Characterization of Cytospora species involved in grapevine decline disease complex in Miyandoab and Malekan Counties

Document Type : Research Article

Authors

1 Department of Plant Protection, Faculty of Agriculture, Urmia University, Iran

2 Higher Education Center Shahid Bakeri Miyandoab, Urmia University, Miyandoab, Iran.

3 Department of plant protection, Faculty of Agriculture, University of Urmia, Iran

Abstract

Grapevine decline disease (GDD) complex is a major global viticulture problem associated with a multi-year decrease in plant productivity and an increase in vine mortality, resulting in important economic losses to the viticulture industry. More than 35 fungal genera have been involved in the GDD complex, and the genus Cytospora has also been reported as one of the genera included in the disease-causing complex. This study aimed to identify Cytospora species involved in GDD complex in the vineyards of Miyandoab (West Azarbaijan province) and Malekan (East Azarbaijan province) Counties. So, during the summer and autumn of 2020-2021, sampling was done from the diseased plants showing symptoms of shoot wilting and die-back, bark and wood discoloration, brown to black discoloration of vascular tissues, and wood canker. The fungal isolation was done based on common phytopathological methods, and 78 isolates with the common characteristics of the genus Cytospora were isolated and purified. Based on the results combining morphological characteristics and sequence data obtained from three genomic regions, ITS-rDNA, TUB2, and RPB2, four species viz., C. chrysosperma (15 isolates), C. ershadii (24 isolates), C. salicina (28 isolates), and C. viticola (11 isolates) were identified. Cytospora viticola is a new species for the fungal biota of Iran, and grapevine is reported as a new host (matrix nova) for C. ershadii in Iran and the world. Pathogenicity of the selected fungal isolates from the identified species was confirmed on shoots of the Thompson seedless cultivar based on Koch's postulates.

