly conserved floral groundplan but which displays considerable variation in other aspects of floral and inflorescence morphology. Their morphological diversity and phylogenetic position make them good candidates for understanding the evolution of floral architecture, in particular the question of the homology of the undifferentiated perianth with the differentiated perianth of core eudicots, and the mechanisms underlying the repeated evolution of zygomorphy. In this paper, we combine a morphological approach to explore floral ontogenesis and a transcriptomic approach to access the genes involved in floral organ identity and development, focusing on Grevillea juniperina, a species from subfamily Grevilleoideae. We present developmental data for Grevillea juniperina and three additional species that differ in their floral symmetry using stereomicroscopy, SEM and High Resolution X-Ray Computed Tomography. We find that the adnation of stamens to tepals takes place at early developmental stages, and that the establishment of bilateral symmetry coincides with the asymmetrical growth of the single carpel. To set a framework for understanding the genetic basis of floral development in Proteaceae, we generated and annotated de novo a reference leaf/flower transcriptome from Grevillea juniperina. We found Grevillea homologs of all lineages of MADS-box genes involved in floral organ identity. Using Arabidopsis thaliana gene expression data as a reference, we found homologs of other genes involved in floral development in the transcriptome of G. juniperina. We also found at least 21 class I and class II TCP genes, a gene family involved in the regulation of growth processes, including floral symmetry. The expression patterns of a set of floral genes obtained from the transcriptome were characterized during floral development to assess their organ specificity and asymmetry of expression.

Highlights

Proteaceae are a family of woody plants comprising approximately 1700 species in 81 genera, distributed mainly in the Southern Hemisphere, with two main centers of diversity, one in Australia and the other in South Africa
Development is similar in the two other species sampled in this study, Alloxylon flammeum and Stenocarpus davallioides, which have flowers with an actinomorphic perianth at early stages and a gynoecium that develops asymmetrically relative to the center of the floral bud (Figures 3A–E)
By describing specific developmental features of flowers within Proteaceae, we found that the adnation of stamens to tepals takes place at early developmental stages, and that the establishment of bilateral symmetry coincides with asymmetrical growth of the single carpel

Summary

Introduction

Proteaceae are a family of woody plants comprising approximately 1700 species in 81 genera, distributed mainly in the Southern Hemisphere, with two main centers of diversity, one in Australia and the other in South Africa. The hypogynous flowers almost invariably consist of four tepals (rarely 3 or 5), four stamens (rarely 3 or 5) opposite the tepals and with filaments that are adnate to the tepals (rarely free), and a single carpel with marginal placentation (Weston, 2007). This floral groundplan is highly conserved, the family displays considerable variation in other aspects of floral and inflorescence morphology. In subfamily Grevilleoideae, all but two genera are characterized by compound inflorescences consisting of racemes of flower pairs described as two-flowered short shoots sharing a common bract (Douglas and Tucker, 1996a). In Proteaceae and in the subfamily Grevilleoideae, the high diversity of carpel orientation (dorso-ventral or oblique) adds further complexity when defining the orientation of the plane of symmetry relative to the common axis of the flower pair (Douglas and Tucker, 1996b)

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Results

Conclusion