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Progress in Research on CYC-like Genes in Fabaceae
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This entry is adapted from the peer-reviewed paper 10.3390/cimb45030131

CYCLOIDEA (CYC)-like genes belong to the TCP transcription factor family and play important roles associated with flower development. The CYC-like genes in the CYC1, CYC2, and CYC3 clades resulted from gene duplication events. The CYC2 clade includes the largest number of members that are crucial regulators of floral symmetry. To date, studies on CYC-like genes have mainly focused on plants with actinomorphic and zygomorphic flowers, such as Fabaceae species, and the effects of CYC-like gene duplication events and diverse spatiotemporal expression patterns on flower development. The Fabaceae species are diverse in floral symmetry and are suitable for exploring the evolution and underlying mechanism of floral symmetry. 

CYCLOIDEA (CYC)-like gene TCP transcription factor family CYC2 clade floral symmetry Fabaceae molecular regulatory mechanism phylogeny

1. Introduction

Cubas et al. first proposed the concept of the TCP transcription factor family, which is named according to the first letters of TEOSINTE BRANCHED 1 (TB1) in maize (Zea mays), CYCLOIDEA (CYC) in snapdragon (Antirrhinum majus), and PROLIFERATING CELL FACTOR 1 and 2 (PCF1 and PCF2) in rice (Oryza sativa) [1][2][3][4][5]. Genes encoding proteins with the TCP domain are involved in the regulation of angiosperm growth and development [6][7][8][9]. The TCP family members contain a highly conserved TCP domain, which forms a basic helix–loop–helix (bHLH) structure associated with DNA binding and protein dimerization [10][11]. TB1 is a major regulator of stem and lateral bud growth and the male flower formation of maize, rice, wheat, and other crops [12][13][14], whereas CYC controls the floral dorsal organ characteristics in snapdragon [1][15], and both PCF1 and PCF2 bind to the promoter of PROLIFERATING CELL NUCLEAR ANTIGEN (PCNA), which is crucial for DNA replication and repair, chromatin structure maintenance, chromosome isolation, and the cell cycle in rice [3]. According to their different domains, the members of the TCP family have been divided into the following two categories: TCP-P and TCP-C [16][17][18]. Moreover, TCP-C has been subdivided into the ECE (CYC/TB1) and CINCINNATA (CIN) clades [19][20].
The CYC genes belong to the ECE clade, which is unique to angiosperms [21][22]. In addition to the TCP and R domain sequences, CYC genes encode the glutamate–cysteine–glutamic acid (ECE) motif specific to core eudicots [23][24][25]. Phylogenetic analysis has indicated that CYC genes in angiosperms experienced two major gene duplication events, which led to the formation of the CYC1, CYC2, and CYC3 clades [26][27][28]. In different evolutionary lineages, gene duplication events occurred in each branch at different time points during evolution [29][30][31][32][33][34][35], as shown in Figure 1. A more thorough analysis of the CYC2 subgroup confirmed that they are key regulatory genes for the bilateral symmetry of flowers [36][37][38].
Cimb 45 00131 g001
Figure 1. Phylogenetic tree of selected CYC-like genes in angiosperms. The number beside each node is the bootstrap support value.

