Isolation and Identification of Endophytic and Grape Trunk Diseases Associated Fungi in Zanjan Province

Document Type : Research Paper

Authors

1 Department of plant disease Varmin-Pishva Branch, Islamic Azad University, Varamin-Pishva, Tehran, Iran

2 Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension (AREEO), Tehran, Iran.

10.22092/bcpp.2022.128596

Abstract

Endophytic and grapevine trunk diseases associated fungi were isolated from Zanjan province and their inhibitory effect on 2 grapevine fungal pathogens Cytospora chrysosperma and Fusarium sp. was investigated. A total of 95 fungal isolates were isolated, of which 63/54% were from healthy and 36.45% were from diseased tissues. Using strong disinfection steps, probability of isolation of saprophytic fungi was decreased to minimum; So, the fungi isolated from healthy and infected tissues considered as endophytes and grapevine trunk diseases associated fungi, respectively. Preliminary molecular identification of 13 representative isolates in terms of morphological characteristics was performed using nucleotide sequencing of ITS–rDNA region was done and 10 genera were identified. The taxa of Alternaria malorum, Alternaria sp., Allocanariomyces tritici, Aaosphaeria arxii, Clonostachys rosea, Chaetomium sp., Daldinia loculata, Daldinia sp., Fusarium oxysporum, Fusarium sp., Macrophomina phaseolina, Phaeoacremonium minimum and Stromatinia narciss were identified. Pathogenicity of A. tritici, C. rosea and F. oxysporum was confirmed. Antagonistic activity of 13 fungal isolates against pathogenic fungi of grapevine trunk diseases (GTDs) including C. chrysosperma and Fusarium sp. using dual–culture method showed that species of F. oxysporum, P. minimum and C. rosea had the greatest potential as biocontrol agents. In this study, two species of A. arxii and S. narcissi were isolated from healthy grape tissue and to the best of our knowledge; are reported for the first time as endophytic fungi of grapevine trees in the world. D. loculata was isolated from infected tissues of grape trunk and is reported for the first time as a fungi associated with grapevine trunk diseases from the world. Moreover, the pathogenicity of A. tritici and F. oxysporum, was proved in green house condition and are reported for the first time as grapevine pathogens from the world.

References

Abed Ashtiani, F., Narmani, A. & Arzanlou, M. 2018. Macrophomina phaseolina associated with grapevine decline in Iran. Phytopathologia Mediterranea, 57(1): 107–111.
Adalat, K., Whiting, C., Rooney, S. & Gubler, W.D. 2000. Pathogenicity of three Phaeoacremonium spp. on grapevine in California. Phytopathologia Mediterranea, 39(1): 92–99.
Ahmadi, K., Abedzadeh, H., Hatami, F., Mohammadnia, Afroze, Sh., Abbas Taghani, R. Yare, Sh. & Kalantare, M. 2021. Agricultural Statistics of 2020 Horticultural Products 3, 157 pp. (In Persian with English summary).
Akgül, D.S. & Ahioğlu, M. 2019. Fungal pathogens associated with young grapevine decline in the Southern Turkey vineyards: Proceedings of the 42nd World Congress of Vine and Wine, July 15–19, Geneva, Switzerland.
Amarloo, O.A., Tajick Ghanbary, M.A., Mohammadi, H. & Mahdian, S.A. 2020. Identification and pathogenicity of fungal species associated with grapevine trunk diseases in Khorasan–Razavi province, Iran. Mycologia Iranica, 7(1): 83 – 94.
Arabnejad, M. & Mohammadi, H. 2013. Detection Of Phaeoacremonium Tuscanum And Botryosphaeriaceae Species Associated With Grapevine Decline In Iran And The Potential Role Of Pruning Debris On The Survival Of The Pathogens Iran. Journal of. Plant Pathology, 49(4): 139–148.
Arabnezhad, M., Mohammadi, H., Massumi, H. & Farahmand, H. 2014. Fungal flora associated with internal symptoms of grapevine decline in Kerman province. Journal of Agricultural Biotechnology, 6(2): 115–132.
Arnold, A.E., Maynard, Z. & Gilbert, G.S. 2001. Fungal endophytes in dicotyledonous Neotropical trees: patterns of abundance and diversity. Mycology Research, 105(12): 1502–1507.