Keywords


Adams, G.C., Roux, J. and Wingfield, M.J. 2006. Cytospora species (Ascomycota, Diaporthales, Valsaceae): introduced and native pathogens of trees in South Africa. Australasian Plant Pathology 35: 521–548.
Adams, G.C., Wingfield, M.J., Common, R. and Roux, J. 2005. Phylogenetic relationships and morphology of Cytospora species and related teleomorphs (Ascomycota, Diaporthales, Valsaceae) from Eucalyptus. Studies in Mycology 52: 1–144.
Ahmadpour, A., Ghosta, Y. and Poursafar, A. 2021. Novel species of Alternaria section Nimbya from Iran as revealed by morphological and molecular data. Mycologia 113: 1073–1088.
Akgül, D.S., Güngör Savaş, N., Yildiz, M., Bülbül, İ. and Özarslandan M. 2023. Current status of grapevine trunk disease pathogens on asymptomatic nursery-produced grapevines in Türkiye. Phytopathologia Mediterranea 62: 151–163.
Alston, J.M. and Sambucci, O. 2019. Grapes in the world economy. pp. 1–24. In: Cantu, D. and Walker, M.A. (eds). The Grape Genome, Compendium of Plant Genomes. Springer Nature Switzerland, AG.
Altschul S.F., Madden T.L., Schaffer AA., Zhang J., Miller W. and Lipman D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389–3402.
Anonymous. 2021. Agricultural statistics of 2019. Third volume: horticultural products. Ministry of Agricultural Jihad, Planning and Economic Deputy, Information and Communication Technology Center. 164 pages.
Arzanlou, M. and Narmani, A. 2015. ITS sequence data and morphology differentiate Cytospora chrysosperma associated with trunk disease of grapevine in northern Iran. Journal of Plant Protection Research 55: 117–125.
Azizi, R., Ghosta, Y. and Ahmadpour, A. 2020. Morphological and molecular characterization of Cytospora species involved in apple decline in Iran. Mycologia Iranica 7: 205–218.
Azizi, R., Ghosta, Y. and Ahmadpour, A. 2024. Apple crown and collar canker and necrosis caused by Cytospora balanejica sp. nov. in Iran. Scientific Reports 14: 6629.
Bahmani, Z., Abdollahzadeh, J., Amini, J. and Evidente, A. 2021. Biscogniauxia rosacearum the charcoal canker agent as a pathogen associated with grapevine trunk diseases in Zagros region of Iran. Scientific Reports 11: 14098.
Bettenfeld, P., Fontaine, F., Trouvelot, S., Fernandez, O. and Courty, P.E. 2020. Woody plant declines. what’s wrong with the microbiome? Trends in Plant Science 25(4): 381–394.
Bills, G.F. 1996. Isolation and analysis of endophytic fungal communities from woody plants. pp. 31–65. In: Redlin, S.C. and Carris, L.M. (eds). Endophytic fungi in grasses and woody plants: systematics, ecology, and evolution. American Phytopathological Society Press, St. Paul, Minnesota, USA.
Bois, B., Zito, S. and Calonnec, A. 2017. Climate vs grapevine pests and diseases worldwide: the first results of a global survey. OENO one 51(2-3): 133–139.
Burgess, T.I., Barber, P.A. and Hardy, G.E. 2005. Botryosphaeria spp. associated with eucalypts in Western Australia, including the description of Fusicoccum macroclavatum sp. nov. Australasian Plant Pathology 34: 557–567.
Bustamante, M.I., Elfar, K., Smith, R.J., Bettiga, L.J., Tian, T., Torres, G.A. and Eskalen, A. 2022. First report of Fusarium annulatum associated with young vine decline in California. Plant Disease 106: 2752.
Carbone, I. and Kohn, L.M. 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91: 553–556.
Carbone, M.J., Gelabert, M., Moreira, V., Mondino, P. and Alaniz, S. 2022. Grapevine nursery propagation material as source of fungal trunk disease pathogens in Uruguay. Frontiers in Fungal Biology 3: 958466.
Chang, L.S., Iezzoni, A.F., Adams, G.C. and Ewers, F.W. 1991. Hydraulic conductance in susceptible versus tolerant peach seedlings infected with Leucostoma persoonii. Journal of the American Society for Horticultural Science 116: 831–834.
Creasy, G.L. and Creasy, L.L. 2018. Grapes. 2nd ed. CABI International, Walligford, UK. 396 p.
