Sexual reproduction in flowering plants takes place without an aqueous environment. Sperm are carried by pollen through air to reach the female gametophyte, though the molecular basis underlying the protective strategy of the male gametophyte is poorly understood. Here we compared the published transcriptomes of Arabidopsis thaliana pollen, and of heat-responsive genes, and uncovered insights into how mature pollen (MP) tolerates desiccation, while developing and germinating pollen are vulnerable to heat stress. Germinating pollen expresses molecular chaperones or “heat shock proteins” in the absence of heat stress. Furthermore, pollen tubes that grew through pistils at basal temperature showed induction of the endoplasmic reticulum (ER) stress response, which is a characteristic of stressed vegetative tissues. Recent studies show MP contains mRNA–protein (mRNP) aggregates that resemble “stress” granules triggered by heat or other stresses to protect cells. Based on these observations, we postulate that mRNP particles are formed in maturing pollen in response to developmentally programmed dehydration. Dry pollen can withstand harsh conditions as it is dispersed in air. We propose that, when pollen lands on a compatible pistil and hydrates, mRNAs stored in particles are released, aided by molecular chaperones, to become translationally active. Pollen responds to osmotic, mechanical, oxidative, and peptide cues that promote ER-mediated proteostasis and membrane trafficking for tube growth and sperm discharge. Unlike vegetative tissues, pollen depends on stress-protection strategies for its normal development and function. Thus, heat stress during reproduction likely triggers changes that interfere with the normal pollen responses, thereby compromising male fertility. This holistic perspective provides a framework to understand the basis of heat-tolerant strains in the reproduction of crops.

中文翻译：

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花粉组学的整体见解：选择应激反应基因和 ER 介导的蛋白质稳态以提高男性生育能力

开花植物的有性繁殖是在没有水环境的情况下进行的。花粉通过空气携带精子到达雌配子体，尽管对雄性配子体保护策略的分子基础知之甚少。在这里，我们比较了拟南芥花粉和热响应基因的已发表转录组，并揭示了成熟花粉 (MP) 如何耐受干燥，而发育和发芽的花粉易受热应激影响的见解。在没有热应激的情况下，发芽的花粉会表达分子伴侣或“热休克蛋白”。此外，在基础温度下通过雌蕊生长的花粉管显示出诱导内质网 (ER) 应激反应，这是应激营养组织的特征。最近的研究表明，MP 含有 mRNA-蛋白质 (mRNP) 聚集体，类似于由热或其他应激触发的“应激”颗粒，以保护细胞。基于这些观察，我们假设 mRNP 颗粒是在成熟花粉中形成的，以响应发育程序性脱水。干花粉分散在空气中，可以承受恶劣的条件。我们建议，当花粉落在相容的雌蕊上并水合时，储存在颗粒中的 mRNA 在分子伴侣的帮助下被释放，变得具有翻译活性。花粉对促进 ER 介导的蛋白质稳态和膜运输以促进管生长和精子排出的渗透、机械、氧化和肽信号作出反应。与营养组织不同，花粉的正常发育和功能依赖于应激保护策略。因此，生殖过程中的热应激可能会引发干扰正常花粉反应的变化，从而影响雄性生育能力。这种整体观点为理解作物繁殖中耐热菌株的基础提供了一个框架。