From leaf to continent: the multi-scale distribution of an invasive cryptic pathogen complex on oak

Article

Desprez-Loustau, Marie-Laure, Massot, Marie, Toigo, Maude, Fort, Tania, Aday Kaya, Ayse Gulden, Boberg, Johanna, Braun, Uwe, Capdevielle, Xavier, Cech, Thomas, Chandelier, Anne, Christova, Petya, Corcobado, Tamara, Dogmus, Tugba, Dutech, Cyril, Fabreguettes, Olivier, Faivre d'Arcier, Julie, Gross, Andrin, Horta Jung, Marilia, Iturritxa, Eugenia, ..., Tack, Ayco J.M.. 2018. "From leaf to continent: the multi-scale distribution of an invasive cryptic pathogen complex on oak." Fungal Ecology. 36, pp. 39-50. https://doi.org/10.1016/j.funeco.2018.08.001
Article Title

From leaf to continent: the multi-scale distribution of an invasive cryptic pathogen complex on oak

ERA Journal ID123202
Article CategoryArticle
AuthorsDesprez-Loustau, Marie-Laure (Author), Massot, Marie (Author), Toigo, Maude (Author), Fort, Tania (Author), Aday Kaya, Ayse Gulden (Author), Boberg, Johanna (Author), Braun, Uwe (Author), Capdevielle, Xavier (Author), Cech, Thomas (Author), Chandelier, Anne (Author), Christova, Petya (Author), Corcobado, Tamara (Author), Dogmus, Tugba (Author), Dutech, Cyril (Author), Fabreguettes, Olivier (Author), Faivre d'Arcier, Julie (Author), Gross, Andrin (Author), Horta Jung, Marilia (Author), Iturritxa, Eugenia (Author), Jung, Thomas (Author), Junker, Corina (Author), Kiss, Levente (Author), Kostov, Kaloyan (Author), Lehtijarvi, Asko (Author), Lyubenova, Aneta (Author), Marcais, Benoit (Author), Oliva, Jonas (Author), Oskay, Funda (Author), Pastircak, Martin (Author), Pastircakova, Katarina (Author), Piou, Dominique (Author), Saint-Jean, Gilles (Author), Sallafranque, Arnaud (Author), Slavov, Slavtcho (Author), Stenlid, Jan (Author), Talgo, Venche (Author), Takamatsu, Susumu (Author) and Tack, Ayco J.M. (Author)
Journal TitleFungal Ecology
Journal Citation36, pp. 39-50
Number of Pages12
Year2018
Place of PublicationUnited Kingdom
ISSN1754-5048
1878-0083
Digital Object Identifier (DOI)https://doi.org/10.1016/j.funeco.2018.08.001
Web Address (URL)https://www.sciencedirect.com/science/article/pii/S1754504818300795
Abstract

The spatial distribution and niche differentiation of three closely related species (Erysiphe alphitoides, Erysiphe quercicola and Erysiphe hypophylla) causing oak powdery mildew was studied at scales ranging from the European continent, where they are invasive, to a single leaf. While E. alphitoides was dominant at all scales, E. quercicola and E. hypophylla had restricted geographic, stand and leaf distributions. The large-scale distributions were likely explained by climatic factors and species environmental tolerances, with E. quercicola being more frequent in warmer climates and E. hypophylla in colder climates. The extensive sampling and molecular analyses revealed the cryptic invasion of E. quercicola in nine countries from which it had not previously been recorded. The presence of the three species was also strongly affected by host factors, such as oak species and developmental stage. Segregation patterns between Erysiphe species were observed at the leaf scale, between and within leaf surfaces, suggesting competitive effects.

