Autoimmunity in Arabidopsis acd11 Is Mediated by Epigenetic Regulation of an Immune Receptor

Abstract

Certain pathogens deliver effectors into plant cells to modify host protein targets and thereby suppress immunity. These target modifications can be detected by intracellular immune receptors, or Resistance (R) proteins, that trigger strong immune responses including localized host cell death. The accelerated cell death 11 (acd11) “lesion mimic” mutant of Arabidopsis thaliana exhibits autoimmune phenotypes such as constitutive defense responses and cell death without pathogen perception. ACD11 encodes a putative sphingosine transfer protein, but its precise role during these processes is unknown. In a screen for lazarus (laz) mutants that suppress acd11 death we identified two genes, LAZ2 and LAZ5. LAZ2 encodes the histone lysine methyltransferase SDG8, previously shown to epigenetically regulate flowering time via modification of histone 3 (H3). LAZ5 encodes an RPS4-like R-protein, defined by several dominant negative alleles. Microarray and chromatin immunoprecipitation analyses showed that LAZ2/SDG8 is required for LAZ5 expression and H3 lysine 36 trimethylation at LAZ5 chromatin to maintain a transcriptionally active state. We hypothesize that LAZ5 triggers cell death in the absence of ACD11, and that cell death in other lesion mimic mutants may also be caused by inappropriate activation of R genes. Moreover, SDG8 is required for basal and R protein-mediated pathogen resistance in Arabidopsis, revealing the importance of chromatin remodeling as a key process in plant innate immunity. Plants defend themselves against pathogens via immune receptors that trigger responses including the suicide of infected cells to limit pathogen growth. The accelerated cell death 11 (acd11) knockout mutant of the model plant Arabidopsis thaliana kills itself in the absence of invading pathogens. By screening for secondary mutations that resurrect acd11, we discovered two LAZARUS (LAZ) genes required for death. The first, LAZ2, encodes an enzyme that methylates histones, the major protein component of chromatin. This particular histone modification is generally involved in epigenetic remodeling of chromatin to a more permissive state for transcription of associated DNA. We show that expression of the second gene, LAZ5, is dependent on LAZ2 activity, suggesting that LAZ5 is a direct target of LAZ2. LAZ5 is a member of an immune receptor class involved in detection of specific pathogens and subsequent cell death. We propose that acd11, and other suicidal mutants, result from autoimmunity triggered by immune receptors controlled by chromosomal modifications. Interestingly, we found that defects in LAZ2 result in enhanced susceptibility to bacterial pathogens, suggesting that it controls other genes involved in innate immunity.