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Title: Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen

Author
item LU, XUNLI - Max Planck Society
item KRACHER, BARBARA - Max Planck Society
item SAUR, ISABEL - Max Planck Society
item BAUER, SASKIA - Max Planck Society
item ELLWOOD, SIMON - Curtin University
item Wise, Roger
item YAENO, TAKASHI - Ehime University
item MAEKAWA, TAKAKI - Max Planck Society
item SCHULZE-LEFERT, PAUL - Max Planck Society

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/13/2016
Publication Date: 10/4/2016
Citation: Lu, X., Kracher, B., Saur, I., Bauer, S., Ellwood, S.R., Wise, R.P., Yaeno, T., Maekawa, T., Schulze-Lefert, P. 2016. Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proceedings of the National Academy of Sciences. 113(42):e6486-6495. doi:10.1073/pnas.1612947113.

Interpretive Summary: Encounters between flowering plants and pathogenic microbes often trigger host immune responses resulting in disease resistance. These responses are the result of the interaction between host resistance proteins and pathogen effector proteins, and how they interact often determines whether a plant succumbs to disease. Resistance proteins are often encoded by large gene families and can evolve through gene duplications, recombination, and unequal crossing-over. Interestingly, there are only a few examples known in plants where multiple alternative forms of an R protein are encoded by the same genome position. Such situations are particularly interesting to explore mechanisms underlying the co-evolution of host and pathogen, i.e. whether the corresponding pathogen effectors evolved by sequence variation in a single effector gene or by evolution of phylogenetically unrelated effectors. Powdery mildew fungi infect greater than 10,000 plant species, including many crops, and their growth and reproduction is entirely dependent on living host cells. Here we report the application of a genome-wide association study among 17 isolates of the barley powdery mildew pathogen collected from Europe, Asia, North America, and Australia to identify and molecularly isolate two unique powdery mildew effectors. These two effector genes are phylogenetically unrelated, implying that they evolved independently in the pathogen. Knowledge from this research will impact how plant breeders select for disease resistance, one of the most important traits that affect crop yield, and thus food security.

Technical Abstract: Disease resistance (R) genes encoding intracellular nucleotide-binding domain and leucine-rich repeat proteins (NLRs) are key components of the plant innate immune system and typically detect the presence of isolate-specific avirulence (AVR) effectors from pathogens. NLRs define the fastest evolving gene family of flowering plants and are often arranged in gene clusters containing multiple paralogs, contributing to extensive copy number and allele-specific NLR variation within a host species. Barley mildew resistance gene locus A (Mla) represents one of only few R genes that have been subject to extreme functional diversification, resulting in allelic resistance specificities each recognizing a cognate but largely unidentified AVRa gene of the powdery mildew fungus, Blumeria graminis f sp hordei (Bgh). We applied a transcriptome-wide association study among 17 Bgh isolates containing different AVRa genes and identified AVRa1 and AVRa13, encoding candidate secreted effectors recognized by Mla1 and Mla13 alleles, respectively. Transient expression of the effector genes in barley leaves or protoplasts was sufficient to trigger an Mla1 or Mla13 allele-specific cell death response, a hallmark of NLR receptor-mediated immunity. AVRa1 and AVRa13 are phylogenetically unrelated, demonstrating that allelic MLA receptors evolved to recognize sequence-unrelated effectors. AVRA1 recognition by barley MLA1 is retained in transgenic Arabidopsis, indicating that AVRA1 directly binds MLA1 or that its recognition involves an evolutionarily conserved host target of AVRA1. Furthermore, analysis of transcriptome-wide sequence variation among the Bgh isolates provides evidence for Bgh population structure that is partly linked to geographic isolation.