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

ABSTRACT: 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.

SUBMITTER: Sugihara Y

PROVIDER: S-EPMC9851567 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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

Sugihara Yu Y Abe Yoshiko Y Takagi Hiroki H Abe Akira A Shimizu Motoki M Ito Kazue K Kanzaki Eiko E Oikawa Kaori K Kourelis Jiorgos J Langner Thorsten T Win Joe J Białas Aleksandra A Lüdke Daniel D Contreras Mauricio P MP Chuma Izumi I Saitoh Hiromasa H Kobayashi Michie M Zheng Shuan S Tosa Yukio Y Banfield Mark J MJ Kamoun Sophien S Terauchi Ryohei R Fujisaki Koki K

PLoS biology 20230119 1

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, enc ...[more]

PMID: 36656825

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Project description:A filamentous fungus, Magnaporthe oryzae, is a causal agent of rice blast disease, which is one of the most serious diseases affecting cultivated rice, Oryza sativa. However, the molecular mechanisms underlying both rice defense and fungal attack are not yet fully understood. Extensive past studies have characterized many infection-responsive genes in the pathogen and host plant, separately. To understand the plant-pathogen interaction comprehensively, it is valuable to monitor the gene expression profiles of both interacting organisms simultaneously in the same infected plant tissue. Although the host-pathogen interaction during the initial infection stage is important for the establishment of infection, the detection of fungal gene expression in infected leaves at the stage has been difficult because very few numbers of fungal cells are present. Using the emerging RNA-Seq technique, which has a wide dynamic range for expression analyses, we analyzed the mixed transcriptome of rice and blast fungus in infected leaves at 24 hours post-inoculation, which is the point when the primary infection hyphae penetrate leaf epidermal cells. We demonstrated that our method detected the gene expression of both the host plant and pathogen simultaneously in the same infected leaf blades in natural infection conditions without any artificial treatments. The upregulation of 240 fungal transcripts encoding putative secreted proteins was observed, suggesting that these candidates of fungal effector genes may play important roles in initial infection processes. The upregulation of transcripts encoding glycosyl hydrolases, cutinases and LysM domain-containing proteins were observed in the blast fungus, whereas pathogenesis-related and phytoalexin biosynthetic genes were upregulated in rice. Furthermore, more drastic changes in expression were observed in the incompatible interactions compared with the compatible ones in both rice and blast fungus at this stage. Our mixed transcriptome analysis is useful for the simultaneous elucidation of the tactics of host plant defense and pathogen attack.

Project description:BackgroundUnderstanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae-the causal agent of blast disease of cereals- is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat, and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined the two largest genomic datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries.ResultsThe global population of the rice blast fungus consists mainly of three well-defined genetic groups and a diverse set of individuals. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in Southeast Asia followed by three independent clonal expansions that took place over the last ~ 200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence and absence of candidate effector genes. These genes encode secreted proteins that modulate plant defense and allow pathogen colonization. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of presence and absence of effector genes define each of the pandemic clonal lineages.ConclusionsOur analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence and absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

Project description:BackgroundNitrogen fertilization is known to increase disease susceptibility, a phenomenon called Nitrogen-Induced Susceptibility (NIS). In rice, this phenomenon has been observed in infections with the blast fungus Magnaporthe oryzae. A previous classical genetic study revealed a locus (NIS1) that enhances susceptibility to rice blast under high nitrogen fertilization. In order to further address the underlying genetics of plasticity in susceptibility to rice blast after fertilization, we analyzed NIS under greenhouse-controlled conditions in a panel of 139 temperate japonica rice strains. A genome-wide association analysis was conducted to identify loci potentially involved in NIS by comparing susceptibility loci identified under high and low nitrogen conditions, an approach allowing for the identification of loci validated across different nitrogen environments. We also used a novel NIS Index to identify loci potentially contributing to plasticity in susceptibility under different nitrogen fertilization regimes.ResultsA global NIS effect was observed in the population, with the density of lesions increasing by 8%, on average, under high nitrogen fertilization. Three new QTL, other than NIS1, were identified. A rare allele of the RRobN1 locus on chromosome 6 provides robust resistance in high and low nitrogen environments. A frequent allele of the NIS2 locus, on chromosome 5, exacerbates blast susceptibility under the high nitrogen condition. Finally, an allele of NIS3, on chromosome 10, buffers the increase of susceptibility arising from nitrogen fertilization but increases global levels of susceptibility. This allele is almost fixed in temperate japonicas, as a probable consequence of genetic hitchhiking with a locus involved in cold stress adaptation.ConclusionsOur results extend to an entire rice subspecies the initial finding that nitrogen increases rice blast susceptibility. We demonstrate the usefulness of estimating plasticity for the identification of novel loci involved in the response of rice to the blast fungus under different nitrogen regimes.

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

Publications

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

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