Patterns of gene expression in pollen of cotton (Gossypium hirsutum) indicate down-regulation as a feature of thermotolerance

Reproductive performance in plants is impaired as maximum temperatures consistently approach 40{degrees}C. However, the timing of heatwaves critically affects their impact. We studied the molecular responses of cotton male reproductive stages, to investigate the vulnerability of maturing pollen to high temperature. Tetrads, uninucleate and binucleate microspores, and mature pollen were subjected to SWATH-MS and RNA-seq analyses after exposure to 38/28{degrees}C (day/night) for 5 days. The results indicated that molecular signatures were down-regulated over developmental stages in response to heat. This was more evident in leaves where three-quarters of differentially changed proteins were decreased in abundance. Functional analysis showed that translation of genes increased in tetrads after exposure to heat; however, the reverse pattern was observed in mature pollen and leaves. Proteins involved in transport were highly abundant in tetrads, whereas in later stages of development and leaves, heat suppressed cell-to-cell communication. Moreover, a large number of heat shock proteins (HSPs) were identified in heat-affected tetrads, but these proteins were less abundant in mature pollen and leaves. We speculate that the sensitivity of tetrad cells to heat is related to increased activity of translation involved in non-essential pathways. Molecular signatures during pollen development after heatwaves provide markers for future genetic improvement.