Bacterial AvrRpt2-Like Cysteine Proteases Block Activation of the Arabidopsis Mitogen-Activated Protein Kinases, MPK4 and MPK11

Abstract

To establish infection, pathogens deliver effectors into host cells to target immune signaling components, including elements of mitogen-activated protein kinase (MPK) cascades. The virulence function of AvrRpt2, one of the first identified Pseudomonas syringae effectors, involves cleavage of the plant defense regulator, RPM1-INTERACTING PROTEIN4 (RIN4), and interference with plant auxin signaling. We show now that AvrRpt2 specifically suppresses the flagellin-induced phosphorylation of Arabidopsis (Arabidopsis thaliana) MPK4 and MPK11 but not MPK3 or MPK6. This inhibition requires the proteolytic activity of AvrRpt2, is associated with reduced expression of some plant defense genes, and correlates with enhanced pathogen infection in AvrRpt2-expressing transgenic plants. Diverse AvrRpt2-like homologs can be found in some phytopathogens, plant-associated and soil bacteria. Employing these putative bacterial AvrRpt2 homologs and inactive AvrRpt2 variants, we can uncouple the inhibition of MPK4/MPK11 activation from the cleavage of RIN4 and related members from the so-called nitrate-induced family as well as from auxin signaling. Thus, this selective suppression of specific mitogen-activated protein kinases is independent of the previously known AvrRpt2 targets and potentially represents a novel virulence function of AvrRpt2.

Similarities between Reproductive and Immune Pistil Transcriptomes of Arabidopsis Species

“…The up-regulation of NOI1 in pistils pollinated with A. lyrata and A. halleri pollen caught our attention because it encodes a RIN4 family member, well-known key regulators of defense. According to the guard hypothesis, the R protein RPM1 is activated by RIN4 phosphorylation and initiates effector-triggered immunity (Eschen-Lippold et al, 2016). The up-regulation of NOI1 during interspecific pollen-pistil interactions suggests that this intracellular protein also might participate in the signaling pathway triggering pollen tube rejection.…”

Ptr1evolved convergently withRPS2andMr5to mediate recognition of AvrRpt2 in diverse solanaceous species

“…The widespread use of the Pto/Prf genes since the 1980s appears to have exerted selection pressure on the pathogen and race 0 Pst strains are becoming less common. Instead, strains of race 1 Pst, which lack AvrPto and AvrPtoB, are becoming more prevalent and represent a new threat in tomato growing areas (Kunkeaw et al, 2010, Thapa andCoaker, 2016).…”

Teaching an old dog new tricks: Suppressing activation of specific mitogen-activated kinases as a potential virulence function of the bacterial AvrRpt2 effector protein

“…AvrRpt2 is a Cys-protease, which upon activation and self-cleavage within plant cells, targets the plant defense regulator RIN4 and Aux/IAA transcription factors through direct cleavage and promoting protein-turnover, respectively 11-14 . While the protease activity of AvrRpt2 is required to suppress MPK4/11 activation, MPK4/11 are not directly cleaved 10 . We also showed that AvrRpt2 functions may be more widespread in bacteria-host interactions than previously anticipated.…”

“…This presumably represents a novel virulence function of AvrRpt2 to manipulate and fine-tune MPK signaling 10 . AvrRpt2 is a Cys-protease, which upon activation and self-cleavage within plant cells, targets the plant defense regulator RIN4 and Aux/IAA transcription factors through direct cleavage and promoting protein-turnover, respectively 11-14 .…”