Modulation of ACD6 dependent hyperimmunity by natural alleles of an Arabidopsis thaliana NLR resistance gene

PLoS Genet. 2018 Sep 20;14(9):e1007628. doi: 10.1371/journal.pgen.1007628. eCollection 2018 Sep.

Abstract

Plants defend themselves against pathogens by activating an array of immune responses. Unfortunately, immunity programs may also cause unintended collateral damage to the plant itself. The quantitative disease resistance gene ACCELERATED CELL DEATH 6 (ACD6) serves to balance growth and pathogen resistance in natural populations of Arabidopsis thaliana. An autoimmune allele, ACD6-Est, which strongly reduces growth under specific laboratory conditions, is found in over 10% of wild strains. There is, however, extensive variation in the strength of the autoimmune phenotype expressed by strains with an ACD6-Est allele, indicative of genetic modifiers. Quantitative genetic analysis suggests that ACD6 activity can be modulated in diverse ways, with different strains often carrying different large-effect modifiers. One modifier is SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1), located in a highly polymorphic cluster of nucleotide-binding domain and leucine-rich repeat (NLR) immune receptor genes, which are prototypes for qualitative disease resistance genes. Allelic variation at SNC1 correlates with ACD6-Est activity in multiple accessions, and a common structural variant affecting the NL linker sequence can explain differences in SNC1 activity. Taken together, we find that an NLR gene can mask the activity of an ACD6 autoimmune allele in natural A. thaliana populations, thereby linking different arms of the plant immune system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Ankyrins / immunology*
  • Ankyrins / metabolism
  • Arabidopsis / genetics
  • Arabidopsis / immunology*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / immunology*
  • Arabidopsis Proteins / metabolism
  • Autoimmunity / genetics*
  • Disease Resistance / genetics
  • Gene Expression Regulation, Plant / immunology*
  • Mutation
  • Plant Diseases / genetics
  • Plant Diseases / immunology*
  • Plant Immunity / genetics*
  • Plants, Genetically Modified
  • Signal Transduction / immunology

Substances

  • ACD6 protein, Arabidopsis
  • Ankyrins
  • Arabidopsis Proteins
  • SNC1 protein, Arabidopsis

Grant support

This work was supported by European Research Council, Advanced Grants, IMMUNEMESIS, and the Max Planck Society. The NLR RenSeq database was generated with generous support from the Gordon and Betty Moore Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.