Regulation of Transcription of Nucleotide-Binding Leucine-Rich Repeat-Encoding Genes SNC1 and RPP4 via H3K4 Trimethylation

Abstract

Plant nucleotide-binding leucine-rich repeat (NB-LRR) proteins serve as intracellular sensors to detect pathogen effectors and trigger immune responses. Transcription of the NB-LRR-encoding Resistance (R) genes needs to be tightly controlled to avoid inappropriate defense activation. How the expression of the NB-LRR R genes is regulated is poorly understood. The Arabidopsis (Arabidopsis thaliana) suppressor of npr1-1, constitutive 1 (snc1) mutant carries a gain-of-function mutation in a Toll/Interleukin1 receptor-like (TIR)-NB-LRR-encoding gene, resulting in the constitutive activation of plant defense responses. A snc1 suppressor screen identified modifier of snc1,9 (mos9), which partially suppresses the autoimmune phenotypes of snc1. Positional cloning revealed that MOS9 encodes a plant-specific protein of unknown function. Expression analysis showed that MOS9 is required for the full expression of TIR-NB-LRR protein-encoding RECOGNITION OF PERONOSPORA PARASITICA 4 (RPP4) and SNC1, both of which reside in the RPP4 cluster. Coimmunoprecipitation and mass spectrometry analyses revealed that MOS9 associates with the Set1 class lysine 4 of histone 3 (H3K4) methyltransferase Arabidopsis Trithorax-Related7 (ATXR7). Like MOS9, ATXR7 is also required for the full expression of SNC1 and the autoimmune phenotypes in the snc1 mutant. In atxr7 mutant plants, the expression of RPP4 is similarly reduced, and resistance against Hyaloperonospora arabidopsidis Emwa1 is compromised. Consistent with the attenuated expression of SNC1 and RPP4, trimethylated H3K4 marks are reduced around the promoters of SNC1 and RPP4 in mos9 plants. Our data suggest that MOS9 functions together with ATXR7 to regulate the expression of SNC1 and RPP4 through H3K4 methylation, which plays an important role in fine-tuning their transcription levels and functions in plant defense.

Monoubiquitination of Histone 2B at the Disease Resistance Gene Locus Regulates Its Expression and Impacts Immune Responses in Arabidopsis

“…Such immune responses involve reprogramming expression of a large number of genes (Dangl and Jones, 2001;Eulgem, 2005;Doehlemann et al, 2008). As an important regulatory mechanism for gene expression, chromatin remodeling is now revealed to play a role in plant immunity (March-Díaz et al, 2008;Dhawan et al, 2009;Berr et al, 2010;Xia et al, 2013).…”

“…It is also involved in many plant defense responses (Zhou et al, 2005;Dhawan et al, 2009;Berr et al, 2010;Palma et al, 2010;Xia et al, 2013). Pathogen infection or chemicals mimicking pathogen infection induce histone acetylation and methylation changes at the promoter of defense-related genes, such as PR1, WRKY6, WRKY29, and WRKY53 (Jaskiewicz et al, 2011;De-La-Peña et al, 2012).…”

“…Mutations in genes coding for histone modification enzymes have been found to alter disease resistance. For instance, an arabidopsis trithoraxrelated7 (atxr7) mutant deficient of an H3K4 methylase is more susceptible to oomycete pathogens (Xia et al, 2013). An impairment in histone methyltransferase SET DOMAIN GROUP8 (SDG8) makes plants more susceptible to hemibiotrophic bacterial pathogen Pseudomonas syringae pv tomato DC3000 (Pst DC3000) and necrotrophic fungi Alternaria brassicicola (Berr et al, 2010).…”

“…Histone modification is also implicated in mediating autoimmune responses. For instance, the expression of a nucleotide-binding Leu-rich repeat (NB-LRR) type of resistance (R) gene, LAZ5, requires trimethylation of H3K36 by SDG8 (Palma et al, 2010), and an H3K4 methyltransferase ATXR7 is required for the expression of two NB-LRR resistance genes: SUPPRESSOR OF npr1-1, CONSTITUTIVE1 (SNC1) and RESISTANCE TO PERONOSPORA PARASITICA 4 (RPP4; Xia et al, 2013).…”

A transposable element is domesticated for service in the plant immune system

“…Early studies of R genes failed to find evidence of substantial up-regulation after pathogen response, but more recent work, including that by Tsuchiya and Eulgem, has identified numerous factors modulating and fine-tuning NLR transcript levels. These factors range from histone modifications and DNA methylation to microRNAs and alternative splicing (17)(18)(19)(20). These factors invariably impact disease resistance responses, indicating that NLR transcript levels are precisely controlled.…”