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Floral Development in Legumes1 Update on Floral Development Floral Development in Legumes1 Shirley C. Tucker* Department of Ecology, Environment, and Marine Biology, University of California, Santa Barbara, California 93106–9610 Species of flowering plants are most reliably iden- center of the flower is superior in position; i.e. its tified by their flowers, the sexually reproductive or- base is attached at the same level as those of the Downloaded from https://academic.oup.com/plphys/article/131/3/911/6111090 by guest on 01 October 2021 gans. A flower is similar to a vegetative short shoot sepals, petals, and stamens. The carpel differentiates (lacking appreciable internodes) that bears four kinds as a gynoecium with ovary, style, and stigma, and of laterally attached organs in successive whorls: se- eventually forms a pod-like fruit. Although most pals, petals, stamens, and carpels. Significant floral people think of papilionoid-type flowers (or flag distinctions among plant families include symmetry, flowers; Fig. 1A, F) as representative of legumes, whether organs are organized in whorls or helically, many legume taxa differ markedly from this type of number of parts per whorl, carpel position relative to flower (Fig. 1, B–E; Tucker, 1987a). the surrounding organs, fusion among organs within Superimposed upon this basic floral ground plan a whorl or between different whorls, and whether are prominent differences among the three legume both male and female organs are present in the same subfamilies. These include differences in flower posi- flower. tion in the inflorescence, floral symmetry, sepal and A flower, like a vegetative shoot, has a terminal petal aestivation, fusion, loss or increase of floral or- floral apical meristem that initiates organs laterally, gan number, heterogeneous organs within a whorl, usually in acropetal succession (although exceptions unisexual flowers, etc. Ontogenetic differences among are common in some taxa): sepals first, followed by the subfamilies are of particular interest. petals, stamens, and carpels. Because each flower With this background in mind, I will describe the lives for a very short time, the floral apical meristem details of floral development in each subfamily of is determinate, meaning that it ceases activity after a legumes. These details are necessary as a foundation certain number of organs have initiated. Vegetative for molecular studies on legume flower develop- apical meristems, in contrast, are usually indetermi- ment and organ identity relative to the ABC model nate, continuing to initiate new organs, such as (Meyerowitz et al., 1991; Irish, 1999; Jack, 2001). leaves, indefinitely. In this Update, I will focus on flowers of the plant SUBFAMILY CAESALPINIOIDEAE family Fabaceae. This family comprises three large subfamilies: Caesalpinioideae, Mimosoideae, and The subfamily Caesalpinioideae encompasses 170 Papilionoideae. Although the family is widely ac- genera and about 3,000 species. It has a basal position cepted as monophyletic (Chappill, 1995; Doyle, 1995; in phylogenetic schemes (Doyle, 1995; Doyle et al., Doyle et al., 2000), these subfamilies differ greatly in 2000; Bruneau et al., 2001) and is highly diverse in floral symmetry. Fabaceae is a large family (about floral form and ontogeny. It is currently divided into 700 genera and about 18,000 species), and is nearly four or five tribes: Cercideae, Caesalpinieae, Cass- ubiquitous over temperate and tropical parts of the ieae, and Detarieae, with Macrolobieae (derived from world (Polhill and Raven, 1981). Many agronomically within Detarieae) recently gaining acceptance. important plants are members of this family. The information base is huge, and the taxa are relatively Inflorescences easy to obtain. Most legume flowers share a pentamerous ground Caesalpinioid inflorescences are usually racemes or plan with five sepals, five petals, two whorls of five panicles, although solitary flowers and cymes occur stamens each, and a single carpel, or 21 organs in all. more often than in either of the other subfamilies. A Members of each of the four whorls alternate with raceme, as in Senna didymobotrya (Fres.) Irwin & Barn. those of the preceding whorl. The single carpel at the (Fig. 2A; Tucker, 1996), is the most common kind of inflorescence among legumes. Racemes, together 1 with panicles, spikes, and some umbels, have a ter- The research was supported in part by the National Science minal apical meristem that grows indeterminately Foundation (grant nos. BSR84–18922, BSR87–22514, DEB92–07671, and DEB94–20158 [DEB–9596281]) and by Louisiana State Univer- and initiates bracts (modified leaves) in acropetal sity (Baton Rouge; Boyd Professor funds). succession along the inflorescence axis. A single flo- * E-mail [email protected]; fax 805–893–4724. ral bud is initiated in the axil of each bract. A pair of Article, publication date, and citation information can be found bracteoles (reduced leafy organs) is usually produced at www.plantphysiol.org/cgi/doi/10.1104/pp.102.017459. below each flower. Developmental differences