Tomato PEPR1 ORTHOLOG RECEPTOR-LIKE KINASE1 Regulates Responses to Systemin, Necrotrophic Fungi, and Insect Herbivory

Abstract

Endogenous peptides regulate plant immunity and growth. Systemin, a peptide specific to the Solanaceae, is known for its functions in plant responses to insect herbivory and pathogen infections. Here, we describe the identification of the tomato (<i>Solanum lycopersicum</i>) PEPR1/2 ORTHOLOG RECEPTOR-LIKE KINASE1 (PORK1) as the TOMATO PROTEIN KINASE1b (TPK1b) interacting protein and demonstrate its biological functions in systemin signaling and tomato immune responses. Tomato <i>PORK1</i> RNA interference (RNAi) plants with significantly reduced <i>PORK1</i> expression showed increased susceptibility to tobacco hornworm (<i>Manduca sexta</i>), reduced seedling growth sensitivity to the systemin peptide, and compromised systemin-mediated resistance to <i>Botrytis cinerea.</i> Systemin-induced expression of <i>Proteinase Inhibitor II</i> (<i>PI-II</i>), a classical marker for systemin signaling, was abrogated in <i>PORK1</i> RNAi plants. Similarly, in response to systemin and wounding, the expression of jasmonate pathway genes was attenuated in <i>PORK1</i> RNAi plants. TPK1b, a key regulator of tomato defense against <i>B. cinerea</i> and <i>M. sexta</i>, was phosphorylated by PORK1. Interestingly, wounding- and systemin-induced phosphorylation of TPK1b was attenuated when <i>PORK1</i> expression was suppressed. Our data suggest that resistance to <i>B. cinerea</i> and <i>M. sexta</i> is dependent on PORK1-mediated responses to systemin and subsequent phosphorylation of TPK1b. Altogether, PORK1 regulates tomato systemin, wounding, and immune responses.