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.

遗传上的雄性不育（GMS）对于杂种优势利用和杂交种子生产至关重要。尽管已在植物中广泛研究了GMS突变体和基因，但尚不清楚叶绿体相关的光合作用和代谢活性是否参与花药发育的调控。在这项研究中，我们表征了ZmMs33 / ZmGPAT6的功能，该功能编码甘油3磷酸酰基转移酶（GPAT）家族的成员，该家族催化甘油脂合成途径的第一步。我们发现，ZmMs33介导的脂质生物合成在绒毡层细胞中维持的内皮（En）叶绿体的正常结构和功能对于玉米花药发育至关重要。ZmMs33在花药发育早期主要在绒毡层中表达，并且在后期对细胞增殖和扩增至关重要。野生型花药的En细胞中的叶绿体在第10阶段之前充当淀粉储存位点，但从第10阶段开始充当光合作用工厂，以实现淀粉代谢和碳水化合物供应。ZmMs的丢失33功能抑制糖脂和磷脂的生物合成，糖脂和磷脂是En叶绿体膜的主要成分，破坏En叶绿体的发育和功能，导致含有大量淀粉颗粒的异常En叶绿体的形成。进一步的分析表明，突变花药极大地抑制了白天的淀粉合成和夜间的淀粉降解，从而导致碳饥饿和低能量状态，低海藻糖-6-磷酸含量和降低的ATP / AMP比证明了这一点。激活了自噬的能量传感器和诱导剂SnRK1，以诱导绒毛细胞中早期和过度的自噬，过早的PCD以及代谢重编程，最终阻止了突变体花药的延长和发育。综上所述，我们的结果不仅表明ZmMs33是En叶绿体正常结构和功能所必需的，而且还揭示了En En叶绿体在不同发育阶段的淀粉代谢和光合活性对于正常花药发育至关重要。这些发现为理解绒毡层中的脂质生物合成，En叶绿体的结构和功能以及能量和物质代谢如何协调以维持玉米花药发育提供了新颖的见解。