Biology subjects

Terauchi, R.

Publications and source records attributed to Terauchi, R..

6 recordsLinked to original sources

bioRxiv2017

An unconventional NOI/RIN4 domain of a rice NLR protein binds host EXO70 protein to confer fungal immunity

As much as 10% of plant immune receptors from the nucleotide-binding domain leucine-rich repeat (NLR) family carry integrated domains (IDs) that can directly bind pathogen effectors. However, it remains unclear whether direct binding to effectors is a universal feature of ID-containing NLRs given that only a few NLR-IDs have been functionally characterized. Here we show that the rice (Oryza sativa) sensor NLR-ID Pii2 confers resistance to strains of the rice blast fungus Magnaporthe oryzae that carry the effector AVR-Pii without directly binding this protein. First, we show that AVR-Pii binds the exocyst subunit OsExo70F2 in rice (Oryza sativa) to dissociate preformed complexes of OsExo70F2 with host RPM1 INTERACTING PROTEIN4 (RIN4) at the conserved NOI motif, facilitating a possible virulence function. Second, we show that in its resting state, Pii2 binds OsExo70F2 and OsExo70F3, essential components of Pii-mediated resistance, through its integrated NOI domain. Remarkably, AVR-Pii binding to OsExo70F2/F3 leads to dissociation of the Pii2-OsExo70F2 and Pii2-OsExo70F3 complexes, destabilization of Pii2, and activation of immunity. These findings support a novel conceptual model in which an NLR-ID monitors alterations of tethered host proteins targeted by pathogen effectors, providing insight into pathogen recognition mechanisms. Significance statementPlant diseases diminish crop yields by over 20% each year, and deploying resistant crops is the most effective way to combat them. Nucleotide-binding domain leucine-rich repeat (NLR)-type receptors are the major player in plant resistance against pathogens, with a subset of NLRs containing unconventional domains called integrated domains (ID) derived from host proteins. Previous studies suggest that pathogen avirulence (AVR) effectors directly bind or modify NLR-IDs before they are recognized by the host. Here, we reveal that the rice NLR-ID receptor Pii2 indirectly recognizes AVR-Pii when the effector dissociates Pii2 from the host Exo70 proteins tethered to Pii2. We propose a new model of how NLRs can recognize pathogens, expanding our understanding of plant immunity.

plant biology↗

bioRxiv2017

Rice blast resistance gene Pii is controlled by a pair of NBS-LRR genes Pii-1 and Pii-2

Nucleotide-binding, leucine-rich repeat receptors (NLRs) are conserved cytosolic receptors that recognize pathogen effectors and trigger immunity in plants. Recent studies indicate that NLRs function in pairs. Rice resistance gene Pii has been known to confer resistance against rice blast pathogen Magnaporthe oryzae carrying AVR-Pii. Previously we reported isolation of Pii gene from the rice cultivar Hitomebore (Takagi et al. 2013). To further understand rice components required for Pii-mediated resistance, we screened 5,600 mutant lines of Hitomebore cultivar and identified two mutants that lost Pii resistance without any changes in Pii gene sequence. Application of MutMap-Gap, the whole genome sequencing-based method of mutation identification, to the two mutants revealed that they have mutations in another NLR gene located close to Pii. The F1 plants derived from a cross of the two mutants showed pii phenotype, demonstrating that the newly identified NLR gene is indeed a component of Pii resistance. We thus designate the previously isolated Pii gene as Pii-1 and the newly isolated NLR gene as Pii-2.

