Stamen Structure and Function

Abstract

Stamens are the male reproductive organs of flowering plants. They consist of an anther, the site of pollen development, and in most species a stalk-like filament, which transmits water and nutrients to the anther and positions it to aid pollen dispersal. Within the anther, male sporogenous cells differentiate and undergo meiosis to produce microspores, which give rise to pollen grains, whereas other cell types contribute to pollen maturation, protection, or release. Pollen development involves an array of extraordinary events, including cell division and differentiation independent of a conventional meristem, the transition from sporophytic to gametophytic generation, and modifications of cell division to produce structures that are unusual in plant development, including coenocytic tissues (the tapetum and the microsporocyte mass), and subsequently free cells (microspores) that give rise to self-contained units for genome dispersal (pollen grains). Reviews of stamen development and gene expression include articles by Bhandari (1984), Scott et al. (1991a), Goldberg et al. (1993), and Irish (1999). A change in emphasis will be apparent since anther development was reviewed in the first Plant Reproduction special issue of The Plant Cell (Goldberg et al., 1993). The earlier review drew largely on studies of tobacco, but this article focuses more tightly on Arabidopsis, which has surpassed other species in the genetic tools publically available, including a sequenced genome, microarrays, well-characterized mutants associated with cloned genes, and knockout collections for reverse genetics. The advances of the last 10 years include an increased understanding of stamen specification, stamen-specific gene expression, internal patterning of the anther, regulation of male meiosis, and anther dehiscence. Stamen and pollen development are intimately linked. We discuss those aspects of pollen genesis that are essentially controlled by the sporophytic genome (differentiation of the male germline, meiosis, and pollen wall formation), but the biology of the male gametophyte, pollen tube growth, and fertilization are covered by other reviews in this volume (Edlund et al., 2004; Hanson and Bentolila, 2004; McCormick, 2004). Anther Development. (A) Scheme of a transverse section through an Arabidopsis floral bud showing the number, position, and orientation of the floral organs (after Hill and Lord, 1989). (B) Schemes of transverse sections through Arabidopsis anthers at different stages (after Sanders et al., 1999). Floral stages are as described by Smyth et al. (1990); anther stages are as described by Sanders et al. (1999). C, connective; E, epidermis; En, endothecium; ML, middle layer; S, septum; St, stomium; StR, stomium region; T, tapetum; Td, tetrads; TPG, tricellular pollen grains; V, vascular bundle. There are many recent reviews of floral organ specification (Jack, 2001, 2004; Theissen, 2001; Lohmann and Weigel, 2002); therefore, the regulation of stamen identity will be treated only briefly here. The identity of floral organ primordia is controlled by three classes (termed A, B, and C) of homeotic selector genes with overlapping areas of activity; stamens develop in the third whorl, where both B and C genes are expressed. It has been discovered that additional transcription factors, encoded by SEPALLATA (SEP) genes in Arabidopsis, are required to confer full activity on the homeotic genes in stamens (as well as petals and carpels). The ABC model was based on genetic studies in Arabidopsis thaliana and Antirrhinum majus (Coen and Meyerowitz, 1991). The B class genes are APETALA3 (AP3) and PISTILLATA (PI) in Arabidopsis and DEFICIENS (DEF) and GLOBOSA (GLO) in Antirrhinum; the C genes are AGAMOUS (AG) and PLENA, respectively. Mutations in any one of the B or C genes result in homeotic conversion of the third-whorl organs to a different type. Loss of B function causes transformation of stamens to carpels, loss of C function converts stamens to petals, and loss of both transforms stamens to sepals. Single-gene mutations of the SEP genes have very subtle phenotypes, but in sep1 sep2 sep3 triple mutants, all floral organs resemble sepals, suggesting that B and C function have been abolished (Pelaz et al., 2000). The signals that determine the number of floral organ primordia in each whorl are unknown (Irish, 1999). However, the number of stamens can be perturbed by various mechanisms: extra stamens develop in clavata1 mutants, which form enlarged meristems (Clark et al., 1993), and in superman mutants, which have an expanded BC domain (Bowman et al., 1992). By contrast, arrest of stamen primordia is a feature of normal development in some species. In the radially asymmetric flowers of Antirrhinum, five stamens initiate, but the dorsal stamen arrests early in development in response to the activity of the CYCLOIDEA gene (Luo et al., 1995). In some species that produce unisexual flowers, such as maize and white campion,