Aquaporins of the PIP2 Class Are Required for Efficient Anther Dehiscence in Tobacco

Abstract

Several processes during sexual reproduction in higher plants involve the movement of water between cells or tissues. Before flower anthesis, anther and pollen dehydration takes place before the release of mature pollen at dehiscence. Aquaporins represent a class of proteins that mediates the movement of water over cellular membranes. Aquaporins of the plasmamembrane PIP2 family are expressed in tobacco (Nicotiana tabacum) anthers and may therefore be involved in the movement of water in this organ. To gain more insight into the role these proteins may play in this process, we have analyzed their localization using immunolocalizations and generated plants displaying RNA interference of PIP2 aquaporins. Our results indicate that PIP2 protein expression is modulated during anther development. Furthermore, in tobacco PIP2 RNA interference plants, anther dehydration was slower, and dehiscence occurred later when compared with control plants. Together, our results suggest that aquaporins of the PIP2 class are required for efficient anther dehydration prior to dehiscence.In plant sexual reproduction, control of water movement plays an important role. During development, for example, young anthers must first take up water for growth, but at later stages anthers and pollen dehydrate before dehiscence. In tobacco (Nicotiana tabacum) and many other species, pollen dehydration starts after the degeneration of the tapetum, and pollen grains are partially dehydrated at dehiscence (Goldberg, 1988;Franchi et al., 2002). The significance of correct pollen dehydration for the functions of the pollen grain is illustrated by the Arabidopsis (Arabidopsis thaliana) mutant raring-to-go (Johnson and McCormick, 2001). In these plants, pollen grains do not dehydrate as wild-type pollen and germinate within the anther when it is exposed to high humidity. However, besides this example, not much is known about the detailed mechanism of pollen dehydration.Correct timing of anther dehiscence is important, as the time of pollen release is crucial for successful fertilization. It was shown that plant hormones are implicated in the dehiscence process. In Arabidopsis, mutations in several genes involved in jasmonic acid biosynthesis all result in delayed anther dehiscence, suggesting the involvement of jasmonic acid signaling in its regulation (Sanders et al., 2000;Ishiguro et al., 2001;Park et al., 2002). In tobacco, however, ethylene has been shown to control the timing of anther dehiscence (Rieu et al., 2003). Other processes associated with dehiscence involve the formation of secondary wall thickenings, the consecutive degeneration of various anther tissues, changes in carbohydrate metabolism, and the movement of water out of the anther (Keijzer, 1987;Bonner and Dickinson, 1990;Clement and Audran, 1995;Beals and Goldberg, 1997;Dawson et al., 1999;Steiner-Lange et al., 2003;Scott et al., 2004; see Table I for an overview of tobacco anther development). It has been suggested that the formation of secondary wall thickenings, in combination wi...

Global Identification of DELLA Target Genes during Arabidopsis Flower Development

“…Interestingly, both AtbZIP1 and ProDH are RGA up-regulated and KIN10-induced genes. The observations of specific expression of AtbZIP1 in anthers and delayed anther dehiscence in 35S:AtbZIP1 indicate that the activity of AtbZIP1 and ProDH regulated by RGA and KIN10 may be relevant to water movement during anther development, in which anthers first take up water for growth but dehydrate before dehiscence (Bots et al, 2005).…”

“…Anther dehiscence involves the processes of thickening of secondary cell walls, consecutive degeneration of various anther tissues, changes in carbohydrate metabolism, and movement of water out of the anther (Keijzer, 1987;Clément and Audran, 1995;Bots et al, 2005). GA deficiency or overdose produces nondehiscent anthers in various plant species (Colombo and Favret, 1996;Murray et al, 2003;Zhang et al, 2007), indicating that a fine-tuned GA signaling is important for anther dehiscence.…”

Mutation of Aquaporin Gene<em> PIP2;5</em> Postpones Pollen Hydration in Arabidopsis

“…The abundance of aquaporins in reproductive organs suggests that these proteins function in plant reproduction. In tobacco, PIP1 and PIP2 show distinct expression patterns during stigma and anther development, and may contribute to the development of these organs in different ways [8,9]. In potato, PIP2a was shown to be highly expressed in the pistil and anther tissues [10].…”

Identification and characterization of plasma membrane aquaporins isolated from fiber cells of Calotropis procera

“…They also exhibit differential water permeability characteristics. Members of the PIP2 subgroup exhibit high water channel activity in different heterologous expression systems (Suga and Maeshima, 2004;Bots et al, 2005). PIP1 is more efficiently involved in the transportation of uncharged solutes like glycerol and urea, and gases like CO 2 and NH 3 as compared to H 2 O conductivity (Fetter et al, 2004).…”