A wheat kinase and immune receptor form host-specificity barriers against the blast fungus

Arora, Sanu; Steed, Andrew; Goddard, Rachel; Gaurav, Kumar; O’Hara, Tom; Schoen, Adam; Rawat, Nidhi; Elkot, Ahmed F.; Korolev, Andrey V.; Chinoy, Catherine; Nicholson, Martha H.; Asuke, Soichiro; Antoniou-Kourounioti, Rea L; Steuernagel, Burkhard; Yu, Guotai; Awal, Rajani; Forner-Martínez, Macarena; Wingen, Luzie U.; Baggs, Erin; Clarke, Jonathan; Saunders, Diane G. O.; Krasileva, Ksenia; Tosa, Yukio; Jones, Jonathan D. G.; Tiwari, Vijay K.; Wulff, Brande B. H.; Nicholson, P.

doi:10.1038/s41477-023-01357-5

Cited by 30 publications

(50 citation statements)

References 34 publications

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“…Morex delimited the candidate locus to two possible genes (Dinh et al ., 2022). Similarly, cloning and characterization of R genes encoding kinase fusion proteins, such as Resistance to Puccinia graminis 1 ( Rpg1 ) (Brueggeman et al ., 2002), Yellow rust resistance 15 ( Yr15 ) (Klymiuk et al ., 2015), Lr9 (Wang et al ., 2023), Stem rust resistance 43 ( Sr43 ) (Yu et al ., 2023), Sr60 (Chen et al ., 2020), Sr62 (Yu et al ., 2022), WTK4 (Gaurav et al ., 2022), Powdery mildew resistance 4 ( Pm4 ) (Sánchez‐Martín et al ., 2021), Pm24 (Lu et al ., 2020), Pm13 (Li et al ., 2023), Pm57 (Liu et al ., 2023) and Rwt4 (synonym of Resistance to Magnaporthe grisea 1 ; Rmg1 ) (Arora et al ., 2023), along with the Kolodziej et al . (2021) and Dinh et al .…”

Section: Pan‐genomics Reveal the Extent Of Variation At R Locimentioning

confidence: 84%

“…Proteins encoded by structurally distinct R gene classes have key roles in forming host specificity barriers. A pertinent example is in wheat, where the two R genes Rwt3 and Rwt4 , encoding an NLR and a tandem kinase, respectively, act as host specificity barriers against non‐ Triticum blast pathotypes (Arora et al ., 2023). In Hordeum spp., orthologous cell wall‐associated receptor kinase genes from cultivated ( H. vulgare ) and bulbous ( H. bulbosum ) barley conferred both partial and non‐host resistance to adapted and non‐adapted leaf rust pathogens, respectively (Wang et al ., 2019).…”

Section: Diverse ‘Gatekeepers’ Of Host Specializationmentioning

confidence: 99%

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Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley

Dracatos

Sánchez‐Martín

et al. 2023

Plant Biotechnology Journal

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SummaryStaying ahead of the arms race against rust and mildew diseases in cereal crops is essential to maintain and preserve food security. The methodological challenges associated with conventional resistance breeding are major bottlenecks for deploying resistance (R) genes in high‐yielding crop varieties. Advancements in our knowledge of plant genomes, structural mechanisms, innovations in bioinformatics, and improved plant transformation techniques have alleviated this bottleneck by permitting rapid gene isolation, functional studies, directed engineering of synthetic resistance and precise genome manipulation in elite crop cultivars. Most cloned cereal R genes encode canonical immune receptors which, on their own, are prone to being overcome through selection for resistance‐evading pathogenic strains. However, the increasingly large repertoire of cloned R genes permits multi‐gene stacking that, in principle, should provide longer‐lasting resistance. This review discusses how these genomics‐enabled developments are leading to new breeding and biotechnological opportunities to achieve durable rust and powdery mildew control in cereals.

