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      Multiple Translocation of the AVR-Pita Effector Gene among Chromosomes of the Rice Blast Fungus Magnaporthe oryzae and Related Species

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          Abstract

          Magnaporthe oryzae is the causal agent of rice blast disease, a devastating problem worldwide. This fungus has caused breakdown of resistance conferred by newly developed commercial cultivars. To address how the rice blast fungus adapts itself to new resistance genes so quickly, we examined chromosomal locations of AVR-Pita, a subtelomeric gene family corresponding to the Pita resistance gene, in various isolates of M. oryzae (including wheat and millet pathogens) and its related species. We found that AVR-Pita ( AVR-Pita1 and AVR-Pita2) is highly variable in its genome location, occurring in chromosomes 1, 3, 4, 5, 6, 7, and supernumerary chromosomes, particularly in rice-infecting isolates. When expressed in M. oryzae, most of the AVR-Pita homologs could elicit Pita-mediated resistance, even those from non-rice isolates. AVR-Pita was flanked by a retrotransposon, which presumably contributed to its multiple translocation across the genome. On the other hand, family member AVR-Pita3, which lacks avirulence activity, was stably located on chromosome 7 in a vast majority of isolates. These results suggest that the diversification in genome location of AVR-Pita in the rice isolates is a consequence of recognition by Pita in rice. We propose a model that the multiple translocation of AVR-Pita may be associated with its frequent loss and recovery mediated by its transfer among individuals in asexual populations. This model implies that the high mobility of AVR-Pita is a key mechanism accounting for the rapid adaptation toward Pita. Dynamic adaptation of some fungal plant pathogens may be achieved by deletion and recovery of avirulence genes using a population as a unit of adaptation.

          Author Summary

          Rice blast disease, caused by Magnaporthe oryzae, is a serious threat to global rice production. Dozens of resistance genes are available for disease control, but the fungus rapidly evolves to overcome a resistance gene within 2 or 3 years in the field. Resistance requires recognition of corresponding pathogen “avirulence effectors”, proteins or small molecules secreted by the fungus in the host plant. Resistance gene breakdown involves mutation of the avirulence effector so that it is no longer recognized by the resistance gene product. We describe evolutionary processes associated with the subtelomeric avirulence effector AVR-Pita corresponding to rice resistance gene Pita. Comparing individuals in the asexual fungal population infecting rice, AVR-Pita has frequently been translocated to different chromosomes, including unstable supernumerary chromosomes. AVR-Pita occurs at different chromosomal localizations in populations from weeds and millet crops lacking Pita, but this location is stable in individuals of each population. Family member AVR-Pita3, which lacks a corresponding rice resistance gene, shows extremely stable localization on a single chromosome throughout all host-adapted populations of the pathogen. Translocation of AVR-Pita might be associated with the frequent transfer of this gene between individuals in the asexual pathogen population responding to selection by sporadic deployment of Pita.

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          The genome of the African trypanosome Trypanosoma brucei.

          African trypanosomes cause human sleeping sickness and livestock trypanosomiasis in sub-Saharan Africa. We present the sequence and analysis of the 11 megabase-sized chromosomes of Trypanosoma brucei. The 26-megabase genome contains 9068 predicted genes, including approximately 900 pseudogenes and approximately 1700 T. brucei-specific genes. Large subtelomeric arrays contain an archive of 806 variant surface glycoprotein (VSG) genes used by the parasite to evade the mammalian immune system. Most VSG genes are pseudogenes, which may be used to generate expressed mosaic genes by ectopic recombination. Comparisons of the cytoskeleton and endocytic trafficking systems with those of humans and other eukaryotic organisms reveal major differences. A comparison of metabolic pathways encoded by the genomes of T. brucei, T. cruzi, and Leishmania major reveals the least overall metabolic capability in T. brucei and the greatest in L. major. Horizontal transfer of genes of bacterial origin has contributed to some of the metabolic differences in these parasites, and a number of novel potential drug targets have been identified.
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            Pathogen population genetics, evolutionary potential, and durable resistance.

            We hypothesize that the evolutionary potential of a pathogen population is reflected in its population genetic structure. Pathogen populations with a high evolutionary potential are more likely to overcome genetic resistance than pathogen populations with a low evolutionary potential. We propose a flexible framework to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. According to this framework, pathogens that pose the greatest risk of breaking down resistance genes have a mixed reproduction system, a high potential for genotype flow, large effective population sizes, and high mutation rates. The lowest risk pathogens are those with strict asexual reproduction, low potential for gene flow, small effective population sizes, and low mutation rates. We present examples of high-risk and low-risk pathogens. We propose general guidelines for a rational approach to breed durable resistance according to the evolutionary potential of the pathogen.
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              Direct interaction of resistance gene and avirulence gene products confers rice blast resistance.

              Rice expressing the Pi-ta gene is resistant to strains of the rice blast fungus, Magnaporthe grisea, expressing AVR-Pita in a gene-for-gene relationship. Pi-ta encodes a putative cytoplasmic receptor with a centrally localized nucleotide-binding site and leucine-rich domain (LRD) at the C-terminus. AVR-Pita is predicted to encode a metalloprotease with an N-terminal secretory signal and pro-protein sequences. AVR-Pita(176) lacks the secretory and pro-protein sequences. We report here that transient expression of AVR-Pita(176) inside plant cells results in a Pi-ta-dependent resistance response. AVR-Pita(176) protein is shown to bind specifically to the LRD of the Pi-ta protein, both in the yeast two-hybrid system and in an in vitro binding assay. Single amino acid substitutions in the Pi-ta LRD or in the AVR-Pita(176) protease motif that result in loss of resistance in the plant also disrupt the physical interaction, both in yeast and in vitro. These data suggest that the AVR-Pita(176) protein binds directly to the Pi-ta LRD region inside the plant cell to initiate a Pi-ta-mediated defense response.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                July 2011
                July 2011
                28 July 2011
                : 7
                : 7
                : e1002147
                Affiliations
                [1 ]Graduate School of Agricultural Sciences, Kobe University, Kobe, Japan
                [2 ]Faculty of Agriculture, Saga University, Saga, Japan
                [3 ]Iwate Biotechnology Research Center, Kitakami, Japan
                [4 ]National Agricultural Research Center, Tsukuba, Japan
                [5 ]Department of Plant Pathology, Kansas State University, Manhattan, Kansas, United States of America
                Virginia Polytechnic Institute and State University, United States of America
                Author notes

                Conceived and designed the experiments: IC YT. Performed the experiments: IC CI YH KI NF. Analyzed the data: IC MK KY RT HN BV YT. Contributed reagents/materials/analysis tools: YF. Wrote the paper: IC BV YT.

                Article
                PPATHOGENS-D-11-00094
                10.1371/journal.ppat.1002147
                3145791
                21829350
                6ba25e44-5da7-4d6d-a5e2-1ac758867423
                Chuma et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 12 January 2011
                : 17 May 2011
                Page count
                Pages: 20
                Categories
                Research Article
                Agriculture
                Crops
                Cereals
                Crop Diseases
                Biology
                Evolutionary Biology
                Genetics
                Molecular Genetics
                Microbiology
                Mycology
                Fungi
                Host-Pathogen Interaction
                Microbial Pathogens
                Plant Microbiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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