The virome of the panglobal, wide host-range plant pathogen <i>Phytophthora cinnamomi</i>: phylogeography and evolutionary insights

<i>Phytophthora cinnamomi</i> 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 <i>P. cinnamomi</i> 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 <i>Ghabrivirales, Martellivirales</i>, and <i>Tolivirales</i>, and the classes <i>Amabiliviricetes, Bunyaviricetes</i>, and the recently proposed <i>Orpoviricetes</i>. Viruses were mainly found in East and Southeast Asian populations, within the geographic origin of <i>P. cinnamomi</i> 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 <i>P. cinnamomi</i> and its virome indicates a dynamic coevolution across diverse geographic regions. Indonesia is indicated to be the viral epicentre of <i>P. cinnamomi</i>, with the highest intra- and interspecies diversity of viruses. Viral diversity is significantly enhanced in regions where sexual recombination of <i>P. cinnamomi</i> 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 <i>P. cinnamomi</i> from a novel virome perspective.

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Publication Details

Journal
Virus Evolution
Published
2025-01-01
DOI
https://doi.org/10.1093/ve/veaf020
Citations
2
Primary Topic
Plant Virus Research Studies
Type
article
Field-Weighted Citation Impact
3.50
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article

The virome of the panglobal, wide host-range plant pathogen Phytophthora cinnamomi: phylogeography and evolutionary insights

Marília Horta Jung, Ivan Milenković, C. M. Brasier, Marthin Tarigan et al.
2 citations
Virus Evolution
Plant Virus Research Studies
3.50
article

The virome of the panglobal, wide host-range plant pathogen Phytophthora cinnamomi: phylogeography and evolutionary insights

Marília Horta Jung, Ivan Milenković, C. M. Brasier, Marthin Tarigan, Michael Rost, Koji Kageyama, Eugenio Sanfuentes, Leticia Botella, Ayaka Hieno, Álvaro Durán, Vladislav Čurn, Milica Raco, Tomáš Kudláček, Edward C. Y. Liew, Nasri Nasri, Nguyen Minh, Bruno Scanu, Marco Forgia, Phạm Quang Thu, Joan Webber, A. Drenth, Muhammad Junaid, Hayato Masuja, Tamara Corcobado, David Guest, Ondřej Hejna, Thomas Jung, Fu ChuenHsu, C. M. B. de F. Maia, Seiji Uematsu, Tun‐Tschu Chang, Kateřina Kovačiková
article en
2 citations

Abstract

<i>Phytophthora cinnamomi</i> 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 <i>P. cinnamomi</i> 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 <i>Ghabrivirales, Martellivirales</i>, and <i>Tolivirales</i>, and the classes <i>Amabiliviricetes, Bunyaviricetes</i>, and the recently proposed <i>Orpoviricetes</i>. Viruses were mainly found in East and Southeast Asian populations, within the geographic origin of <i>P. cinnamomi</i> 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 <i>P. cinnamomi</i> and its virome indicates a dynamic coevolution across diverse geographic regions. Indonesia is indicated to be the viral epicentre of <i>P. cinnamomi</i>, with the highest intra- and interspecies diversity of viruses. Viral diversity is significantly enhanced in regions where sexual recombination of <i>P. cinnamomi</i> 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 <i>P. cinnamomi</i> from a novel virome perspective.

Virus EvolutionVol. 11(1)
The University of Sydney (AU), University of Sassari (IT), University of Concepción (CL), Universitätsmedizin Greifswald (DE), University of South Bohemia in České Budějovice (CZ), Universität Greifswald (DE), Micromun (DE), Institute for Sustainable Plant Protection (IT), Forest Industry Research Institute (VN), Taiwan Forestry Research Institute (TW), Royal Botanic Garden Sydney (AU), Forest Research (GB), Forestry and Forest Products Research Institute (JP), Pacific Engineering (United States) (US), Department of Primary Industries (AU), Gifu University (JP), Mendel University in Brno (CZ), University of Algarve (PT), Tokyo University of Agriculture and Technology (JP), Hasanuddin University (ID)
Openalex Percentile: Top 8%
Plant Virus Research Studies
3.50
DOIOpen Access PDFOpenAlex
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