Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora

Abstract Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus...

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Main Authors: Martin S. Mullett, Kris Van Poucke, Annelies Haegeman, Fran Focquet, Nicholas C. Cauldron, Brian J. Knaus, Marilia Horta Jung, Koji Kageyama, Ayaka Hieno, Hayato Masuja, Seiji Uematsu, Joan F. Webber, Clive M. Brasier, József Bakonyi, Kurt Heungens, Niklaus J. Grünwald, Thomas Jung
Format: Article
Language:English
Published: BMC 2023-02-01
Series:IMA Fungus
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Online Access:https://doi.org/10.1186/s43008-023-00109-6
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author Martin S. Mullett
Kris Van Poucke
Annelies Haegeman
Fran Focquet
Nicholas C. Cauldron
Brian J. Knaus
Marilia Horta Jung
Koji Kageyama
Ayaka Hieno
Hayato Masuja
Seiji Uematsu
Joan F. Webber
Clive M. Brasier
József Bakonyi
Kurt Heungens
Niklaus J. Grünwald
Thomas Jung
author_facet Martin S. Mullett
Kris Van Poucke
Annelies Haegeman
Fran Focquet
Nicholas C. Cauldron
Brian J. Knaus
Marilia Horta Jung
Koji Kageyama
Ayaka Hieno
Hayato Masuja
Seiji Uematsu
Joan F. Webber
Clive M. Brasier
József Bakonyi
Kurt Heungens
Niklaus J. Grünwald
Thomas Jung
author_sort Martin S. Mullett
collection DOAJ
description Abstract Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first damaging invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined its population genetic history in Europe, North and South America, Australia and East Asia (mainly Japan) using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, those in North America are highly clonal yet show some degree of sexual reproduction, and those in East Asia are partially sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on fagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. × cambivora, which may potentially be a separate sister species and has likely been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen. Further surveys in unsampled, temperate regions of East Asia are needed to more precisely identify the location and range of the centre of diversity.
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spelling doaj-art-251b0a79296a4f7f8f03b208e74035d12025-02-02T15:34:27ZengBMCIMA Fungus2210-63592023-02-0114111810.1186/s43008-023-00109-6Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivoraMartin S. Mullett0Kris Van Poucke1Annelies Haegeman2Fran Focquet3Nicholas C. Cauldron4Brian J. Knaus5Marilia Horta Jung6Koji Kageyama7Ayaka Hieno8Hayato Masuja9Seiji Uematsu10Joan F. Webber11Clive M. Brasier12József Bakonyi13Kurt Heungens14Niklaus J. Grünwald15Thomas Jung16Phytophthora Research Centre, Department of Forest Protection and Wildlife Management, Mendel University in BrnoFlanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Sciences UnitFlanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Sciences UnitFlanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Sciences UnitDepartment of Botany and Plant Pathology, Oregon State UniversityDepartment of Horticulture, Oregon State UniversityPhytophthora Research Centre, Department of Forest Protection and Wildlife Management, Mendel University in BrnoRiver Basin Research Center, Gifu UniversityRiver Basin Research Center, Gifu UniversityForestry and Forest Products Research Institute (FFPRI)Department of Bioregulation and Biointeraction, Laboratory of Molecular and Cellular Biology, Tokyo University of Agriculture and TechnologyForest Research, Alice Holt LodgeForest Research, Alice Holt LodgePlant Protection Institute, Centre for Agricultural Research, ELKHFlanders Research Institute for Agriculture, Fisheries and Food (ILVO), Plant Sciences UnitHorticultural Crops Research Unit, United States Department of Agriculture, Agricultural Research ServicePhytophthora Research Centre, Department of Forest Protection and Wildlife Management, Mendel University in BrnoAbstract Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first damaging invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined its population genetic history in Europe, North and South America, Australia and East Asia (mainly Japan) using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, those in North America are highly clonal yet show some degree of sexual reproduction, and those in East Asia are partially sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on fagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. × cambivora, which may potentially be a separate sister species and has likely been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen. Further surveys in unsampled, temperate regions of East Asia are needed to more precisely identify the location and range of the centre of diversity.https://doi.org/10.1186/s43008-023-00109-6Invasive pathogenHybridizationPolyploidyPopulation genetics
spellingShingle Martin S. Mullett
Kris Van Poucke
Annelies Haegeman
Fran Focquet
Nicholas C. Cauldron
Brian J. Knaus
Marilia Horta Jung
Koji Kageyama
Ayaka Hieno
Hayato Masuja
Seiji Uematsu
Joan F. Webber
Clive M. Brasier
József Bakonyi
Kurt Heungens
Niklaus J. Grünwald
Thomas Jung
Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
IMA Fungus
Invasive pathogen
Hybridization
Polyploidy
Population genetics
title Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
title_full Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
title_fullStr Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
title_full_unstemmed Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
title_short Phylogeography and population structure of the global, wide host-range hybrid pathogen Phytophthora × cambivora
title_sort phylogeography and population structure of the global wide host range hybrid pathogen phytophthora cambivora
topic Invasive pathogen
Hybridization
Polyploidy
Population genetics
url https://doi.org/10.1186/s43008-023-00109-6
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