Keywordscryptic invasion, cryptic species, Erysiphe, Oak, plant pathogen, powdery mildew, Quercus, spatial distribution, emission inventory, species coexistence
ANZSRC Field of Research 2020310705. Mycology
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Byline AffiliationsUniversity of Bordeaux, France
Suleyman Demirel University, Turkiye
Swedish University of Agricultural Sciences, Sweden
Martin Luther University Halle-Wittenberg, Germany
Ministry of Agriculture Forestry Regions and Water Management, Austria
Wallon Centre for Agronomic Research, Belgium
AgroBioInstitute, Bulgaria
Austrian Federal Office and Research Centre for Forests, Austria
Mendel University, Czech Republic
Basque Institute for Agricultural Research and Development, Spain
Julius Kuhn Institute, Germany
Centre for Crop Health
Bursa Technical University, Turkiye
University of Lorraine, France
Cankırı Karatekin University, Turkiye
National Agricultural and Food Centre, Slovakia
Slovak Academy of Sciences, Slovakia
Ministry of Agriculture, France
Norwegian Institute of Bioeconomy Research, Norway
Mie University, Japan
Institution of OriginUniversity of Southern Queensland
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Takamatsu, Susumu, Ito, Hanako, Shiroya, Yoshiaki, Kiss, Levente and Heluta, Vasyl. 2015. "First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage." Mycologia. 107 (3), pp. 475-489. https://doi.org/10.3852/15-007
Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (Impatiens glandulifera)
Tanner, Robert A., Ellison, Carol A., Seier, Marion K., Kovacs, Gabor M., Kassai-Jager, Edit, Bereczky, Zsolt, Varia, Sonal, Djeddour, Djami, Singh, Mool Chand, Csiszar, Agnes, Csontos, Péter, Kiss, Levente and Evans, Harry C.. 2014. "Puccinia komarovii var. glanduliferae var. nov.: a fungal agent for the biological control of Himalayan balsam (Impatiens glandulifera)." European Journal of Plant Pathology. 141 (2), pp. 247-266. https://doi.org/10.1007/s10658-014-0539-x
First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) II. The Uncinula lineage
Takamatsu, Susumu, Ito, Hanako, Shiroya, Yoshiaki, Kiss, Levente and Heluta, Vasyl. 2015. "First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) II. The Uncinula lineage." Mycologia. 107 (5), pp. 903-914. https://doi.org/10.3852/15-062
Nuclear and chloroplast microsatellites show multiple introductions in the worldwide invasion history of common ragweed, Ambrosia artemisiifolia
Gaudeul, Myriam, Giraud, Tatiana, Kiss, Levente and Shykoff, Jacqui A.. 2011. "Nuclear and chloroplast microsatellites show multiple introductions in the worldwide invasion history of common ragweed, Ambrosia artemisiifolia." PLoS One. 6 (3). https://doi.org/10.1371/journal.pone.0017658
New records of microcyclic conidiogenesis in some powdery mildew fungi
Pintye, Alexandra, Legler, Sara Elisabetta and Kiss, Levente. 2011. "New records of microcyclic conidiogenesis in some powdery mildew fungi." Mycoscience. 52 (3), pp. 213-216. https://doi.org/10.1007/s10267-010-0093-0
Peach rusty spot is caused by the apple powdery mildew fungus, Podosphaera leucotricha
Jankovics, Tünde, Dolovac, Nenad, Bulajic, Aleksandra, Krstic, Branka, Pascal, Thierry, Bardin, Marc, Nicot, Philippe C. and Kiss, Levente. 2011. "Peach rusty spot is caused by the apple powdery mildew fungus, Podosphaera leucotricha." Plant Disease: an international journal of applied plant pathology. 95 (6), pp. 719-724. https://doi.org/10.1094/PDIS-10-10-0711
Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for Fungi
Kiss, Levente. 2012. "Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for Fungi." University of Adelaide. 109 (27), p. 1811. https://doi.org/10.1073/pnas.1207143109
Host phenology and geography as drivers of differentiation in generalist fungal mycoparasites
