Time of day and genotype sensitivity adjust molecular responses to temperature stress in Sorghum

Sorghum is one of the four major C4 crops that are considered to be tolerant to environmental extremes. Sorghum shows distinct growth responses to temperature stress depending on the sensitivity of the genetic background. About half of the transcripts in sorghum exhibit diurnal rhythmic expressions emphasizing significant coordination with the environment. However, an understanding of how molecular dynamics contribute to genotype-specific stress responses in the context of the time of day is not known. We examined whether temperature stress and the time of day impact the gene expression dynamics in cold-sensitive and tolerant and heat-sensitive and tolerant sorghum genotypes. We found that time of day is highly influencing the temperature stress responses, which can be explained by the rhythmic expression of most thermo-responsive genes. This effect is more pronounced in thermo-tolerant genotypes, suggesting a stronger regulation of gene expression by the time of day and/or by the circadian clock. Genotypic differences were mostly observed on average gene expression levels, but we identified groups of genes regulated by temperature stress in a time-of-day and genotype-specific manner. These include transcriptional regulators and several members of the Ca2+-binding EF-hand protein family. We speculate that expression variation of these genes between genotypes may be responsible for contrasting sensitivities to temperature stress in tolerant vs susceptible sorghum varieties. These findings offer a new opportunity to selectively target specific genes in efforts to develop climate-resilient crops based on their time of day and genotype variation responses to temperature stress. Overall design: We performed a transcriptomic analysis from leaves that were collected in control conditions or after 1 h temperature stress (either cold or heat stress), applied at four different times of day (ZT1, ZT6, ZT9 and ZT15), in the thermo-sensitive genotype RTX430 and in tolerant genotypes (SC224 and Macia for the cold stress and heat stress experiments, respectively).