Ampelomyces strains isolated from diverse powdery mildew hosts in Japan: Their phylogeny and mycoparasitic activity, including timing and quantifying mycoparasitism of Pseudoidium neolycopersici on tomato

Article


Nemeth, Mark Z., Mizuno, Yuusaku, Kobayashi, Hiroki, Seress, Diana, Shishido, Naruki, Kimura, Yutaka, Takamatsu, Susumu, Suzuki, Tomoko, Takikawa, Yoshihiro, Kakutani, Koji, Matsuda, Yoshinori, Kiss, Levente and Nonomura, Teruo. 2021. "Ampelomyces strains isolated from diverse powdery mildew hosts in Japan: Their phylogeny and mycoparasitic activity, including timing and quantifying mycoparasitism of Pseudoidium neolycopersici on tomato." PLoS One. 16 (5), pp. 1-20. https://doi.org/10.1371/journal.pone.0251444
Article Title

Ampelomyces strains isolated from diverse powdery mildew hosts in Japan: Their phylogeny and mycoparasitic activity,
including timing and quantifying mycoparasitism of Pseudoidium neolycopersici on tomato

ERA Journal ID39745
Article CategoryArticle
AuthorsNemeth, Mark Z. (Author), Mizuno, Yuusaku (Author), Kobayashi, Hiroki (Author), Seress, Diana (Author), Shishido, Naruki (Author), Kimura, Yutaka (Author), Takamatsu, Susumu (Author), Suzuki, Tomoko (Author), Takikawa, Yoshihiro (Author), Kakutani, Koji (Author), Matsuda, Yoshinori (Author), Kiss, Levente (Author) and Nonomura, Teruo (Author)
Journal TitlePLoS One
Journal Citation16 (5), pp. 1-20
Article Numbere0251444
Number of Pages20
Year2021
PublisherPublic Library of Science (PLoS)
Place of PublicationUnited States
ISSN1932-6203
Digital Object Identifier (DOI)https://doi.org/10.1371/journal.pone.0251444
Web Address (URL)https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0251444
Abstract

A total of 26 Ampelomyces strains were isolated from mycelia of six different powdery mildew species that naturally infected their host plants in Japan. These were characterized based on morphological characteristics and sequences of ribosomal DNA internal transcribed spacer (rDNA-ITS) regions and actin gene (ACT) fragments. Collected strains represented six different genotypes and were accommodated in three different clades of the genus Ampelomyces. Morphology of the strains agreed with that of other Ampelomyces strains, but none of the examined characters were associated with any groups identified in the genetic analysis. Five powdery mildew species were inoculated with eight selected Ampelomyces strains to study their mycoparasitic activity. In the inoculation experiments, all Ampelomyces strains successfully infected all tested powdery mildew species, and showed no significant differences in their mycoparasitic activity as determined by the number of Ampelomyces pycnidia developed in powdery mildew colonies. The mycoparasitic interaction between the eight selected Ampelomyces strains and the tomato powdery mildew fungus (Pseudoidium neolycopersici strain KTP-03) was studied experimentally in the laboratory using digital microscopic technologies. It was documented that the spores of the mycoparasites germinated on tomato leaves and their hyphae penetrated the hyphae of Ps. neolycopersici. Ampelomyces hyphae continued their growth internally, which initiated the atrophy of the powdery mildew conidiophores 5 days post inoculation (dpi); caused atrophy 6 dpi; and complete collapse of the parasitized conidiphores 7 dpi. Ampelomyces strains produced new intracellular pycnidia in Ps. neolycopersici conidiophores ca. 8–10 dpi, when Ps. neolycopersici hyphae were successfully destroyed by the mycoparasitic strain. Mature pycnidia released spores ca. 10–14 dpi, which became the sources of subsequent infections of the intact powdery mildew hyphae. Mature pycnidia contained each ca. 200 to 1,500 spores depending on the mycohost species and Ampelomyces strain. This is the first detailed analysis of Ampelomyces strains isolated in Japan, and the first timing and quantification of mycoparasitism of Ps. neolycopersici on tomato by phylogenetically diverse Ampelomyces strains using digital microscopic technologies. The developed model system is useful for future biocontrol and ecological studies on Ampelomyces mycoparasites.

Keywordsmycoparasitism; phylogeny; powdery mildew; tomato
ANZSRC Field of Research 2020310705. Mycology
Public Notes

Copyright: © 2021 Nemeth et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Byline AffiliationsHungarian Academy of Sciences, Hungary
Kindai University, Japan
Centre for Agricultural Research, Hungary
Mie University, Japan
Tohoku University, Japan
Institution of OriginUniversity of Southern Queensland
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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
New insight into photosynthetic acclimation to elevated CO2: the role of leaf nitrogen and ribulose-1,5-bisphosphate carboxylase/oxygenase content in rice leaves
Seneweera, Saman, Makino, Amane, Hirotsu, Naoki, Norton, Robert and Suzuki, Yuji. 2011. "New insight into photosynthetic acclimation to elevated CO2: the role of leaf nitrogen and ribulose-1,5-bisphosphate carboxylase/oxygenase content in rice leaves ." Environmental and Experimental Botany. 71 (2), pp. 128-136. https://doi.org/10.1016/j.envexpbot.2010.11.002