Tomato cultivars that produce fruit at high temperature show distinct pathways promoting enhanced pollen tube performance

Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Grain and fruit production depend on development of sufficient numbers of pollen grains and on their ability to generate a cellular extension, the pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. These critical phases of the life cycle are sensitive to temperature and could limit productivity under high temperature (HT). Previous studies have investigated the effects of HT on pollen development, but little is known about how HT applied during the pollen tube growth phase affects fertility. Here, we used tomato as a model fruit crop to determine how HT affects the pollen tube growth phase, capitalizing on cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to HT 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 thermotolerant cultivars have enhanced growth in vivo and in vitro under HT. Analysis of the pollen tube transcriptome's response to HT allowed us to distinguish among hypotheses for the molecular basis of cellular thermotolerance in the pollen tube. We found that a combination of enhanced induction and priming of stress responses is associated with thermotolerant pollen tube growth under HT. Importantly, we define key components of the pollen tube stress response and identify ROS production/scavenging pathways and callose synthesis and deposition as major focal points for selection that resulted in significant reproductive thermotolerance. Our work identifies the pollen tube growth phase as a target to enhance reproductive thermotolerance and delineates key pathways altered by selection of crop varieties capable of fruiting under HT conditions.