Danger-Associated Peptides Close Stomata by OST1-Independent Activation of Anion Channels in Guard Cells

The plant elicitor peptides (Peps), a family of damage/danger-associated molecular patterns (DAMPs), are perceived by two receptors, PEPR1 and PEPR2, and contribute to plant defense against pathogen attack and abiotic stress. Here, we show that the Peps-PEPR signaling pathway functions in stomatal immunity by activating guard cell anion channels in Arabidopsis thaliana . The mutant plants lacking both PEPR1 and PEPR2 ( pepr1 pepr2 ) displayed enhanced bacterial growth after being sprayed with Pseudomonas syringae pv tomato ( Pst ) DC3000, but not after pathogen infiltration into leaves, implicating PEPR function in stomatal immunity. Indeed, synthetic Arabidopsis Peps ( At Peps) effectively induced stomatal closure in wild-type but not pepr1 pepr2 mutant leaves, suggesting that the At Peps-PEPR signaling pathway triggers stomatal closure. Consistent with this finding, patch-clamp recording revealed At Pep1-induced activation of anion channels in the guard cells of wild-type but not pepr1 pepr2 mutant plants. We further identified two guard cell-expressed anion channels, SLOW ANION CHANNEL1 (SLAC1) and its homolog SLAH3, as functionally overlapping components responsible for At Pep1-induced stomatal closure. The slac1 slah3 double mutant, but not slac1 or slah3 single mutants, failed to respond to At Pep1 in stomatal closure assays. Interestingly, disruption of OPEN STOMATA1 ( OST1 ), an essential gene for abscisic acid-triggered stomatal closure, did not affect the At Pep1-induced anion channel activity and stomatal response. Together, these results illustrate a DAMP-triggered signaling pathway that, unlike the flagellin22-FLAGELLIN-SENSITIVE2 pathway, triggers stomata immunity through an OST1-independent mechanism.