Matching NLR Immune Receptors to Autoimmunity in camta3 Mutants Using Antimorphic NLR Alleles

Abstract

To establish infection, pathogens deploy effectors to modify or remove host proteins. Plant immune receptors with nucleotide-binding, leucine-rich repeat domains (NLRs) detect these modifications and trigger immunity. Plant NLRs thus guard host "guardees." A corollary is that autoimmunity may result from inappropriate NLR activation because mutations in plant guardees could trigger corresponding NLR guards. To explore these hypotheses, we expressed 108 dominant-negative (DN) Arabidopsis NLRs in various lesion mimic mutants, including camta3, which exhibits autoimmunity. CAMTA3 was previously described as a negative regulator of immunity, and we find that autoimmunity in camta3 is fully suppressed by expressing DNs of two NLRs, DSC1 and DSC2. Additionally, expression of either NLR triggers cell death that can be suppressed by CAMTA3 expression. These findings support a model in which DSC1 and DSC2 guard CAMTA3, and they suggest that other negative regulators of immunity may similarly represent guardees.

Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector‐ and PAMP‐triggered immunity in plants

“…Notably, similar constitutive or overactivation of immunity was seen in null mutants of other positive regulators of immune signaling, such as BAK1, BIK1, POWDERY MILDEW RESISTANT‐4 (PMR4) and MITOGEN‐ACTIVATED PROTEIN KINASE‐4 (MPK4) (Petersen et al ., ; Nishimura et al ., ; He et al ., ; Kemmerling et al ., ; J. Zhang et al ., ; Z. Zhang et al ., , ). A possible explanation is that these components are guarded by NLR proteins, as seen for MPK4 (Z. Zhang et al ., ), whose kinase activity on CALMODULIN‐BINDING RECEPTOR‐LIKE CYTOPLASMIC KINASE 3 (CRCK3) is monitored by NLR protein SUMM2 (Lolle et al ., ; Z. Zhang et al ., ).…”

“…A possible explanation is that these components are guarded by NLR proteins, as seen for MPK4 (Z. Zhang et al, 2012), whose kinase activity on CALMODULIN-BINDING RECEPTOR-LIKE CYTOPLASMIC KINASE 3 (CRCK3) is monitored by NLR protein SUMM2 (Lolle et al, 2017;Z. Zhang et al, 2017).…”

A dominant‐interfering camta3 mutation compromises primary transcriptional outputs mediated by both cell surface and intracellular immune receptors in Arabidopsis thaliana

“…Given the observed regulatory function of CAMTAs in both PTI and ETI, CAMTAs might be targeted by pathogen effectors to promote pathogen virulence. Consistent with this idea, the loss of CAMTA3 activates NLRs, which results in host cell death (Lolle et al ., ). Hence, several NLRs are able to reboot resistance, possibly via host cell death activation, even when effectors disable the CAMTA‐mediated transcriptional machinery (Lolle et al ., ).…”

“…Consistent with this idea, the loss of CAMTA3 activates NLRs, which results in host cell death (Lolle et al ., ). Hence, several NLRs are able to reboot resistance, possibly via host cell death activation, even when effectors disable the CAMTA‐mediated transcriptional machinery (Lolle et al ., ). Monitoring of CAMTA activity by NLRs further underlines the importance of this protein family in plant innate immunity.…”

The Mediator kinase module serves as a positive regulator of salicylic acid accumulation and systemic acquired resistance

“…In support of this, CAMTA3 was found to act as a transcriptional repressor to directly suppress the expression of EDS1 (Du et al ., ) and NDR1 (Nie et al ., ). Lastly, adding to the complexity is a recent report on CAMTA3 serving as a guardee monitored by two TNLs DSC1 and DSC2 (Lolle et al ., ).…”