Tomato SlIDA has a critical role in tomato fertilization by modifying reactive oxygen species homeostasis

Summary Anther development and pollen tube elongation are key steps for pollination and fertilization. The timing and spatial distribution of reactive oxygen species (ROS) and programmed cell death are central to these processes, but the regulatory mechanism of ROS production is not well understood. Inflorescence deficient in abscission (IDA) is implicated in many plant development and responses to environmental stimuli. However, their role in reproductive development is still unknown. We generated tomato knockout lines (CR‐slida) of an IDA homolog (SlIDA), which is expressed in the tapetum, septum and pollen tube, and observed a severe defect in male gametes. Further analysis indicated that there was a programmed cell death defect in the tapetum and septum and a failure of anther dehiscence in the CR‐slida lines, likely related to insufficient ROS signal. Liquid chromatography‐tandem mass spectrometry identified mature SlIDA as a 14‐mer EPIP peptide, which was shown to be secreted, and a complementation experiment showed that application of a synthetic 14‐mer EPIP peptide rescued the CR‐slida defect and enhanced the ROS signal. Moreover, the application of the ROS scavengers diphenyleneiodonium or Mn‐TMPP suppressed peptide function. Collectively, our results revealed that SlIDA plays an essential role in pollen development and pollen tube elongation by modulating ROS homeostasis. Significance Statement Optimal and timing reactive oxygen species (ROS) is essential for fertilization. We found SlIDA, which is expressed in tapetum, septum and pollen tube. Knockout SlIDA showed a severely disrupted male gamete. The further analysis indicated tapetum and septum programmed cell death defect and failure of anther dehiscence in CRslida are related to downregulated ROS signal. The result uncovers novel ROS‐dependent function of SlIDA in regulating fertilization.