Patterning the Asteraceae Capitulum: Duplications and Differential Expression of the Flower Symmetry CYC2-Like Genes.

Jie Chen,Chu-Ze Shen,Yan-Ping Guo,Guang-Yuan Rao

doi:10.3389/fpls.2018.00551

Jie Chen, Chu-Ze Shen + Show 2 more

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https://doi.org/10.3389/fpls.2018.00551

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Abstract

There are several types of capitulum in the Asteraceae due to different combinations of florets varying in corolla shape and stamen development. Previous studies have shown that the formation of ray florets on a radiate capitulum may be related to the parallel co-option of CYC2-like genes among independent Asteraceae lineages. The present work tests that hypothesis and attempts to shed light on the pattern of evolution of the Asteraceae capitulum and floral heteromorphism under the regulation of CYC2-like genes. In this study, the evolutionary history of CYC2-like genes in the Asterales was reconstructed and their expression patterns were examined in species representing different capitulum types and several major Asteraceae lineages. To clarify the role of CYC2d clade genes in morphogenesis of ray flowers, overexpression of ClCYC2d was conducted in Chrysanthemum lavandulifolium. Our results show that there are six CYC2-like members in the Asteraceae; they are results of five duplication events starting from a single-copy gene in the common ancestor of the Goodeniaceae-Calyceraceae-Asteraceae group and completing before the divergence of the subfamily Carduoideae of Asteraceae. Spatial expression pattern of each of the Asteraceae CYC2-like members is conserved across the family. All the six members contribute to the development of the complexity of a capitulum: To form a ray floret, either CYC2c or CYC2g plays an essential role, while CYC2d represses the development of dorsal corolla lobes and stamens of the floret. In sum, the developmental program of making a ray flower is conserved involving functionally divergent CYC2-like genes. Based on extensive species sampling, this study provides an overview of the mode of regulation of CYC2-like genes that patterns the capitulum architectures and their transitions.

Highlights

Morphological and structural innovations of flowers and inflorescences are intimately linked to the reproduction and adaptation of angiosperms (Endress, 2011; Kirchoff and Claßen-Bockhoff, 2013; Teo et al, 2014)
34 contigs were assembled from the genome and transcriptome data in the GenBank; 28 CYC2-like homologs were retrieved from the genome sequencing data of Cy. cardunculus var. scolymus (Scaglione et al, 2016), L. sativa (Reyes-Chin-Wo et al, 2017), H. annuus (Badouin et al, 2017), and E. canadensis (Peng et al, 2014); together with the previously reported genes, in total 243 CYC2-like sequences were identified from 59 species of Asterales and two outgroup species of Dipsacales (Figure 1 and Table S1)
When the less conserved sequences between the TCP and R domains were added, four clades were resolved with bootstrap supports above 50%: (i) the clade consisting of all sequences except the CYC2-like sequences of ancestral status, (ii) the clade consisting of all Asteraceae CYC2-like sequences except CYC2a, (iii) the CYC2bg clade, and (iv) the CYC2d clade (Figure S2B)

Summary

Introduction

Morphological and structural innovations of flowers and inflorescences are intimately linked to the reproduction and adaptation of angiosperms (Endress, 2011; Kirchoff and Claßen-Bockhoff, 2013; Teo et al, 2014). Mainly the recently diverged lineages, exhibit a tendency to maximize reproductive efficiency by condensing heterogeneous flowers into a head-like inflorescence (Harris, 1999; Reuther and Claßen-Bockhoff, 2013). The evolution of such head-like inflorescences is usually correlated with the morphology and the arrangement of their component flowers (Classen-Bockhoff, 1990; Coen and Nugent, 1994). A heterogeneous capitulum has a flat radiate form, and its flowers differentiate into the marginal ray and the central tubular disc florets Such differentiation makes the capitulum functionally like a single flower and is termed a pseudanthium. Various types of capitulum are scattered throughout the phylogeny of the family, implying that parallel or convergent evolution may be involved in patterning the capitulum architecture (Harris, 1995; Panero and Funk, 2002, 2008; Funk et al, 2009)

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