Increasing global temperatures threaten food security through impaired fertility and subsequent reduction in grain yield and quality. Reproductive tissues in plants, particularly male gametophytes, are highly susceptible to heatwaves relative to vegetative tissues. Therefore, conducting experiments to understand molecular mechanisms underlying the thermotolerance of male gametophytes will identify targets for crop improvement.
We investigated male gametophytes in cotton, a heat-tolerant crop, to demonstrate how heatwaves compromise pollen function. Plants during meiosis (tetrads) and mitosis (uninucleate and binucleate microspores, and mature pollen) were exposed to moderate (36/25°C, day/night) and extreme heat (38/28°C and 40/30°C) for five days to analyse their morphological and physiological changes. Additionally, molecular responses of the pollen developmental stages were analysed to reveal their mechanisms of heat tolerance.
Severe cell damage was observed when tetrads were exposed to extreme heat, resulting in failed dehiscence, smaller pollen grains, and yield loss. Molecular analysis demonstrated that each stage of pollen development has qualitatively distinct transcriptome and proteome profiles. Moreover, extreme heat led to unique expression patterns in tetrads, most of which were suppressed in the relatively heat-tolerant tissues, mature pollen and leaves. We demonstrated that although molecular chaperones were abundant during meiosis, where they putatively refold aggregated proteins, they were not highly up-regulated in the late stages of pollen development. We speculate that failure to slow down metabolism contributes to the susceptibility of meiotic cells to heat. Identifying the precise molecular events underlying the susceptibility of pollen formation to heat is a top priority for improving strategic crops, including wheat.