Green fluorescent protein transformation sheds more light on a widespread mycoparasitic interaction

Article

Nemeth, Mark Z., Pintye, Alexandra, Horvath, Aron N., Vagi, Pal, Kovacs, Gabor M., Gorfer, Markus and Kiss, Levente. 2019. "Green fluorescent protein transformation sheds more light on a widespread mycoparasitic interaction." Phytopathology: International Journal of the American Phytopathological Society. 109 (8), pp. 1404-1416. https://doi.org/10.1094/PHYTO-01-19-0013-R
Article Title

Green fluorescent protein transformation sheds more light on a widespread mycoparasitic interaction

ERA Journal ID2639
Article CategoryArticle
AuthorsNemeth, Mark Z. (Author), Pintye, Alexandra (Author), Horvath, Aron N. (Author), Vagi, Pal (Author), Kovacs, Gabor M. (Author), Gorfer, Markus (Author) and Kiss, Levente (Author)
Journal TitlePhytopathology: International Journal of the American Phytopathological Society
Journal Citation109 (8), pp. 1404-1416
Number of Pages13
Year2019
PublisherAmerican Phytopathological Society
Place of PublicationUnited States
ISSN0031-949X
1943-7684
Digital Object Identifier (DOI)https://doi.org/10.1094/PHYTO-01-19-0013-R
Web Address (URL)https://apsjournals.apsnet.org/doi/10.1094/PHYTO-01-19-0013-R
Abstract

Powdery mildews, ubiquitous obligate biotrophic plant pathogens, are often attacked in the field by mycoparasitic fungi belonging to the genus Ampelomyces. Some Ampelomyces strains are commercialized biocontrol agents of crop pathogenic powdery mildews. Using Agrobacterium tumefaciens-mediated transformation (ATMT), we produced stable Ampelomyces transformants that constitutively expressed green fluorescent protein (GFP) to (i) improve the visualization of the mildew–Ampelomyces interaction and (ii) decipher the environmental fate of Ampelomyces fungi before and after acting as a mycoparasite. Detection of Ampelomyces structures, and especially hyphae, was greatly enhanced when diverse powdery mildew, leaf, and soil samples containing GFP transformants were examined with fluorescence microscopy compared with brightfield and differential interference contrast optics. We showed for the first time, to our knowledge, that Ampelomyces strains can persist up to 21 days on mildew-free host plant surfaces, where they can attack powdery mildew structures as soon as these appear after this period. As saprobes in decomposing, powdery mildew-infected leaves on the ground and also in autoclaved soil, Ampelomyces strains developed new hyphae but did not sporulate. These results indicate that Ampelomyces strains occupy a niche in the phyllosphere where they act primarily as mycoparasites of powdery mildews. Our work has established a framework for a molecular genetic toolbox for the genus Ampelomyces using ATMT.

Keywordstritrophic interactions; GFP transformation; powdery mildew; plant pathology
ANZSRC Field of Research 2020310705. Mycology
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Byline AffiliationsHungarian Academy of Sciences, Hungary
Eotvos Lorand University (ELTE), Hungary
University of Natural Resources and Life Sciences, Austria
Centre for Crop Health
Institution of OriginUniversity of Southern Queensland
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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
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