Starch Biosynthesis during Pollen Maturation Is Associated with Altered Patterns of Gene Expression in Maize

Abstract

Starch biosynthesis during pollen maturation is not well understood in terms of genes/proteins and intracellular controls that regulate it in developing pollen. We have studied two specific developmental stages: "early," characterized by the lack of starch, before or during pollen mitosis I; and "late," an actively starch-filling post-pollen mitosis I phase in S-type cytoplasmic male-sterile (S-CMS) and two related male-fertile genotypes. The male-fertile starch-positive, but not the CMS starch-deficient, genotypes showed changes in the expression patterns of a large number of genes during this metabolic transition. In addition to a battery of housekeeping genes of carbohydrate metabolism, we observed changes in hexose transporter, plasma membrane H ϩ -ATPase, ZmMADS1, and 14-3-3 proteins. Reduction or deficiency in 14-3-3 protein levels in all three major cellular sites (amyloplasts [starch], mitochondria, and cytosol) in male-sterile relative to male-fertile genotypes are of potential interest because of interorganellar communication in this CMS system. Further, the levels of hexose sugars were significantly reduced in male-sterile as compared with male-fertile tissues, not only at "early" and "late" stages but also at an earlier point during meiosis. Collectively, these data suggest that combined effects of both reduced sugars and their reduced flux in starch biosynthesis along with a strong possibility for altered redox passage may lead to the observed temporal changes in gene expressions, and ultimately pollen sterility.Several excellent reviews on male gametophyte development in plants (Mascarenhas, 1989; Bewley et al., 2000) and maize (Zea mays) in particular (Bedinger, 1992;McCormick, 1993) have been written recently and provide overviews of events from meiosis to mature pollen development. In brief, haploid gametes as tetrads are encased in a callose wall and are well nourished through the sporophytic cell layer, tapetum. The role of the tapetum in pollen development is recently elaborated (Liu et al., 2001). Release of single, free microspores from each tetrad is achieved by callase secreted from the tapetal cells, which degenerate and lead to the symplastic isolation of microspores from the mother plant. All nourishments for developing microspores are transported presumably from the nutrient-rich locular fluid inside the anthers. Most importantly, symplastic discontinuity requires that the individual microspores be programmed with appropriate signals or at least be activated for major functions, including the two mitotic divisions, intracellular vacuolar biogenesis, and several metabolic changes such as starch biosynthesis.Starch biosynthesis during the final phases of pollen maturation is critical not only because starch is a reserve source of energy for pollen germination but it also serves as a checkpoint of pollen maturity. Very often, pollen maturation appears to be prematurely terminated if starch levels remain lower than a certain threshold point as evident from several genetically controlled...

Critical Roles of Vacuolar Invertase in Floral Organ Development and Male and Female Fertilities Are Revealed through Characterization of GhVIN1-RNAi Cotton Plants

“…S7). These data indicate that starch turnover is disrupted in the GhVIN1-RNAi stamen, which could result in not only a delay in anther dehiscence but also poor pollen viability, as starch abundance is critically required for pollen vigor (Clément et al, 1994;Goetz et al, 2001;Datta et al, 2002). Suppression of GhVINs also reduced the transcript levels of GhMYB24 and GhLOX1 in the transgenic stamens (Fig.…”

Isoform-specific Subcellular Localization among 14-3-3 Proteins inArabidopsisSeems to be Driven by Client Interactions

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