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Section: Pan‐genomics Reveal the Extent Of Variation At R Locimentioning

confidence: 84%

Section: Diverse ‘Gatekeepers’ Of Host Specializationmentioning

confidence: 99%

Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley

Dracatos

Sánchez‐Martín

et al. 2023

Plant Biotechnology Journal

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“…A possible example of such a mechanism is the non-MAX effector PWT3 of P. oryzae that is specifically absent from the Triticum -infecting lineage [29]. PWT3 triggers resistance in wheat cultivars possessing the RWT3 resistance gene [58], and its loss was shown to coincide with the widespread deployment of RWT3 wheat. Similarly, the loss of the effector AVR1-CO39 (MAX86) , which is specifically absent from the Oryza -infecting lineage and that is detected by the rice NLR immune receptor complex RGA4/RGA5, has been suggested to have contributed to the initial colonization of rice by the Setaria -infecting lineage [20, 31, 59].…”

Section: Discussionmentioning

confidence: 99%

Adaptive evolution in virulence effectors of the rice blast fungusPyricularia oryzae

Naour—Vernet

Charriat

Gracy

et al. 2023

Preprint

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Plant pathogens secrete proteins called effectors that target host cellular processes to promote disease. Recently, structural genomics has identified several families of fungal effectors that share a similar three-dimensional structure despite remarkably variable amino-acid sequences and surface properties. To explore the selective forces that underlie the sequence variability of structurally-analogous effectors, we focused on MAX effectors, a structural family of effectors that are major determinants of virulence in the rice blast fungus Pyricularia oryzae. Using structure-informed gene annotation, we identified 58 to 78 MAX effector genes per genome in a set of 120 isolates representing seven host-associated lineages. The expression of MAX effector genes was primarily restricted to the early biotrophic phase of infection and strongly influenced by the host plant. Pangenome analyses of MAX effectors demonstrated extensive presence/absence polymorphism and identified gene loss events possibly involved in host range adaptation. However, gene knock-in experiments did not reveal a strong effect on virulence phenotypes suggesting that other evolutionary mechanisms are the main drivers of MAX effector losses. MAX effectors displayed high levels of standing variation and high rates of non-synonymous substitutions, pointing to widespread positive selection shaping the molecular diversity of MAX effectors. The combination of these analyses with structural data revealed that positive selection acts mostly on residues located in particular structural elements and at specific positions. Our work provides unique insights into the evolutionary history of an extended fungal effector family and opens up new research avenues to deepen our understanding of the molecular coevolutionary interactions of fungi with plant hosts.

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“…Blast Pm4 gene discovery and Proof of Function. Seedling leaves of a set of 300 diverse Watkins genotypes were screened for resistance to two isolates of Magnaporthe oryzae pathotype triticum ( MoT ) that carry the effector AVR-Rmg8 using the methods described 77 . Spike resistance to these isolates was assessed using the methods described 77 .…”

Section: Methodsmentioning

confidence: 99%

“…Seedling leaves of a set of 300 diverse Watkins genotypes were screened for resistance to two isolates of Magnaporthe oryzae pathotype triticum ( MoT ) that carry the effector AVR-Rmg8 using the methods described 77 . Spike resistance to these isolates was assessed using the methods described 77 . Validation of the candidate gene recognising AVR-Rmg8 was undertaken using the loss of function mutants and overexpressing transformant lines described for Pm4 (ref 37 ).…”

Section: Methodsmentioning

confidence: 99%

Harnessing Landrace Diversity Empowers Wheat Breeding for Climate Resilience

Cheng,

Feng,

Wingen

et al. 2023

Preprint

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Breeding crops resilient to climate change is urgently needed to help ensure food security. A key challenge is to harness genetic diversity to optimise adaptation, yield, stress resilience and nutrition. We examined the genetic and phenotypic diversity of the A.E. Watkins landrace collection of bread wheat (Triticum aestivum), a major global cereal, through whole-genome re-sequencing (827 Watkins landraces and 208 modern cultivars) and in-depth field evaluation spanning a decade. We discovered that modern cultivars are derived from just two of the seven ancestral groups of wheat, leaving five groups as previously untapped sources for breeding. This provides access to landrace-specific functional variations using structured germplasm, genotyping and informatics resources. Employing complementary genetic populations and approaches, we identified thousands of high-resolution quantitative trait loci (QTL) and significant marker–trait associations for major traits, revealing many Watkins-unique loci that can confer superior traits in modern wheat. Furthermore, we identified and functionally verified causative genes for climate-change adaptation, nutritional enhancement and resistance to wheat blast. Finally, we assessed the phenotypic effects of 44,338 Watkins-unique haplotypes, introgressed from 143 prioritised QTL in the context of modern cultivars, bridging the gap between landrace diversity and current breeding. This study establishes a framework for systematically utilising genetic diversity in crop improvement to achieve sustainable food security.

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A wheat kinase and immune receptor form host-specificity barriers against the blast fungus

Cited by 30 publications

References 34 publications

Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley

Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley

Adaptive evolution in virulence effectors of the rice blast fungusPyricularia oryzae

Harnessing Landrace Diversity Empowers Wheat Breeding for Climate Resilience

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