Amold, A. & Herre, E. 2003. Canopy cover and leaf age affect coloniza–tion by tropical fungal endophytes: ecological pattern and processin Theobroma cacao (Malvaceae). Mycologia, 95(3): 388–98.
Arzanlou M. & 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(2).
Asgari, B. Zare, R. & Peyghami, E. 2004. Hyphomycetous fungal community of barley phylloplane in East Azarbaijan province with emphasis on new taxa for Iranian fungal flora. Rostaniha, 5(2): 171–197.
Avilés, M. Castillo S. Bascon J. Zea Bonilla T. Martín Sánchez PM. & Pérez–Jiménez R.M.  2008. First report of Macrophomina phaseolina causing crown and root rot of strawberry in Spain. Plant Pathology, 57(2): 382.
Bagherabadi, Sh. & Zafari, D. 2022. Isolation and characterization of Alternaria malorum as a causal agent of bark canker on walnut trees. Journal of Plant Protection, 62(1):102–106.
Bahmani, Z., Abdollahzadeh, J., Amini, J. & Evidente, A. 2021. Biscogniauxia rosacearum the charcoal canker agentas a pathogen associated with grapevine trunk diseases in Zagros region of Iran. Scientific Reports, 11:14098.
Baloyi, M.A., Halleen, F., Mostert, L. & Eskalen, A. 2013. First report of Togninia minima perithecia on esca– and Petri–diseased grapevines in South Africa. Plant Disease, 97:1247.
Basandrai, A.k., Pande, A.k., Somta, P. & Basandra, D. 2020. Macrophomina phaseolina host interface: Insights into an emerging dry root rot pathogen of mungbean and urdbean, and its mitigation strategies. Plant Pathogen Impact Reviews, 70(6): 1263–1275.
Bérdy, J. 2005. Bioactive microbial metabolites A personal view. Review. Journal of Antibiot, 58:1–26.
Cannon P.F. & Simmons CM. 2002. Diversity and host preference of leaf endophytic fungi in the Iwokrama forest reserve, Guyana. Mycologia, 942: 210–220.
Casieri, L., Hofstetter, V., Viret, O. & Gindro, K. 2009 Fungal communities living in the wood of different cultivars of young Vitis vinifera plants. Phytopathologia Mediterranea, 48:73–83.
Ciancio, A. & Mukerji, K.G. 2008. Integrated Management of Diseases Caused by Fungi, Phytoplasma and Bacteria, DOA – 10.1007/978–1–4020–8571–0.
Cui, J.L., Guo, S.X. & Xiao, P.G. 2011. Antitumor and antimicrobial activities of endophytic fungi from medicinal parts of Aquilaria sinensis. Journal of Zhejiang University Science B, 125: 385–392.
Das, J., Lahan, J. P. & Srivastav, R.B. 2010. Solanum melongena: A potential source of antifungal agent. Indian Journal of Microbiology, 50(1): 62–69.
Díaz, G.A. & Latorre, B.A. 2014. Infection caused by Phaeomoniella chlamydospora associated with Esca like symptoms in grapevine in Chile. Plant Disease, 98: 351–360.
Dissanayak, A.j., Purahong, W., Wubet, T., Hyde, K.D., Zhang, W., Xu, H., Zhang, G., Fu, C., Liu, M., Xing, Q., Li, X. & Yan, J. 2018. Direct comparison of culture–dependent and culture–independent molecular approaches reveal the diversity of fungal endophytic communities in stems of grapevine (Vitis vinifera). Fungal Diversity Diversity, 90: 85–107.
Edwards, J. & Pascoe, L. 2004. Occurrence of Phaeomoniella chlamydospora and Phaeoacremonium aleophilum associated with Petri disease and esca in Australian grapevines. Australasian Plant Pathology, 33: 273–279.
Eskalen, A., Feliciano, A.J. & Gubler, W.D. 2007. Susceptibility of grapevine pruning wounds and symptom development in response to infection by Phaeoacremonium aleophilum and Phaeomoniella chlamydospora. Plant Disease, 91: 1100–1104.
