Male Sterility in Maize after Transient Heat Stress during the Tetrad Stage of Pollen Development

Male Sterility in Maize after Transient Heat Stress during the Tetrad Stage of Pollen Development
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DOI:
10.1104/pp.19.00707
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发表时间:
2019-10-01
期刊:
影响因子:
7.4
通讯作者:
Dresselhaus, Thomas
Dresselhaus, Thomas
中科院分区:
生物学1区
文献类型:
--
作者:
Begcy, Kevin;Nosenko, Tetyana;Dresselhaus, Thomas

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环境温度的持续时间和强度的变化会损害植物的发育和繁殖,特别是雄性配子的发生。应激暴露导致雄性生殖器官减数分裂缺陷或孢子过早败育,导致雄性不育。然而,对压力和雄性不育的潜在机制知之甚少。为了阐明这些机制,我们施加了一个温和的短暂的热胁迫玉米(玉米)植物花粉发育的四分体阶段。在最佳条件下完成花粉发育后,在成熟花粉中评估应激反应。短暂的热胁迫导致淀粉含量降低,酶活性降低,花粉萌发减少,导致不育。一个转录组学的比较指出了淀粉,脂质和能量生物合成相关基因的失调。代谢组学研究表明,Suc及其单糖组分增加,丙酮酸减少。脂质组学分析显示不饱和脂肪酸水平升高,饱和脂肪酸水平降低。相反,大多数参与发育过程的基因,如生长素和未折叠蛋白反应,信号传导和细胞壁生物合成所需的基因保持不变。值得注意的是,即使花粉在最佳条件下的进一步发育过程中可以恢复,转录和代谢途径基因以及热应激蛋白的调控变化仍然改变。总之,我们的研究结果表明,在高度敏感的四分体阶段的短中度热胁迫强烈影响基本代谢途径,从而产生萌发缺陷的花粉,最终导致玉米产量严重损失。
Shifts in the duration and intensity of ambient temperature impair plant development and reproduction, particularly male gametogenesis. Stress exposure causes meiotic defects or premature spore abortion in male reproductive organs, leading to male sterility. However, little is known about the mechanisms underlying stress and male sterility. To elucidate these mechanisms, we imposed a moderate transient heat stress on maize (Zea mays) plants at the tetrad stage of pollen development. After completion of pollen development at optimal conditions, stress responses were assessed in mature pollen. Transient heat stress resulted in reduced starch content, decreased enzymatic activity, and reduced pollen germination, resulting in sterility. A transcriptomic comparison pointed toward misregulation of starch, lipid, and energy biosynthesis-related genes. Metabolomic studies showed an increase of Suc and its monosaccharide components, as well as a reduction in pyruvate. Lipidomic analysis showed increased levels of unsaturated fatty acids and decreased levels of saturated fatty acids. In contrast, the majority of genes involved in developmental processes such as those required for auxin and unfolded protein responses, signaling, and cell wall biosynthesis remained unaltered. It is noteworthy that changes in the regulation of transcriptional and metabolic pathway genes, as well as heat stress proteins, remained altered even though pollen could recover during further development at optimal conditions. In conclusion, our findings demonstrate that a short moderate heat stress during the highly susceptible tetrad stage strongly affects basic metabolic pathways and thus generates germination-defective pollen, ultimately leading to severe yield losses in maize.