Genetic control of floral zygomorphy in pea ( Pisum sativum L.)

Abstract

Floral zygomorphy (flowers with bilateral symmetry) has multiple origins and typically manifests two kinds of asymmetries, dorsoventral (DV) and organ internal (IN) asymmetries in floral and organ planes, respectively, revealing the underlying key regulators in plant genomes that generate and superimpose various mechanisms to build up complexity and different floral forms during plant development. In this study, we investigate the loci affecting these asymmetries during the development of floral zygomorphy in pea (Pisum sativum L.). Two genes, LOBED STANDARD 1 (LST1) and KEELED WINGS (K), were cloned that encode TCP transcription factors and have divergent functions to constitute the DV asymmetry. A previously undescribed regulator, SYMMETRIC PETALS 1 (SYP1), has been isolated as controlling IN asymmetry. Genetic analysis demonstrates that DV and IN asymmetries could be controlled independently by the two kinds of regulators in pea, and their interactions help to specify the type of zygomorphy. Based on the genetic analysis in pea, we suggest that variation in both the functions and interactions of these regulators could give rise to the wide spectrum of floral symmetries among legume species and other flowering plants.symmetric petal ͉ dorsoventral asymmetry ͉ organ internal asymmetry ͉ KEELED WINGS ͉ LOBED STANDARD 1 F lower development in higher plants gives rise to an enormous variation of flower morphology and immense aesthetic diversification in nature. An important aspect for divergent floral developments is the establishment of floral symmetries, where a few distinct basic forms could be distinguished (1, 2): the monosymmetry (zygomorphy, with one symmetric plane), polysymmetry (actinomorphy, with several symmetric planes), and left-right asymmetry (with no symmetric plane). Among these, zygomorphy is considered the more specialized form and has been the most under investigation for its origin and underlying mechanisms.Fabaceae (legumes) is one of the largest families in angiosperm, with a range of floral symmetric forms, and its success is thought to be coupled with its predominant zygomorphic flowers (3, 4). Most zygomorphic flowers are found in the subfamily Papilionoideae (5, 6), which attracted the attention of researchers since the end of the 18th century (7). Darwin (8) demonstrated the role of this type of zygomorphy in pollination biology, and the special floral shape of papilionoid legumes was an important factor in Mendel's groundbreaking work on the laws of genetic inheritance in the 1850s. Pea flowers, like most zygomorphic flowers, possess prominent corolla with three petal types, which are arranged along a dorsoventral (DV) axis, and manifest two types of asymmetries: DV asymmetry in the floral plane and organ internal (IN) asymmetry in the floral organ plane (Fig. 1a). It is well documented that DV asymmetry in papilionoid legumes commences in the floral meristem when the asymmetric development of floral organ primordia occurs (Fig. 2a) (5, 6). However, IN asymmetry is variable among pet...

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

“…In snapdragon, floral zygomorphy is established mainly through the CYC/DICH dorsal identity function in controlling the fate of dorsal organs, namely, promoting dorsal petal growth and arresting dorsal stamen development (Luo et al, 1996(Luo et al, , 1999. Similar to CYC, L. japonicus CYC1/2 and pea (Pisum sativum) CYC1/2 in the Fabaceae specifically promote the growth of the single dorsal petal (Feng et al, 2006;Wang et al, 2008Wang et al, , 2010. However, in I. amara, a close relative of Arabidopsis, TCP1 dorsalspecific expression inhibits the growth of two dorsal petals (Busch and Zachgo, 2007).…”

“…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). Nevertheless, as a linkage between genotype and phenotype, the maintenance of expression of a gene that controls a key developmental process would be crucial in generating phenotypic effects (Crews and Pearson, 2009).…”

Evolution of flower shape in Plantago lanceolata

“…CYC-like genes are expressed in a generalized dorsoventral pre-pattern in meristems involved in both flower and shoot formation, even in species with actinomorphic flowers, suggesting that the origin of the genes predates their role in zygomorphy (Cubas et al 2001;Clark and Coen 2002). However, it is only in zygomorphic species that CYC-like gene expression is maintained during flower development in dorsal floral organs (Luo et al 1996;Luo et al 1999;Cubas et al 1999b;Feng et al 2006;Citerne et al 2006;Wang et al 2008). This acquisition and maintenance of CYC expression in dorsal floral organs may have been the driving force behind the evolution of dorsoventral floral asymmetry (Clark and Coen 2002).…”

“…In Mohavea, an expansion of the domain of expression of CYC-like genes during flower development correlates with this derived floral morphology . CYC-like genes have also played a role in the evolution of flower shape in legumes (Feng et al 2006;Citerne et al 2006;Wang et al 2008). In the zygomorphic papilinonoid legume Lupinus nanus, a CYC-like gene is expressed in dorsal floral regions in a pattern similar to Antirrhinum (Citerne et al 2006).…”

Comparative Morphology and Anatomy of Floral Symmetry in Legumes (Fabaceae)

“…The order of petal initiation in legumes is unidirectional, from dorsal to ventral, in its whorl (Tucker, 1987;. Some cyc-like genes were also isolated from various legumes, and it has been determined that floral zygomorphy of this group involves, not single, but duplicated cyc-like genes (Citerne et al, 2003;Fukuda et al, 2003;Feng et al, 2006;Wang et al, 2008). Gene duplication is probably the most important mechanism for generating new genes, new biochemical processes, and new functions that have facilitated the evolution of complex organisms from primitive ones (Force et al, 1999;Hughes, 1999;Lynch & Conery, 2000;Lynch & Force, 2000).…”