Differentiation and degeneration of cells that play a major role in tobacco anther dehiscence

Abstract

Dehiscence is the terminal step in anther development that releases pollen grains from the wall of each theca at a specific site between the two locules. In tobacco, two groups of cells-the circular cell cluster and the stomium-are required for anther dehiscence and define the position at which pollen is released. The processes responsible for the differentiation of the circular cell cluster and the stomium from cells in specific anther regions are unknown. Nor is it understood what initiates the programmed degeneration of these cell types that ultimately is responsible for pollen release from the anther. We characterized stomium and circular cell cluster differentiation and degeneration using both light and transmission electron microscopy throughout anther development, from the emergence of stamen primordia to anther dehiscence at flower opening. We observed that histological changes within primordium L1 and L2 cells destined to become the stomium and circular cell cluster occur at the same time after the differentiation of surrounding locule regions. Sub-epidermal cells that differentiate into the circular cell cluster divide, enlarge, and generate vacuoles with calcium oxalate crystals prior to any detectable changes in prestomium epidermal cells. Differentiation and division of cells that generate the stomium occur after cell degeneration initiates in the circular cell cluster. Prior to dehiscence, the stomium consists of a small set of cytoplasmically dense cells that are easily distinguished from their larger, highly vacuolate epidermal neighbors. Plasmodesmata connections within and between cells of the stomium and circular cell cluster were observed at different developmental stages, suggesting that these cells communicate with each other. Circular cell cluster and stomium cell death is programmed developmentally and occurs at different times. Degeneration of the circular cell cluster occurs first, contributes to the formation of a bilocular anther, and generates the site of anther wall breakage. The stomium cell death process is complete at flower opening and provides an opening for pollen release from each theca. We used laser capture microdissection and real-time quantitative reverse-transcription polymerase chain reactions to demonstrate that stomium cells can be isolated from developing anthers and studied for the presence of specific mRNAs. Our data suggest that a cascade of unique gene expression events throughout anther development is required for the dehiscence program, and that the differentiation of the stomium and circular cell cluster in the interlocular region of the anther probably involves cell signaling processes.

Sporogenesis and development of gametophytes in an endangered plant, Tetracentron sinense Oliv

“…Interestingly in T. sinense, the endothecial layer fi brously thickens after the U-shaped thickening, and then the intersporangial septum degenerates and the stomium splits, leading to anther dehiscence. The result suggests that the anther dehiscence of T. sinense should be attributed to a synergetic eff ect between the fi brous thickening of endothecium and the degeneration of the intersporangial septum and stomium, which is in disagreement with previous reports (Beals and Goldberg, 1997;Matsui et al, 1999;Sanders et al, 2005). Further studies on the cytological and cytochemical dynamics of the endothecium and intersporangial septum during development in this species will probably reveal the mechanism of anther dehiscence.…”

“…(2) In tobacco and other solanaceous plants, two specialized cell types, the stomium and the circular cell, cluster within the notch region and are associated with anther dehiscence (Beals and Goldberg, 1997). (3) In most non-solanaceous plants (D'Arcy, 1996;Sanders et al, 2005), specialized septum cells in the notch region of these anthers function analogously in dehiscence. (4) In rice, the U-shaped thickening in the endothecium wall and the rupture of the septum and splitting of the stomium contribute to anther dehiscence (Matsui et al, 1999).…”

Using Genomics to Study Legume Seed Development

“…5). LCM technology has been used successfully in rice (Oryza sativa), maize (Zea mays), tobacco, soybean, and Arabidopsis in which a variety of plant tissues and cell types have been isolated and studied, including those in an early Arabidopsis embryo (Asano et al, 2002;Kerk et al, 2003;Nakazono et al, 2003;Casson et al, 2005;Klink et al, 2005;Sanders et al, 2005;Spencer et al, 2007).…”

Ricinosomes Predict Programmed Cell Death Leading to Anther Dehiscence in Tomato

“…The histological details of anther development and some cytological details of cell death in the sporophytic tissues, particularly the tapetum (Papini et al, 1999;Wang et al, 1999;Wu and Cheung, 2000), have been documented for a number of species, including members of the Solanaceae (Bonner and Dickinson, 1989;Koltunow et al, 1990;Goldberg et al, 1993;Sanders et al, 2005;Varnier et al, 2005). However, with limited exceptions (Sanders et al, 2005;Varnier et al, 2005), ultrastructural details of the progression of PCD in anther tissues other than the tapetum have been largely ignored and limited to documenting mitochondrial and nuclear changes that occur as the cells approach death.…”

“…However, with limited exceptions (Sanders et al, 2005;Varnier et al, 2005), ultrastructural details of the progression of PCD in anther tissues other than the tapetum have been largely ignored and limited to documenting mitochondrial and nuclear changes that occur as the cells approach death. Common ultrastructural features consistent with the progression of PCD in plant cells have been provided (Gunawardena et al, 2004, and references therein;DeBono and Greenwood, 2006) and include the following: progressive condensation of chromatin with nuclear shrinkage, invagination, and lobing; aberrant morphologies and changes in electron density of mitochondria and plastids; vesiculation and vacuolization of the cytoplasm with changes in electron density of the tonoplast and cytoplasm; shrinkage of the plasma membrane from the cell wall; and vacuolar collapse.…”