Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

Klymiuk, Valentyna; Yaniv, Elitsur; Huang, Lin; Raats, Dina; Fatiukha, Andrii; Chen, Shisheng; Feng, Lu; Frenkel, Zeev; Krugman, Tamar; Lidzbarsky, Gabriel; Chang, Wei; Jääskeläinen, Marko; Schudoma, Christian; Paulín, Lars; Laine, Pia; Bariana, Harbans; Sela, Hanan; Saleem, Kamran; Sørensen, Chris K.; Hovmøller, Mogens S.; Distelfeld, Assaf; Chalhoub, Boulos; Dubcovsky, Jorge; Korol, Abraham B.; Schulman, Alan H.; Fahima, Tzion

doi:10.1038/s41467-018-06138-9

Cited by 252 publications

(258 citation statements)

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“…The microscopic phenotype of Yr15 showed that the resistance response of this gene was distinct from other R genes and activated shorty after inoculation. This result supports the finding of the Yr15 cloning studies (Klymiuk et al , ). The cloning of Yr15 revealed that it encodes a putative kinase‐pseudokinase protein, designated as a wheat tandem kinase 1 (WTK1) belonging to the family of receptor‐like cytoplasmic kinases (RLCK) (Klymiuk et al , ).…”

Section: Discussionsupporting

confidence: 91%

“…This result supports the finding of the Yr15 cloning studies (Klymiuk et al , ). The cloning of Yr15 revealed that it encodes a putative kinase‐pseudokinase protein, designated as a wheat tandem kinase 1 (WTK1) belonging to the family of receptor‐like cytoplasmic kinases (RLCK) (Klymiuk et al , ). The decoy role, where host R protein mimics effector target to trap the pathogen, has been proposed as one of the potential mechanisms of function of RLCK family members in plant immunity (van der Hoorn & Kamoun, ).…”

Section: Discussionsupporting

confidence: 91%

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Spatiotemporal changes in fungal growth and host responses of six yellow rust resistant near‐isogenic lines of wheat

et al. 2019

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The objective of the present study was to investigate to what extent the macroscopic phenotype of incompatible host–pathogen interactions reflects differences in fungal development and host responses at the histological level. This was done by conventional and advanced microscopic analysis of six wheat near‐isogenic lines differing by individual R genes and inoculated with an avirulent isolate of Puccinia striiformis. Wheat line AvocetYr15 had the lowest macroscopic infection type (IT) 0–1, in which fungal growth was stopped at early stages due to extensive expression of a hypersensitive response (HR) at all time points (4, 8 and 16 days post‐inoculation, dpi) without any sign of haustorial bodies. AvocetYr5 and AvocetYr1 had IT 1, in which most fungal colonies developed secondary hyphae. Many colonies were encased by HR at 16 dpi, more extensively in AvocetYr1 than AvocetYr5. In AvocetYr6 (IT 2), HR was expressed after the formation of secondary hyphae at 4 dpi, after which fungal growth and HR increased simultaneously until most colonies became encased by HR. AvocetYr27 (IT 2–3) and AvocetYr17 (IT 4–5) showed similar fungal growth and HR at 4 dpi, where HR was only weakly expressed in a few host cells. Encasement of secondary and runner hyphae increased significantly in AvocetYr27, but at 16 dpi, HR was often circumvented by large, intermingled fungal colonies in both lines. No resistance responses were observed in Avocet S (susceptible control). The very different histological patterns conferred by the six R genes suggests differences in the timing of the host–pathogen recognition and onset of host defence pathways.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 91%

Spatiotemporal changes in fungal growth and host responses of six yellow rust resistant near‐isogenic lines of wheat

et al. 2019

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“…So far, six WEW - derived Yr genes have been recognized ( Yr15, YrH52, Yr35, Yr36, YrTz2 , and YrSM139-1B ) on chromosome arms 1BS and 6BS (Huang et al , 2016a; Klymiuk et al , 2019a). Among these, only Yr36 (Fu et al , 2009) and Yr15 (Klymiuk et al , 2018) have been cloned so far.…”

Section: Introductionmentioning

confidence: 99%

Three previously characterized resistances to yellow rust are encoded by a single locusWtk1

