Activation of the Arabidopsis thaliana immune system by combinations of common ACD6 alleles

PLoS Genet. 2014 Jul 10;10(7):e1004459. doi: 10.1371/journal.pgen.1004459. eCollection 2014 Jul.

Abstract

A fundamental question in biology is how multicellular organisms distinguish self and non-self. The ability to make this distinction allows animals and plants to detect and respond to pathogens without triggering immune reactions directed against their own cells. In plants, inappropriate self-recognition results in the autonomous activation of the immune system, causing affected individuals to grow less well. These plants also suffer from spontaneous cell death, but are at the same time more resistant to pathogens. Known causes for such autonomous activation of the immune system are hyperactive alleles of immune regulators, or epistatic interactions between immune regulators and unlinked genes. We have discovered a third class, in which the Arabidopsis thaliana immune system is activated by interactions between natural alleles at a single locus, ACCELERATED CELL DEATH 6 (ACD6). There are two main types of these interacting alleles, one of which has evolved recently by partial resurrection of a pseudogene, and each type includes multiple functional variants. Most previously studies hybrid necrosis cases involve rare alleles found in geographically unrelated populations. These two types of ACD6 alleles instead occur at low frequency throughout the range of the species, and have risen to high frequency in the Northeast of Spain, suggesting a role in local adaptation. In addition, such hybrids occur in these populations in the wild. The extensive functional variation among ACD6 alleles points to a central role of this locus in fine-tuning pathogen defenses in natural populations.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ankyrins / genetics*
  • Ankyrins / immunology
  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis / immunology*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / immunology
  • Cell Death / genetics
  • Gene Frequency
  • Plant Immunity / genetics*
  • Signal Transduction / genetics
  • Spain

Substances

  • ACD6 protein, Arabidopsis
  • Ankyrins
  • Arabidopsis Proteins

Grant support

This work was supported by an Academy of Finland Fellowship (www.aka.fi) and a Human Frontier Science Program Long-Term Fellowship (RAEL; www.hfsp.org), a NIH Ruth Kirschstein NRSA fellowship (KB; www.nih.gov), the European Community FP6 IP AGRON-OMICS (contract LSHG-CT-2006-037704), a European Community FP7 Marie Curie Fellowship (PIEF-GA-2008-221553; ec.europa.eu/research) and an EMBO Long-Term fellowship (LMS; www.embo.org), a Gottfried Wilhelm Leibniz Award of the DFG (www.dfg.de) and the Max Planck Society (DW; www.mpg.de). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.