Genome-wide functional analyses of plant coiled-coil NLR-type pathogen receptors reveal essential roles of their N-terminal domain in oligomerization, networking, and immunity

PLoS Biol. 2018 Dec 12;16(12):e2005821. doi: 10.1371/journal.pbio.2005821. eCollection 2018 Dec.

Abstract

The ability to induce a defense response after pathogen attack is a critical feature of the immune system of any organism. Nucleotide-binding leucine-rich repeat receptors (NLRs) are key players in this process and perceive the occurrence of nonself-activities or foreign molecules. In plants, coevolution with a variety of pests and pathogens has resulted in repertoires of several hundred diverse NLRs in single individuals and many more in populations as a whole. However, the mechanism by which defense signaling is triggered by these NLRs in plants is poorly understood. Here, we show that upon pathogen perception, NLRs use their N-terminal domains to transactivate other receptors. Their N-terminal domains homo- and heterodimerize, suggesting that plant NLRs oligomerize upon activation, similar to the vertebrate NLRs; however, consistent with their large number in plants, the complexes are highly heterometric. Also, in contrast to metazoan NLRs, the N-terminus, rather than their centrally located nucleotide-binding (NB) domain, can mediate initial partner selection. The highly redundant network of NLR interactions in plants is proposed to provide resilience to perturbation by pathogens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Genome, Plant / genetics
  • Genome, Plant / immunology
  • Immunity, Innate
  • Lettuce / genetics
  • NLR Proteins / genetics*
  • NLR Proteins / immunology*
  • Plant Diseases / immunology
  • Plant Immunity / genetics
  • Plant Immunity / immunology
  • Plant Proteins / genetics*
  • Plants / genetics
  • Plants / immunology
  • Protein Domains / genetics
  • Sequence Analysis, Protein
  • Signal Transduction

Substances

  • NLR Proteins
  • Plant Proteins

Grant support

European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement (grant number 676480 (Bestpass)). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NWO-Earth and Life Sciences funded VICI project (grant number 865.14.003). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Romanian Ministry of Research and Innovation, CNCS – UEFISCDI (grant number PN-III-ID-PCE-2016-0650 and PN-III-P1-1.1-TE-2016-1852 within PNCDI III). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Romanian Academy (grant number 1 and 3 of IBAR). and other resources. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.