Farashiani, A., Mousavi Jurf, S.A. & Karimi Shahri, M.R. 2012. Study of Esca Disease of Grapevine in Bojnourd. Plant patgology, 48(2): 143–153. (In Persian with English summary).
Femandes, E.G., Pereira, O.L., DaSilva, C.C. & Bento, C.B.P. Queiroza, M.V. 2015. Diversity of endophytic fungi in Glycine max. Microbiological Research, 181: 84–92.
Fierro–Cruz, J.E., Jiménez, P. & Coy–Barrera, E. 2017. Fungal endophytes isolated from Protium heptaphyllum and Trattinnickia rhoifolia as antagonists of Fusarium oxysporum. Revista Argentina de microbiologia, 49(3): 255–263.
Fischer, M. 2002. A new wood–decaying basidiomycete species associated with esca of grapevine: Fomitiporia mediterranea (Hymenochaetales). Mycological Progress, 1(3): 315–324.
Fotouhifar, K.B., Hedjaroude, G.A., Ershad, D., Moussavi, S.M. & Okhovvat, S.M. 2007. New informationon the form–genus Cytospora in Iran. Rostaniha, 8 (2): 129–149.
Fotouhifar, K., Hedjaroude, G. & Leuchtmann, A. 2010. ITS rDNA phylogeny of Iranian strains of Cytospora and associated teleomorphs. Mycologia, 102: 1369–82.
Ghanbary Tajick, M.A., Mahdian, S.A., Mohammadi, H. & Amarloo, O.A. 2020. Identification and pathogenicity of fungal species associated with grapevine trunk diseases in Khorasan–Razavi province, Iran. Mycologia Iranica, 7(1): 83–94.
Ghasemi Esfahlan, S. & Arzanlou, M. 2019. Morphological and molecular characterization of endophytic fungi from oak trees in Arasbaran forests. Plant Protection, 8(1): 1–17.
Ghimire, S.R., Charlton, N.D., Bell, J.D., Krishnamurthy, Y.L. & Craven, K.D. 2011. Biodiversity of fungal endophyte communities inhabiting switchgrass (Panicum virgatum L) growing in the native tallgrass prairie of northern Oklahoma. Fungal Diversity, 47: 19–27.
González, V. & Tello, M.L. 2011. The endophytic mycota associated with Vitis vinifera in central Spain. Fungal Diversity, 471: 29–42.
Goveas, S.W., Madtha, R., Nivas, S.K. & D’Souza, L. 2011. Isolation of endophytic fungi from Coscinium fenestratum –a red listed endangered medicinal plant Eurasian. Journal of biosciences, 5(1): 48–5.
Gramaje, D., Úrbez Torres, J.R. & Sosnowski, M.R. 2018. Managing grapevine trunk diseases with respect to etiology and epidemiology: Current strategies and future prospects. Plant Disease, 102: 12–39.
Hall, T.A. 1999. BioEdit: A user–friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41: 95–98.
Hergholi, N. 2013. Isolation and Identification ofendophytic fungi in grapvinic trees (Vitis viniferaL.) in West Azarbaijan province. MSc thesis plantpathology, University of Tehran, Iran (In Persian with English summary).
Highet, A. S. & Nair, N.G. 2008. Fusarium oxysporum associated with grapevine decline in the Hunter Valley. Nucleic Acids Symposium Series, 1(1):48–50.
Johannesson, H., Læssøe, T. & Stenlid, J. 2000. Molecular and morphological investigation of Daldinia in northern Europe. Mycological Research, 104(3):275–280.
Khan, A., Whiting, C., Rooney, S. & Gubler, W.D. 2000. Pathogenicity of three Phaeoacremonium spp. on grapevine in California. Phytopathologia Mediterranea, 39: 92–99.
Khaledi, E., Moghadam, J.N., Abdollahzadeh, J. & Amini, J. 2021. Fungi associated with grapevine trunk diseases (GTDs) with emphasize on pestalotioid species in Kurdistan Province, Iran. Biology.Reaserch square, DOI: 10.21203/rs.3.rs–192033/v1.
Ko, Y.M., Choi, J., Lee, Y.H. & Kim, H.T. 2020. First report of charcoal rot caused by Macrophomina phaseolina on Glycine max in Korea. Research in Plant Disease, 26: 2 9– 37.
