Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function

Crop protection anilinopyrimidine (AP) fungicides were introduced more than 20 years ago for the control of a range of diseases caused by ascomycete plant pathogens, and in particular for the control of gray mold caused by Botrytis cinerea. Although early mode of action studies suggested an inhibiti...

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Main Authors: Andreas Mosbach, Dominique Edel, Andrew D. Farmer, Stephanie Widdison, Thierry Barchietto, Robert A. Dietrich, Andy Corran, Gabriel Scalliet
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02361/full
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spelling doaj-c4f9d33a3482494188c401a31013ed972020-11-24T23:24:07ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-11-01810.3389/fmicb.2017.02361304532Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial FunctionAndreas Mosbach0Dominique Edel1Andrew D. Farmer2Andrew D. Farmer3Stephanie Widdison4Thierry Barchietto5Robert A. Dietrich6Andy Corran7Gabriel Scalliet8Syngenta Crop Protection AG, Stein, SwitzerlandSyngenta Crop Protection AG, Stein, SwitzerlandNational Center for Genome Resources, Santa Fe, NM, United StatesSyngenta Biotechnology Inc., Research Triangle Park, NC, United StatesSyngenta Jealott's Hill International Research Centre, Bracknell, United KingdomBIOtransfer, Montreuil, FranceSyngenta Biotechnology Inc., Research Triangle Park, NC, United StatesSyngenta Jealott's Hill International Research Centre, Bracknell, United KingdomSyngenta Crop Protection AG, Stein, SwitzerlandCrop protection anilinopyrimidine (AP) fungicides were introduced more than 20 years ago for the control of a range of diseases caused by ascomycete plant pathogens, and in particular for the control of gray mold caused by Botrytis cinerea. Although early mode of action studies suggested an inhibition of methionine biosynthesis, the molecular target of this class of fungicides was never fully clarified. Despite AP-specific resistance having been described in B. cinerea field isolates and in multiple other targeted species, the underlying resistance mechanisms were unknown. It was therefore expected that the genetic characterization of resistance mechanisms would permit the identification of the molecular target of these fungicides. In order to explore the widest range of possible resistance mechanisms, AP-resistant B. cinerea UV laboratory mutants were generated and the mutations conferring resistance were determined by combining whole-genome sequencing and reverse genetics. Genetic mapping from a cross between a resistant field isolate and a sensitive reference isolate was used in parallel and led to the identification of an additional molecular determinant not found from the characterized UV mutant collection. Together, these two approaches enabled the characterization of an unrivaled diversity of resistance mechanisms. In total, we report the elucidation of resistance-conferring mutations within nine individual genes, two of which are responsible for almost all instances of AP resistance in the field. All identified resistance-conferring genes encode proteins that are involved in mitochondrial processes, suggesting that APs primarily target the mitochondria. The functions of these genes and their possible interactions are discussed in the context of the potential mode of action for this important class of fungicides.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02361/fullanilinopyrimidinefungicide resistanceBotrytis cinereagray moldmitochondriaABC transporter
collection DOAJ
language English
format Article
sources DOAJ
author Andreas Mosbach
Dominique Edel
Andrew D. Farmer
Andrew D. Farmer
Stephanie Widdison
Thierry Barchietto
Robert A. Dietrich
Andy Corran
Gabriel Scalliet
spellingShingle Andreas Mosbach
Dominique Edel
Andrew D. Farmer
Andrew D. Farmer
Stephanie Widdison
Thierry Barchietto
Robert A. Dietrich
Andy Corran
Gabriel Scalliet
Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
Frontiers in Microbiology
anilinopyrimidine
fungicide resistance
Botrytis cinerea
gray mold
mitochondria
ABC transporter
author_facet Andreas Mosbach
Dominique Edel
Andrew D. Farmer
Andrew D. Farmer
Stephanie Widdison
Thierry Barchietto
Robert A. Dietrich
Andy Corran
Gabriel Scalliet
author_sort Andreas Mosbach
title Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
title_short Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
title_full Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
title_fullStr Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
title_full_unstemmed Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function
title_sort anilinopyrimidine resistance in botrytis cinerea is linked to mitochondrial function
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2017-11-01
description Crop protection anilinopyrimidine (AP) fungicides were introduced more than 20 years ago for the control of a range of diseases caused by ascomycete plant pathogens, and in particular for the control of gray mold caused by Botrytis cinerea. Although early mode of action studies suggested an inhibition of methionine biosynthesis, the molecular target of this class of fungicides was never fully clarified. Despite AP-specific resistance having been described in B. cinerea field isolates and in multiple other targeted species, the underlying resistance mechanisms were unknown. It was therefore expected that the genetic characterization of resistance mechanisms would permit the identification of the molecular target of these fungicides. In order to explore the widest range of possible resistance mechanisms, AP-resistant B. cinerea UV laboratory mutants were generated and the mutations conferring resistance were determined by combining whole-genome sequencing and reverse genetics. Genetic mapping from a cross between a resistant field isolate and a sensitive reference isolate was used in parallel and led to the identification of an additional molecular determinant not found from the characterized UV mutant collection. Together, these two approaches enabled the characterization of an unrivaled diversity of resistance mechanisms. In total, we report the elucidation of resistance-conferring mutations within nine individual genes, two of which are responsible for almost all instances of AP resistance in the field. All identified resistance-conferring genes encode proteins that are involved in mitochondrial processes, suggesting that APs primarily target the mitochondria. The functions of these genes and their possible interactions are discussed in the context of the potential mode of action for this important class of fungicides.
topic anilinopyrimidine
fungicide resistance
Botrytis cinerea
gray mold
mitochondria
ABC transporter
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02361/full
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