Stigma receptors control intraspecies and interspecies barriers in Brassicaceae

Flowering plants have evolved numerous intraspecific and interspecific prezygotic reproductive barriers to prevent production of unfavourable offspring(1). Within a species, self-incompatibility (SI) is a widely utilized mechanism that rejects self-pollen(2,3) to avoid inbreeding depression. Interspecific barriers restrain breeding between species and often follow the SI x self-compatible (SC) rule, that is, interspecific pollen is unilaterally incompatible (UI) on SI pistils but unilaterally compatible (UC) on SC pistils(1,4-6). The molecular mechanisms underlying SI, UI, SC and UC and their interconnections in the Brassicaceae remain unclear. Here we demonstrate that the SI pollen determinant S-locus cysteine-rich protein/S-locus protein 11 (SCR/SP11)(2,3) or a signal from UI pollen binds to the SI female determinant S-locus receptor kinase (SRK)(2,3), recruits FERONIA (FER)(7-9) and activates FER-mediated reactive oxygen species production in SI stigmas(10,11) to reject incompatible pollen. For compatible responses, diverged pollen coat protein B-class(12-14) from SC and UC pollen differentially trigger nitric oxide, nitrosate FER to suppress reactive oxygen species in SC stigmas to facilitate pollen growth in an intraspecies-preferential manner, maintaining species integrity. Our results show that SRK and FER integrate mechanisms underlying intraspecific and interspecific barriers and offer paths to achieve distant breeding in Brassicaceae crops.

Automated summary

Flowering plants have developed self-incompatibility and interspecific barriers to prevent the production of unfavorable offspring. Self-incompatibility is achieved by the interaction between S-Locus proteins and S-Locus receptor kinases to reject self-pollen, while interspecific barriers follow the rule of unilateral incompatibility on self-incompatible pistils and unilateral compatibility on self-compatible pistils. In Brassicaceae, S-Locus proteins and S-Locus receptor kinases activate FER-mediated reactive oxygen species production to reject incompatible pollen, while diverged pollen coat proteins trigger nitric oxide to facilitate pollen growth in a preferential manner, maintaining species integrity.