Köhl, J., Scheer, C., Holb, I.J., Masny, S., Molhoek, W. 2015. Toward an integrated use of biological control by Cladosporium cladosporioides H39 in Apple Scab (Venturia Inaequalis) management. Plant Disease, 99: 535–543.
Langoni, P., Rodolfi, M., Pantaleoni, L., Doria, E., Concia, L., Picco, A.M. & Cella, R. 2012. Functional analysis of the degradation of cellulosic substrates by a Chaetomium globosum endophytic isolate. Applied and Enviromental. Microbiology, 3693–3705.
Larignon, P.B. & Dubos, B. 1997. Fungi associated with esca disease in grapevine. European Journal of Plant Pathology, 103:147–157.
Latz, M.A.C., Jensen, B. Collinge D.B. & Jørgensen H.J.L. 2018. Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecology Diversity, 11: 555–567.
Lee, D.J, Lee, J.S., Lee, H.B. & Choi, Y.J. 2019. Four Endophytic Ascomycetes New to Korea: Cladosporium anthropophilum, C. pseudocladosporioides, Daldinia eschscholtzii, and Nigrospora chinensis. The Korean Journal of Mycology, 47(3): 187–97.
Liarzi, O., Bar, E., Lewinsohn, E. & Ezra, D. 2016. Use of the endophytic fungus Daldinia cf. concentrica and its volatiles as bio–control agents. Plos One, 11(12): DOI.org/10.1371/journal.pone.0168242
Linnakoski, R., Puhakka–Tarvainen, H. & Pappinen, A. 2012. Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecology, 53: 298–308.
Mahmoudzadeh, H., Rasouli, V., Nejatian, M.A. & Dolati, H. 2010. Variety of grape cultivars in Iran, a factor for survival and possibility of organic grape production. In: the first national conference on sustainable agriculture and healthy crop production. Isfahan, Iran. (In Persian with English summary).
Ma, X. & Kang, J. 2015. Non–mycorrhizal endophytic fungi from orchids. Current Science, 109(1): 72–87.
Mehrabi, M., Asgari, B. & Zare, R. 2020. Description of Allocanariomyces and Parachaetomium, two new genera, and Achaetomium aegilopis sp. nov. in the Chaetomiaceae. Mycological Progress, 19: 1415–1427.
Mogg, R.J., & Bond, J.M. 2003. A cheap, reliable and rapid method of extracting high–quality DNA from plants. Molecular Ecology Notes, 3(4):666–668
Mohammadi, H. & Banihashemi, Z. 2007. Grapevine Decline in Fars Province. Iran. Journal of. Plant Pathology, 43: 294–310.
Mohammadi, H. & Banihashemi, Z. 2012. First Report of Phaeoacremonium inflatipes and Phaeoacremonium mortoniae Associated with Grapevine Petri Disease in Iran. Journal of Agricultural Science and Technology, 14: 1405–1414 (In Persian with English summary).
Mohammadi, H., Banihashemi, Z., Gramaje, D. & Armengol, J. 2013. Fungal pathogens associated with grapevine trunk diseases. Journal of Agricultural Science and Technology, 15: 137–150 (In Persian with English summary).
Mohammadi, M., Hemmati, R. & Mehrabi, M. 2019. Fungi associated with grapevine decline in Zanjan province, Iran. Proceedings of the province. 23rd Iranian plant protection congress, 27–30 Aug. Gorgan University of Agricultural Sciences and Natural Resources, 235–236 (In Persian with English summary).
Moshari, S. 2011. Identification of fungi causing hair loss in West Azerbaijan province. Master Thesis. School of Agriculture, Plant Protection Group Urmia University, Iran (In Persian with English summary n)
Mostert, L. & Groenewald, J.Z. 2006a. Taxonomy and pathology of Togninia (Diaporthales) and its Phaeoacremonium anamorphs. Studies in Mycology, 54: 115 pp.
Mostert L. Abeln E.C. Halleen A.F. & Crous P.W. 2006b. Genetic diversity among isolates of Phaeomoniella chlamydospora on grapevines. Australasian Plant Pathology 35: 453–460.
