Flower bud cooling protects pollen development and improves fertility during heatwaves

Early pollen development is a bottleneck for plant fertility in heatwave conditions, thus affecting yield stability. Mechanisms that protect this process and explain variation in tolerance level between genotypes are poorly understood. Here we show that sepal transpiration in young, still closed, flower buds reduces the impact of heat on developing tomato pollen and that this mechanism is enhanced by the major tomato pollen thermotolerance QTL, qPV11. By direct measurement of the flower bud core temperature and transpiration we show this process, which we term flower bud cooling, depends on heat-induced opening of sepal stomata and that the transpiration enhancing effect of qPV11 requires functional stomatal regulation and is specific to the sepals. Large-scale evaluation of populations in both a production field and greenhouse showed that qPV11 improves pollen viability and fruit set in heatwave-affected complex cultivation environments. These findings highlight enhanced flower bud cooling as a naturally evolved protection mechanism against heatwaves and qPV11 as genetic component in the differential regulation of transpiration between reproductive and vegetative tissues and candidate variant for the breeding of climate-resilient tomato cultivars.