distin- Plant Physiology, March 2003, Vol. 131, pp. 911–926, www.plantphysiol.org © 2003 American Society of Plant Biologists 911 Tucker Downloaded from https://academic.oup.com/plphys/article/131/3/911/6111090 by guest on 01 October 2021 Figure 1. A through F, Drawings of legume flowers. A, “Papilionaceous” flower of redbud (Cercis canadensis) with three forms of petals: standard or vexillum, wing, and keel. B, Paramacrolobium caeruleum, zygomorphic flower with large bracteoles, five tiny sepals, one large petal, the carpel, and three stamens. C, Saraca declinata, radially symmetrical flower with sepals, no petals, a carpel, and only four stamens. D, Labichea lanceolata, asymmetric flower with sepals, four reduced petals, carpel (not shown), and only two stamens. E, Strongly zygomorphic flower of Amherstia nobilis, with petalloid bracteoles, four sepals, three large petals, 10 stamens, and an elongate hypanthium. F, Papilionoid flower of Lupinus succulentus, with standard or vexillum, wings, and keel. Bl, Bracteole; C, calyx; G, gynoecium; H, hypanthium; K, keel petal; P, petal; V, standard or vexillum petal; S, sepal; St, stamen; Sy, style; W, wing petal. Scale bars ϭ 4 mm for A through C, E, and F; scale bar ϭ 2 mm for D. 912 Plant Physiol. Vol. 131, 2003 Floral Development in Legumes Figure 2. A through L, Floral initiation in Cae- salpinioideae (SEM micrographs). Abaxial side is at base of figure in C through L. Scale bar ϭ 25 ␮m in G; scale bars ϭ 50 ␮m in H through K; scale bars ϭ 100 ␮m in B, E, F, and L; scale bar ϭ 500 ␮m in A; scale bars ϭ 1mminCand D. A and B, Inflorescences with most bracts removed. A, Successive raceme of Senna didy- mobotrya with the oldest, first formed flowers at base, and successively younger ones above. B, Cyme of Chamaecrista nictitans, with oldest flower at top, younger one below. C, Radially symmetrical flower bud of Isoberlinia angolen- Downloaded from https://academic.oup.com/plphys/article/131/3/911/6111090 by guest on 01 October 2021 sis. Sepals are removed, and petals are all sim- ilar. D, Zygomorphic symmetry in flower bud of Gilbertiodendron klainei, sepals removed, with one large petal, four smaller. E, Floral bud of Bauhinia malabarica (polar view) showing me- dian petal on adaxial (upper) side, and alternat- ing whorls of organs. F, Ascending cochleate petal aestivation in Cercis canadensis.G through L, Organ initiation series of redbud (C. canadensis). G, Bracteole initiation. H, First se- pal initiated on abaxial side in median sagittal plane. I, All five sepals initiated in helical order and first two petals initiating on abaxial side (at arrowheads). J, All five petals initiated and first three stamens of outer whorl initiated (at arrow- heads). K, All petals, outer stamens (A), and at least two inner stamens (at arrowheads) initi- ated. L, All organs initiated; sepals and petals removed. Two whorls of stamens alternate. The carpel cleft is forming. A, Outer-whorl stamen; a, inner-whorl stamen; Ap, inflorescence apical meristem; B, bract; Bl, bracteole; C, carpel; F, flower bud/floral apex; K, keel petal; P, petal; S, sepal/calyx tube; S1 - S5, order of sepal initia- tion; V, standard or vexillum petal; W, wing petal. guish variations on the raceme, e.g. a spike has flow- cyme has bracteoles, the pattern of successive flower ers that lack pedicels and are crowded along the axis initiation in bracteole axils can be repeated indefi- without appreciable internodes, and a panicle has nitely. Cymes are found in Dialium guineense Willd. second order branches along the first order axis. (Tucker, 1998), Gleditsia triacanthos (Tucker, 1991), Racemes of caesalpinioids (Fig. 2A) show successive, and Poeppigia procera Presl. (Kantz, 1996) among cae- acropetal initiation and development among the salpinioids. Solitary flowers, each subtended by a flowers. In other words, each inflorescence includes foliage leaf, occur in the caesalpinioid Petalostylis flowers of many ages, with the oldest at the bottom labicheoides R. Br. (Tucker, 1998). and the younger ones above. A cymose inflorescence (Fig. 2B, Chamaecrista nicti- Symmetry tans L. Moensch) has determinate growth, with a terminal flower forming first, followed by younger Floral symmetry among Caesalpinioideae is highly flowers in the axils of two bracteoles that are located variable, reflecting the fact that the subfamily is basal below the terminal flower. Because every flower in a and polyphyletic, based on molecular phylogenies Plant Physiol. Vol. 131, 2003 913 Tucker (Doyle, 1995; Doyle et al., 2000). Most caesalpinioid mechanisms have evolved for increase or decrease in flowers are radially symmetrical through midstage of organ number among caesalpinioids. Is their ontog- development, when all organs have formed but have eny abbreviated as well, or is ontogeny normal but not yet differentiated. In radial symmetry (Fig. 2C), with subsequent suppression of organs? an object can be bisected along any radius to produce Reductions in the number of organs initiated are two halves that are mirror images. Radial symmetry seen in some examples.
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