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 disease outbreaks. This paper reviews the evolution of fungal pathogens from natural habitats to agricultural settings, focusing on eight significant phytopathogens: Pyricularia oryzae, Botrytis cinerea, Puccinia spp., Fusarium graminearum, F. oxysporum, Blumeria graminis, Zymoseptoria tritici, and Colletotrichum 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.