From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi

Since the domestication of plants, pathogenic fungi have consistently threatened crop production, evolving genetically to develop increased virulence under various selection pressures. Understanding their evolutionary trends is crucial for predicting and designing control measures against future dis...

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Main Authors: Asanka Madhushan, Dulan Bhanuka Weerasingha, Evgeny Ilyukhin, Paul W. J. Taylor, Amila Sandaruwan Ratnayake, Jian-Kui Liu, Sajeewa S. N. Maharachchikumbura
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Journal of Fungi
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Online Access:https://www.mdpi.com/2309-608X/11/1/25
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author Asanka Madhushan
Dulan Bhanuka Weerasingha
Evgeny Ilyukhin
Paul W. J. Taylor
Amila Sandaruwan Ratnayake
Jian-Kui Liu
Sajeewa S. N. Maharachchikumbura
author_facet Asanka Madhushan
Dulan Bhanuka Weerasingha
Evgeny Ilyukhin
Paul W. J. Taylor
Amila Sandaruwan Ratnayake
Jian-Kui Liu
Sajeewa S. N. Maharachchikumbura
author_sort Asanka Madhushan
collection DOAJ
description Since the domestication of plants, pathogenic fungi have consistently threatened crop production, evolving genetically to develop increased virulence under various selection pressures. Understanding their evolutionary trends is crucial for predicting and designing control measures against future disease outbreaks. This paper reviews the evolution of fungal pathogens from natural habitats to agricultural settings, focusing on eight significant phytopathogens: <i>Pyricularia oryzae</i>, <i>Botrytis cinerea</i>, <i>Puccinia</i> spp., <i>Fusarium graminearum</i>, <i>F. oxysporum</i>, <i>Blumeria graminis</i>, <i>Zymoseptoria tritici</i>, and <i>Colletotrichum</i> spp. Also, we explore the mechanism used to understand evolutionary trends in these fungi. The studied pathogens have evolved in agroecosystems through either (1) introduction from elsewhere; or (2) local origins involving co-evolution with host plants, host shifts, or genetic variations within existing strains. Genetic variation, generated via sexual recombination and various asexual mechanisms, often drives pathogen evolution. While sexual recombination is rare and mainly occurs at the center of origin of the pathogen, asexual mechanisms such as mutations, parasexual recombination, horizontal gene or chromosome transfer, and chromosomal structural variations are predominant. Farming practices like mono-cropping resistant cultivars and prolonged use of fungicides with the same mode of action can drive the emergence of new pathotypes. Furthermore, host range does not necessarily impact pathogen adaptation and evolution. Although halting pathogen evolution is impractical, its pace can be slowed by managing selective pressures, optimizing farming practices, and enforcing quarantine regulations. The study of pathogen evolution has been transformed by advancements in molecular biology, genomics, and bioinformatics, utilizing methods like next-generation sequencing, comparative genomics, transcriptomics and population genomics. However, continuous research remains essential to monitor how pathogens evolve over time and to develop proactive strategies that mitigate their impact on agriculture.
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spelling doaj-art-1dc7dc0782e747369bf95f0cf9b3da3f2025-01-24T13:37:16ZengMDPI AGJournal of Fungi2309-608X2025-01-011112510.3390/jof11010025From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic FungiAsanka Madhushan0Dulan Bhanuka Weerasingha1Evgeny Ilyukhin2Paul W. J. Taylor3Amila Sandaruwan Ratnayake4Jian-Kui Liu5Sajeewa S. N. Maharachchikumbura6School of Life Science and Technology, Center for Informational Biology, University of Electronic Science and Technology of China, Chengdu 611731, ChinaSchool of Life Science and Technology, Center for Informational Biology, University of Electronic Science and Technology of China, Chengdu 611731, ChinaLaboratory of Plant Pathology, Swift Current Research and Development Centre, Agriculture and Agri-Food Canada, Swift Current, SK S9H 3X2, CanadaFaculty of Science, The University of Melbourne, Parkville, VIC 3010, AustraliaDepartment of Applied Earth Sciences, Faculty of Applied Sciences, Uva Wellassa University, Passara Road, Badulla 90000, Sri LankaSchool of Life Science and Technology, Center for Informational Biology, University of Electronic Science and Technology of China, Chengdu 611731, ChinaSchool of Life Science and Technology, Center for Informational Biology, University of Electronic Science and Technology of China, Chengdu 611731, ChinaSince the domestication of plants, pathogenic fungi have consistently threatened crop production, evolving genetically to develop increased virulence under various selection pressures. Understanding their evolutionary trends is crucial for predicting and designing control measures against future disease outbreaks. This paper reviews the evolution of fungal pathogens from natural habitats to agricultural settings, focusing on eight significant phytopathogens: <i>Pyricularia oryzae</i>, <i>Botrytis cinerea</i>, <i>Puccinia</i> spp., <i>Fusarium graminearum</i>, <i>F. oxysporum</i>, <i>Blumeria graminis</i>, <i>Zymoseptoria tritici</i>, and <i>Colletotrichum</i> spp. Also, we explore the mechanism used to understand evolutionary trends in these fungi. The studied pathogens have evolved in agroecosystems through either (1) introduction from elsewhere; or (2) local origins involving co-evolution with host plants, host shifts, or genetic variations within existing strains. Genetic variation, generated via sexual recombination and various asexual mechanisms, often drives pathogen evolution. While sexual recombination is rare and mainly occurs at the center of origin of the pathogen, asexual mechanisms such as mutations, parasexual recombination, horizontal gene or chromosome transfer, and chromosomal structural variations are predominant. Farming practices like mono-cropping resistant cultivars and prolonged use of fungicides with the same mode of action can drive the emergence of new pathotypes. Furthermore, host range does not necessarily impact pathogen adaptation and evolution. Although halting pathogen evolution is impractical, its pace can be slowed by managing selective pressures, optimizing farming practices, and enforcing quarantine regulations. The study of pathogen evolution has been transformed by advancements in molecular biology, genomics, and bioinformatics, utilizing methods like next-generation sequencing, comparative genomics, transcriptomics and population genomics. However, continuous research remains essential to monitor how pathogens evolve over time and to develop proactive strategies that mitigate their impact on agriculture.https://www.mdpi.com/2309-608X/11/1/25emerging strainsresistanceSordariomycetesvirulence
spellingShingle Asanka Madhushan
Dulan Bhanuka Weerasingha
Evgeny Ilyukhin
Paul W. J. Taylor
Amila Sandaruwan Ratnayake
Jian-Kui Liu
Sajeewa S. N. Maharachchikumbura
From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
Journal of Fungi
emerging strains
resistance
Sordariomycetes
virulence
title From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
title_full From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
title_fullStr From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
title_full_unstemmed From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
title_short From Natural Hosts to Agricultural Threats: The Evolutionary Journey of Phytopathogenic Fungi
title_sort from natural hosts to agricultural threats the evolutionary journey of phytopathogenic fungi
topic emerging strains
resistance
Sordariomycetes
virulence
url https://www.mdpi.com/2309-608X/11/1/25
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