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Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat

Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable—a phenomenon that remains poorly understood, as the co...

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Autores principales: Müller, Marion C., Kunz, Lukas, Schudel, Seraina, Lawson, Aaron W., Kammerecker, Sandrine, Isaksson, Jonatan, Wyler, Michele, Graf, Johannes, Sotiropoulos, Alexandros G., Praz, Coraline R., Manser, Beatrice, Wicker, Thomas, Bourras, Salim, Keller, Beat
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335242/
https://www.ncbi.nlm.nih.gov/pubmed/35857869
http://dx.doi.org/10.1073/pnas.2108808119
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author Müller, Marion C.
Kunz, Lukas
Schudel, Seraina
Lawson, Aaron W.
Kammerecker, Sandrine
Isaksson, Jonatan
Wyler, Michele
Graf, Johannes
Sotiropoulos, Alexandros G.
Praz, Coraline R.
Manser, Beatrice
Wicker, Thomas
Bourras, Salim
Keller, Beat
author_facet Müller, Marion C.
Kunz, Lukas
Schudel, Seraina
Lawson, Aaron W.
Kammerecker, Sandrine
Isaksson, Jonatan
Wyler, Michele
Graf, Johannes
Sotiropoulos, Alexandros G.
Praz, Coraline R.
Manser, Beatrice
Wicker, Thomas
Bourras, Salim
Keller, Beat
author_sort Müller, Marion C.
collection PubMed
description Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable—a phenomenon that remains poorly understood, as the corresponding fungal avirulence genes are largely unknown. Until its breakdown, the Pm17 resistance gene introgressed from rye to wheat provided broad resistance against powdery mildew (Blumeria graminis). Here, we used quantitative trait locus (QTL) mapping to identify the corresponding wheat mildew avirulence effector AvrPm17. It is encoded by two paralogous genes that exhibit signatures of reoccurring gene conversion events and are members of a mildew sublineage specific effector cluster. Extensive haplovariant mining in wheat mildew and related sublineages identified several ancient virulent AvrPm17 variants that were present as standing genetic variation in wheat powdery mildew prior to the Pm17 introgression, thereby paving the way for the rapid breakdown of the Pm17 resistance. QTL mapping in mildew identified a second genetic component likely corresponding to an additional resistance gene present on the 1AL.1RS translocation carrying Pm17. This gene remained previously undetected due to suppressed recombination within the introgressed rye chromosomal segment. We conclude that the initial effectiveness of 1AL.1RS was based on simultaneous introgression of two genetically linked resistance genes. Our results demonstrate the relevance of pathogen-based genetic approaches to disentangling complex resistance loci in wheat. We propose that identification and monitoring of avirulence gene diversity in pathogen populations become an integral part of introgression breeding to ensure effective and durable resistance in wheat.
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spelling pubmed-93352422022-07-30 Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat Müller, Marion C. Kunz, Lukas Schudel, Seraina Lawson, Aaron W. Kammerecker, Sandrine Isaksson, Jonatan Wyler, Michele Graf, Johannes Sotiropoulos, Alexandros G. Praz, Coraline R. Manser, Beatrice Wicker, Thomas Bourras, Salim Keller, Beat Proc Natl Acad Sci U S A Biological Sciences Introgressions of chromosomal segments from related species into wheat are important sources of resistance against fungal diseases. The durability and effectiveness of introgressed resistance genes upon agricultural deployment is highly variable—a phenomenon that remains poorly understood, as the corresponding fungal avirulence genes are largely unknown. Until its breakdown, the Pm17 resistance gene introgressed from rye to wheat provided broad resistance against powdery mildew (Blumeria graminis). Here, we used quantitative trait locus (QTL) mapping to identify the corresponding wheat mildew avirulence effector AvrPm17. It is encoded by two paralogous genes that exhibit signatures of reoccurring gene conversion events and are members of a mildew sublineage specific effector cluster. Extensive haplovariant mining in wheat mildew and related sublineages identified several ancient virulent AvrPm17 variants that were present as standing genetic variation in wheat powdery mildew prior to the Pm17 introgression, thereby paving the way for the rapid breakdown of the Pm17 resistance. QTL mapping in mildew identified a second genetic component likely corresponding to an additional resistance gene present on the 1AL.1RS translocation carrying Pm17. This gene remained previously undetected due to suppressed recombination within the introgressed rye chromosomal segment. We conclude that the initial effectiveness of 1AL.1RS was based on simultaneous introgression of two genetically linked resistance genes. Our results demonstrate the relevance of pathogen-based genetic approaches to disentangling complex resistance loci in wheat. We propose that identification and monitoring of avirulence gene diversity in pathogen populations become an integral part of introgression breeding to ensure effective and durable resistance in wheat. National Academy of Sciences 2022-07-20 2022-07-26 /pmc/articles/PMC9335242/ /pubmed/35857869 http://dx.doi.org/10.1073/pnas.2108808119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Müller, Marion C.
Kunz, Lukas
Schudel, Seraina
Lawson, Aaron W.
Kammerecker, Sandrine
Isaksson, Jonatan
Wyler, Michele
Graf, Johannes
Sotiropoulos, Alexandros G.
Praz, Coraline R.
Manser, Beatrice
Wicker, Thomas
Bourras, Salim
Keller, Beat
Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title_full Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title_fullStr Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title_full_unstemmed Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title_short Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat
title_sort ancient variation of the avrpm17 gene in powdery mildew limits the effectiveness of the introgressed rye pm17 resistance gene in wheat
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9335242/
https://www.ncbi.nlm.nih.gov/pubmed/35857869
http://dx.doi.org/10.1073/pnas.2108808119
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