Regulation of Ovule Development

Abstract

Ovule development in Arabidopsis and other plants has been the focus of classic and molecular genetic analyses in recent years. This has been an exciting time to be involved in plant developmental biology, because many genetic pathways and regulatory mechanisms have been elucidated. Continued studies of ovule mutants have contributed to and benefited from these advances. Ovule development involves the same basic processes necessary for the formation of other plant organs, such as primordium initiation and specification, directed cell division and expansion, and asymmetric growth and differentiation. However, ovules differ from other plant structures in their reproductive function and apparent evolutionary origin from sporangiophores (Herr, 1995), allowing the basic developmental processes to be studied in a unique context. Researchers today are using both the wealth of botanical knowledge and new molecular insights to achieve a more comprehensive understanding of ovule morphogenesis and evolution. Recent reviews by Grossniklaus and Schneitz (1998)and Gasser et al. (1998)describe progress in the analysis of several ovule mutants. Here, we extend these earlier reviews with the latest information on the roles and nature of genes involved in the formation of the placenta as the site of ovule initiation, ovule identity, patterning of the ovule primordium, and control of integument morphogenesis. We focus primarily on recent results in Arabidopsis and indicate when results from other species are being discussed. Arabidopsis Ovule Development. All images are oriented with the gynobasal direction (toward the base of the gynoecium, or receptacle) to the left and the gynoapical direction (toward the apex of the gynoecium, or stigma) to the right. (A) to (D) Wild-type Landsberg erecta ovules. (A) Primordia at stage 11 of flower development. The first cells of the inner integument form a ring around the primordium. The outer integument is initiating on the gynobasal side of the ovule primordium, below the inner integument. (B) Primordium at same stage as in (A) showing derivation of the integuments from the L1 layer and differentiation of the megasporocyte. (C) Mature ovules at anthesis. The integuments have grown to cover the nucellus, and the funiculus has curved in the opposite direction. (D) Mature ovule showing the cell layers of the integuments and the embryo sac. (E) to (G) Composite differential interference contrast and laser confocal images of wild-type Landsberg erecta ovules with an INO:GFP reporter fusion protein expressed under the control of the INO promoter. (E) The fusion protein accumulates in the nuclei of cells in the proximal half of the region that will give rise to the outer integument at stage 10. (F) Fluorescence persists in this region as the integument grows in stage 11. (G) The fusion protein is visible only in the outermost cell layer of the outer integument as it continues to grow in stage 12. es, embryo sac; f, funiculus; ii, inner integument; m, megasporocyte; mi, micropyle; n, nucellus; oi, outer integument. Bars = 25 μm. Images in (A), (C), and (D) courtesy of K. Robinson-Beers; (B) courtesy of J.M. McAbee; (E) to (G) courtesy of R.J. Meister. Molecular genetic analyses with genes important for ovule development that have contributed to recent advances revealing the genetic pathways and regulatory mechanisms involved in plant development are the focus of this review. Development of Carpel Marginal Tissues. (A) Scheme of a cross-section of the Arabidopsis gynoecium. Structural components are indicated at the top, and the bottom shows gene expression patterns. The medial domain is formed by congenital fusion of the lateral margins (separated by the vertical line). The internal medial region comprises both the medial ridge and the placentas (p). STM, CUC1, CUC2, and SPT are expressed in the medial region. This expression overlaps with PHAVOLUTA and REV expression in the regions from which ovule primordia will emerge, the placentas. This overlap may be an important factor in the formation of the placentas. (B) Unfused carpel (c) of an ant-9 lug-3 double mutant. Medial regions are lost, including placenta and ovules. Bar = 100 μm. (C) Apparently free placentas decorated with ovule primordia (op) form in the absence of other carpel structures in the tsl-1 ettin-2 double mutant. Bar = 50 μm. Image in (B) courtesy of X. Liu; (C) courtesy of J.L. Roe and P.C. Zambryski. To understand the relationship of the placenta to the rest of the gynoecium, it is useful to consider the possible evolutionary origins of the carpels. The apparent monophyly of the seed plants (Chaw et al., 2000) and the extensive gymnosperm fossil record show that carpels arose after ovules (Stewart, 1983). Carpels are proposed to have evolved from organs, that to the ovules or structures that ovules The evolutionary origin of the placenta and the of the carpel are of by et al. the that the medial ridge is an of of a domain th