A hyperparasite affects the population dynamics of a wild plant pathogen

Article

Tollenaere, C., Pernechele, B., Makinen, H. S., Parratt, S. R., Nemeth, M. Z., Kovacs, G. M., Kiss, L., Tack, A. J. M. and Laine, A.-L.. 2014. "A hyperparasite affects the population dynamics of a wild plant pathogen." Molecular Ecology. 23 (23), pp. 5877-5887. https://doi.org/10.1111/mec.12908
Article Title

A hyperparasite affects the population dynamics of a wild plant pathogen

ERA Journal ID3289
Article CategoryArticle
AuthorsTollenaere, C. (Author), Pernechele, B. (Author), Makinen, H. S. (Author), Parratt, S. R. (Author), Nemeth, M. Z. (Author), Kovacs, G. M. (Author), Kiss, L. (Author), Tack, A. J. M. (Author) and Laine, A.-L. (Author)
Journal TitleMolecular Ecology
Journal Citation23 (23), pp. 5877-5887
Number of Pages11
Year2014
Place of PublicationUnited Kingdom
ISSN0962-1083
1365-294X
Digital Object Identifier (DOI)https://doi.org/10.1111/mec.12908
Web Address (URL)http://onlinelibrary.wiley.com/doi/10.1111/mec.12908/pdf
Abstract

Assessing the impact of natural enemies of plant and animal pathogens on their host's population dynamics is needed to determine the role of hyperparasites in affecting disease dynamics, and their potential for use in efficient control strategies of pathogens. Here, we focus on the long-term study describing metapopulation dynamics of an obligate pathogen, the powdery mildew (Podosphaera plantaginis) naturally infecting its wild host plant (Plantago lanceolata) in the fragmented landscape of the Åland archipelago (southwest Finland). Regionally, the pathogen persists through a balance of extinctions and colonizations, yet factors affecting extinction rates remain poorly understood. Mycoparasites of the genus Ampelomyces appear as good candidates for testing the role of a hyperparasite, i.e. a parasite of other parasites, in the regulation of their fungal hosts' population dynamics. For this purpose, we first designed a quantitative PCR assay for detection of Ampelomyces spp. in field-collected samples. This newly developed molecular test was then applied to a large-scale sampling within the Åland archipelago, revealing that Ampelomyces is a widespread hyperparasite in this system, with high variability in prevalence among populations. We found that the hyperparasite was more common on leaves where multiple powdery mildew strains coexist, a pattern that may be attributed to differential exposure. Moreover, the prevalence of Ampelomyces at the plant level negatively affected the overwinter survival of its fungal host. We conclude that this hyperparasite may likely impact on its host population dynamics and argue for increased focus on the role of hyperparasites in disease dynamics.

Keywordsdisease; hyperparasite; metapopulation; molecular detection; plant pathogen; regulation; Ascomycota; fungal DNA; DNA, ribosomal spacer; Finland; host-pathogen interactions; plant diseases; Plantago; population dynamics; applied microbiology and biotechnology; microbial diseases and parasites; plant pathology; fungal pathogens and diseases; plant science; biochemistry; molecular biology; plant/microbe interactions; plant science; plant pathology and symbioses; plant pathology; fungi - general;
ANZSRC Field of Research 2020310704. Microbial genetics
310805. Plant pathology
310705. Mycology
410404. Environmental management
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Byline AffiliationsUniversity of Helsinki, Finland
Hungarian Academy of Sciences, Hungary
Institution of OriginUniversity of Southern Queensland
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Li, Chengwei, Faino, Luigi, Dong, Lin, Fan, Junmei, Kiss, Levente, de Giovanni, Claudio, Lebeda, Ales, Scott, John, Matsuda, Yoshinori, Toyoda, Hideyoshi, Lindhout, Pim, Visser, Richard G. F., Bonnema, Guusje and Bai, Yuling. 2012. "Characterization of polygenic resistance to powdery mildew in tomato at cytological, biochemical and gene expression level." Molecular Plant Pathology. 13 (2), pp. 148-159. https://doi.org/10.1111/j.1364-3703.2011.00737.x
Variation in the nrDNA ITS sequences of some powdery mildew species: do routine molecular identification procedures hide valuable information?
Kovacs, Gabor M., Jankovics, Tunde and Kiss, Levente. 2011. "Variation in the nrDNA ITS sequences of some powdery mildew species: do routine molecular identification procedures hide valuable information?" European Journal of Plant Pathology. 131 (1), pp. 135-141. https://doi.org/10.1007/s10658-011-9793-3
First comprehensive phylogenetic analysis of the genus Erysiphe (Erysiphales, Erysiphaceae) I. The Microsphaera lineage
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
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