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Elevated temperatures impair pollen performance and reproductive success, resulting in lower crop yields. The tomato (Solanum lycopersicum) anthocyanin reduced (are) mutant harbors a mutation in FLAVANONE 3-HYDROXYLASE (F3H), resulting in impaired flavonol antioxidant biosynthesis. The are mutant has reduced pollen performance and seed set relative to the VF36 parental line, phenotypes that are accentuated at elevated temperatures. Transformation of are with the wild-type F3H gene, or chemical complementation with flavonols, prevented temperature-dependent reactive oxygen species (ROS) accumulation in pollen and restored the reduced viability, germination, and tube elongation of are to VF36 levels. Overexpression of F3H in VF36 prevented temperature-driven ROS increases and impaired pollen performance, revealing that flavonol biosynthesis promotes thermotolerance. Although stigmas of are had reduced flavonol and elevated ROS levels, the growth of are pollen tubes was similarly impaired in both are and VF36 pistils. RNA-seq was performed at optimal and stress temperatures in are, VF36, and the F3H overexpression line at multiple timepoints across pollen tube elongation. The number of differentially expressed genes increased over time under elevated temperatures in all genotypes, with the greatest number in are. These findings suggest potential agricultural interventions to combat the negative effects of heat-induced ROS in pollen that lead to reproductive failure.
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Enhanced pollen tube performance at high temperature contributes to thermotolerant fruit and seed production in tomato
Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Flowering plant reproduction depends on the ability of pollen grains to generate a pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. We used tomato as amodel fruit croptodeterminehowhigh temperature affects the pollen tube growthphase, takingadvantage of cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to high temperature solely during the pollen tube growth phase limits fruit biomass and seed set more significantly in thermosensitive cultivars than in thermotolerant cultivars. Importantly, we found that pollen tubes from the thermotolerantTamaulipas cultivar have enhanced growth in vivo and in vitro under high temperature. Analysis of the pollen tube transcriptome’s response to high temperature allowed us to define two responsemodes (enhanced induction of stress responses and higher basal levels of growth pathways repressed by heat stress) associated with reproductive thermotolerance. Importantly, we define key components of the pollen tube stress response, identifyingenhancedreactive oxygenspecies (ROS)homeostasis andpollen tubecallose synthesis and deposition as important components of reproductive thermotolerance in Tamaulipas. Our work identifies the pollen tube growth phase as a viable target to enhance reproductive thermotolerance and delineates key pathways that are altered in crop varieties capable of fruiting under high-temperature conditions.
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- Award ID(s):
- 1939255
- PAR ID:
- 10572723
- Publisher / Repository:
- Elsevier Inc.
- Date Published:
- Journal Name:
- Current Biology
- Volume:
- 34
- Issue:
- 22
- ISSN:
- 0960-9822
- Page Range / eLocation ID:
- 5319 to 5333.e5
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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