Pintye, Alexandra, Ropars, Jeanne, Harvey, Nick, Shin, Hyeon Dong, Leyronas, Christel, Nicot, Philippe C., Giraud, Tatiana and Kiss, Levente. 2015. "Host phenology and geography as drivers of differentiation in generalist fungal mycoparasites." PLoS One. 10 (3). https://doi.org/10.1371/journal.pone.0120703
Does the parasite follow its host? Occurrence of morphologically barely distinguishable powdery mildew anamorphs on Oenothera spp. in different parts of the world
Bereczky, Zsolt, Pintye, Alexandra, Csontos, Peter, Braun, Uwe and Kiss, Levente. 2015. "Does the parasite follow its host? Occurrence of morphologically barely distinguishable powdery mildew anamorphs on Oenothera spp. in different parts of the world." Mycoscience. 56 (3), pp. 267-272. https://doi.org/10.1016/j.myc.2014.08.001
First detection of tomato powdery mildew caused by Oidium neolycopersici in South Africa
Lebeda, A., Mieslerova, B., Jankovics, T., Kiss, L. and van der Linde, E. J.. 2015. "First detection of tomato powdery mildew caused by Oidium neolycopersici in South Africa." South African Journal of Botany. 99, pp. 153-157. https://doi.org/10.1016/j.sajb.2015.03.196
Naming and outline of Dothideomycetes–2014 including proposals for the protection or suppression of generic names
Wijayawardene, Nalin N., Crous, Pedro W., Kirk, Paul M., Hawksworth, David L., Boonmee, Saranyaphat, Braun, Uwe, Dai, Dong Qin, D'souza, Melvina J., Diederich, Paul, Dissanayake, Asha, Phookamsak, Rungtiwa, Hyde, Kevin D., Doilom, Mingkhuan, Hongsanan, Singang, Jayawardena, Ruvishika, Liu, Jian-Kui, Manamgoda, Dimuthu S., Thambugala, Kasun M., Wanasinghe, Dhanushka N., ..., Jaklitsch, Walter M.. 2014. "Naming and outline of Dothideomycetes–2014 including proposals for the protection or suppression of generic names." Fungal Diversity. 69 (1), pp. 1-55. https://doi.org/10.1007/s13225-014-0309-2
Fungal planet description sheets: 214-280
Crous, P. W., Shivas, R. G., Quaedvlieg, W., Lombard, L., Groenewald, J. Z., van der Bank, M., Zhang, Y., Summerell, B. A., Guarro, J., Wingfield, M. J., Tan, Y. P., Cano-Lira, J. F., García, D., Marin-Felix, Y., Alvarado, P., Gené, J., Hernández-Restrepo, M., Marin-Felix, Y., Stchigel, A. M., ..., Wong, P. T. W.. 2014. "Fungal planet description sheets: 214-280." Persoonia. 32, pp. 184-306. https://doi.org/10.3767/003158514X682395
Refining a method for ascospore viability testing in overwintering chasmothecia of Erysiphe necator
Vagi, Pal, Caffi, Tito, Vaczy, Kalman Zoltan, Nemeth, Mark Z. and Kiss, Levente. 2016. "Refining a method for ascospore viability testing in overwintering chasmothecia of Erysiphe necator." European Journal of Plant Pathology. 144 (4), pp. 799-802. https://doi.org/10.1007/s10658-015-0797-2
Sporulation rate in culture and mycoparasitic activity, but not mycohost specificity, are the key factors for selecting Ampelomyces strains for biocontrol of grapevine powdery mildew (Erysiphe necator)
Legler, Sara Elisabetta, Pintye, Alexandra, Caffi, Tito, Gulyas, Szilvia, Bohar, Gyula, Rossi, Vittorio and Kiss, Levente. 2016. "Sporulation rate in culture and mycoparasitic activity, but not mycohost specificity, are the key factors for selecting Ampelomyces strains for biocontrol of grapevine powdery mildew (Erysiphe necator)." European Journal of Plant Pathology. 144 (4), pp. 723-736. https://doi.org/10.1007/s10658-015-0834-1
Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range
Kassai-Jager, Edit, Seier, Marion K., Evans, Harry C. and Kiss, Levente. 2016. "Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (Ambrosia artemisiifolia) in its native North American range." European Journal of Plant Pathology. 145 (1), pp. 81-87. https://doi.org/10.1007/s10658-015-0815-4