title: Multiple Avirulence Loci and Allele-Specific Effector Recognition Control the Pm3 Race-Specific Resistance of Wheat to Powdery Mildew.
abstract: In cereals, several mildew resistance genes occur as large allelic series; for example, in wheat (Triticum aestivum and Triticum turgidum), 17 functional Pm3 alleles confer agronomically important race-specific resistance to powdery mildew (Blumeria graminis). The molecular basis of race specificity has been characterized in wheat, but little is known about the corresponding avirulence genes in powdery mildew. Here, we dissected the genetics of avirulence for six Pm3 alleles and found that three major Avr loci affect avirulence, with a common locus_1 involved in all AvrPm3-Pm3 interactions. We cloned the effector gene AvrPm3(a2/f2) from locus_2, which is recognized by the Pm3a and Pm3f alleles. Induction of a Pm3 allele-dependent hypersensitive response in transient assays in Nicotiana benthamiana and in wheat demonstrated specificity. Gene expression analysis of Bcg1 (encoded by locus_1) and AvrPm3 (a2/f2) revealed significant differences between isolates, indicating that in addition to protein polymorphisms, expression levels play a role in avirulence. We propose a model for race specificity involving three components: an allele-specific avirulence effector, a resistance gene allele, and a pathogen-encoded suppressor of avirulence. Thus, whereas a genetically simple allelic series controls specificity in the plant host, recognition on the pathogen side is more complex, allowing flexible evolutionary responses and adaptation to resistance genes.
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Salim
authors.identifier: http://orcid.org/0000-0003-0855-5433
authors.initials: S
authors.lastname: Bourras
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Kaitlin Elyse
authors.identifier: http://orcid.org/0000-0002-9107-2661
authors.initials: KE
authors.lastname: McNally
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Roi
authors.identifier: http://orcid.org/0000-0003-2576-2063
authors.initials: R
authors.lastname: Ben-David
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Francis
authors.identifier: http://orcid.org/0000-0003-1455-3979
authors.initials: F
authors.lastname: Parlange
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Stefan
authors.initials: S
authors.lastname: Roffler
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Coraline Rosalie
authors.identifier: http://orcid.org/0000-0002-9133-4406
authors.initials: CR
authors.lastname: Praz
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Simone
authors.identifier: http://orcid.org/0000-0002-2116-1685
authors.initials: S
authors.lastname: Oberhaensli
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Fabrizio
authors.identifier: http://orcid.org/0000-0002-7885-4482
authors.initials: F
authors.lastname: Menardo
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Daniel
authors.initials: D
authors.lastname: Stirnweis
authors.affiliation: Institute of Evolution, University of Haifa, Mount Carmel, 31905 Haifa, Israel.
authors.forename: Zeev
authors.identifier: http://orcid.org/0000-0003-0211-6966
authors.initials: Z
authors.lastname: Frenkel
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Luisa Katharina
authors.identifier: http://orcid.org/0000-0003-1195-4996
authors.initials: LK
authors.lastname: Schaefer
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Simon
authors.identifier: http://orcid.org/0000-0002-7165-6811
authors.initials: S
authors.lastname: Flückiger
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Georges
authors.initials: G
authors.lastname: Treier
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Gerhard
authors.initials: G
authors.lastname: Herren
authors.affiliation: Institute of Evolution, University of Haifa, Mount Carmel, 31905 Haifa, Israel.
authors.forename: Abraham B
authors.initials: AB
authors.lastname: Korol
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland.
authors.forename: Thomas
authors.initials: T
authors.lastname: Wicker
authors.affiliation: Institute of Plant Biology, University of Zurich, CH-8008 Zürich, Switzerland bkeller@botinst.uzh.ch.
authors.forename: Beat
authors.identifier: http://orcid.org/0000-0003-2379-9225
authors.initials: B
authors.lastname: Keller
mesh_terms: D000483:Alleles; D000595:Amino Acid Sequence; D001203:Ascomycota / Q000472:pathogenicity*; D003433:Crosses, Genetic; D060467:Disease Resistance / Q000235:genetics*; D019143:Evolution, Molecular; D015870:Gene Expression; D008957:Models, Genetic; D058977:Molecular Sequence Annotation; D010935:Plant Diseases / Q000276:immunology* / Q000382:microbiology; D018515:Plant Leaves / Q000235:genetics / Q000276:immunology / Q000382:microbiology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D011110:Polymorphism, Genetic; D016415:Sequence Alignment; D017422:Sequence Analysis, DNA; D013045:Species Specificity; D014026:Nicotiana / Q000235:genetics / Q000276:immunology / Q000382:microbiology; D014908:Triticum / Q000235:genetics* / Q000276:immunology / Q000382:microbiology; D014774:Virulence
chemical_list: D010940:Plant Proteins