Three ARID proteins involved in chromatin remodeling PEAT complexes are targeted by the Ralstonia solanacearum effector PopP2 and contribute to bacterial wilt disease.

Like many gram-negative phytopathogenic bacteria, Ralstonia solanacearum uses a type III secretion system to deliver into host cells a cocktail of effector proteins that can interfere with plant defenses and promote infection. One of these effectors, the nuclear-targeted PopP2 acetyltransferase, was reported to inhibit many defensive WRKY transcription factors through acetylation. To gain a better understanding of the mechanisms by which PopP2 might exert its virulence functions, we searched for other PopP2-interacting partners. Here we report the identification of the Arabidopsis thaliana AT-Rich Interaction Domain protein 3 (ARID3) and its close homologs, ARID2 and ARID4, as additional targets of PopP2. These ARID proteins are core components of the chromatin remodeling PEAT complexes that regulate gene expression through histone (de)acetylation and deubiquitination. In yeast, PopP2 binds the conserved C-terminal part of ARID2/3/4, which contains an α-crystallin domain putatively involved in their homo-oligomerization. ARID2/3/4 behave as substrates of PopP2 acetyltransferase activity, which causes the acetylation of several lysine residues conserved between these three proteins and located near their α-crystallin domain. Interestingly, while PopP2 negatively affects ARID3 and ARID4 self-interactions in planta, it promotes the interaction of ARID3 and ARID4 with PWWP1, another component of PEAT complexes, with which PopP2 can also interact. This study also reveals that disruption of ARID2/3/4 results in reduced growth of R. solanacearum. Overall, our data are consistent with a model in which PopP2 targets several components of PEAT complexes to interfere with their epigenetic regulatory functions and promote Ralstonia infection in Arabidopsis.