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Control of Petal Shape and Floral Zygomorphy in Lotus Japonicus

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Control of Petal Shape and Floral Zygomorphy in Lotus Japonicus Control of petal shape and floral zygomorphy in Lotus japonicus Xianzhong Feng*†, Zhong Zhao†‡, Zhaoxia Tian*†, Shilei Xu*, Yonghai Luo*, Zhigang Cai*, Yumei Wang*, Jun Yang*, Zheng Wang*, Lin Weng*, Jianghua Chen*, Leiying Zheng*, Xizhi Guo*, Jianghong Luo*, Shusei Sato§, Satoshi Tabata§, Wei Ma¶, Xiangling Cao*, Xiaohe Hu*, Chongrong Sun‡ʈ, and Da Luo*¶ʈ *National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Graduate School of the Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200032, China; ‡School of Life Sciences, Fudan University, Shanghai 200433, China; §Kazusa DNA Research Institute, 2-6-7 Kazusa-kamatari, Kisarazu, Chiba 292-0818, Japan; and ¶School of Life Science and Biotechnology, Shanghai Jiao Tong University, Shanghai 200030, China Communicated by Enrico Coen, John Innes Centre, Norwich, United Kingdom, January 26, 2006 (received for review November 8, 2005) Zygomorphic flowers, with bilateral (dorsoventral) symmetry, are genes (15–17). When both CYC and DICH are mutated, more considered to have evolved several times independently in flow- petals and stamens are developed in the dorsal region, and all petals ering plants. In Antirrhinum majus, floral dorsoventral symmetry resemble the shape of ventral petal. Thus, CYC and DICH could depends on the activity of two TCP-box genes, CYCLOIDEA (CYC) have a dual role in the control of zygomorphic development: an and DICHOTOMA (DICH). To examine whether the same molecular early one affecting primordium initiation and controlling floral mechanism of floral asymmetry operates in the distantly related asymmetry, and a later one affecting organ asymmetry and other Rosid clade of eudicots, in which asymmetric flowers are thought morphological characters (11, 12). It has been further proposed that to have evolved independently, we investigated the function of a the petal asymmetry arises through a series of steps in which the CYC homologue LjCYC2 in a papilionoid legume, Lotus japonicus. expression patterns of CYC and DICH are progressively elaborated We showed a role for LjCYC2 in establishing dorsal identity by and maintained (12), and thus development of floral and petal altering its expression in transgenic plants and analyzing its mu- asymmetries are closely related. Because TCP-box genes have been tant allele squared standard 1 (squ1). Furthermore, we identified a found widely in higher plant genomes (7, 14), it is possible to test lateralizing factor, Keeled wings in Lotus 1 (Kew1), which plays a whether CYC like genes are involved in the development of key role in the control of lateral petal identity, and found LjCYC2 zygomorphy in different species. In some close relatives of Antir- interacted with Kew1, resulting in a double mutant that bore all rhinum, several CYC orthologues have been found to play a similar petals with ventralized identity to some extents. Thus, we dem- role in the control of floral symmetry (18, 19), but other studies onstrate that CYC homologues have been independently re- suggest that the bilaterally symmetrical flowers in some families of cruited as determinants of petal identities along the dorsoventral the same Asterid clade might not require orthologues or functional axis in two distant lineages of flowering plants, suggesting a analogues of CYC or DICH (6, 20). So far, because of lack of an common molecular origin for the mechanisms controlling floral amenable experimental system, most studies have relied on iden- zygomorphy. tification of CYC homologues and investigation of their expression patterns, and little robust functional analysis in the distantly related dorsoventral axis ͉ floral development ͉ keeled wings in Lotus ͉ species has been reported. LjCYC2 ͉ squared standard In legumes, a number of CYC-like genes have been isolated and found to have undergone repeated duplication events, loral zygomorphy (dorsoventral asymmetry) is an evolution- suggesting that they might have divergent functions (21, 22). To Fary adaptation that facilitates outcrossing by attracting pol- investigate the molecular mechanisms underlying the develop- linators (1–7). The phenomenal diversity in Leguminosae (Rosid ment of different zygomorphic flowers among angiosperms, we clade of eudicots), the third largest family of flowering plants explored a model legume, Lotus japonicus (9, 10), and examined with Ϸ20,000 species (8), is often explained by successful co- whether the CYC homologues also play a role in the control of evolution with pollinators. In the subfamily Papilionoideae floral asymmetry in this papilionoid legume. We demonstrated (12,000 spp.) to which Lotus japonicus (9, 10) belongs, most that a CYC-like gene in L. japonicus, LjCYC2, has a dorsalizing species have specialized zygomorphic ‘‘pea’’ flowers with three activity during petal development, similar to CYC and DICH, types of petals, which are arranged along a dorsoventral axis: a even though the zygomorphy of