Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens

Panagiotis F Sarris, Volkan Cevik, Gulay Dagdas, Jonathan D G Jones, Ksenia V Krasileva

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

BACKGROUND: Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Intracellular plant immune receptors called nucleotide-binding leucine-rich repeat (NLR) proteins contain a central nucleotide-binding (NB) domain followed by a series of leucine-rich repeats (LRRs), and are key initiators of plant defense responses. However, recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity. These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as "baits" for the pathogen-derived effector proteins, thus enabling pathogen recognition. Several names have been proposed to describe these proteins, including "integrated decoys" and "integrated sensors". We adopt and argue for "integrated domains" or NLR-IDs, which describes the product of the fusion without assigning a universal mode of action.

RESULTS: We have scanned available plant genome sequences for the full spectrum of NLR-IDs to evaluate the diversity of integrations of potential sensor/decoy domains across flowering plants, including 19 crop species. We manually curated wheat and brassicas and experimentally validated a subset of NLR-IDs in wild and cultivated wheat varieties. We have examined NLR fusions that occur in multiple plant families and identified that some domains show re-occurring integration across lineages. Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen. While some of the integrated domains have been previously implicated in disease resistance, others provide new targets for engineering durable resistance to plant pathogens.

CONCLUSIONS: We have built a robust reproducible pipeline for detecting variable domain architectures in plant immune receptors across species. We hypothesize that NLR-IDs that we revealed provide clues to the host proteins targeted by pathogens, and that this information can be deployed to discover new sources of disease resistance.

Original languageEnglish
Article number8
JournalBMC Biology
Volume14
DOIs
Publication statusPublished - 19 Feb 2016

Fingerprint

Pathogens
leucine
Leucine
Nucleotides
pathogen
nucleotides
protein
pathogens
Proteins
proteins
Disease Resistance
Fusion reactions
disease resistance
bait
baits
Triticum
sensors (equipment)
wheat
Plant Immunity
sensor

Keywords

  • Amino Acid Sequence
  • Disease Resistance
  • Gene Fusion
  • Host-Pathogen Interactions
  • Molecular Sequence Data
  • Phylogeny
  • Plant Diseases
  • Plant Immunity
  • Plant Proteins
  • Plants
  • Protein Structure, Tertiary
  • Triticum
  • Comparative Study
  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

Cite this

Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. / Sarris, Panagiotis F; Cevik, Volkan; Dagdas, Gulay; Jones, Jonathan D G; Krasileva, Ksenia V.

In: BMC Biology, Vol. 14, 8, 19.02.2016.

Research output: Contribution to journalArticle

Sarris, Panagiotis F ; Cevik, Volkan ; Dagdas, Gulay ; Jones, Jonathan D G ; Krasileva, Ksenia V. / Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. In: BMC Biology. 2016 ; Vol. 14.
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T1 - Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens

AU - Sarris, Panagiotis F

AU - Cevik, Volkan

AU - Dagdas, Gulay

AU - Jones, Jonathan D G

AU - Krasileva, Ksenia V

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N2 - BACKGROUND: Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Intracellular plant immune receptors called nucleotide-binding leucine-rich repeat (NLR) proteins contain a central nucleotide-binding (NB) domain followed by a series of leucine-rich repeats (LRRs), and are key initiators of plant defense responses. However, recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity. These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as "baits" for the pathogen-derived effector proteins, thus enabling pathogen recognition. Several names have been proposed to describe these proteins, including "integrated decoys" and "integrated sensors". We adopt and argue for "integrated domains" or NLR-IDs, which describes the product of the fusion without assigning a universal mode of action.RESULTS: We have scanned available plant genome sequences for the full spectrum of NLR-IDs to evaluate the diversity of integrations of potential sensor/decoy domains across flowering plants, including 19 crop species. We manually curated wheat and brassicas and experimentally validated a subset of NLR-IDs in wild and cultivated wheat varieties. We have examined NLR fusions that occur in multiple plant families and identified that some domains show re-occurring integration across lineages. Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen. While some of the integrated domains have been previously implicated in disease resistance, others provide new targets for engineering durable resistance to plant pathogens.CONCLUSIONS: We have built a robust reproducible pipeline for detecting variable domain architectures in plant immune receptors across species. We hypothesize that NLR-IDs that we revealed provide clues to the host proteins targeted by pathogens, and that this information can be deployed to discover new sources of disease resistance.

AB - BACKGROUND: Plants deploy immune receptors to detect pathogen-derived molecules and initiate defense responses. Intracellular plant immune receptors called nucleotide-binding leucine-rich repeat (NLR) proteins contain a central nucleotide-binding (NB) domain followed by a series of leucine-rich repeats (LRRs), and are key initiators of plant defense responses. However, recent studies demonstrated that NLRs with non-canonical domain architectures play an important role in plant immunity. These composite immune receptors are thought to arise from fusions between NLRs and additional domains that serve as "baits" for the pathogen-derived effector proteins, thus enabling pathogen recognition. Several names have been proposed to describe these proteins, including "integrated decoys" and "integrated sensors". We adopt and argue for "integrated domains" or NLR-IDs, which describes the product of the fusion without assigning a universal mode of action.RESULTS: We have scanned available plant genome sequences for the full spectrum of NLR-IDs to evaluate the diversity of integrations of potential sensor/decoy domains across flowering plants, including 19 crop species. We manually curated wheat and brassicas and experimentally validated a subset of NLR-IDs in wild and cultivated wheat varieties. We have examined NLR fusions that occur in multiple plant families and identified that some domains show re-occurring integration across lineages. Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen. While some of the integrated domains have been previously implicated in disease resistance, others provide new targets for engineering durable resistance to plant pathogens.CONCLUSIONS: We have built a robust reproducible pipeline for detecting variable domain architectures in plant immune receptors across species. We hypothesize that NLR-IDs that we revealed provide clues to the host proteins targeted by pathogens, and that this information can be deployed to discover new sources of disease resistance.

KW - Amino Acid Sequence

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KW - Host-Pathogen Interactions

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KW - Plant Proteins

KW - Plants

KW - Protein Structure, Tertiary

KW - Triticum

KW - Comparative Study

KW - Journal Article

KW - Research Support, N.I.H., Extramural

KW - Research Support, Non-U.S. Gov't

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DO - 10.1186/s12915-016-0228-7

M3 - Article

VL - 14

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

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ER -