Phytophthora cinnamomi stands out as one of the most devastating plant pathogens worldwide, rapidly expanding its range and impacting a wide range of host species. In this study, we investigated the virome of P. cinnamomi across 222 isolates from Africa, Asia, Europe, Oceania, and the Americas using stranded total RNA sequencing, reverse transcription polymerase chain reaction screening, and Sanger sequencing of selected isolates. Our analysis revealed that virus infections were prevalent across all sampled populations, including RNA viruses associated with the orders Ghabrivirales, Martellivirales, and Tolivirales, and the classes Amabiliviricetes, Bunyaviricetes, and the recently proposed Orpoviricetes. Viruses were mainly found in East and Southeast Asian populations, within the geographic origin of P. cinnamomi but have also spread to new regions where the pathogen has emerged as a clonal destructive pathogen. Among the identified viruses, eight species, including two bunya-like viruses, one narna-like virus, and five ormycoviruses, exhibit a global distribution with some genetic divergence between continents. The interaction between P. cinnamomi and its virome indicates a dynamic coevolution across diverse geographic regions. Indonesia is indicated to be the viral epicentre of P. cinnamomi, with the highest intra- and interspecies diversity of viruses. Viral diversity is significantly enhanced in regions where sexual recombination of P. cinnamomi occurs, while regions with predominantly asexual reproduction harbour fewer viral species. Interestingly, only the partially self-fertile mating type (MAT) A2, associated with the global pandemic, facilitates the spread of viruses across different biogeographic regions, whereas viruses are absent in the self-sterile MAT A1 in its areas of introduction like Australia and South Africa. Intriguingly, the presence of a plant tombusvirus suggests a potential cross-kingdom infection among Chilean isolates and a plant host. This study sheds further light on the geographical origin of P. cinnamomi from a novel virome perspective.

Center for Environmental and Societal Sustainability Gifu University Gifu 501 1193 Japan

Centre for Horticultural Science The University of Queensland Ecosciences Precinct 41 Boggo Road Dutton Park Brisbane Qld 4001 Australia

Centre of Marine Sciences University of Algarve Gambelas Campus 8005 139 Faro 8005 139 Portugal

Department of Agricultural Sciences University of Sassari Viale Italia 39A Sassari 07100 Italy

Department of Bioregulation and Biointeraction Laboratory of Molecular and Cellular Biology Tokyo University of Agriculture and Technology Fuchu TK 183 8509 Japan

Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 Brno 613 00 Czech Republic

Department of Genetics and Agrobiotechnology Faculty of Agriculture and Technology University of South Bohemia in České Budějovice Na Sádkách 1780 České Budějovice 370 05 Czech Republic

Department of Plant Pest and Disease Faculty of Agriculture Hasanuddin University Jalan Perintis Kemerdekaan Km 10 Makassar SN 90245 Indonesia

Faculty of Forestry Hasanuddin University Jalan Perintis Kemerdekaan km 10 Makassar SN 90245 Indonesia

Fiber Research and Development Asia Pacific Resources International Limited Kabupaten Pelalawan Pangkalan Kerinci RI 28300 Indonesia

Forest Protection Division Taiwan Forestry Research Institute No 53 Nanhai Rd Taipei Taiwan

Forest Protection Research Centre Vietnamese Academy of Forest Sciences 46 Duc Thang Road Hanoi 10000 Vietnam

Forest Research Alice Holt Lodge GU10 4LH Farnham Surrey United Kingdom

Forestry and Forest Products Research Institute Ibaraki Tsukuba IB 305 8687 Japan

Institute for Mathematics and Computer Science and Center for Functional Genomics of Microbes University of Greifswald Walther Rathenau Straße 47 Greifswald 17489 Germany

Institute for Sustainable Plant Protection National Research Council of Italy Strada delle Cacce 73 10135 Torino 10135 Italy

Laboratorio de Patología Forestal Facultad Ciencias Forestales y Centro de Biotecnología Universidad de Concepción Barrio Universitario s n Concepción 4030000 Chile

Phytophthora Research Centre Department of Forest Protection and Wildlife Management Faculty of Forestry and Wood Technology Mendel University in Brno Zemědělská 3 Brno 613 00 Czech Republic

Research Centre for Ecosystem Resilience Australian Institute of Botanical Science The Royal Botanic Gardens and Domain Trust Mrs Macquaries Rd Sydney NSW 2006 Australia

Sydney Institute of Agriculture School of Life and Environmental Sciences The University of Sydney NSW 2006 Australia

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