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

Abstract

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.

High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements

“…In maize, the first RNA-seq study of male and female gametophyte transcriptomes (mature pollen and embryo sacs) similarly identified subsets of developmentally specific genes, with pollen showing the most specialized transcriptome relative to other tissues assessed [23]. More recently, RNA-seq has been carried out on additional stages of maize reproductive development, including pre-meiotic and meiotic anther cells [24][25][26], as well as sperm cells, egg cells, and early stages of zygotic development [27].…”

Genome-Wide Development and Validation of Cost-Effective KASP Marker Assays for Genetic Dissection of Heat Stress Tolerance in Maize

“…Most of the methods detecting variation are based on sequencing data derived either from whole-genome sequencing (WGS) or whole-exome sequencing (WES) [ 10 , 11 ]. In the last few years, NGS approaches in the form of RNA-seq have been co-opted to provide global insights into the gene expression patterns to understand the genetic networks and metabolic pathways involved in maize responses to heat stress [ 12 , 13 , 14 , 15 , 16 , 17 , 18 ]. Apart from gene expression analysis, RNA-seq can also be used to identify genomic variants in expressed genes alongside WGS and WES [ 19 ].…”

Transcriptome and translatome changes in germinated pollen under heat stress uncover roles of transporter genes involved in pollen tube growth

“…Molecular studies have uncovered heat responses in pollen subjected to high temperature similar to other plant cell types including the heat shock response, the unfolded ER protein response or the formation of reactive oxygen species (20). In addition, a number of untargeted transcriptomics, metabolomics, and proteomics studies have been performed to characterize the response of pollen under heat stress conditions at the molecular level (21)(22)(23)(24). However, the limitations of the proteomics and metabolomics technologies compared to highresolution approaches based on next generation sequencing of nucleic acids (NGS) techniques (25), qualify these NGS approaches as very appropriate to gain deeper insight in the response of pollen to heat stress conditions.…”