Decoding virulence in Penicillium italicum: A functional link between NRPS-derived cyclic peptides and citrus infection

Penicillium italicum is a postharvest pathogen responsible for the blue mold disease in citrus fruit, particularly under cold and dry storage conditions. Although the disease poses significant economic losses in global citrus production, the molecular basis of P. italicum virulence remains largely u...

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Detalles Bibliográficos
Autores: Silva, Evandro, Barbosa, Julio Cesar, González-García, Adrián, Berlinck, Roberto G.S., Ballester Frutos, Ana Rosa, González-Candelas, Luis, Fill, Taicia
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/408644
Acceso en línea:http://hdl.handle.net/10261/408644
Access Level:acceso embargado
Palabra clave:Blue mold disease
Postharvest pathology
Secondary metabolites
Fungal virulence factors
HcpA gene
Cyclic tetrapeptides
postharvest diseases
Penicillium italicum
virulence
Descripción
Sumario:Penicillium italicum is a postharvest pathogen responsible for the blue mold disease in citrus fruit, particularly under cold and dry storage conditions. Although the disease poses significant economic losses in global citrus production, the molecular basis of P. italicum virulence remains largely unexplored. In this study, we uncover a direct link between the fungus’s secondary metabolism and its pathogenicity by integrating untargeted metabolomics, gene deletion, and functional assays. LC-HRMS analysis of extracts of infected citrus tissues revealed the active production of cyclic peptides, including fungisporin and structurally related tetrapeptides, during host colonization. These compounds are functionally characterized for the first time as secondary metabolites of P. italicum. Targeted deletion of hcpA, encoding a multimodular nonribosomal peptide synthetase (NRPS), abolished the production of these metabolites, confirming its essential role in their biosynthesis. Although the ΔhcpA mutant exhibited normal growth and sporulation, it was more susceptible to osmotic stress and caused smaller lesions on orange fruit, indicating impaired virulence. Taken together, our findings reveal that HcpA-dependent cyclic peptides function as time-regulated virulence factors and offer novel insights into the infection strategy of P. italicum. This study identifies a promising molecular target for the development of innovative approaches to postharvest disease control in citrus.