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

Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV - BMC Biol. (2016)

Bottom Line: 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.Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen.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.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich Research Park, Norwich, UK.

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.

No MeSH data available.


Evolutionary analyses of the WRKY domain in NLR-WRKYs family. a Multiple sequence alignment logo of the WRKY domains found in all NLR-IDs shows conserved core structural tryptophan and incomplete conservation of tyrosine and lysine that have been shown to be essential for recognizing the W-box DNA. b Maximum likelihood phylogeny of all Arabidopsis WRKY domain-containing proteins (black nodes) and the WRKYs detected as fusions in all flowering plants (strawberry nodes). Distinct Arabidopsis WRKY clades that form fusions are highlighted as the following: green, RRS1 clade; yellow, WRKY46; pink, WRKY70 and WRKY54; blue, WRKY16; and purple, WRKY19/MEKK4. Arabidopsis WRKY41 known to be the host target is marked with red asterisk
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4759884&req=5

Fig5: Evolutionary analyses of the WRKY domain in NLR-WRKYs family. a Multiple sequence alignment logo of the WRKY domains found in all NLR-IDs shows conserved core structural tryptophan and incomplete conservation of tyrosine and lysine that have been shown to be essential for recognizing the W-box DNA. b Maximum likelihood phylogeny of all Arabidopsis WRKY domain-containing proteins (black nodes) and the WRKYs detected as fusions in all flowering plants (strawberry nodes). Distinct Arabidopsis WRKY clades that form fusions are highlighted as the following: green, RRS1 clade; yellow, WRKY46; pink, WRKY70 and WRKY54; blue, WRKY16; and purple, WRKY19/MEKK4. Arabidopsis WRKY41 known to be the host target is marked with red asterisk

Mentions: The current integrated decoy model suggests that the fused proteins might lose their biochemical activity after integration while retaining effector-binding properties [25]. To test whether NLR-kinase fusions follow the current model of integrated decoy, we have tested whether the kinase activity is likely to be conserved. After aligning all kinase regions from NLR-IDs, we examined conservation of active site region and catalytic residues. We explored sequence conservation by mapping alignment of all kinases found in NLRs on the 3D structural model of the kinase, with the active site conserved (red) while most of the other regions are variable (blue) (Fig. 5b). The catalytic lysine and aspartate are also conserved in all kinases as can be seen from the structure as well as alignment consensus logo (Fig. 5c). Overall, these data indicate that the kinases fused with NLRs encode intact full-length kinase domains that are potentially catalytically active.Fig. 5


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

Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV - BMC Biol. (2016)

Evolutionary analyses of the WRKY domain in NLR-WRKYs family. a Multiple sequence alignment logo of the WRKY domains found in all NLR-IDs shows conserved core structural tryptophan and incomplete conservation of tyrosine and lysine that have been shown to be essential for recognizing the W-box DNA. b Maximum likelihood phylogeny of all Arabidopsis WRKY domain-containing proteins (black nodes) and the WRKYs detected as fusions in all flowering plants (strawberry nodes). Distinct Arabidopsis WRKY clades that form fusions are highlighted as the following: green, RRS1 clade; yellow, WRKY46; pink, WRKY70 and WRKY54; blue, WRKY16; and purple, WRKY19/MEKK4. Arabidopsis WRKY41 known to be the host target is marked with red asterisk
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4759884&req=5

Fig5: Evolutionary analyses of the WRKY domain in NLR-WRKYs family. a Multiple sequence alignment logo of the WRKY domains found in all NLR-IDs shows conserved core structural tryptophan and incomplete conservation of tyrosine and lysine that have been shown to be essential for recognizing the W-box DNA. b Maximum likelihood phylogeny of all Arabidopsis WRKY domain-containing proteins (black nodes) and the WRKYs detected as fusions in all flowering plants (strawberry nodes). Distinct Arabidopsis WRKY clades that form fusions are highlighted as the following: green, RRS1 clade; yellow, WRKY46; pink, WRKY70 and WRKY54; blue, WRKY16; and purple, WRKY19/MEKK4. Arabidopsis WRKY41 known to be the host target is marked with red asterisk
Mentions: The current integrated decoy model suggests that the fused proteins might lose their biochemical activity after integration while retaining effector-binding properties [25]. To test whether NLR-kinase fusions follow the current model of integrated decoy, we have tested whether the kinase activity is likely to be conserved. After aligning all kinase regions from NLR-IDs, we examined conservation of active site region and catalytic residues. We explored sequence conservation by mapping alignment of all kinases found in NLRs on the 3D structural model of the kinase, with the active site conserved (red) while most of the other regions are variable (blue) (Fig. 5b). The catalytic lysine and aspartate are also conserved in all kinases as can be seen from the structure as well as alignment consensus logo (Fig. 5c). Overall, these data indicate that the kinases fused with NLRs encode intact full-length kinase domains that are potentially catalytically active.Fig. 5

Bottom Line: 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.Domains fused to NLRs overlap with previously identified pathogen targets confirming that they act as baits for the pathogen.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.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich Research Park, Norwich, UK.

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.

No MeSH data available.