Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi

Article

Kiss, Levente, Pintye, Alexandra, Kovacs, Gabor M., Jankovics, Tunde, Fontaine, Michael C., Harvey, Nick, Xu, Xiangming, Nicot, Philippe C., Bardin, Marc, Shykoff, Jacqui A. and Giraud, Tatiana. 2011. "Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi." Molecular Ecology. 20 (7), pp. 1492-1507. https://doi.org/10.1111/j.1365-294X.2011.05007.x
Article Title

Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi

ERA Journal ID3289
Article CategoryArticle
AuthorsKiss, Levente (Author), Pintye, Alexandra (Author), Kovacs, Gabor M. (Author), Jankovics, Tunde (Author), Fontaine, Michael C. (Author), Harvey, Nick (Author), Xu, Xiangming (Author), Nicot, Philippe C. (Author), Bardin, Marc (Author), Shykoff, Jacqui A. (Author) and Giraud, Tatiana (Author)
Journal TitleMolecular Ecology
Journal Citation20 (7), pp. 1492-1507
Number of Pages16
Year2011
Place of PublicationUnited Kingdom
ISSN0962-1083
1365-294X
Digital Object Identifier (DOI)https://doi.org/10.1111/j.1365-294X.2011.05007.x
Web Address (URL)http://onlinelibrary.wiley.com/doi/10.1111/j.1365-294X.2011.05007.x/abstract;jsessionid=34FD53A4FFBBA787865C92805B41359E.f02t01
Abstract

Understanding the mechanisms responsible for divergence and specialization of pathogens on different hosts is of fundamental importance, especially in the context of the emergence of new diseases via host shifts. Temporal isolation has been reported in a few plants and parasites, but is probably one of the least studied speciation processes. We studied whether temporal isolation could be responsible for the maintenance of genetic differentiation among sympatric populations of Ampelomyces, widespread intracellular mycoparasites of powdery mildew fungi, themselves plant pathogens. The timing of transmission of Ampelomyces depends on the life cycles of the powdery mildew species they parasitize. Internal transcribed spacer sequences and microsatellite markers showed that Ampelomyces populations found in apple powdery mildew (Podosphaera leucotricha) were genetically highly differentiated from other Ampelomyces populations sampled from several other powdery mildew species across Europe, infecting plant hosts other than apple. While P. leucotricha starts its life cycle early in spring, and the main apple powdery mildew epidemics occur before summer, the fungal hosts of the other Ampelomyces cause epidemics mainly in summer and autumn. When two powdery mildew species were experimentally exposed to Ampelomyces strains naturally occurring in P. leucotricha in spring, and to strains naturally present in other mycohost species in autumn, cross-infections always occurred. Thus, the host-related genetic differentiation in Ampelomyces cannot be explained by narrow physiological specialization, because Ampelomyces were able to infect powdery mildew species they were unlikely to have encountered in nature, but instead appears to result from temporal isolation.

Keywordsbiotrophic pathogens; isolation in time; speciation; tri-trophic interactions
ANZSRC Field of Research 2020310705. Mycology
310599. Genetics not elsewhere classified
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Byline AffiliationsHungarian Academy of Sciences, Hungary
Paris-Sud University, France
Genetic Marker Services, United Kingdom
National Institute of Agricultural Botany, United Kingdom
National Research Institute for Agriculture, Food and Environment (INRAE), France
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
The evolution of species concepts and species recognition criteria in plant pathogenic fungi
Cai, Lei, Giraud, Tatiana, Zhang, Ning, Cai, Guohong, Begerow, Dominik and Shivas, Roger G.. 2011. "The evolution of species concepts and species recognition criteria in plant pathogenic fungi." Fungal Diversity. 50 (1), pp. 121-133. https://doi.org/10.1007/s13225-011-0127-8
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
HAT-P-57b: A Short-period Giant Planet Transiting a Bright Rapidly Rotating A8V Star Confirmed Via Doppler Tomography
Hartman, J. D., Bakos, G. A., Buchhave, L. A., Torres, G., Latham, D. W., Kovacs, G., Bhatti, W., Csubry, Z., de Val-Borro, M., Penev, K., Huang, C. X., Beky, B., Bieryla, A., Quinn, S. N., Howard, A. W., Marcy, G. W., Johnson, J. A., Isaacson, H., Fischer, D. A., ..., Sari, P.. 2015. "HAT-P-57b: A Short-period Giant Planet Transiting a Bright Rapidly Rotating A8V Star Confirmed Via Doppler Tomography." The Astronomical Journal. 150 (6), pp. 1-17. https://doi.org/10.1088/0004-6256/150/6/197
HAT-P-56b: An Inflated Massive Hot Jupiter Transiting a Bright F Star Followed Up with K2 Campaign 0 Observations
Huang, C. X., Hartman, J. D., Bakos, G. A., Penev, K., Bhatti, W., Bieryla, A., de Val-Borro, M., Latham, D. W., Buchhave, L. A., Csubry, Z., Kovacs, G., Beky, B., Falco, E., Berlind, P., Calkins, M. L., Esquerdo, G. A., Lazar, J., Papp, I. and Sari, P.. 2015. "HAT-P-56b: An Inflated Massive Hot Jupiter Transiting a Bright F Star Followed Up with K2 Campaign 0 Observations." The Astronomical Journal. 150 (3), pp. 1-11. https://doi.org/10.1088/0004-6256/150/3/85
HAT-P-44b, HAT-P-45b, and HAT-P-46b: Three Transiting Hot Jupiters in Possible Multi-planet Systems
Hartman, J. D., Bakos, G. A., Torres, G., Kovacs, G., Johnson, J. A., Howard, A. W., Marcy, G. W., Latham, D. W., Bieryla, A., Buchhave, L. A., Bhatti, W., Beky, B., Csubry, Z., Penev, K., de Val-Borro, M., Noyes, R. W., Fischer, D. A., Esquerdo, G. A., Everett, M., ..., Sari, P.. 2014. "HAT-P-44b, HAT-P-45b, and HAT-P-46b: Three Transiting Hot Jupiters in Possible Multi-planet Systems." The Astronomical Journal. 147 (6), pp. 1-18. https://doi.org/10.1088/0004-6256/147/6/128
HATSouth: A Global Network of Fully Automated Identical Wide-Field Telescopes
Bakos, G. A., Csubry, Z., Penev, K., Bayliss, D., Jordan, A., Afonso, C., Hartman, J. D., Henning, T., Kovacs, G., Noyes, R. W., Beky, B., Suc, V., Csak, B., Rabus, M., Lazar, J., Papp, I., Sari, P., Conroy, P., Zhou, G., ..., Ueltzhoeffer, K.. 2013. "HATSouth: A Global Network of Fully Automated Identical Wide-Field Telescopes." Publications of the Astronomical Society of the Pacific. 125 (924), pp. 154-182. https://doi.org/10.1086/669529