ROS and redox homeostasis in pollen fertility under heat stress: a tale of two pollen subpopulations

To ensure reproductive success, flowering plants produce an excess of pollen to fertilize a limited number of ovules. However, in many flowering plants the male gametophyte is considered to be the most sensitive tissue to high temperatures, with even a single hot day being able to cause male sterility. Using flow cytometry approach, we recently showed that pollen grains mature into two distinct subpopulations – those that display high metabolic activity and elevated reactive oxygen species (ROS) levels immediately after hydration (high-ROS/active), and those that maintain an extended period of dormancy with low metabolic activity (low-ROS/dormant). We show that while the high-ROS pollen grains are highly susceptible to heat stress, low-ROS pollen grains may survive even extreme temperatures. We propose that the dormant pollen serves as a backup to provide a second chance for successful fertilization when the `first wave` of pollen encounters an unpredictable growth condition such as heat stress. Pollen grains expressing redox-sensitive ro-GFP further reveals two distinct subpopulations with the majority being highly reduced, yet the relationship between the redox status and the active/dormant state of the pollen awaits further investigation. In addition, FACS-purified active and dormant pollen revealed different ribosomal RNA and transcriptomics profiles, pointing to mechanisms involved in dormancy initiation/release and resilience. Our findings suggest that by regulating the activity state of pollen, thus modulating the composition of the pollen population, flowering plants may optimize their reproductive success to best-fit changes in their environment.