Darriaut, R., Tran, J., Martins, G., Ollat, N., Masneuf-Pomarède, I. and Lauvergeat, V. 2023. In grapevine decline, microbiomes are affected differently in symptomatic and asymptomatic soils. Applied Soil Ecology 183: 104767.
DeKrey, D.H., Klodd, A.E., Clark, M.D. and Blanchette, R.A. 2022. Grapevine trunk diseases of cold-hardy varieties grown in northern Midwest vineyards coincide with canker fungi and winter injury. PloS One 17: e0269555.
Donk, M.A. 1964. Nomina conservanda proposita 1. Proposals in fungi. Deuteromycetes. Regnum Vegetabile 34: 7–15.
Fan, X., Hyde, K.D., Liu, M., Liang, Y. and Tian, C. 2015. Cytospora species associated with walnut canker disease in China, with description of a new species C. gigalocus. Fungal Biology 119: 310–319.
Fan, X.L., Bezerra, J.D.P., Tian, C.M. and Crous, P.W. 2020. Cytospora (Diaporthales) in China. Persoonia 45: 1–45.
Fan, X.L., Tian, C.M., Yang, Q., Liang, Y.M., You, C.J. and Zhang, Y.B. 2014. Cytospora from Salix in Northern China. Mycotaxon 129: 303–315.
FAOSTAT. 2024. Food and Agriculture Organization of the United Nations. Retrieved from http://faostat.fao.org, Accessed June 10, 2024.
Fischer, M. and Peighami Ashnaei, S. 2019. Grapevine, esca complex, and environment: the disease triangle. Phytopathologia Mediterranea 58: 17–37.
Fotouhifar, K.B., Hedjaroude, Gh.A. and Leuchtmann, A. 2010. ITS rDNA phylogeny of Iranian strains of Cytospora and associated teleomorphs. Mycologia 102: 1369–1382.
Giménez-Jaime, A., Aroca, A., Raposo, R., García-Jiménez, J. and Armengol, J. 2006. Occurrence of fungal pathogens associated with grapevine nurseries and the decline of young vines in Spain. Journal of Phytopathology 154: 598–602.
Glass, N.L. and Donaldson, G.C. 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology 61: 1323–1330.
Gonzalez, V. and Tello, M.L. 2011. The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Diversity 47: 29–42.
Gramaje, D., Úrbez-Torres, J.R. and Sosnowski, M.R., 2018. Managing grapevine trunk diseases with respect to etiology and epidemiology: Current strategies and future prospects. Plant Disease 102: 12–39.
Guarnaccia, V., Kraus, C., Markakis, E., Alves, E., Armengol, J., Eichmeier, A., Compant, S. and Gramaje, D. 2022. Fungal trunk diseases of fruit trees in Europe: pathogens, spread and future directions. Phytopathologia Mediterranea 61: 563–599.
Guerin-Dubrana, L., Fontaine, F. and Mugnai, L. 2019. Grapevine trunk disease in European and Mediterranean vineyards: occurrence, distribution and associated disease-affecting cultural factors. Phytopathologia Mediterranea 58: 49–71.
Haavik, L.J., Billings, S.A., Guldin, J.M. and Stephen, F.M. 2015. Emergent insects, pathogens and drought shape changing patterns in oak decline in North America and Europe. Forest Ecology and Management 354: 190–205.
Hanifeh, S., Zafari, D., Soleimani, M.J. and Arzanlou, M. 2022. Multigene phylogeny, morphology, and pathogenicity trials reveal novel Cytospora species involved in perennial canker disease of apple trees in Iran. Fungal Biology 126: 707–726.
Hayova, V.P. and Minter, D.V. 1998. Leucostoma persoonii. IMI Descriptions of Fungi and Bacteria. Set 137, No. 1367, CAB International, UK.
Hergholi, N., Ghosta, Y., Javan-Nikkhah, M., Campisano, A. and Pancher, M. 2015. New species of endophytic fungi from grapevine (Vitis vinifera) in Iran. Rostaniha 16: 17–35.
Hibben, C.R. 1962. Investigations of sugar maple decline in New York woodlands. Ph.D. Thesis, Cornell University. 301 p.
Holland, L., Grove, G.G. and Glawe, D.A. 2015. Washington grapevine trunk disease survey. Viticulture and Enology Extension News 2015: 4.
Hrycan, J., Hart, M., Bowen, P., Forge, T. and and Úrbez-Torres, J.R. 2020. Grapevine trunk disease fungi: their roles as latent pathogens and stress factors that favour disease development and symptom expression. Phytopathologia Mediterranea 59: 395–424.
