Proline Isomerization of the Immune Receptor-Interacting Protein RIN4 by a Cyclophilin Inhibits Effector-Triggered Immunity in Arabidopsis

Abstract

SUMMARY In the absence of pathogen infection, plant effector-triggered immune (ETI) receptors are maintained in a preactivation state by intermolecular interactions with other host proteins. Pathogen effector-induced alterations activate the receptor. In Arabidopsis, the ETI receptor RPM1 is activated via bacterial effector AvrB-induced phosphorylation of the RPM1-interacting protein RIN4 at Threonine 166. We find that RIN4 also interacts with the prolyl-peptidyl isomerase (PPIase) ROC1, which is reduced upon RIN4 Thr166 phosphorylation. ROC1 suppresses RPM1 immunity in a PPIase-dependent manner. Consistent with this, RIN4 Pro149 undergoes cis/trans isomerization in the presence of ROC1. While the RIN4P149V mutation abolishes RPM1 resistance, the deletion of Pro149 leads to RPM1 activation in the absence of RIN4 phosphorylation. These results support a model in which RPM1 directly senses conformational changes in RIN4 surrounding Pro149 that is controlled by ROC1. RIN4 Thr166 phosphorylation indirectly regulates RPM1 resistance by modulating the ROC1-mediated RIN4 isomerization.

On plant defense signaling networks and early land plant evolution

“…ETI requires the presence of R proteins to detect pathogen secreted effector proteins either through direct binding or by monitoring whether other host proteins are altered by the actions of effectors [51]; such alterations can include changes in protein conformation and/or phosphorylation status [82,83]. Once R proteins detect an effector protein of a pathogen, they induce pathogen-specific immune responses [84-86].…”

Peptidyl-prolyl isomerization targets rice Aux/IAAs for proteasomal degradation during auxin signalling

“…In plants, cyclophilin-like genes have been identified from a variety of species, including both Arabidopsis and rice [20][21][22] . A number of plant CYP genes, mainly in Arabidopsis, have been functionally characterized, involved in a variety of physiological and developmental processes, including in flowering, phytohormone signalling, stress responses and immune responses [22][23][24][25][26][27] . Mutations in LRT2-like genes of the tomato DIAGEOTROPICA (DGT) and the moss Physcomitrella patens PpDGT genes also caused an auxin-resistant phenotype [28][29][30] , indicating that this class of highly conserved genes plays an important role in regulating auxin signalling in both lower and higher plants.…”

Phosphorylation of the Plant Immune Regulator RPM1-INTERACTING PROTEIN4 Enhances Plant Plasma Membrane H+-ATPase Activity and Inhibits Flagellin-Triggered Immune Responses in Arabidopsis

“…RIN4 phosphorylation mimics exhibit constitutive activation of RPM1-mediated defense responses, Thr-166 phosphorylation is induced by AvrB/ AvrRpm1, and RIN4 Thr-166 phosphorylation mimics are sufficient to activate RPM1 in the absence of pathogen effectors Liu et al, 2011). Recently, the cyclophilin ROC1 has been demonstrated to isomerize RIN4 Pro-149 and has been implicated in the activation of RPM1 (Li et al, 2014b). RIN4 Thr-166 phosphorylation inhibits the ROC1-RIN4 association, and RIN4 ΔP149 is also sufficient to activate RPM1-mediated responses (Li et al, 2014b).…”

“…Recently, the cyclophilin ROC1 has been demonstrated to isomerize RIN4 Pro-149 and has been implicated in the activation of RPM1 (Li et al, 2014b). RIN4 Thr-166 phosphorylation inhibits the ROC1-RIN4 association, and RIN4 ΔP149 is also sufficient to activate RPM1-mediated responses (Li et al, 2014b).…”