RGI-GOLVEN signalling promotes FLS2 abundance to regulate plant immunity

Abstract

Endogenous plant signalling peptides regulate developmental and growth-related processes. Recent research indicates that some of these peptides are classified as phytocytokines as they have regulatory functions during plant immune responses. However, the mechanistic basis for phytocytokine-mediated immune modulation remains largely elusive. Here, we identify GOLVEN2 (GLV2) peptides as novel phytocytokines in Arabidopsis thaliana. By peptide application, precursor overexpression and loss-of-function studies we show that GLV2 enhances sensitivity of plants to elicitation with the bacterial flagellin epitope flg22. GLV2 is perceived by ROOT MERISTEM GROWTH FACTOR 1 INSENSITIVE (RGI) receptors and RGI3 forms an flg22-induced complex with the flg22-receptor FLAGELLIN SENSITIVE 2, suggesting that RGIs are part of activated pattern recognition receptor signalling platforms. GLV2 perception increases posttranscriptional FLS2 abundance and RGIs promote FLS2 protein accumulation. Thus, GLV-RGI signalling controls above ground plant immunity via a novel mechanism of phytocytokine activity.

Phytocytokines function as immunological modulators of plant immunity

“…It would be interesting to test in the future if FER and ANX1 compete with each other for their association with the FLS2-BAK1 complex to either enhance or dampen PTI responses and if this FER-ANX balance is under the control of different RALF peptides. RGI3 forms an flg22-induced complex with FLS2, suggesting RGI3 is part of the activated PRR signaling platform (Stegmann et al 2021). Interestingly, RGF9/GLV2 perception by RGI receptors increases FLS2 abundance and thus promotes FLS2 signaling output (Fig.…”

“…Interestingly, RGF9/GLV2 perception by RGI receptors increases FLS2 abundance and thus promotes FLS2 signaling output (Fig. 2) (Stegmann et al 2021). It will be interesting to investigate the potential relationship between FLS2 abundance and RGI3-FLS2 association.…”

“…The RGF peptide family comprises 11 members in Arabidopsis (Matsuzaki et al 2010). Among them, RGF7/GLV4 and RGF9/GLV2, which are transcriptionally regulated in plants upon infection by P. syringae, contribute to the activation of immune responses and the increase of resistance to P. syringae (Stegmann et al 2021;Wang et al 2021).…”

“…Leucine-rich repeat-RLKs (LRR-RLKs) with extracellular LRRs constitute the largest subfamily of RLKs and function as receptors of some immunological phytocytokines. Of these, tomato SYSTEMIN RE-CEPTOR 1 (SYR1) and SYR2 perceive systemin (Wang et al 2018), Arabidopsis PEP1 RECEPTOR 1 (PEPR1)/ PEPR2 recognize PEPs (Yamaguchi et al 2006), Arabidopsis RECEPTOR-LIKE 7 (RLK7) recognizes PIP1 and PIP2 (Hou et al 2014), Arabidopsis MALE DISCOV-ERER 1-INTERACTING RECEPTOR-LIKE KINASE 2 (MIK2) recognizes SCOOPs (Hou et al 2021a;Rhodes et al 2021), HAESA and HAESA-LIKE2 (HSL2) recognize IDA (Santiago et al 2016), RGF1 INSENSI-TIVE 3 (RGI3) itself or together with RGI4 recognizes RGF7 and RGF9/GLV2 (Stegmann et al 2021;Wang et al 2021), PSK RECEPTOR 1 (PSKR1) recognizes PSKs (Matsubayashi et al 2002;Wang et al 2015), and PSY1R likely recognizes PSY1 (Amano et al 2007). These phytocytokine receptors all belong to LRR X and LRR XI clades of LRR-RLKs, which are phylogenetically close to the LRR XII subfamily of LRR-RLKs, including some of the well-studied receptors of proteinaceous MAMPs, such as the bacterial flagellin receptor FLAGELLIN SENSING 2 (FLS2) and ELONGATION FACTOR-Tu RECEPTOR (EFR).…”

“…For instance, the expression of preRGF9/GLV2 is suppressed in leaves upon infection with P. syringae pv. maculicola and Pst DC3000 (Stegmann et al 2021). It remains to be determined how down-regulation of preRGF9/GLV2 plays a positive role in plant immunity.…”