Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper
ABSTRACT The evolving threat of new pathogen variants in the face of global environmental changes poses a risk to a sustainable crop production. Predicting and responding to how climate change affects plant‐pathosystems is challenging, as environment affects host–pathogen interactions from molecular...
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| Format: | Article |
| Language: | English |
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Wiley
2025-01-01
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| Series: | Evolutionary Applications |
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| Online Access: | https://doi.org/10.1111/eva.70069 |
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| author | Amanpreet Kaur Ivory Russell Ranlin Liu Auston Holland Rishi Bhandari Neha Potnis |
| author_facet | Amanpreet Kaur Ivory Russell Ranlin Liu Auston Holland Rishi Bhandari Neha Potnis |
| author_sort | Amanpreet Kaur |
| collection | DOAJ |
| description | ABSTRACT The evolving threat of new pathogen variants in the face of global environmental changes poses a risk to a sustainable crop production. Predicting and responding to how climate change affects plant‐pathosystems is challenging, as environment affects host–pathogen interactions from molecular to the community level, and with eco‐evolutionary feedbacks at play. To address this knowledge gap, we studied short‐term within‐host eco‐evolutionary changes in the pathogen, Xanthomonas perforans, on resistant and susceptible pepper in the open‐top chambers (OTCs) under elevated Ozone (O3) conditions in a single growing season. We observed increased disease severity with greater variance on the resistant cultivar under elevated O3, yet no apparent change on the susceptible cultivar. Despite the dominance of a single pathogen genotype on the susceptible cultivar, the resistant cultivar supported a heterogeneous pathogen population. Altered O3 levels led to a strain turnover, with a relatively greater gene flux on the resistant cultivar. Both standing genetic variation and de novo parallel mutations contributed toward evolutionary modifications during adaptation onto the resistant cultivar. The presence of elevated O3, however, led to a relatively higher genetic polymorphism, with random and transient mutations. Population heterogeneity along with genetic variation, and the promotion of interdependency are mechanisms by which pathogen responds to stressors. While parallel mutations may provide clues to predicting long‐term pathogen evolution and adaptive potential. And, a high proportion of transient mutations suggest less predictable pathogen evolution under climatic alterations. This knowledge is relevant as we study the risk of pathogen emergence and the mechanisms and constraints underlying long‐term pathogen adaptation under climatic shifts. |
| format | Article |
| id | doaj-art-7365f92b16c44e5c8e1e4bb28af214d2 |
| institution | Kabale University |
| issn | 1752-4571 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Wiley |
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| series | Evolutionary Applications |
| spelling | doaj-art-7365f92b16c44e5c8e1e4bb28af214d22025-02-07T03:58:50ZengWileyEvolutionary Applications1752-45712025-01-01181n/an/a10.1111/eva.70069Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on PepperAmanpreet Kaur0Ivory Russell1Ranlin Liu2Auston Holland3Rishi Bhandari4Neha Potnis5Department of Entomology and Plant Pathology Auburn University Auburn Alabama USADepartment of Entomology and Plant Pathology Auburn University Auburn Alabama USADepartment of Entomology and Plant Pathology Auburn University Auburn Alabama USADepartment of Entomology and Plant Pathology Auburn University Auburn Alabama USADepartment of Entomology and Plant Pathology Auburn University Auburn Alabama USADepartment of Entomology and Plant Pathology Auburn University Auburn Alabama USAABSTRACT The evolving threat of new pathogen variants in the face of global environmental changes poses a risk to a sustainable crop production. Predicting and responding to how climate change affects plant‐pathosystems is challenging, as environment affects host–pathogen interactions from molecular to the community level, and with eco‐evolutionary feedbacks at play. To address this knowledge gap, we studied short‐term within‐host eco‐evolutionary changes in the pathogen, Xanthomonas perforans, on resistant and susceptible pepper in the open‐top chambers (OTCs) under elevated Ozone (O3) conditions in a single growing season. We observed increased disease severity with greater variance on the resistant cultivar under elevated O3, yet no apparent change on the susceptible cultivar. Despite the dominance of a single pathogen genotype on the susceptible cultivar, the resistant cultivar supported a heterogeneous pathogen population. Altered O3 levels led to a strain turnover, with a relatively greater gene flux on the resistant cultivar. Both standing genetic variation and de novo parallel mutations contributed toward evolutionary modifications during adaptation onto the resistant cultivar. The presence of elevated O3, however, led to a relatively higher genetic polymorphism, with random and transient mutations. Population heterogeneity along with genetic variation, and the promotion of interdependency are mechanisms by which pathogen responds to stressors. While parallel mutations may provide clues to predicting long‐term pathogen evolution and adaptive potential. And, a high proportion of transient mutations suggest less predictable pathogen evolution under climatic alterations. This knowledge is relevant as we study the risk of pathogen emergence and the mechanisms and constraints underlying long‐term pathogen adaptation under climatic shifts.https://doi.org/10.1111/eva.70069genetic variationglobal environmental changepathogen evolutionplant diseaseresistance durability |
| spellingShingle | Amanpreet Kaur Ivory Russell Ranlin Liu Auston Holland Rishi Bhandari Neha Potnis Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper Evolutionary Applications genetic variation global environmental change pathogen evolution plant disease resistance durability |
| title | Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper |
| title_full | Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper |
| title_fullStr | Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper |
| title_full_unstemmed | Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper |
| title_short | Navigating Host Immunity and Concurrent Ozone Stress: Strain‐Resolved Metagenomics Reveals Maintenance of Intraspecific Diversity and Genetic Variation in Xanthomonas on Pepper |
| title_sort | navigating host immunity and concurrent ozone stress strain resolved metagenomics reveals maintenance of intraspecific diversity and genetic variation in xanthomonas on pepper |
| topic | genetic variation global environmental change pathogen evolution plant disease resistance durability |
| url | https://doi.org/10.1111/eva.70069 |
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