Dataset Information

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures.

ABSTRACT: Many fungal pathogens have short generation times, large population sizes, and mixed reproductive systems, providing high potential to adapt to heterogeneous environments of agroecosystems. Such adaptation complicates disease management and threatens food production. A better understanding of pathogen population biology in such environments is important to reveal key aspects of adaptive divergence processes to allow improved disease management. Here, we studied how evolutionary forces shape population structure of Botrytis cinerea, the causal agent of gray mold, in the Pacific Northwest agroecosystems. Populations of B. cinerea from adjacent fields of small fruit hosts were characterized by combining neutral markers (microsatellites) with markers that directly respond to human-induced selection pressures (fungicide resistance). Populations were diverse, without evidence for recombination and association of pathogen genotype with host. Populations were highly localized with limited migration even among adjacent fields within a farm. A fungicide resistance marker revealed strong selection on population structure due to fungicide use. We found no association of resistance allele with genetic background, suggesting de novo development of fungicide resistance and frequent extinction/recolonization events by different genotypes rather than the spread of resistance alleles among fields via migration of a dominant genotype. Overall our results showed that in agroecosystems, B. cinerea populations respond strongly to selection by fungicide use with greater effect on population structure compared to adaptation to host plant species. This knowledge will be used to improve disease management by developing strategies that limit pathogen local adaptation to fungicides and other human-induced selection pressures present in Pacific Northwest agroecosystems and elsewhere.IMPORTANCE Agroecosystems represent an efficient model for studying fungal adaptation and evolution in anthropogenic environments. In this work, we studied what evolutionary forces shape populations of one of the most important fungal plant pathogens, B. cinerea, in small fruit agroecosystems of the Pacific Northwest. We hypothesized that host, geographic, and anthropogenic factors of agroecosystems structure B. cinerea populations. By combining neutral markers with markers that directly respond to human-induced selection pressures, we show that pathogen populations are highly localized and that selection pressure caused by fungicide use can have a greater effect on population structure than adaptation to host. Our results give a better understanding of population biology and evolution of this important plant pathogen in heterogeneous environments but also provide a practical framework for the development of efficient management strategies by limiting pathogen adaptation to fungicides and other human-induced selection pressures present in agroecosystems of the Pacific Northwest and elsewhere.

SUBMITTER: Kozhar O

PROVIDER: S-EPMC7170486 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Publications

Fungal Evolution in Anthropogenic Environments: <i>Botrytis cinerea</i> Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures.

Kozhar Olga O Larsen Meredith M MM Grünwald Niklaus J NJ Peever Tobin L TL

Applied and environmental microbiology 20200417 9

Many fungal pathogens have short generation times, large population sizes, and mixed reproductive systems, providing high potential to adapt to heterogeneous environments of agroecosystems. Such adaptation complicates disease management and threatens food production. A better understanding of pathogen population biology in such environments is important to reveal key aspects of adaptive divergence processes to allow improved disease management. Here, we studied how evolutionary forces shape popu ...[more]

PMID: 32086310

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Project description:The pathogen Botrytis cinerea is a very dangerous pathogen that infects many economically important crops such as grape, strawberry, tomato, and eggplant. Cyprodinil, a pyrimidine amine fungicide, and fenhexamid, an amide fungicide, are new reagents for controlling gray mold with special efficacy. It is necessary to understand the change trends in the toxicological and physiological characteristics of B. cinerea with successive selective pressures of cyprodinil and fenhexamid to elongate the serving life of these fungicides for effective disease control. The toxicities of cyprodinil and fenhexamid at successive concentrations of EC25, EC50 and EC75 on B. cinerea strain BO5.10 were assayed along with mycelial growth-inhibition capacity. The results showed that the EC50 value of the cyprodinil-treated F27 strain increased approximately 18-fold, whereas of which in the fenhexamid-treated F27 strain increased only 3-fold compared with that of the F0 strain. The conductivities and glycerinum contents of the strains resistant to cyprodinil and fenhexamid were obviously enhanced; in contrast, the oxalic acid contents were decreased compared with those in the F0 strain. The transcriptomes of the F27 control (T01), cyprodinil-treated (T02) and fenhexamid- treated (T03) strains were analyzed, and the expression levels of functional genes in the T02 and T03 strains were significantly increased compared with those in the T01 strain; these results were further validated using qRT-PCR. The results indicated that the relative expression of two genes encoding mixed-functional oxidases (MFOs) BC1G_16062 and BC1G_16084, two genes encoding transmembrane proteins BC1G_12366 and BC1G_13768, two genes encoding Zinc finger proteins BC1G_13764 and BC1G_10483,one gene encoding citrate synthase enzyme BC1G_09151, one gene encoding gluconolactonase BC1G_15612 in the T02 and T03 strains and one gene encoding lysophospholipids enzyme BC1G_04893 in the T3 strain increased substantially compared with that in the T1 strain (P < 0.01). Functional prediction analysis of upregulated gene expression and structural verification was also performed, and the results showed that BC1G_10483 was a ZnF_C2HC transcriptional regulator interacting with the Sp1 element of these genes to respond to the pressures from cyprodinil and fenhexamid. Our results could contribute to a better understanding of the resistance mechanism of B. cinerea against cyprodinil and fenhexamid.

Dataset Information

Fungal Evolution in Anthropogenic Environments: Botrytis cinerea Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures.

Publications

Fungal Evolution in Anthropogenic Environments: <i>Botrytis cinerea</i> Populations Infecting Small Fruit Hosts in the Pacific Northwest Rapidly Adapt to Human-Induced Selection Pressures.

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