Mugnai, L., Graniti, A. & Surico, G. 1999. Esca (black measles) and crown wood–streaking: Two old and elusive diseases of grapevines. Plant Disease, 83: 404–418.
Muvea, A.M., Meyh€ofer, R., Subramanian, S., Poehling, H.M., Ekesi, S. & Maniania, N.K. 2014. Colonization ofonions by endophytic fungi and their impacts on thebiology of Thrips tabaci. PloS One 9 DOI:10.1371/journal.pone.0108242Corpus ID: 4630824
Nair, D.N. & Padmavathy, S. 2014. Impact of endophytic microorganisms on plants, environment and humans. The Scientific World Journal, 2014(11).
Nouri, N.T., Lawrence, D.P., Kallsen, C.E. & Trouillas, F.P. 2020. Macrophomina crown and root rot of pistachio in California. Plants, 9(2): 134.
Petrini, O. 1992. Taxonomy of endophytic fungi of aerial plant tissues. In; Fokkema NJ, Van den Hevel J (eds). Micro– biology of the phyllosphere. Academic Press, Cambridge University Press, UK.
Pimentel, M.R. & Molina, G. 2011. Use of endophytes to obtain bioactive compounds and their application in bio transformation process. Biotechnology Research International, DOI:org/10.4061/2011/576286
Pourmoghaddam, M.J., Khodaparast, S.A. & Pedramfar, H. 2014. The genus Daldinia in Guilan province (IN Iran). Rostaniha, 15(2): 122–132.
Pancher, M., Ceol, M., Corneo, P.E., Longa, C.M.O., Pertot, S.Y.I. & Campisano, A. 2012. Fungal endophytic communities in grapevines (Vitisvinifera L.) respond to crop management. Appliedand Environmental Microbiology, 78: 4308.
Purushotham, N., Jones, A., Poudel, B., Nasim, J., Adorada, D. & Sparks, A. 2020. Draft genome resource for Macrophomina phaseolina associated with charcoal rot in sorghum. Molecular Plant Microbe Interactions, 33: 724–726.
Qadri, M., Johri, S., Shah, B.A., Khajuria, A., Sidiq, T., Lattoo, S.K. & Abdin, M.Z. 2013. Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. SpringerPlus, 2(8).
Raja, H.A., Kaur, A., El–Elimat, T., Figueroa, M. & Kumar, R., Deep, G. & Agarwal, R. 2015. Phylogenetic and chemical diversity of fungal endophytes isolated from Silybum marianum (L) Gaertn. (milk thistle). Mycology, 6(1):8–27.
Razghandi, M., Mohammadi, A., Ghorbani, M. & Mirzaee, M.R. 2020. New fungal pathogens and endophytes associated with Salsola. Journal of plant protection Research, 60(4): 362–368.
Rivera Orduña, F.N. & Suarez Sanchez, R.A. 2011. Diversity of endophytic fungi of Taxus globosa (Mexican yew). Fungal Diversity, 47(1): 65–74.
Safarnejad, M.R. & Gholamian, G.h. 2011. Identification and determination of fungi with grape blight in Sistan region. Agricultural Research Center Sistan Iran 294pp. (In Persian with English summary) https://civilica.com/doc/1057915/.
Saleh, A.A., Ahmed, H.U., Todd, T.C., Travers, S.E., Zeller, K.A. & Leslie, J.F. 2010. Relatedness of Macrophomina phaseolina isolates from tallgrass prairie, maize, soybean and sorghum. Molecular Ecology 19: 79– 91.
Scheck, H.J., Vasquez, S.J., Fogle, D. & Gubler, W.D. 1998. First Report of Three Phaeoacremonium spp. cause young grapevine decline in California. Plant Disease, 82(5): 590.
Schulz, B. & Boyle, C. 2002. Endophytic fungi: a source of biologically active secondary metabolites. Mycological Research, 106(9): 996–1004.
Schulz, B. & Boyle, C. 2005. The Endophytic Continuum. Mycological Research, 109(6): 661–86.
Shipunov, A. Newcombe, G., Raghavendra, A.K. & Anderson, C.L. 2008. Hidden diversity of endophytic fungi in an invasive plant. American Journal of Botany, 959: 1096–1108.