genetics↗

bioRxiv2017

Coexistence of multiple endemic and pandemic lineages of the rice blast pathogen

The rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae) is both a threat to global food security and a model for plant pathology. Molecular pathologists need an accurate understanding of the origins and line of descent of M. oryzae populations, to identify the genetic and functional bases of pathogen adaptation, and to guide the development of more effective control strategies. We used a whole-genome sequence analysis of samples from different times and places to infer details about the genetic makeup of M. oryzae from a global collection of isolates. Analyses of population structure identified six lineages within M. oryzae, including two pandemic on japonica and indica rice, respectively, and four lineages with more restricted distributions. Tip-dating calibration indicated that M. oryzae lineages separated about a millenium ago, long after the initial domestication of rice. The major lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and evidence of DNA acquisition from multiple lineages. Tests for weak natural selection revealed that the pandemic spread of clonal lineages entailed an evolutionary cost, in terms of the accumulation of deleterious mutations. Our findings reveal the coexistence of multiple endemic and pandemic lineages with contrasting population and genetic characteristics within a widely distributed pathogen.\n\nImportanceThe rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae) is a textbook example of a rapidly adapting pathogen, and is responsible for one of the most damaging diseases of rice. Improvements in our understanding of Magnaporthe oryzae diversity and evolution are required, to guide the development of more effective control strategies. We used genome sequencing data for samples from around the world to infer the evolutionary history of M. oryzae. We found that M. oryzae diversified about a thousand years ago ago, separating into six main lineages: two pandemic on japonica and indica rice, respectively, and four with more restricted distributions. We also found that a lineage endemic to continental Southeast Asia displayed signatures of sexual recombination and the acquisition of genetic material from multiple lineages. This work provides a population-level genomic framework for defining molecular markers for the control of rice blast and investigations of the molecular basis of differences in pathogenicity between M. oryzae lineages.

evolutionary biology↗

bioRxiv2017

Lessons in effector and NLR biology of plant-microbe systems

A diversity of plant-associated organisms secrete effectors--proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plant-microbe systems.

plant biology↗

bioRxiv2017

Gene flow between divergent cereal- and grass-specific lineages of the rice blast fungus Magnaporthe oryzae

Delineating species and epidemic lineages in fungal plant pathogens is critical to our understanding of disease emergence and the structure of fungal biodiversity, and also informs international regulatory decisions. Pyricularia oryzae (syn. Magnaporthe oryzae) is a multi-host pathogen that infects multiple grasses and cereals, is responsible for the most damaging rice disease (rice blast), and of growing concern due to the recent introduction of wheat blast to Bangladesh from South America. However, the genetic structure and evolutionary history of M. oryzae, including the possible existence of cryptic phylogenetic species, remain poorly defined. Here, we use whole-genome sequence information for 76 M. oryzae isolates sampled from 12 grass and cereal genera to infer the population structure of M. oryzae, and to reassess the species status of wheat-infecting populations of the fungus. Species recognition based on genealogical concordance, using published data or extracting previously-used loci from genome assemblies, failed to confirm a prior assignment of wheat blast isolates to a new species (Pyricularia graminis tritici). Inference of population subdivisions revealed multiple divergent lineages within M. oryzae, each preferentially associated with one host genus, suggesting incipient speciation following host shift or host range expansion. Analyses of gene flow, taking into account the possibility of incomplete lineage sorting, revealed that genetic exchanges have contributed to the makeup of multiple lineages within M. oryzae. These findings provide greater understanding of the eco-evolutionary factors that underlie the diversification of M. oryzae and highlight the practicality of genomic data for epidemiological surveillance in this important multi-host pathogen.\n\nImportanceInfection of novel hosts is a major route for disease emergence by pathogenic micro-organisms. Understanding the evolutionary history of multi-host pathogens is therefore important to better predict the likely spread and emergence of new diseases. Magnaporthe oryzae is a multi-host fungus that causes serious cereal diseases, including the devastating rice blast disease, and wheat blast, a cause of growing concern due to its recent spread from South America to Asia. Using whole genome analysis of 76 fungal strains from different hosts, we have documented the divergence of M. oryzae into numerous lineages, each infecting a limited number of host species. Our analyses provide evidence that inter-lineage gene flow has contributed to the genetic makeup of multiple M. oryzae lineages within the same species. Plant health surveillance is therefore warranted to safeguard against disease emergence in regions where multiple lineages of the fungus are in contact with one another.

microbiology↗

bioRxiv2016

NLR signaling network mediates immunity to diverse plant pathogens

Plant and animal nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins often function in pairs to mediate innate immunity to pathogens. However, the degree to which NLR proteins form signaling networks beyond genetically linked pairs is poorly understood. In this study, we discovered that a large NLR immune signaling network with a complex genetic architecture confers immunity to oomycetes, bacteria, viruses, nematodes, and insects. The network emerged over 100 million years ago from a linked NLR pair that diversified into up to one half of the NLR of asterid plants. We propose that this NLR network increases robustness of immune signaling to counteract rapidly evolving plant pathogens.

plant biology↗