Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The Solanum lycopersicum anthocyanin reduced (are) mutant has a defect in the FLAVANONE 3 HYDROXYLASE (F3H) gene and impaired synthesis of flavonol antioxidants. We identified multiple aspects of pollen performance in are that were hypersensitive to elevated temperatures relative to the VF36 parental line, including heat-increased accumulation of reactive oxygen species (ROS). Transformation of are with an F3H transgene, or chemical complementation with flavonols, prevented temperature-dependent ROS accumulation in pollen and restored pollen performance to VF36 levels. Transformation of this F3H construct into VF36 (VF36-F3H-T3) prevented both temperature driven ROS increases and impaired pollen performance. RNA-Seq was performed at optimal and stress temperatures in are, VF36, and VF36-F3H-T3 at multiple timepoints across pollen tube emergence and elongation. All genotypes had increasing numbers of differentially expressed genes with duration of elevated temperature, with the largest number in are at all time points. These analyses also identified upregulated transcripts in are, relative to VF36, even at optimal temperatures, revealing a flavonol-regulated transcriptome. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that leads to reproductive failure and crop loss.
Keywords: flavonols; heat shock proteins; heat stress; pollen; reactive oxygen species; tomato.