From Plants to Animals: Cross-Kingdom Infection by Fungal Phytopathogens

Plant pathogenic fungi exhibit significant ecological diversity that is under pressure from climate change, yet their relevance to both human and ecosystem health remains underexplored within the One Health framework. Several phytopathogenic lineages have demonstrated the ability to infect vertebrate hosts. Herein, we introduce the ecological characteristics and genomic plasticity of selected phytopathogenic fungi. Some species adopt generalist lifestyle strategies as endophytes and epiphytes, whereas others develop specialized biotrophic, necrotrophic, or hemibiotrophic modes of infection. Their ecological diversity is facilitated by the horizontal transfer of accessory chromosomes, enabling rapid adaptation and potentially giving rise to new versatile hybrids. Opportunism is defined when traits acquired in a pathogen's preferred niche coincidentally allow survival in other hosts, despite reduced fitness that prevents subsequent transmission. We highlight three filamentous ascomycetes that exemplify ecological versatility and genomic plasticity associated with cross-kingdom opportunistic infections. In Alternaria alternata, melanogenesis and induction of Type 2 inflammation may predispose vulnerable populations to infection. Colletotrichum spp. can cause keratitis and infections in immunocompromised individuals; its pathogenic potential is further supported by melanin production and resistance to dual-use azole antifungals. By contrast, the Fusarium oxysporum species complex demonstrates a broad host range, causing disease in immunocompromised and immunocompetent individuals, with the latter particularly concerning onychomycosis. Its One Health implications are further supported by outbreaks in aquatic vertebrates, the identification of virulence factors implicated in both plant and vertebrate pathogenicity, and resistance to dual-use azole antifungals. Cross-disciplinary and cross-sectoral collaborations should be encouraged to develop mitigation strategies.