Flavonols improve thermotolerance in tomato pollen during germination and tube elongation by maintaining ROS homeostasis

Abstract

ABSTRACTElevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. TheSolanum lycopersicum anthocyanin reduced(are) mutant has a defect in theFLAVANONE 3 HYDROXYLASE(F3H) gene and impaired synthesis of flavonol antioxidants. We identified multiple aspects of pollen performance inarethat were hypersensitive to elevated temperatures relative to the VF36 parental line, including heat-increased accumulation of reactive oxygen species (ROS). Transformation ofarewith anF3Htransgene, or chemical complementation with flavonols, prevented temperature-dependent ROS accumulation in pollen and restored pollen performance to VF36 levels. Transformation of thisF3Hconstruct into VF36 (VF36-F3H-T3) prevented both temperature driven ROS increases and impaired pollen performance. RNA-Seq was performed at optimal and stress temperatures inare, 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 inareat all time points. These analyses also identified upregulated transcripts inare, 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.One sentence summaryFlavonol antioxidants reduce the negative impacts of elevated temperatures on pollen performance by reducing levels of heat induced reactive oxygen species synthesis and modulation of heat induced changes in the pollen transcriptome.