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An Apparent Reversal in Floral Symmetry in the Legume Cadia Is a Homeotic Transformation

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An Apparent Reversal in Floral Symmetry in the Legume Cadia Is a Homeotic Transformation An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation He´ le` ne L. Citerne*†‡, R. Toby Pennington*, and Quentin C. B. Cronk§ *Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh EH3 5LR, United Kingdom; †Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom; and §University of British Columbia Botanical Garden, Room 206, Campbell Building, 6804 Southwest Marine Drive, Vancouver, BC, Canada V6T 1Z4 Edited by Michael J. Donoghue, Yale University, New Haven, CT, and approved June 26, 2006 (received for review February 8, 2006) Within papilionoid legumes, characterized by flowers with strong bilateral symmetry, a derived condition within angiosperms, Cadia (Cadia purpurea) has reverted to radially symmetrical flowers. Here, we investigate the genetic basis of this morphological reversal. Two orthologues of the floral symmetry gene CYCLOIDEA (CYC) demarcate the adaxial (dorsal) region of the flower in typical papilionoid legumes. In the model legume Lotus japonicus, one of these LegCYC genes has been shown, like CYC, to be required for the establishment of floral bilateral symmetry. This study shows that these genes are expressed in the adaxial region of the typical papilionoid flower of Lupinus, which belongs to the same papil- ionoid subclade as Cadia.InCadia, these genes also are expressed, but the expression pattern of one of these has expanded from the adaxial to the lateral and abaxial regions of the corolla. This result suggests that the radial flowers of Cadia are dorsalized and, therefore, are not a true evolutionary reversal but an innovative homeotic transformation, where, in this case, all petals have acquired dorsal identity. This study raises a question over other putative reversals in animals and plants, which also may be cryptic innovations. developmental gene ͉ floral evolution ͉ CYCLOIDEA ͉ Leguminosae Fig. 1. Mature whole and dissected flower of L. nanus and C. purpurea.(a) (Fabaceae) Detail of an L. nanus flower, showing strong bilateral symmetry typical of papilionoid flowers. Individual standard (D, dorsal), wing (L, lateral), and keel (V, ventral) petals are shown, as well as the monadelphous (with united ost members of the plant family Leguminosae (Fabaceae) filaments) androecium with stamens of different lengths (lateral view on the Mhave flowers that are characterized by a single axis of left, and dissected dorsal and lateral͞ventral stamens on the right; the three symmetry (bilateral symmetry or zygomorphy). The majority of dorsal stamens are shorter than the lateral and ventral ones). (b) C. purpurea legume species, from the subfamily Papilionoideae and account- flowers are radially symmetrical, with equal dorsal (D), lateral (L), and ventral ing for Ϸ5% of all flowering plant species, are characterized by (V) petals and stamens. having typical ‘‘pea’’ (papilionoid) flowers with pronounced bilateral symmetry particularly in the corolla (illustrated here by The early development of Cadia (Cadia purpurea) flowers is Lupinus nanus; Fig. 1a). The typical papilionoid flower has three similar to that of most papilionoid species with zygomorphic distinctive petal types: a single upper (adaxial or dorsal) petal flowers where sepals, petals, and stamens are initiated unidi- (the ‘‘standard’’), two lateral petals (‘‘wings’’), and two lower rectionally, starting on the abaxial side (6). In typical papilionoid (abaxial or ventral) petals (‘‘keel’’ petals). The androecium of legumes, although organogenesis is asymmetric, a phase of typical papilionoids also is bilaterally symmetrical, with stamens uniform organ growth precedes the unequal development along of different lengths along the dorsoventral axis, the adaxial the dorsoventral axis, and differential organ development occurs EVOLUTION stamens being shorter (Fig. 1a). However, within the Papilion- at an advanced stage of floral ontogeny (7). By contrast, in C. oideae, a number of unrelated genera have radially or nearly purpurea, floral organs continue to develop equally after orga- radially symmetrical flowers. The flowers of these atypical nogenesis until maturity (6). Tucker (6) therefore interpreted the species frequently have been considered primitive (reviewed in phenotype of C. purpurea as ‘‘neotenous,’’ that is, retaining the ref. 1), but more recent phylogenetic studies suggest that they are characteristics of early flower development (uniform growth) derived from a zygomorphic ancestral state (2, 3). An example and not entering the asymmetric phase. In genetic terms, this is Cadia Forsk., a genus of seven species of small shrubs from interpretation suggests that the