Barley MLA3 recognizes the host-specificity determinant PWL2 from rice blast (<i>M. oryzae</i>)

Brabham, Helen J.; Cruz, Diana Gómez de la; Were, Vincent M.; Shimizu, Mitsuru; Saitoh, Hiromasa; Hernández-Pinzón, Inmaculada; Green, Phon; Lorang, J. M.; Fujisaki, Koki; Sato, Kazuhiro; Molnár, István; Šimková, Hana; Doležel, Jaroslav; Russell, J.; Taylor, Jodie; Smoker, Matthew; Gupta, Yogesh K.; Wolpert, T J; Talbot, Nicholas J.; Terauchi, Ryohei; Moscou, Matthew J.

doi:10.1101/2022.10.21.512921

Cited by 14 publications

(19 citation statements)

References 162 publications

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“…Two other orthologous P. oryzae effectors, PWL1 and PWL2 , exclude Eleusine and rice-associated isolates from infecting Eragrostis curvula , and can, therefore, also be considered as host-specificity determinants [28, 60]. Interestingly, ALPHAFOLD predicts PWL2 to adopt a MAX effector fold [61]. In our study, however, gene knock-in experiments with MAX79 , MAX83 , and MAX89 - specifically absent from the Oryza -infecting lineage - did not reveal a strong effect on virulence towards a large panel of rice varieties.…”

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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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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“…Despite the primary sequence dissimilarity between AVR-Mgk1 and AVR-Pik, AlphaFold2 [108] predicted that AVR-Mgk1 adopts a MAX fold structure (Fig 6C) similar to AVR-Pik and several other M. oryzae effectors [27][28][29][30]35,124]. However, the region that includes the highly polymorphic residues of AVR-Pik effectors, which determine their binding to the HMA domain of Pik-1 and are modulated by arms race coevolution [70,71,96], differs structurally in AVR-Mgk1 (Fig 6C -6E).…”

Section: Avr-mgk1 Is Predicted To Adopt a Max Fold Structurementioning

confidence: 99%

Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector

et al. 2023

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Studies focused solely on single organisms can fail to identify the networks underlying host–pathogen gene-for-gene interactions. Here, we integrate genetic analyses of rice (Oryza sativa, host) and rice blast fungus (Magnaporthe oryzae, pathogen) and uncover a new pathogen recognition specificity of the rice nucleotide-binding domain and leucine-rich repeat protein (NLR) immune receptor Pik, which mediates resistance to M. oryzae expressing the avirulence effector gene AVR-Pik. Rice Piks-1, encoded by an allele of Pik-1, recognizes a previously unidentified effector encoded by the M. oryzae avirulence gene AVR-Mgk1, which is found on a mini-chromosome. AVR-Mgk1 has no sequence similarity to known AVR-Pik effectors and is prone to deletion from the mini-chromosome mediated by repeated Inago2 retrotransposon sequences. AVR-Mgk1 is detected by Piks-1 and by other Pik-1 alleles known to recognize AVR-Pik effectors; recognition is mediated by AVR-Mgk1 binding to the integrated heavy metal-associated (HMA) domain of Piks-1 and other Pik-1 alleles. Our findings highlight how complex gene-for-gene interaction networks can be disentangled by applying forward genetics approaches simultaneously to the host and pathogen. We demonstrate dynamic coevolution between an NLR integrated domain and multiple families of effector proteins.

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“…hordei. In addition, each gene confers resistance against a barley non-adapted pathogen: Mla3 confers resistance to the rice blast pathogen Magnaporthe oryzae by specifically recognizing the Pwl2 effector protein 58 , and Mla7 and Mla8 confer resistance against the wheat stripe rust pathogen Pst 59,60 .…”

Section: Lr/yr548 Confers Quantitative Resistance In Seedlings and Ad...mentioning

confidence: 99%

A single NLR gene confers resistance to leaf and stripe rust in wheat

Sharon,

Sharma,

Avni

et al. 2023

Preprint

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Nucleotide-binding site leucine-rich repeat (NLR) disease-resistance genes typically confer resistance against races of a single pathogen. We report that Lr/Yr548, an NLR gene from Aegilops sharonensis and Aegilops longissima, confers specific resistance against Puccinia triticina (Pt) and P. striiformis tritici (Pst) that cause leaf and stripe rust, respectively. Lr/Yr548 prevented disease development in wheat introgression as well as transgenic wheat lines. Comparative analysis of Lr/Yr548 and all cloned Triticeae NLR disease-resistance genes showed that Lr/Yr548 contains a distinctive coiled-coil domain and that it is unique to Ae. sharonensis and Ae. longissima. A phylogenetic analysis indicated multiple events of gene flow of Lr/Yr548 between the two species, and suggested loss of resistance in susceptible isolates. The confinement of Lr/Yr548 to Ae. longissima and Ae. sharonensis and the cross resistance that it confers against Pt and Pst in wheat highlight the potential of these species as sources of novel disease-resistance genes for wheat improvement.

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Barley MLA3 recognizes the host-specificity determinant PWL2 from rice blast (M. oryzae)

Cited by 14 publications

References 162 publications

Adaptive evolution in virulence effectors of the rice blast fungusPyricularia oryzae

Adaptive evolution in virulence effectors of the rice blast fungusPyricularia oryzae

Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector

A single NLR gene confers resistance to leaf and stripe rust in wheat

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