RALF-FERONIA Signaling: Linking Plant Immune Response with Cell Growth

Abstract

Plants perceive various external and internal signals to self-modulate biological processes through members of the receptor-like kinase (RLK) family, among which Catharanthus roseus receptor-like kinase 1-like (CrRLK1L) proteins with their ligands, rapid alkalinization factor (RALF) peptides, have attracted considerable interest. FERONIA (FER), a CrRLK1L member, was initially reported to act as a major plant cell growth modulator in distinct tissues. Subsequently, the RALF-FER pathway was confirmed to function as an essential regulator of plant stress responses, including but not limited to immune responses. Furthermore, the RALF-FER pathway modulates immune responses and cell growth in a context-specific manner, and the vital roles of this pathway are beginning to be appreciated in crop species. The recent remarkable advances in understanding the functions and molecular mechanisms of the RALF-FER pathway have also raised many interesting questions that need to be answered in the future. This review mainly focuses on the roles of FER and other CrRLK1L members in modulating immune responses in the context of cell growth in response to their RALF peptide ligands and presents a brief outlook for future research.

Keywords: FER receptor kinase; RALF peptide; cell expansion; cell wall; immune responses.

Figure 1

Network of RALF–FER Signaling in Plant Immunity. FER and LLGs respond to RALF23, which is cleaved by S1P, and modulate plant immunity, whereas LRXs mediate RALF signaling to maintain cell growth. RALF23-FER-LLGs destabilize the formation of the FLS2–BAK1 complex. Fusarium oxysporum secretes F-RALF peptides that hijack the RALF–FER pathway, leading to the phosphorylation of F. oxysporum MAPK FMK1 and potentially facilitating host infection, together with the suppression of PDF1.2 expression. FER modulates auxin, abscisic acid (ABA), ethylene (ET), Ca²⁺, reactive oxygen species (ROS), MAPK phosphorylation, and pH to affect cell growth and immunity. FER interacts with and phosphorylates RIPK, modulating AHA2 activity. RIPK phosphorylates RIN4, which is detected by RPM1 and RPS2, triggering immune responses. ANX1 also inhibits ETI responses by inhibiting RPM1 and RPS2. PBL13, a homolog of RIPK, interacts with RBOHD to regulate NADPH oxidase-induced ROS production. FER mediates RALF1-induced mRNA alternative splicing via GRP7, which also interacts with FLS2, EFR, and their transcripts. Positive regulatory actions are indicated by arrows, negative regulatory actions are indicated by bars, physical interactions between different proteins are indicated by solid lines and potential physical interactions are indicated by dashedotted lines. Question marks denote mechanisms that remain to be empirically demonstrated.