Ilyukhin, E., Nguyen, H.D.T., Castle, A.J. and Ellouze, W. 2023. Cytospora paraplurivora sp. nov. isolated from orchards with fruit tree decline syndrome in Ontario, Canada. PLoS ONE 18(1): e0279490.
Kanetis, L., Taliadoros, D., Makris, G. and Christoforou, M. 2022. A novel Seimatosporium and other Sporocadaceae species associated with grapevine trunk diseases in Cyprus. Plants 11: 2733.
Katoh K., Rozewicki J. and Yamada K.D. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 108: 1–7.
Kenfaoui, J., Radouane, N., Mennani, M., Tahiri, A., El Ghadraoui, L., Belabess, Z., Fontaine, F., El Hamss, H., Amiri, S., Lahlali, R. and Barka, E.A. 2022. A panoramic view on grapevine trunk diseases threats: case of Eutypa dieback, Botryosphaeria dieback, and Esca disease. Journal of Fungi 8: 595.
Lawrence, D.P., Holland, L.A., Nouri, M.T., Travadon, R., Abramians, A., Michailides, T.J. and Trouillas, F.P. 2018. Molecular phylogeny of Cytospora species associated with canker diseases of fruit and nut crops in California, with the descriptions of ten new species and one new combination. IMA Fungus 9: 330–370.
Lawrence, D.P., Travadon, R., Pouzoulet, J., Rolshausen, P.E., Willcox, W.F. and Baumgartner, K. 2017. Characterization of Cytospora isolates from wood cankers of declining grapevine in North America, with the descriptions of two new Cytospora species. Plant Pathology 66: 713–725.
Li, J.R., Li, J.T., and Jiang, N. 2024b. Morphology and phylogeny of Cytospora (Cytosporaceae, Diaporthales) species associated with plant cankers in Tibet, China. Mycokeys, 104: 51–70.
Li, J.T., Li, J.R. and Jiang, N. 2024a. Identification of Cytospora species isolated from branch canker diseases of woody plants in Tibet, China. Forests, 15: 121.
Liu, Y.J., Whelen, S. and Hall, B.D. 1999. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16: 1799–1808.
Luque, J.D., Sierra, E., Torres, E, and Garcia, F. 2006. Cryptovalsa ampelina on grapevines in N.E. Spain: identification and pathogenicity. Phytopathology Mediterranea 45: 101–109.
Merot, A., Coulouma, G., Smits, N., Robelot, E., Gary, C., Dubrana, L.G., Poulmarch, J., Burgun, X., Pellegrino, A. and Fermaud, M. 2023. A sysetmic approach to grapevine decline diagnosed using three key indicators: plant mortality, yield loss and vigor decrease. OENO One 57: 133–149.
Meza, L., Deyett, E., Vallance, J., Gendre, L., Garcia, J.F., Cantu, D., Rey, P., Lecomte, P. and Rolshausen, P.E. 2024. Grapevine pruning strategy affects trunk disease symptoms, wood pathobiome and mycobiome. Phytopathologia Mediterranea 63: 91–102.
Mohammadi, H., Banihashemi, Z., Gramaje, D. and Armengol, J. 2013. Fungal pathogens associated with grapevine trunk diseases in Iran. Journal of Agricultural Science and Technology 15: 137–150.
Morton, L. 2000. Viticulture and grapevine declines: lessons of black goo. Phythopathologia Mediteranea 39: 59–67.
Mugnai, L., Graniti, A. and Surico, G. 1999. Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease 83: 404–418.
Nabi, A., Shah, M.U.D., Padder, B.A. and Ahmad, M. 2018. Morpho-cultural, pathological and molecular variability in Thyrostroma carpophilum causing shot hole of stone fruits in India. European Journal of Plant Pathology 151: 613–627.
Norphanphoun, C., Doilom, M., Daranagama, D.A., Phookamsak, R., Wen, T.C., Bulgakov, T.S. and Hyde, K.D. 2017. Revisiting the genus Cytospora and allied species. Mycosphere 8: 51–97.
Nylander J.A.A. 2004. MrModeltest v2.0. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
Oksal, E., Çelik, Y. and Özer, G. 2020. First report of canker and dieback caused by Cytospora viticola on grapevine in Turkey. Journal of Plant Pathology 102: 239.
Pan, M., Zhu, H., Liang, L., Tian, C. and Fan, X. 2021a. Studies of canker and dieback of oak tree in China, with two Cytospora species described. Plant Pathology 70: 2005–2015.