Leguminosae is believed to have single bilaterally symmetrical petal (standard) in the dorsal evolved separately from the Lamiales (1, 6, 7, 13). Furthermore, position, two asymmetric lateral petals (‘‘wings’’) and two asym- we identified a lateralizing factor, keeled wings in Lotus 1 (Kew1), metric ventral petals which form a ‘‘keel’’ (Fig. 1 A and B). In which plays a key role in the control of lateral petal identity, and contrast, Antirrhinum majus, a well studied member in Lamiales found that LjCYC2 interacted with Kew1, resulting in a double (Asterid clade) (11, 12), possesses two asymmetrical dorsal mutant bearing all petals with ventralized identity to a different petals, two asymmetrical lateral petals, and a single bilaterally extent. Our data show that CYC homologues have been inde- symmetrical ventral petal (Fig. 1 C and D). It is believed that the pendently recruited to the control of floral zygomorphy in zygomorphy of Leguminosae has evolved separately from the distantly related lineages, suggesting that their dorsal activity Lamiales (6, 13). Although the different internal symmetries of should be a primary and synapomorphic function during the the counterpart petals in L. japonicus and A. majus are consistent evolution of dorsoventral specification. with the independent evolution of zygomorphy in these two lineages, both are a response to a dorsoventral axis, suggesting that there could be a divergence in the make up of the mecha- Conflict of interest statement: No conflicts declared. nism to determine the axis in the control of zygomorphic See Commentary on page 4801. developments in the two distantly related species. †X.F., Z.Z., and Z.T. contributed equally to this work. In A. majus, the development of zygomorphic flower requires the ʈTo whom correspondence may be addressed. E-mail: [email protected] or kmcao@ activity of two TCP-box genes (14), CYC and DICH (11, 12), whose fudan.edu.cn. function is mediated through an interaction with some specific MYB © 2006 by The National Academy of Sciences of the USA 4970–4975 ͉ PNAS ͉ March 28, 2006 ͉ vol. 103 ͉ no. 13 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0600681103 Downloaded by guest on September 24, 2021 SEE COMMENTARY Fig. 1. Development and comparison of zygomorphic flowers. Zygomorphic flowers and petals of L. japonicus (A and B) and Antirrhinum (C and D) are shown. In the case of Antirrhinum, only the lobes of petals are shown. Lines Fig. 2. Molecular and phylogenetic analysis of LjCYC2 and identification of a with arrow show the direction of floral dorsoventral axis; triangle indicates mutant allele. (A) Alignment of putative protein sequences of LjCYC2 and CYC. the keel; D, V, direction of the floral dorsoventral axis. Red broken lines TCP domain is underlined with straight lines and R domain is underlined with indicate internal symmetry of different petals; DP, dorsal petal; LP, lateral waved lines (7). Triangle indicates position of the intron in LjCYC2.(B) A point mutation (blue) occurred at the intron (red) splicing site of LjCYC2 in squ1, which petal; VP, ventral petal. (Scale bars, 1.0 cm.) (E–K) Developmental stages of I2 consequently gives rise to a putative shorter protein with five new amino acids at in L. japonicus Gifu B-129. At stage 1 (I2-1), I2 initiates in the axil of compound the C terminus. (C) The unsplicing of intron in squ1 was confirmed by RT-PCR using leaf in I1 (E). When all floral meristems are developed at I2-7, the unidirectional BIOLOGY development of floral organs manifests the direction of the dorsoventral axis two primers nested to the intron. The transcript from squ1 is unspliced, larger (380 bp) than the one from wild type (150 bp), and LjUbi is used as the control for DEVELOPMENTAL (K, lines with arrow). Star, degenerate meristem of I2; triangle, bract primor- dium; F, floral meristem. (Scale bars, 50 ␮m.) (L–N) The shapes of dorsal, lateral, template quantity. (D) Unrooted phylogram of protein NJ analysis of TCP domain and ventral petals in the wild type at late developmental stages. The mature region suing MGA3.1 (24). Branches with bootstrap support (1,000 replicates) Ն dorsal petal processes blade (triangle) and claw (arrow), and the lateral and 50% are indicated for each branch. All of the TCPs genes are from Arabidopsis ventral petals have blades (triangles) and stipes (arrows). (Scale bars, 1.0 mm.) (25); CYC and DICH, Antirrhinum; LCYC, Linaria vulgaris; LjCYCs, L. japonicus; PCFs, rice; TB1, maize. Results more slowly than those in the ventral region. During late floral Inflorescence and Floral Development in L. japonicus. L. japonicus development, three types of petals develop along the dorsoven- (Gifu B-129) (9) is a perennial herb. When starting reproductive tral axis, and a key morphological landmark is the differentiation growth, each shoot becomes a primary inflorescence (I1), and produces a secondary inflorescence meristem (I ) at each node. of the vascular veins in petals. The various shapes of different 2 petals are distinctive (Fig. 1L) when the primary veins initiate in Floral meristems are generated from I2.
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