Pollen tube integrity is critical for thermotolerance in tomato and is enhanced by loss of SlRALF1

Reproductive success of angiosperms depends on the ability of pollen to build a highly polarized cellular extension (the pollen tube) that delivers sperm to female gametes for fertilization. This process is highly temperature sensitive, but we lack information about how heat stress affects pollen function and the molecular pathways that impart thermotolerance. Here we show that maintaining cellular integrity during pollen tube germination and extension is the pollen performance parameter that distinguishes thermosensitive from thermotolerant tomato cultivars and that loss-of-function of one of four pollen-expressed Rapid Alkalinization Factor (RALF) signaling peptides can enhance thermotolerance. Moreover, we found that heat stress antagonizes RALF signaling required to maintain patterns of pectin distribution in the pollen tube cell wall to ensure integrity. These findings establish a molecular framework for understanding how pollen tube growth is modulated in response to the environment and show that RALF signaling can be altered to achieve thermotolerant pollen tube growth.