Abstract
Genic male sterility (GMS) is critical for heterosis utilization and hybrid seed production. Although GMS mutants and genes have been studied extensively in plants, it has remained unclear whether chloroplast-associated photosynthetic and metabolic activities are involved in the regulation of anther development. In this study, we characterized the function of ZmMs33/ZmGPAT6, which encodes a member of the glycerol-3-phosphate acyltransferase (GPAT) family that catalyzes the first step of the glycerolipid synthetic pathway. We found that normal structure and function of endothecium (En) chloroplasts maintained by ZmMs33-mediated lipid biosynthesis in tapetal cells are crucial for maize anther development. ZmMs33 is expressed mainly in the tapetum at early anther developmental stages and critical for cell proliferation and expansion at late stages. Chloroplasts in En cells of wild-type anthers function as starch storage sites before stage 10 but as photosynthetic factories since stage 10 to enable starch metabolism and carbohydrate supply. Loss of ZmMs33 function inhibits the biosynthesis of glycolipids and phospholipids, which are major components of En chloroplast membranes, and disrupts the development and function of En chloroplasts, resulting in the formation of abnormal En chloroplasts containing numerous starch granules. Further analyses reveal that starch synthesis during the day and starch degradation at night are greatly suppressed in the mutant anthers, leading to carbon starvation and low energy status, as evidenced by low trehalose-6-phosphate content and a reduced ATP/AMP ratio. The energy sensor and inducer of autophagy, SnRK1, was activated to induce early and excessive autophagy, premature PCD, and metabolic reprogramming in tapetal cells, finally arresting the elongation and development of mutant anthers. Taken together, our results not only show that ZmMs33 is required for normal structure and function of En chloroplasts but also reveal that starch metabolism and photosynthetic activities of En chloroplasts at different developmental stages are essential for normal anther development. These findings provide novel insights for understanding how lipid biosynthesis in the tapetum, the structure and function of En chloroplasts, and energy and substance metabolism are coordinated to maintain maize anther development.
Highlights
Biological studies on genic male sterility (GMS) genes have fundamentally deepened our understanding of plant male reproduction
We found that ms33-6038 anthers showed normal morphology compared with wild-type (WT) anthers during anther developmental stages 5– 8b based on a previously published anther developmental calendar for maize (Wan et al, 2019) (Figure 1A)
The number and length of epidermal cells in WT anthers gradually increased during anther development, whereas those in mutant anthers stopped increasing after stage 8b (Figure 1C)
Summary
Biological studies on genic male sterility (GMS) genes have fundamentally deepened our understanding of plant male reproduction. Little is known about the metabolic mechanisms that underlie male sterility in maize or about the changes in production, distribution, and utilization of energy and nutrients (e.g., saccharides, lipids, and proteins) that result in male sterility of GMS mutant anthers. The four layers surround the inner sporogenous cells and are finely regulated throughout anther development to ensure mature pollen formation (Wilson and Zhang, 2009; Wilson et al, 2011; Zhang and Yang, 2014; Walbot and Egger, 2016). The tapetum, the innermost layer of the anther wall, contributes to microspore release, nutrition, pollen wall formation, and pollen coat deposition (Li et al, 2006; Zhang and Yang, 2014). Few studies have shown possible interactions among the four layers
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