Klymiuk

Fatiukha

Raats

et al. 2020

Preprint

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The wild emmer wheat (Triticum turgidum ssp. dicoccoides; WEW) yellow (stripe) rust resistance genes Yr15, YrG303 and YrH52 were discovered in natural populations from different geographic locations. They all localize to chromosome 1B but were thought to be non-allelic based on differences in resistance response. We recently cloned Yr15 as a Wheat Tandem Kinase 1 (WTK1) and showed here that these three resistance loci co-segregate in fine-mapping populations and share identical full-length genomic sequence of functional Wtk1. Independent EMS mutagenized susceptible yrG303 and yrH52 lines carried single nucleotide mutations in Wtk1 that disrupted function. A comparison of the mutations for yr15, yrG303 and yrH52 mutants showed that while key conserved residues were intact, other conserved regions in critical kinase subdomains were frequently affected. Thus, we concluded that Yr15-, YrG303- and YrH52-mediated resistances to yellow rust are encoded by a single locus Wtk1. Introgression of Wtk1 into multiple genetic backgrounds resulted in variable phenotypic responses, confirming that Wtk1-mediated resistance is part of a complex immune response network. WEW natural populations subjected to natural selection and adaptation have potential to serve as a good source for evolutionary studies of different traits and multifaceted gene networks.HighlightWe demonstrate that Yr15, YrG303 and YrH52 resistances are encoded by the Wtk1 locus, but express variable resistance responses to yellow rust in a genetic background dependent manner.

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“…Early surveys of the complete kinase domain complements from organisms including human, mouse, Caenorhabditis elegans , Dictyostelium and Arabidopsis found that pseudokinases like ZED1 account for ∼10% of the kinase domains in higher eukaryotes and 20% of Arabidopsis RLCKs [25,26]. Plant pseudokinases are emerging as important mediators of development and immunity [27–29]. Rather than mere non-functional kinases resulting from relaxed (or absent) selective constraints, there is instead a growing body of evidence indicating that pseudokinases are important signaling molecules in spite of their predicted lack of catalytic activity, often functioning as adaptors or scaffolds that modulate the activity of true kinase partners [25,28,30,31].…”

Section: Introductionmentioning

confidence: 99%

Perturbations of a Kinase-Pseudokinase Module Activate Plant Immunity

Bastedo

Seto

Martel

et al. 2019

Preprint

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The Pseudomonas syringae acetyltransferase HopZ1a is delivered directly into host cells by the type III secretion system to promote bacterial growth. However, in the model plant host Arabidopsis thaliana, HopZ1a activity results in an effector-triggered immune response (ETI) that limits bacterial proliferation. HopZ1a-triggered immunity requires the nucleotide-binding, leucine-rich repeat domain (NLR) protein, ZAR1, and the ZED1 pseudokinase. Here we demonstrate that HopZ1a can acetylate members of a family of ‘receptor-like cytoplasmic kinases’ (RLCK family VII; also known as PBS1-like kinases, or PBLs) and promote their interaction with ZED1 and ZAR1 to form a ZAR1/ZED1/PBL ternary complex. Interactions between ZED1 and PBL kinases are determined by the pseudokinase features of ZED1, and mutants designed to restore ZED1 kinase motifs can (1) bind to PBLs, (2) recruit ZAR1, and (3) trigger immunity in planta, all independently of HopZ1a. Our results suggest that interactions between these two RLCK families are promoted by perturbations of structural features that distinguish active from inactive kinase domain conformations. We propose that effector-induced interactions between ZED1/ZRK pseudokinases (RLCK family XII) and PBL kinases (RLCK family VII) provide a sensitive mechanism for detecting perturbations of either kinase family and activating ZAR1-mediated ETI.AUTHOR SUMMARYAll plants must ward off potentially infectious microbes, and those grown in large-scale crop operations are especially vulnerable to the rapid spread of disease by successful pathogens. Although many bacteria and fungi can supress plant immune responses by producing specialized virulence proteins called ‘effectors’, these effectors can also trigger immune responses that render plants resistant to infection. We studied the molecular mechanisms underlying one such effector-triggered immune response elicited by the bacterial effector HopZ1a in the model plant host Arabidopsis thaliana. We have shown that HopZ1a promotes binding between a ZED1, a ‘pseudokinase’ required for HopZ1a-triggered immunity, and several ‘true kinases’ (known as PBLs) that are likely targets of HopZ1a activity in planta. HopZ1a-induced ZED1-PBL interactions also recruit ZAR1, an Arabidopsis ‘resistance protein’ previously implicated in HopZ1a-triggered immunity. Importantly, ZED1 mutants that restore degenerate kinase motifs can bridge interactions between PBLs and ZAR1 (independently of HopZ1a) and trigger immunity in planta. Our results suggest that equilibria between active and inactive kinase domain conformations regulate ZED1-PBL interactions and formation of ternary complexes with ZAR1. Improved models describing molecular interactions between immunity determinants, effectors and effector targets will inform efforts to exploit natural diversity for development of crops with enhanced disease resistance.

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Cloning of the wheat Yr15 resistance gene sheds light on the plant tandem kinase-pseudokinase family

Cited by 252 publications

References 63 publications

Spatiotemporal changes in fungal growth and host responses of six yellow rust resistant near‐isogenic lines of wheat

Spatiotemporal changes in fungal growth and host responses of six yellow rust resistant near‐isogenic lines of wheat

Three previously characterized resistances to yellow rust are encoded by a single locusWtk1

Perturbations of a Kinase-Pseudokinase Module Activate Plant Immunity

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