14-3-3 proteins facilitate the activation of MAP kinase cascades by upstream immunity-related kinases

Abstract

Activation of mitogen-activated protein kinase (MAPK) cascades is essential for plant immunity. Upon activation by surface-localized immune receptors, receptor-like cytoplasmic kinases (RLCKs) in the cytoplasm phosphorylate MAP kinase kinase kinases (MAPKKKs) to initiate MAPK activation. Surprisingly, we found that both the phosphorylation of Arabidopsis (Arabidopsis thaliana) MAPKKKs and the subsequent activation of MAPK cascades require the λ and κ isoforms of 14-3-3 proteins, which directly interact with multiple RLCKs and MAPKKKs. The N- and C-termini of MAPKKK5 interact intramolecularly to inhibit the access to the C terminus by RLCKs, whereas the 14-3-3 proteins relieve this inhibition and facilitate the interaction of RLCKs with the C-terminus of MAPKKK5. This enables the phosphorylation of MAPKK5 at Ser599 and Ser682, thus promoting MAPK activation and enhancing plant disease resistance. Our study reveals a role of 14-3-3 proteins as scaffolds and activators in the regulation of the RLCK-MAPKKK5 module and provides insight into the mechanism of plant immune signaling.

Formation of HopQ1:14-3-3 complex in the host cytoplasm modulates nuclear import rate of Pseudomonas syringae effector in Nicotiana benthamiana cells

“…The function of the elements of MAP kinase cascades that play a role in the plant immunity depends on 14-3-3 proteins ( Cooper et al., 2003 ; Oh et al., 2010 ; Oh and Martin, 2011 ; Dong et al., 2023 ). Their activity and stability is controlled by 14-3-3s.…”

A 14-3-3 Protein Ca16R Acts Positively in Pepper Immunity against Ralstonia solanacearum by Interacting with CaASR1

“…Ca16R may support the function of CaASR1 by affecting phosphorylation modification so that it can affect the transcriptional regulation of CabZIP63 in the nucleus. Given that CaCDPK15 [57] and CaCDPK29 [27] are involved in pepper immunity against RSI, and CDPKs and MAPKs coordinate with 14-3-3s in regulating diverse aspects of plant biology including metabolism, development, and stress responses [14,16], we speculate that some unidentified kinases might be involved in the functional relationship between Ca16R and CaASR1; however, further study is required to confirm this speculation.…”

“…It has been found that 14-3-3 proteins fulfill their functions in regulation of plant immunity by interacting with client proteins as adaptor molecules stimulating protein-protein interactions, or as regulators to regulate the subcellular localization of proteins or their activity [14]. Our data showed that Ca16R interacts with CaASR1 (Figure 5), and CaASR1 was previously found to promote SA-signaling-mediated immunity by interacting with CabZIP63, thereby promoting the binding of CabZIP63 to its SA-dependent immunityrelated target genes and their corresponding transcriptional activation [33].…”

“…The members of this family act as adaptors for protein-protein interactions, regulators of the localization of proteins or their activities [8], and thus crucial regulators of a wide range of target proteins in signal transduction in plant growth, development, and defense response to stress. 14-3-3 proteins have been found to be involved in the regulation of plant immunity [9][10][11][12][13][14] by targeting NLRs [15], MAPKKKs [9,14,15], substrates of CDPKs [16], RIN4 and GCN4 [17], and transcription factors such as GRAS proteins (by regulating its stability) [18]. Their roles as crucial regulators in plant immunity is reflected in their frequent attack or hijacking by pathogen effectors to weaken plant immune responses or increase pathogen virulence [10,[19][20][21][22][23][24].…”

Paradigms of receptor kinase signaling in plants

“…In other cases, ligand-binding receptors might directly activate MAPK cascades via interaction with and phosphorylation of MAP3Ks [ 185 ]. In immunity, PBL27 as well as PBLs from the RLCK-VII-4 subclade are required for MAPK signaling downstream of chitin perception by CERK1 [ 153 , 159 , 161 , 186 ]. It is not clear whether PBLs activate MAPK signaling downstream of other immune receptors, however such a role might be fulfilled by BSKs [ 153 , 159 , 164 , 186 , 187 ].…”