Regulation of Stomatal Immunity by Interdependent Functions of a Pathogen-Responsive MPK3/MPK6 Cascade and Abscisic Acid

Abstract

Activation of mitogen-activated protein kinases (MAPKs) is one of the earliest responses after plants sense an invading pathogen. Here, we show that MPK3 and MPK6, two pathogen-responsive MAPKs, and their upstream MAPK kinases, MKK4 and MKK5, are essential to both stomatal and apoplastic immunity. Loss of function of and , or their upstream and , abolishes pathogen/microbe-associated molecular pattern- and pathogen-induced stomatal closure. Gain-of-function activation of MPK3/MPK6 induces stomatal closure independently of abscisic acid (ABA) biosynthesis and signaling. In contrast, exogenously applied organic acids such as malate or citrate are able to reverse the stomatal closure induced by MPK3/MPK6 activation. Gene expression analysis and in situ enzyme activity staining revealed that malate metabolism increases in guard cells after activation of MPK3/MPK6 or inoculation of pathogen. In addition, pathogen-induced malate metabolism requires functional MKK4/MKK5 and MPK3/MPK6. We propose that the pathogen-responsive MPK3/MPK6 cascade and ABA are two essential signaling pathways that control, respectively, the organic acid metabolism and ion channels, two main branches of osmotic regulation in guard cells that function interdependently to control stomatal opening/closure.

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

“…MPK3 and MPK6 contribute redundantly to stomatal closure in response to Pto DC3000, which is reversed by COR (8,37,38). We found that Pto DC3000 is able to reopen stomata both in the wild type and hai1 (SI Appendix, Fig.…”

A plant effector‐triggered immunity signaling sector is inhibited by pattern‐triggered immunity

“…EMPIS should have three characteristics: (i) It can mediate ETI signaling even in the absence of the four signaling sectors, (ii) its ETI signaling function is compensated by the four signaling sectors, (iii) its ETI signaling function is inhibited by PTI signaling. However, a recent report of a successful application of engineered MPK3 and 6 (MPK3/6SR) that are chemically inhibitable (Su et al, 2017) could open a route to directly test the hypothesis using quad mpk3 mpk6 MPK6SR plants. Previously, we showed that signaling mediated by MPK3/6 can compensate SA signaling during ETI , which possibly confers characteristics (i) and (ii).…”

Constant vigilance: plant functions guarded by resistance proteins

“…It is interesting to note that mutants of the MEKK1–MKK1/MKK2–MPK4 cascade such as mekk1 , mkk1 mkk2 , and mpk4 , all show autoimmune phenotypes and enhanced resistance against Pseudomonas (Suarez‐Rodriguez et al ., ; Gao et al ., ; Qiu et al ., ), while mutants of the MKK4/MKK5–MPK3/MPK6 pathway ( mkk4 mkk5 and mpk3 mpk6 ) show compromised resistance (Su et al ., ). Constitutive activation of MPK3/MPK6 leads to HR‐like cell death and accumulation of defensive phytoalexins (Ren et al ., , ); however, constitutive MPK4 activation compromises both PTI and ETI mediated by the TNL proteins RPS4 and RPP4 (Berriri et al ., ).…”