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Title: Changing the game: using integrative genomics to probe virulence mechanisms of the stem rust pathogen Puccinia graminis f. sp. tritici

Author
item FIGUEROA, MELANIA - University Of Minnesota
item UPADHYAYA, NARAYANA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item SPERSCHNEIDER, JANA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item PARK, ROBERT - University Of Sydney
item Szabo, Les
item STEFFENSON, BRIAN - University Of Minnesota
item ELLIS, JEFFERY - Commonwealth Scientific And Industrial Research Organisation (CSIRO)
item DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: Frontiers in Plant Science
Publication Type: Review Article
Publication Acceptance Date: 2/6/2016
Publication Date: 2/24/2016
Citation: Figueroa, M., Upadhyaya, N.M., Sperschneider, J., Park, R., Szabo, L.J., Steffenson, B.J., Ellis, J., Dodds, P. 2016. Changing the game: using integrative genomics to probe virulence mechanisms of the stem rust pathogen Puccinia graminis f. sp. tritici. Frontiers in Plant Science. 7(205):1-10.

Interpretive Summary: The recent resurgence of wheat stem rust caused by new virulent races of Puccinia graminis f. sp. tritici poses a threat to food security. These concerns have catalyzed an extensive global effort towards controlling this disease. Substantial research and breeding programs target the identification and introduction of new stem rust resistance genes in cultivars for genetic protection against the disease. Such resistance genes typically encode receptor proteins that recognize specific components of the pathogen, known as avirulence proteins. A significant drawback to deploying cultivars with single resistnace genes is that they are often overcome by evolution of the pathogen. Thus, a key element in achieving durable rust control is the deployment of multiple effective resistance genes in combination, either through conventional breeding or transgenic approaches, to minimize the risk of resistance breakdown. In this situation, evolution of the pathogen would require simultaneous changes in avirulence genes in order to overcome host resistance. However, choosing the optimal resistance gene combinations to deploy is a challenge that requires detailed knowledge of the pathogen population existing in nature and the detailed information of the variation within the different avirulence genes. Identifying specific avirulence genes inovoled in this system from Puccinia graminis f. sp. tritici will provide screening tools to enhance pathogen monitoring, and confirm individual resistance gene functions in crop varieties carrying multiple effective resistance genes. Towards this goal, much progress has been made in assembling a high quality reference genome sequence for Puccinia graminis f. sp. tritici, as well as a Pan-genome encompassing variation between multiple field isolates. In turn this has allowed prediction of candiate avirulence genes involved in this interaction. Here, we review progress in stem rust fungus pathogenomics and approaches currently underway to identify the pathogrecognized by wheat.

Technical Abstract: The recent resurgence of wheat stem rust caused by new virulent races of Puccinia graminis f. sp. tritici (Pgt) poses a threat to food security. These concerns have catalyzed an extensive global effort towards controlling this disease. Substantial research and breeding programs target the identification and introduction of new stem rust resistance (Sr) genes in cultivars for genetic protection against the disease. Such resistance genes typically encode immune receptor proteins that recognize specific components of the pathogen, known as avirulence (Avr) proteins. A significant drawback to deploying cultivars with single Sr genes is that they are often overcome by evolution of the pathogen to escape recognition through alterations in Avr genes. Thus, a key element in achieving durable rust control is the deployment of multiple effective Sr genes in combination, either through conventional breeding or transgenic approaches, to minimize the risk of resistance breakdown. In this situation, evolution of pathogen virulence would require simultaneous changes in multiple Avr genes in order to bypass recognition. However, choosing the optimal Sr gene combinations to deploy is a challenge that requires detailed knowledge of the pathogen Avr genes with which they interact and the virulence phenotypes of Pgt existing in nature. Identifying specific Avr genes from Pgt will provide screening tools to enhance pathogen virulence monitoring, assess heterozygosity and propensity for mutation in pathogen populations, and confirm individual Sr gene functions in crop varieties carrying multiple effective resistance genes. Towards this goal, much progress has been made in assembling a high quality reference genome sequence for Pgt, as well as a Pan-genome encompassing variation between multiple field isolates with diverse virulence spectra. In turn this has allowed prediction of Pgt effector gene candidates based on known features of Avr genes in other plant pathogens, including the related flax rust fungus. Up regulation of gene expression in haustoria and evidence for diversifying selection are two useful parameters to identify candidate Avr genes. Recently, we have also applied machine learning approaches to agnostically predict candidate effectors. Here, we review progress in stem rust pathogenomics and approaches currently underway to identify Avr genes recognized by wheat.