Phylogenetic analysis of the “ECE” (CYC/TB1) clade reveals duplications predating the core eudicots

Abstract

Flower symmetry is of special interest in understanding angiosperm evolution and ecology. Evidence from the Antirrhineae (snapdragon and relatives) indicates that several TCP gene-family transcription factors, especially CYCLOIDEA (CYC) and DICHO-TOMA (DICH), play a role in specifying dorsal identity in the corolla and androecium of monosymmetric (bilateral) flowers. Studies of rosid and asterid angiosperms suggest that orthologous TCP genes may be important in dorsal identity, but there has been no broad phylogenetic context to determine copy number or orthology. Here, we compare published data from rosids and asterids with newly collected data from ranunculids, caryophyllids, Saxifragales, and Asterales to ascertain the phylogenetic placement of major duplications in the ''ECE'' (CYC͞TB1) clade of TCP transcription factors. Bayesian analyses indicate that there are three major copies of ''CYC'' in the ECE clade, and that duplications leading to these copies predate the core eudicots. CYC1 contains no subsequent duplications and may not be expressed in floral tissue. CYC3 exhibits similar patterns of duplication to CYC2 in several groups. Using RT-PCR, we show that, in flowers of Lonicera morrowii (Caprifoliaceae), DipsCYC2B is expressed in the four dorsal petals and not in the ventral petal. DipsCYC3B is expressed in flower and petal primordia, possibly most strongly in the ventral petal.CYCLOIDEA ͉ ECE clade ͉ floral symmetry ͉ gene duplication ͉ TCP

A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence

“…The greater genetic similarity within rather than among these groups suggests that many functionally important duplication events in the ECE gene subfamily occurred after the divergence of the Lamiales, Fabales, and Asteraceae lineages, respectively. The results of Howarth and Donoghue (16) are similar in this respect in that groupings within subclades CYC1, CYC2, and CYC3 are largely consistent with organismal phylogeny. Given this concurrence, we tested the phylogenetic distribution of our gene data when combined with many of the less-complete Dipsacales and Asterales sequences published by the former authors, and all well supported relationships were consistent with the results reported here (data not shown).…”

“…In Gerbera ray flowers, the expression of GhCYC2 was specifically excluded from the dorsal rudimentary petals, suggesting functional deviation from Lamiales and Fabaceae. A similarly ventral expression pattern was documented for a CYC3-subclade gene from Lonicera (Dipsacales), whereas a CYC2-subclade gene expressed dorsally (16). However, preliminary phylogenetic analyses including some of these authors' shorter sequences suggest that GhCYC2 belongs to the CYC2 subclade (data not shown).…”

“…Phylogenetic analysis based on the TCP domain has uncovered two subfamilies; PCF proteins form one clade (class I) whereas CYC/TB1 and CINCINNATA (CIN) group together to form the class II TCP proteins (15). The CYC/TB1 group is also called the ECE clade, within which three subclades, CYC1, -2, and -3, have been identified in core eudicots (16). TB1 has played a major role in the evolution of maize from its wild ancestor teosinte.…”

Evolution of Double Positive Autoregulatory Feedback Loops in CYCLOIDEA2 Clade Genes Is Associated with the Origin of Floral Zygomorphy

“…CYC and DICH encode proteins belonging to the plant-specific TEOSINTE BRANCHED1, CYCLOIDEA, and PCF (TCP) family of transcription factors (Cubas et al, 1999). Based on the TCP domain, members of the TCP family are classified into PCF (TCP-P or class I) and CYC/TB1 (TCP-C or class II) subfamilies (Cubas et al, 1999;Navaud et al, 2007), and the latter is further divided into CIN and ECE lineages (Howarth and Donoghue, 2006). Phylogenetic analyses show that two major duplication events within the ECE lineage took place just before the radiation of core eudicots; these duplication events gave rise to three clades, CYC1, CYC2, and CYC3 (Howarth and Donoghue, 2006).…”

“…Based on the TCP domain, members of the TCP family are classified into PCF (TCP-P or class I) and CYC/TB1 (TCP-C or class II) subfamilies (Cubas et al, 1999;Navaud et al, 2007), and the latter is further divided into CIN and ECE lineages (Howarth and Donoghue, 2006). Phylogenetic analyses show that two major duplication events within the ECE lineage took place just before the radiation of core eudicots; these duplication events gave rise to three clades, CYC1, CYC2, and CYC3 (Howarth and Donoghue, 2006). Increasing evidence indicates that CYC2 clade genes, specific for the core eudicots, were repeatedly recruited to function in the control of floral zygomorphy based on their strong, dorsoventrally asymmetric expression (Luo et al, 1996(Luo et al, , 1999Feng et al, 2006;Zachgo, 2007, 2009;Broholm et al, 2008;Gao et al, 2008;Kim et al, 2008;Wang et al, 2008Wang et al, , 2010Preston and Hileman, 2009;Song et al, 2009;Zhang et al, 2010;Howarth et al, 2011).…”