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 (Solanum lycopersicum) 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 PORK1 RNA interference (RNAi) plants with significantly reduced PORK1 expression showed increased susceptibility to tobacco hornworm (Manduca sexta), reduced seedling growth sensitivity to the systemin peptide, and compromised systemin-mediated resistance to Botrytis cinerea. Systemin-induced expression of Proteinase Inhibitor II (PI-II), a classical marker for systemin signaling, was abrogated in PORK1 RNAi plants. Similarly, in response to systemin and wounding, the expression of jasmonate pathway genes was attenuated in PORK1 RNAi plants. TPK1b, a key regulator of tomato defense against B. cinerea and M. sexta, was phosphorylated by PORK1. Interestingly, wounding-and systemin-induced phosphorylation of TPK1b was attenuated when PORK1 expression was suppressed. Our data suggest that resistance to B. cinerea and M. sexta is dependent on PORK1-mediated responses to systemin and subsequent phosphorylation of TPK1b. Altogether, PORK1 regulates tomato systemin, wounding, and immune responses.

Systemin‐mediated long‐distance systemic defense responses

“…SYR1 is a close relative of the plant elicitor peptide receptors (PEPRs), which recognize endogenous peptides as danger signals in Arabidopsis (Yamaguchi et al , 2010). Intriguingly, tomato PEPR1/2 ortholog receptor‐like kinase 1 (PORK1) has recently been found to play a role in regulating the responses to wounding or SYS treatment (Xu et al , 2018). PORK1 interacts with and phosphorylates the tomato protein kinase 1b (TPK1b) (Xu et al , 2018), a key cytoplasmic regulator of defense responses to insects and fungal pathogens (Abuqamar et al , 2008).…”

“…Intriguingly, tomato PEPR1/2 ortholog receptor‐like kinase 1 (PORK1) has recently been found to play a role in regulating the responses to wounding or SYS treatment (Xu et al , 2018). PORK1 interacts with and phosphorylates the tomato protein kinase 1b (TPK1b) (Xu et al , 2018), a key cytoplasmic regulator of defense responses to insects and fungal pathogens (Abuqamar et al , 2008). Notably, tomato PORK1 RNAi lines carrying functional SYR1 lack SYS responses.…”

“…Notably, tomato PORK1 RNAi lines carrying functional SYR1 lack SYS responses. This implies that PORK1 is critical for the SYS‐mediated plant defense responses and is involved in SYS‐related functions, acting in collaboration with other components, including SYR1 (Xu et al , 2018).…”

“…The tomato RLKs BRI1 and FLAGELLIN SENSING 2 (FLS2), the receptor for bacterial flagellin (Lu et al , 2010), interact with TPK1b (Xu et al , 2018). It is currently unknown whether TPK1b can serve as a substrate for multiple RLKs in a similar manner to Arabidopsis BIK1, which interacts with several receptors including PEPR1, FLS2 and the elongation factor Tu (EF‐Tu) receptor (EFR) to integrate the responses from diverse recognition events (Lu et al , 2010; Zhang et al , 2010; Liu et al , 2013; Xu et al , 2018). As Pro‐SYS possesses a flexible structure that enables it to interact with numerous partners (Buonanno et al , 2018), we speculate that SYS may bind to multiple RLK proteins to integrate different signaling pathways and orchestrate wound/pathogen signaling and development.…”

Surface Sensor Systems in Plant Immunity

“…The LRR-RK SlSYR1 was recently identified as the systemin receptor . The closely related SlPORK1 associates with SlSYR1 and SlSYR2 and is critical for systemin response (Xu et al, 2018). AtPEPR1 and 2 bind endogenous AtPep1-8 peptides derived from the C-termini of their AtPROPEP1-8 precursors (Yamaguchi et al, 2006;Krol et al, 2010;Yamaguchi et al, 2010).…”