Pan, M., Zhu, H., Tian, C., Huang, M. and Fan, X. 2021b. Assessment of Cytospora isolates from conifer cankers in China, with the descriptions of four new Cytospora species. Frontiers in Plant Sciences 12: 636460.
Phillips A.J.L. 2002. Botryosphaeria species associated with diseases of grapevines in Portugal. Phytopathology Mediterranea 41: 3–18.
Raimondo, M.L., Carlucci, A., Ciccarone, C., Sadallah, A. and Lops, F. 2019. Identification and pathogenicity of lignicolous fungi associated with grapevine trunk diseases in Southern Italy. Phytopathologia Mediterranea 58: 639–662.
Rambaut A. 2019. FigTree, a graphical viewer of phylogenetic trees. Available from: http://tree.bio.ed.ac.uk/software/figtree.
Rayner, R.W. 1970. A Mycological Colour Chart. Kew: Commonwealth Mycological Institute, UK.
Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A. and Huelsenbeck J.P. 2012. MrBayes 3: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.
Scheck, H.J., Vasquez, S.J. and Gubler, W.D. 1998. First report of three Phaeoacremonium spp. causing grapevine decline in California. Plant Disease 8: 590.
Senanayake, I.C., Crous, P.W., Groenewald, J.Z., Maharachchikumbura, S.S., Jeewon, R., Phillips, A.J., Bhat, J.D., Perera, R.H., Li, Q.R., Li, W.J. and Tangthirasunun, N. 2017. Families of Diaporthales based on morphological and phylogenetic evidence. Studies in Mycology 86: 217–296.
Sinclair, W.A. 1965. Comparisons of recent declines of white ash, oaks, and sugar maple in northeastern woodlands. Cornell Plant 20: 62–67.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
Stukenbrock, E.V. and Mc Donald, B.A. 2008. The origin of plant pathogen in agro-ecosystems. Annual Review of Phytopathology 46: 75–100.
Sung, G.H., Sung, J.M., Hywel-Jones, N.L. and Spatafora, J.W. 2007. A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Molecular Phylogenetics and Evolution 44: 1204–1223.
Swofford, D.L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other methods). version 4. Sinauer Associates, Sunderland, Massachusetts.
Tamura, K., Dudley, J., Nei, M. and Kumar, S. 2007. MEGA6: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.
Testempasis, S.I., Markakis, E.A., Tavlaki, G.I., Soultatos, S.K., Tsoukas, C., Gkizi, D., Tzima, A.K., Paplomatas, E. and Karaoglanidis, G.S. 2024. Grapevine trunk diseases in Greece: disease incidence and fungi involved in discrete geographical zones and varieties. Journal of Fungi 10: 2.
Travadon, R., Lawrence, D.P., Moyer, M., Fujiyoshi, P.T. and Baumgartner, K. 2022. Fungal species associated with grapevine trunk diseases in Washington wine grapes and California table grapes, with novelties in the genera Cadophora, Cytospora, and Sporocadus. Frontiers in Fungal Biology, 3: 1018140.
Úrbez-Torres, J.R., Boulé, J., Hrycan, J. and O’Gorman, D.T. 2023. Potential role of Fusarium spp. in grapevine decline. Phytopathologia Mediterranea 62: 269–281.
Van Niekerk J.M., Crous P.W., Groenewald J.Z., Fourie P.H. and Halleen F. 2004. DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96: 781–798.
Van Niekerk, J.M., Groenewald, J.Z., Farr, D.F., Fourie, P., Hallen, H.F. and Crous, P.W. 2005. Reassessment of Phomopsis species on grapevines. Australasian Plant Pathology 34: 27–39.
Wang, X.L., Kang, Z.S., Huang, L.L. and Wei, J. 2011. Re-evaluation of pathogens causing Valsa canker on apple in China. Mycologia 103: 317–324.
White, T.J., Bruns, T., Lee, S.J.W.T. and Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. pp. 315–322. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J. (eds.), PCR protocols: a guide to methods and applications. New York: Academic Press.
Zhu, H., Pan, M., Bezerra, J.D.P., Tian, C. and Fan, X. 2020. Discovery of Cytospora species associated with canker disease of tree hosts from Mount Dongling of China. Mycokeys 62: 97–121.