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...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2017-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02361/full |
| _version_ | 1811266669100662784 |
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| author | Andreas Mosbach Dominique Edel Andrew D. Farmer Andrew D. Farmer Stephanie Widdison Thierry Barchietto Robert A. Dietrich Andy Corran Gabriel Scalliet |
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-12T20:46:18Z |
| format | Article |
| id | doaj.art-c4f9d33a3482494188c401a31013ed97 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-12T20:46:18Z |
| publishDate | 2017-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-c4f9d33a3482494188c401a31013ed972022-12-22T03:17:15ZengFrontiers 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 |
| 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 |
| title | 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_short | Anilinopyrimidine Resistance in Botrytis cinerea Is Linked to Mitochondrial Function |
| title_sort | anilinopyrimidine resistance in botrytis cinerea is linked to mitochondrial function |
| 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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