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Disruption of the Petal Identity Gene APETALA3-3 Is Highly Correlated with Loss of Petals Within the Buttercup Family (Ranunculaceae)

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Disruption of the Petal Identity Gene APETALA3-3 Is Highly Correlated with Loss of Petals Within the Buttercup Family (Ranunculaceae) Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae) Rui Zhanga,b,1, Chunce Guoa,b,1, Wengen Zhanga,b,1, Peipei Wanga,b, Lin Lia,b, Xiaoshan Duana,b,c, Qinggao Duc, Liang Zhaoc, Hongyan Shana, Scott A. Hodgesd, Elena M. Kramere, Yi Renc,2, and Hongzhi Konga,2 aState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; bUniversity of Chinese Academy of Sciences, Beijing 100049, China; cCollege of Life Sciences, Shaanxi Normal University, Xi’an 710062, China; dDepartment of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106; and eDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138 Edited by Masatoshi Nei, Pennsylvania State University, University Park, PA, and approved February 11, 2013 (received for review November 12, 2012) Absence of petals, or being apetalous, is usually one of the most plants (including the basal-most lineage, Amborella) (13-16), important features that characterizes a group of flowering plants raises the possibility that the genetic program for petal de- at high taxonomic ranks (i.e., family and above). The apetalous velopment was established before the diversification of extant condition, however, appears to be the result of parallel or angiosperms. Then, during evolution, this program has been fi convergent evolution with unknown genetic causes. Here we modi ed in different directions and to varying degrees, giving show that within the buttercup family (Ranunculaceae), apetalous rise to the production of a huge variety of petals and petaloid genera in at least seven different lineages were all derived from structures (6, 17). The petal identity program may have also been petalous ancestors, indicative of parallel petal losses. We also inactivated multiple times, leading to the independent origins of show that independent petal losses within this family were apetalous groups in different evolutionary lineages (2, 4, 18, 19). Interestingly, some of the apetalous groups, such as the piper strongly associated with decreased or eliminated expression of (Piperaceae), sandalwood (Santalaceae), mulberry (Moraceae), a single floral organ identity gene, APETALA3-3 (AP3-3), appar- fi elm (Ulmaceae), nettle (Urticaceae), birch (Betulaceae), oak ently owing to species-speci c molecular lesions. In an apetalous (Fagaceae), and walnut (Juglandaceae) families, as well as several mutant of Nigella, insertion of a transposable element into the genera within the buttercup family (Ranunculaceae), are very second intron has led to silencing of the gene and transformation rich in species diversity, suggesting that loss of petals is not of petals into sepals. In several naturally occurring apetalous gen- necessarily disadvantageous. era, such as Thalictrum, Beesia, and Enemion, the gene has either Ranunculaceae is a large, globally distributed family that con- been lost altogether or disrupted by deletions in coding or regu- sists of around 1,800 species in about 50 genera (20). The family latory regions. In Clematis, a large genus in which petalous species has been the focus of centuries of morphological, anatomical, evolved secondarily from apetalous ones, the gene exhibits hall- systematic, evolutionary, and phytochemical studies owing to its marks of a pseudogene. These results suggest that, as a petal unusual position in the angiosperm phylogeny, enormous di- identity gene, AP3-3 has been silenced or down-regulated by dif- versity in reproductive and vegetative structures, and wide orna- ferent mechanisms in different evolutionary lineages. This also mental and medical uses. Petals in this family are of particular suggests that petal identity did not evolve many times indepen- interest because they show tremendous diversity in both appear- dently across the Ranunculaceae but was lost in numerous instan- ance and function (20). In many species, petals are laminar, pel- ces. The genetic mechanisms underlying the independent petal tate, tubular, labiate, or cup-shaped and possess spurs or scale-/ losses, however, may be complex, with disruption of AP3-3 being pocket-like structures that secrete nectar. In others, petals are either cause or effect. equally showy, attractive, and specialized but do not produce nectar, suggestive of shifts in function. There are also genera in ABC model | development | flower | parallel evolution which petals are entirely missing and the attractive function is fulfilled mostly by sepals, which are commonly showy, attractive, and petaloid across the family, while stamens occupy the positions etals