radial phenotype of C. purpurea Arabia, Madagascar, and eastern Africa. Cadia has actinomor- may be caused by a loss of expression of genes that affect floral phic pendent flowers in solitary or few-flowered axillary racemes (ref. 4; Fig. 1b). These flowers produce abundant nectar but no scent, suggesting these may be pollinated by birds (1). Conflict of interest statement: No conflicts declared. Cadia occupies a relatively isolated phylogenetic position (J. S. This paper was submitted directly (Track II) to the PNAS office. Boatwright and D. Edwards, personal communications) within Data deposition: The sequences reported in the paper for Lupinus nanus LEGCYC1A and the genistoid clade of papilionoid legumes (83 genera and 2,350 LEGCYC1B and Cadia purpurea LEGCYC1A and LEGCYC1B have been deposited in the species; ref. 5). Its closest relatives are from the tribe Podalyrieae GenBank database (accession nos. AY382156, AY382155, AY225826, and AY225825). (J. S. Boatwright and D. Edwards, personal communications), ‡To whom correspondence should be addressed. E-mail: h࿝[email protected]. which have typical zygomorphic papilionoid flowers. © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0600986103 PNAS ͉ August 8, 2006 ͉ vol. 103 ͉ no. 32 ͉ 12017–12020 Downloaded by guest on September 24, 2021 Fig. 3. RT-PCR analysis of LegCYC1A (1A) and LegCYC1B (1B) from whole- flower buds at early developmental stages (Ϸ1 mm diameter) and dissected floral tissue from L. nanus and C. purpurea flowers are later stages. The corolla and androecium in both species were dissected as described in Materials and Methods. Intron splicing in both genes allowed to distinguish between cDNA and genomic DNA. cDNA products amplified by actin-specific primers were used as a positive control. gDNA, genomic DNA; Ϫve, negative control (no template); D, dorsal; L, lateral; V, ventral. Fig. 2. Patterns of RNA in situ hybridization of LegCYC1A and LegCYC1B in L. nanus inflorescenses (a and b, respectively), with details of floral meristems at different development stages (d–f, LegCYC1A; g–i, LegCYC1B). Longitudi- side throughout floral development in another papilionoid le- nal sections of L. nanus inflorescences show floral meristems (fm) in the axil of gume, Lupinus (L. nanus), from the genistoid clade. L. nanus has bracts (B) on the abaxial side. More mature flowers are at the base of the inflorescence. RNA from LegCYC1A and LegCYC1B is detected in the adaxial typical zygomorphic pea flowers, suggesting that these genes are part of floral meristems before organogenesis (d and g) and during floral candidates for the control of floral symmetry in genistoid organ development (e, f, h, and i). Although both copies have a similar legumes. The expression of these two LegCYC genes is examined expression pattern, LegCYC1B appears to have a wider expression domain in the radially symmetrical flowers of Cadia (C. purpurea), which, than LegCYC1A. Negative control (sense probe) is shown (c). Ad, adaxial; Ab, like Lupinus, is a genistoid legume (2). Comparison of LegCYC abaxial; St, stamen; AbS, abaxial sepal. (Scale bars: a–c, 500 ␮m; d–h, 200 ␮m; expression pattern between an unusual legume such as C. f and i, 250 ␮m.) purpurea and a related zygomorphic species can illuminate the genetic basis of morphological reversal in relation to floral symmetry in legumes. The reversibility of evolution is an im- organ differentiation during the latter stage of development of portant problem, but few examples of apparent phenotypic typical zygomorphic papilionoid flowers. reversals have been investigated genetically (reviewed in ref. 13). Genes that are important for the control of floral symmetry Here, we establish whether the apparent reversal of floral have been identified in Antirrhinum majus L. (Veronicaceae, symmetry in Cadia is the result of loss of expression of candidate Lamiales) (8–10). Two closely related genes CYCLOIDEA genes, which could be described as ‘‘true reversal,’’ or is due to (CYC) and DICHOTOMA (DICH) demarcate the dorsal region modified gene expression causing the replication of ancestral of the flower and affect the development of floral organs along states. the dorsoventral axis. CYC and DICH expression is maintained throughout floral development in the adaxial region (8, 9). Results Double knockout mutants for CYC and DICH have a fully LegCYC1A and LegCYC1B RNA was detected in floral tissue of radially symmetric phenotype characterized by ventralization of L. nanus in a pattern similar to Antirrhinum CYC (ref. 8; Fig. 2). floral organs (i.e., resembling the ventral phenotype of wild-type Both genes were detected in floral meristems before organo- flowers) (8). genesis, on the adaxial side of the meristem (Fig. 2 d and g). At CYC͞DICH homologues have been identified in legumes, more advanced developmental stages, both
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