Botrytis cinerea, causal agent of gray mold, is one of the most important pathogens affecting raspberry in the U.S. Pacific Northwest and worldwide. Fungicides are currently applied to control the disease starting from 5 to 10% bloom and continuing on a calendar basis throughout the season rather than according to inoculum level or infection risk primarily because the disease cycle on red raspberry is poorly understood. Botrytis cinerea was isolated from raspberry flowers and fruit sampled at seven developmental stages during each of 2015 and 2016 in a northwestern Washington raspberry field untreated with fungicides. Incidence of colonization of flowers was low (15% of total sampled flowers), but increased as fruit developed, and peaked in mature fruit (67% of total sampled fruit). In the early stages of flower development, B. cinerea recovery was greatest from the carpel (80% of carpels colonized) compared with other floral organs. As fruit matured, additional floral parts were colonized by B. cinerea, possibly facilitating secondary internal or external infections of mature fruit. Average weekly minimum air temperature, average weekly night air temperature, cumulative rain, average weekly leaf wetness percentage, and duration of leaf wetness >90% were significantly positively correlated with B. cinerea colonization of raspberry in NW Washington during two seasons of this study. Our data does not support the hypothesis that the bloom period is the critical window for B. cinerea colonization of red raspberry and suggest that later colonization of developing fruit may be more important for gray mold development on raspberry. The outcomes of this research provide useful information for improvement of gray mold disease management strategies for red raspberry in NW Washington and elsewhere.
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.
Colonization of red raspberry flowers and fruit by Botrytis cinerea was determined during 2017–2018 growing seasons under commercial fungicide application programmes used for grey mould management in northwestern Washington, USA. Colonization of flowers and fruit was assessed qualitatively (incidence, %) and quantitatively (abundance, number of colonies) by recovering B. cinerea from surface‐disinfested samples. Both incidence and abundance of flower colonization were significantly lower than fruit colonization in both untreated and fungicide‐treated plots. Incidence of flower colonization did not differ significantly between untreated and fungicide‐treated plots (43% vs. 45%, respectively). In contrast, significantly greater colonization incidence was detected at green fruit stage in untreated compared to fungicide‐treated plots (96% vs. 77%, respectively). Ripe fruit had the greatest colonization incidence among the three stages sampled and colonization was not significantly different between untreated and fungicide‐treated plots (100% vs. 92%, respectively). Similarly, colonization abundance of flowers did not differ significantly between untreated and fungicide‐treated plots (1.0 colonies per colonized flower in both treatments), but colonization abundance of green and ripe fruit was decreased 2.3‐ and 2.1‐fold, respectively, in fungicide‐treated plots. DNA fingerprinting analysis of the pathogen revealed that different multilocus genotypes colonized flowers and fruit within the same inflorescence and that genotypic diversity increased through time, suggesting independent infection events. Overall, our results demonstrate that under current environmental conditions, raspberry flowers may not be the exclusive or major route of infection for grey mould of red raspberry in northwestern Washington. Implications of current findings for management and further research are discussed.
Emerging plant pathogens have been increasing exponentially over the last century. To address this issue, it is critical to determine whether these pathogens are native to ecosystems or have been recently introduced. Understanding the ecological and evolutionary processes fostering emergence can help to manage their spread and predict epidemics/epiphytotics. Using restriction site‐associated DNA sequencing data, we studied genetic relationships, pathways of spread and the evolutionary history of Phellinus noxius, an emerging root‐rotting fungus of unknown origin, in eastern Asia, Australia and the Pacific Islands. We analysed patterns of genetic variation using Bayesian inference, maximum‐likelihood phylogeny, population splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent‐based theory using Approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from an unsampled population to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that this pathogen was recently introduced to multiple geographical regions. Our results suggest that recent emergence of P. noxius in eastern Asia, Australia and the Pacific Islands has probably been driven by anthropogenic and natural disturbances, such as deforestation, land‐use change, severe weather events and/or introduction of exotic plants. This study provides a novel example of applying genome‐wide allele frequency data to unravel the dynamics of pathogen emergence under changing ecosystem conditions.
Emerging plant pathogens have been increasing exponentially over the last century. To address this issue, it is critical to determine whether these pathogens are native to ecosystems or have been recently introduced. Understanding the ecological and evolutionary processes fostering emergence can help to manage their spread and predict epidemics/epiphytotics. Using restriction site-associated DNA sequencing data, we studied genetic relationships, pathways of spread, and evolutionary history of Phellinus noxius, an emerging root-rotting fungus of unknown origin, in eastern Asia, Australia, and the Pacific Islands. We analyzed patterns of genetic variation using Bayesian inference, maximum likelihood phylogeny, populations splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent based theory using Approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from ghost population to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate that P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that this pathogen was recently introduced to multiple geographic regions. Our results suggest that recent emergence of P. noxius in eastern Asia, Australia, and the Pacific Islands is likely driven by anthropogenic and natural disturbances, such as deforestation, land-use change, severe weather events, and/or introduction of exotic plants. This study provides a novel example of applying genome-wide allele frequency data to unravel dynamics of pathogen emergence under changing ecosystem conditions.
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