Evolution and Expression Patterns of TCP Genes in Asparagales

Abstract

CYCLOIDEA-like genes are involved in the symmetry gene network, limiting cell proliferation in the dorsal regions of bilateral flowers in core eudicots. CYC-like and closely related TCP genes (acronym for TEOSINTE BRANCHED1, CYCLOIDEA, and PROLIFERATION CELL FACTOR) have been poorly studied in Asparagales, the largest order of monocots that includes both bilateral flowers in Orchidaceae (ca. 25.000 spp) and radially symmetrical flowers in Hypoxidaceae (ca. 200 spp). With the aim of assessing TCP gene evolution in the Asparagales, we isolated TCP-like genes from publicly available databases and our own transcriptomes of Cattleya trianae (Orchidaceae) and Hypoxis decumbens (Hypoxidaceae). Our matrix contains 452 sequences representing the three major clades of TCP genes. Besides the previously identified CYC specific core eudicot duplications, our ML phylogenetic analyses recovered an early CIN-like duplication predating all angiosperms, two CIN-like Asparagales-specific duplications and a duplication prior to the diversification of Orchidoideae and Epidendroideae. In addition, we provide evidence of at least three duplications of PCF-like genes in Asparagales. While CIN-like and PCF-like genes have multiplied in Asparagales, likely enhancing the genetic network for cell proliferation, CYC-like genes remain as single, shorter copies with low expression. Homogeneous expression of CYC-like genes in the labellum as well as the lateral petals suggests little contribution to the bilateral perianth in C. trianae. CIN-like and PCF-like gene expression suggests conserved roles in cell proliferation in leaves, sepals and petals, carpels, ovules and fruits in Asparagales by comparison with previously reported functions in core eudicots and monocots. This is the first large scale analysis of TCP-like genes in Asparagales that will serve as a platform for in-depth functional studies in emerging model monocots.

Evolution of RADIALIS and DIVARICATA gene lineages in flowering plants with an expanded sampling in non‐core eudicots

“…In Phalaenopsis equestris , two CYC genes exhibit differential dorsiventral expression in the floral bud, suggesting species specific roles in bilateral symmetry establishment, but no studies have been done on downstream MYB target genes (Lin et al., ). Our results suggest important variation in the genetic control of perianth symmetry across studied species in Orchidaceae that should be integrated with the expression pattern of the AGL6‐like and AP3‐like genes responsible for lip identity and differentiation from the lateral petals (Hsu et al., ; Huang and Irish, ; Madrigal et al., ; Zhang et al., ). However, the genetic regulatory network for bilateral symmetry is at least partially conserved in the differentiation between lateral petals and the lip in different species of Orchidaceae.…”

“…Homogeneous dorsiventral expression of RAD and DIV genes in A. fimbriata coincides with previous observations of broad CYC ‐ like expression patterns in the perianth in this and other Aristolochia species (our unpublished data; Horn et al., ). Altogether, the data point to early‐diverging angiosperms with bilateral flowers having recruited genes other than CYC , RAD , and DIV to control cell proliferation (Hsu et al., ; Pabón‐Mora et al., ; Suárez‐Baron et al., ; Madrigal et al., ). Thus, it is possible that the ancestral function of all CYC‐RAD‐DIV genes is not linked to the establishment of dorsiventral symmetry and that the bilateral symmetry genetic network established for model species like A. majus was established before the diversification of eudicots and monocots.…”

“…It is likely that the duplication event responsible for the AspDIV1 and AspDIV2 clades is linked to the WGD identified in the Asparagus genome likely predating all Asparagales (Harkess et al., ). As in other gene lineages, there are Orchidaceae‐specific duplications that increase gene copy number and may be linked to the species diversification and morphological changes within the family (Cai et al., ; Lin et al., ; Madrigal et al., ; Mondragón‐Palomino, ; Mondragón‐Palomino and Theißen, , ; Yan et al., ; Zhang et al., , ).…”

“…Available genomes for orchids include Phalaenopsis equestris and Dendrobium catenatum (Cai et al., ; Zhang et al., ). In addition to these databases, we performed searches on our own generated transcriptomes from Aristolochia fimbriata , Cattleya trianae , and Hypoxis decumbens (Madrigal et al., ; Pabón‐Mora et al., ). These were generated from pooled reproductive meristems, floral buds at different developmental stages, fruits, and leaves.…”

Evolution of the process underlying floral zygomorphy development in pentapetalous angiosperms

“…Some of these shifts in floral symmetry seem related to shifts in species diversification rates (Cubas, 2004; Sargent, 2004; Armbruster and Muchhala, 2009; Vamosi and Vamosi, 2010; O’Meara et al, 2016). Recent work in developmental genetics has begun to reveal the molecular mechanisms underlying the development of the diverse zygomorphic flowers in angiosperms (Citerne et al, 2010; Busch et al, 2014; Hileman, 2014b; Madrigal et al, 2017). While these researches have advanced our knowledge on the evolution of floral symmetry, how the particularities of development in individual clades influence the course of morphological evolution of zygomorphy in those clades has rarely been investigated.…”