Revisiting the intron hypothesis of QoI resistance in Phyllosticta ampelicida, the causal agent of grape black rot, and other Phyllosticta species

Article

Horvath, Áron N., Molnar, Orsolya, Nemeth, Márk Z., Pintye, Alexandra, Dankó, Tamás, Spitzmüller, Zsolt, Vaczy, Zsuzsanna, Vaczy, Kálmán Z., Onesti, Giovanni, Reis, Pedro, Rego, Cecilia, Bereczky, Zsolt, Kiss, Levente and Kovacs, Gábor M.. 2024. "Revisiting the intron hypothesis of QoI resistance in Phyllosticta ampelicida, the causal agent of grape black rot, and other Phyllosticta species." Plant Pathology. 73 (6), pp. 1491-1505. https://doi.org/10.1111/ppa.13912
Article Title

Revisiting the intron hypothesis of QoI resistance in Phyllosticta ampelicida, the causal agent of grape black rot, and other Phyllosticta species

ERA Journal ID2652
Article CategoryArticle
AuthorsHorvath, Áron N., Molnar, Orsolya, Nemeth, Márk Z., Pintye, Alexandra, Dankó, Tamás, Spitzmüller, Zsolt, Vaczy, Zsuzsanna, Vaczy, Kálmán Z., Onesti, Giovanni, Reis, Pedro, Rego, Cecilia, Bereczky, Zsolt, Kiss, Levente and Kovacs, Gábor M.
Journal TitlePlant Pathology
Journal Citation73 (6), pp. 1491-1505
Number of Pages15
Year2024
PublisherJohn Wiley & Sons
ISSN0032-0862
1365-3059
Digital Object Identifier (DOI)https://doi.org/10.1111/ppa.13912
Web Address (URL)https://bsppjournals.onlinelibrary.wiley.com/doi/10.1111/ppa.13912
AbstractChemical control of grape black rot, caused by Phyllosticta ampelicida, relies mainly on the use of demethylation inhibitors (DMIs) and quinone outside inhibitors (QoIs). The effectiveness of QoI fungicides is influenced by alternative respiration activity, and the exon/intron structure and point mutations in the target protein's gene, the cytochrome b (cytb) gene. Our study aims to investigate the QoI fungicide sensitivity of 48 P. ampelicida isolates in vitro by measuring EC50 and the molecular characteristics of the cytb gene and its mRNA in P. ampelicida and other Phyllosticta species. Mycelial growth tests revealed that the P. ampelicida isolates were sensitive to both azoxystrobin and trifloxystrobin; baseline EC50 values were 0.029 and 0.022 μg/mL, respectively. Addition of salicylhydroxamic acid (SHAM) resulted in lower EC50 values (0.024 and 0.017 μg/mL, respectively). None of the typical point mutations conferring resistance to QoIs in some fungi were detected. A group I intron was present right after the 143rd codon in the cytb gene in four of the six Phyllosticta species examined. The sequence and exon/intron structure of the cytb gene of P. ampelicida isolated from Vitis vinifera is studied in detail and published here. Our results indicate a low risk of QoI resistance development via the G143A mutation in P. ampelicida.
Keywordsalternative oxidase; cytochrome b; fungicide resistance; grape black rot; Guignardia bidwelli; strobilurins
Contains Sensitive ContentDoes not contain sensitive content
ANZSRC Field of Research 2020300409. Crop and pasture protection (incl. pests, diseases and weeds)
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Byline AffiliationsHUN-REN Centre for Agricultural Research, Hungary
Eszterházy Károly Catholic University, Hungary
Catholic University of the Sacred Heart, Italy
University of Lisbon, Portugal
Centre for Crop Health
Eotvos Lorand University (ELTE), Hungary
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Characterization of polygenic resistance to powdery mildew in tomato at cytological, biochemical and gene expression level
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
A hyperparasite affects the population dynamics of a wild plant pathogen
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