are sterile floral organs that lie between the outer sepals where petals are expected to be. Based on comparative morpho- Pand the inner reproductive parts (i.e., stamens and carpels) of logical and anatomical studies, it has been proposed that petals in a flower with a dimorphic perianth. Compared with sepals, which this and related families (such as Berberidaceae, Menispermaceae, are the outermost parts of the flower, petals are usually brightly and Lardizabalaceae) are all andropetals that resulted from in- colored and/or unusually shaped to attract pollinators. Petals dependent modifications of stamens (1, 2). Recent phylogenetic show tremendous diversity in number, size, shape, structure, analyses, however, tend to support the idea that having petals, or arrangement, orientation, and coloration, and are believed to be being petalous, is an ancestral character state whereas being results of both divergent and parallel/convergent evolution (1, 2). apetalous is a derived one (21, 22). Indeed, when the two states of Traditional morphological and anatomical studies have proposed this character were mapped onto the phylogenetic tree of the that petals originated multiple times in different lineages, either family, it became evident that in at least seven lineages apetalous from stamens (andropetals) or from sepals (bractopetals) (3, 4). Recent studies, however, tend to suggest that although andro- petals and bractopetals are morphologically and anatomically Author contributions: C.G., Y.R., and H.K. designed research; R.Z., W.Z., P.W., L.L., X.D., Q.D., distinguishable, they share a common developmental program L.Z., and H.S. performed research; R.Z., C.G., W.Z., and H.K. analyzed data; and R.Z., H.S., (i.e., process homology) (5–7). According to the “ABC”, “ABCE”, S.A.H., E.M.K., and H.K. wrote the paper. and “Quartet” models for flower development, this program The authors declare no conflict of interest. requires combinational activities of A-, B-, and E-class genes, the This article is a PNAS Direct Submission. representatives in the model plant Arabidopsis thaliana (here- 1R.Z., C.G., and W.Z. contributed equally to this work. after called Arabidopsis) being APETALA1 (AP1), APETALA3 2To whom correspondence may be addressed. E-mail: [email protected] or renyi@snnu. (AP3) and PISTILLATA (PI), and SEPALLATA1-4 (SEP1-4), edu.cn. – respectively (8 12). The fact that counterparts (or orthologs) of This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. these genes are expressed in petaloid organs across flowering 1073/pnas.1219690110/-/DCSupplemental. 5074–5079 | PNAS | March 26, 2013 | vol. 110 | no. 13 www.pnas.org/cgi/doi/10.1073/pnas.1219690110 Downloaded by guest on September 24, 2021 genera have had petalous ancestors (Fig. 1 and Fig. S1). This heracleifolia; hereafter called Thalictrum, Beesia, Enemion,and suggests that, rather than being independently gained many times, apetalous Clematis, respectively) were sampled, each of which petals have been lost in parallel in different lineages during the represents a separate lineage (Fig. 1 and Fig. S1). Because these evolution of the Ranunculaceae. apetalous species are only distantly related to each other, we also The mechanism underlying the parallel petal losses within the included four petalous species (Leptopyrum fumarioides, Souliea Ranunculaceae is still unclear. However, recent studies indicated vaginata, Isopyrum manshuricum,andClematis macropetala; that absences of petals in this and related families are correlated hereafter called Leptopyrum, Souliea, Isopyrum,andpetalous with lack of the expression of a floral organ identity gene, AP3-3 Clematis, respectively) as references. In addition, as has been (7, 23, 24). AP3-3 is an AP3-like gene, which, along with its two pointed out by several authors, petals of the Clematis species may closest paralogs, AP3-1 and AP3-2, was generated through two have been derived from stamens secondarily and recently, and as successive gene duplication events before the divergence of the such are no longer homologous to those in other petalous genera Ranunculaceae from its allies (7, 24). In the species that possess (20, 25); our own ancestral character state reconstruction also petals, AP3-3 orthologs are specifically expressed in petal pri- supports this viewpoint (Fig. S1). For this reason, we included mordia and developing petals, with their transcripts being de- Ranunculus japonicus (hereafter called Ranunculus)asasecond tectable by using the conventional reverse transcription- petalous reference to the apetalous Clematis. More interestingly, polymerase chain reaction (RT-PCR) and in situ hybridization during the study, we encountered a “Double Sepal” mutant of techniques. In the species lacking petals, however, AP3-3 ex- Nigella damascena (hereafter called
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