2. Progress in Research on CYC-like Genes in Fabaceae

The Fabaceae species are distributed worldwide. Because of their diversity in floral symmetry, legumes are suitable for exploring the evolution and underlying mechanism of floral symmetry [39]. Researchers have screened the Fabaceae for homologs of snapdragon CYC genes and then analyzed their functions to clarify the role of CYC-like genes in angiosperm floral development. The differences among the diverse species in terms of the CYC-like genes responsible for floral symmetry revealed a new regulatory system.
The duplication of CYC homologues gave rise to three copies of ECE clade genes in the TCP family in Lotus Japonicus [40]. In L. japonicus, both LjCYC1 and LjCYC2 mediate the development of asymmetrical inflorescences and flowers, and changes in the number of petals and wing and keel morphology were observed in transgenic plants separately overexpressing LjCYC1 and LjCYC2 [40]. The asymmetrical expression pattern of LjCYC2 is similar to that of the snapdragon CYC gene in the developing flower primordium [40]. However, LjCYC2 is also expressed in the inflorescence primordium of L. japonicus, whereas the CYC gene is expressed only during floral primordium development in snapdragon [4].
Citerne et al. reported that the homologous genes of CYC in legumes can be divided into two major classes, ECE groups I and II, which are the result of an early duplication event [41]. ECE I can be further divided into two subclasses, IA and IB, which originated from duplication near or prior to the divergence of legumes. The LEGCYC genes in Lupinus are homologous to the regulatory gene CYC that controls the floral symmetry and paraxial floral organ characteristics of snapdragon and its related species [42]. Ree et al. suggested based on a molecular evolutionary analysis that positive selection has played a role in the evolution of the LEGCYC1B lineage, which is closely associated with floral morphological changes in Lupinus. Papilionoideae have strongly bilaterally symmetrical flowers, whereas Cadia purpurea flowers show radial symmetry associated with the expression of two CYC homologous genes (LEGCYCs) in the dorsal region of the flower [39]. In addition, the expression pattern of one gene has expanded from the paraxial to the lateral and posterior regions of the corolla, which may result in reversion to evolutionarily regressive petal characters.
Wang et al. determined that the expression of three endogenous LjCYC genes is specifically inhibited by different RNAi transgenes [43]. A chimeric RNAi transgene containing LjCYC1- and LjCYC2-specific sequences down-regulated the expression of both endogenous genes. The effect of silencing the three LjCYC genes was mainly confined to the dorsal or lateral part of the petals, implying that the genes are associated with dorsal and lateral activities during the development of zygomorphic flowers [43]. Knockdown of the three LjCYC genes may result in wild-type petals that resemble ventral petals, complete organ internal (IN) asymmetry, and the lack of dorsoventral (DV) pathway-differentiated flowers. This suggests that DV asymmetry during the development of zygomorphic flowers is controlled by LjCYC genes, whereas floral organ IN asymmetry is independently determined by other genetic factors.
The mutation of CYC2 in Lathyrus odoratus causes a change in dorsoventral petal type, resulting in a hooded (hdd) flower mutant with an epidermis and the pigmentation characteristic of a wing petal, and with a concave standard petal, the same as the lobed standard (lst1) mutant in Pisum [44]. Differences in CYC expression and activity may lead to differences in dorsal petal morphology in Fabaceae, and play a role in the negative regulation of petal edge growth in Lathyrus, mainly maintaining the flatness of the dorsal petal [45]. Interestingly, Ojeda et al. found that changes in the timing of LjCYC2 expression during pollination of Lotus by bees and birds may be responsible for changes in flower petal micromorphology and size, whereas changes in the spatial distribution of gene expression had no effect on pollination [46].
Feng et al. determined that the upstream promoter regions of GmCYC genes vary in number and type of hormone response elements in Glycine max [47]. The expression of GmCYC genes is involved in different growth and developmental stages, induced by abscisic acid, brassinosteroids, aminocyclopropane–1–carboxylic acid, salicylic acid, and methyl jasmonate signals [47]. The CYC-like genes may have undergone multiple duplications and losses in different Fabaceae lineages and formed the distinct homologous clades CYC1 and CYC2, but the CYC3 clade was most likely lost [48]. The ancestors of Papilionoideae and Caesalpinioideae probably possessed two CYC1 gene copies, but one of the copies was subsequently lost in Papilionoideae and was retained only in a few species of Caesalpinioideae [48]. The CYC2 gene was replicated more frequently in Papilionoideae than in other legumes [48]. The diversity patterns of CYC1 and CYC2 genes are not associated with floral symmetry in non-papilionoid legumes, but the replication and functional differentiation of CYC2 genes is necessary for floral symmetry in Papilionoideae [48].
The expression pattern of VrCYC3, which is homologous to L. japonicus LjCYC3 and pea PsCYC3, differs from that of VrCYC1 and VrCYC2 in the dorsal, lateral, and ventral petals in mung bean (Vigna radiata) [49]. In addition, VrCYC3, which is localized to the nucleus, can induce transcription [49]. Moreover, it can interact with VrCYC1 and VrCYC2 in yeast cells, but this interaction is weakened by the deletion of two amino acid residues in its R domain [49]. This suggests that LjCYC3/PsCYC3/VrCYC3 play a conserved role in determining the lateral petals' shape, and the formation of symmetrical and asymmetrical flowers in Fabaceae.

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Subjects: Biochemistry & Molecular Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Yuhong Chai
,
Hua Liu
,
Wendan Chen
,
Chenghu Guo
,
Haixia Chen
,
Xi Cheng
,
Dongliang Chen
,
Chang Luo
,
Xiumei Zhou
,
Conglin Huang
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Update Date: 09 Mar 2023
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