Silva Valderrama, I., Toapanta, D., Miccono, M.D., Lolas, M., Díaz, G.A., Cantu, D. & Castro, A. 2021. Biocontrol potential of grapevine endophytic and rhizospheric fungi against trunk pathogens. Frontiers in Microbiology, 11 DOI:10.3389/fmicb.2020.614620.
Stadler, M., Læssøe, T., Fournier, J., Decock, C., Schmieschek, B., Tichy, H.V. & Peršoh, D. 2014. A polyphasic taxonomy of Daldinia (Xylariaceae). Studies in Mycology, 77: 1–14.
Strobel, G.A. 2003. Endophytes as sources of bioactive products. Microbes and Infection, 5(6): 535–544.
Strobel, G. & Daisy, B. 2003. Bioprospecting for microbial endophytes and their natural products. Microbiology and Molecular Biology Reviews, 67: 491–502.
Sun, Z., Li, S., Ren, Q., Xu, J., Lu, X. & Sun, M. 2020, Biology and applications of Clonostachys rosea. Journal of Applied Microbiology,129: 486–495. https://doi.org/10.1111/jam.14625
Surico, G., Mugnai, L. & Marchi, G. 2006. Older and Recent Observation on Esca: A Critical Overview. Phytopathologia Mediterranea, 45(4): S68–S86.
Sutjaritvorakul, T., Whalley, A.J.S., Sihanonth, P. & Roengsumran, S. 2011. Antimicrobial activity from endophytic fungi isolated from plant leaves in Dipterocarpous forest at Viengsa district Nan province. Thailand Journal of Agricultural Technology, 71: 115–121.
Tamura, K., Stecher, G. & Kumar, S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38(7):3022–3027 doi:10.1093/molbev/msab120
Vega, F.E., Posada, F., Aime, M.C., Pava–Ripoll, M., Infante, F. & Rehner, S.A. 2008. Entomopathogenic fungal endophytes. Biological Control 46: 72–82.
Vilvert, E., Costa, M.D., Cangahuala–Inocente, G.C. & Lovato, P.E. 2017. Root proteomic analysis of grapevine root stocks inoculated with Rhizophagus irregularis and Fusarium oxysporum f. sp. herbemontis. Revista Brasileira de Ciencia do Solo, 41:1–14.
Waqas, M., Latif Khan, A., Kamran, M., Hamayun, M., Kang, S.M., Kim, Y.H. & Lee, I.J. 2012. Endophytic fungi produce gibberellins and indole acetic acid and promotes Host–Plant growth during stress. Molecules, 17: 10754–10773.
Weber, D. 2009. Endophytic fungi, occurrence and metabolites. In Physiology and Genetics. Springer, Berlin, Heidelberg, 153–195.
Wilson, D. 1995. Endophyte – the evolution of a term, and clarification of its use and definition. Oikos, 73: 274–276.
Whalley, A.J.S. 1996. The xylariaceous way of life. Mycological Research 100: 897–922.
White, T.J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Inis MA, Gelfand DH, Sninsky JJ, White TJ (eds). PCR Protocols: A guide to Methods and Applications. Academic Press, San Diego, U.S.A. 315–322.
Wightwick, A., Walters, R., Allinson, G., Reichman, S. & Menzies, N. 2010. Environmental Risks of Fungicides Used in Horticultural Production Systems. In: Odile C (eds). Fungicides, Canada, 272–303
Yu, H., Zhang, L., Li, L., Zheng, Ch., Guo., L., LiW, o., Sun, P. & Qin, L. 2010. Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiological Research, 165(6): 437–449.
Zhao, J., Zhou, L., Wang, J., Shan, T., Zhong, L., Liu, X. & Gao, X. 2010b. Endophytic fungi for producing bioactive compounds originally from their host plants. Current Research, Technology and Education Topics Applied Microbiology and Microbial Biotechnology, 1: 567–576.
Živanov, D., Živanov, S.T., Nagl, N., Savić, A., Katanski, S. & Milić, D. 2019. First report of Macrophomina phaseolina causing dry root rot of chickpea (Cicer arietinum L.) in Serbia. Plant Disease, 103(10): 2685–2686.

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