New fungal canker pathogens of apple trees in Iran

Volume 9, Issue 4
December 2020
Pages 669-681

Document Type : Original Research

Authors

1 Department of Plant Protection, Faculty of Agriculture and Natural Resources, Urmia University, Urmia, Iran.

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

Abstract
Apples are the main horticultural crops grown in West Azarbaijan province of Iran. In recent surveys of apple orchards in Urmia and Miyandoab, West Azarbaijan Province, symptoms including branch and twig bark cracks, cankers, dieback and tree decline were commonly seen. Isolation of the fungi from cracked and cankered branches yielded fungal isolates with typical characteristics of the genera Paecilomyces and Paramyrothecium. Based on combination of morphological characteristics and sequence data obtained from ITS-rDNA and β-tubulin gene sequences for Paecilomyces isolates and ITS-rDNA region for Paramyrothecium isolates, they were identified as Paecilomyces formosus and Paramyrothecium foliicola. Results of the pathogenicity tests on detached shoots of ‘Golden Delicious’ and ‘Red Delicious’ cultivars showed that isolates of P. formosus were pathogenic only on ‘Red Delicious’ cultivar, but Pa. foliicola isolates were pathogenic on both cultivars and showed symptoms of infection. Re-isolation of the fungi from inoculated shoots confirmed Koch’s postulates. To the best of our knowledge, the involvement of P. formosus and Pa. foliicola in the development of canker disease of apple trees is reported for the first time. Also, Pa. foliicola is a new record to Iran mycobiota.

Keywords

Subjects
Ahmadi, K., Ebadzadeh, H. R., Hatami, F., Hoseinpour, R. and Abdshah, H. 2018. Agricultural Statistics, vol. 3. Horticultural Crops. Ministry of Agriculture-Jahad, Planning and Economic Affairs, Communication and Information Technology Center, Tehran.
Barker, A. P., Horan, J. L., Slechta, E. S., Alexander, B. D. and Hanson, K. E. 2014. Complexities associated with the molecular and proteomic identification of Paecilomyces species in the clinical laboratory. Medical Mycology, 52: 535–543.
Ben, H. Y., Gao, W. and Qu, H. Y. 2016. New host record of Myrothecium roridum causing leaf spot on Abutilon megapotamicum from China. Journal of Phytopathology, 164: 563–566.
Borges, R. C. F., Rossato, M., Santos, M. D. M., Ferreira, M. A., Fonesca, M. E. N., Reis, A. and Boiteux, L. S. 2018. First report of a leaf spot caused by Paramyrothecium roridum on Tectona grandis in Brazil. Plant Disease, 102(8): 1661.
Brown-Rytlewski, D. E. and McManus, P. S. 2000. Virulence of Botryosphaeria dothidea and Botryosphaeria obtusa on apple and management of stem cankers with fungicides. Plant Disease, 84: 1031–1037.
Bruton, B. D. and Fish, W. W. 2012. Myrothecium roridum leaf spot and stem canker on watermelon in the southern Great Plains: Possible factors for its outbreak. Plant Health Progress, doi:10.1094/PHP-2012-0130-01-BR.
Chavhan, R. L., Hinge, V. R., Kadam, U. S., Kalbande, B. B. and Chakrabarty, P. K. 2018. Real-time PCR assay for rapid, efficient and accurate detection of Paramyrothecium roridum a leaf spot pathogen of Gossypium species. Journal of Plant Biochemistry and Biotechnology, 27: 199–207.
Chen, Z. D., Li, P. L., Chai, A. L., Guo, W. T., Shi, Y. X., Xie, X. W. and Li, B. J. 2018. Crown canker caused by Paramyrothecium roridum on greenhouse muskmelon (Cucumis melo) in China. Canadian Journal of Plant Pathology, 40: 115–120.
Cloete, M., Fourie, P. H., Damm, U., Crous, P. W. and Mostert, L. 2011. Fungi associated with die-back symptoms of apple and pear trees, a possible inoculum source of grapevine trunk disease pathogens. Phytopathologia Mediterranea, 50 (Supplement): S176–S190.
Cooke, T., Denis, M. P. and Susan, H. 2009. Diseases of Fruit Crops in Australia. CSIRO Publishing, Collingwood, Australia.
Elzebroek, A. T. G. and Wind, K. 2008. Guide to cultivated plants. CAB International, Wallingford, UK.
Ershad, D. 2009. Fungi of Iran. 3rd ed. Iranian Research Institute of Plant Protection. Tehran, Iran.
FAOSTAT, Food and Agriculture Organization of the United Nations, 2019. Available from: http://fao.org/faostat/en/#data/QC. [accessed 12.8.19].
Farr, D. F. and Rossman, A. Y. 2019. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Available from: https://nt.ars-grin.gov/fungaldatabases/. [Retrieved April 1, 2019]
Farzaneh, M., Javan-Nikkhah, M., Fotouhifar, Kh. B., and Karim-Moojeni, H. 2009. Fungi associated with leaf spots of nutsedge plants (Cyperus spp.) in North of Iran. Rostaniha, 10(1): 68–79. (In Persian with English summary)
Garibaldi, A., Gilardi, G., Franco-Ortega, S. and Gullino, M. L. 2016. First report of leaf spot of lamb’s lettuce (Valerianella olitoria) caused by Myrothecium roridum in Italy. Plant Disease, 100: 1237.
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.
Gooya, M., Ershad, D. and Riahi, H. 2000. An investigation on mycoflora of sesame seeds in Iran. Rostaniha, 1: 27–31.
Han, K. S., Choi, S. K., Kim, H. H., Lee, S. C., Park, J. H., Cho, M. R. and Park, M. J. 2014. First report of Myrothecium roridum causing leaf and stem rot disease on Peperomia quadrangularis in Korea. Mycobiology, 42: 203–205.
Hanifeh, S., Ghosta,Y., Abbasi, S. and Phillips, A. J. L. 2013. First report of Diplodia malorum Fuckel the causal agent of canker disease of apple trees in Iran. Iranian Journal of Plant Pathology, 49: 83–84.
Haudenshield, J. S., Pawlowski, M., Miranda, C. and Hartman, G. L. 2018. First report of Paramyrothecium roridum causing Myrothecium leaf spot on soybean in Africa. Plant Disease, 102: 2638.
Heidarian, R., Fotouhifar, K. B., Debets, A. J. M. and Aanen, D. K. 2018. Phylogeny of Paecilomyces, the causal agent of pistachio and some other trees dieback disease in Iran. PLoS ONE, 13(7): e0200794. Available from: http://doi.org/10.1371/journal.pone.0200794.
Katoh, K., Rozewicki, J. and Yamada, K. D. 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, bbx108: 1–7.
Khezrinejad, N., Niknam, Gh. and Ghosta, Y. 2007. Fungi associated with sugarbeet cyst nematode from fields of West Azarbaijan (I). Rostaniha, 7(2): 149–162. (In Persian with English summary)
Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111–120.
Krisai-Greilhuber, I., Chen, Y., Jabeen, S., Madrid, H., Marincowitz, S., Razaq, A., Ševčíková, H., Voglmayr, H., Yazici, K., Aptroot, A., Aslan, A., Boekhout, T., Borovička, J., Crous, P. W., Ilyas, S., Jami, F., Jiang, Y. L., Khalid, A. N., Kolecka, A., Konvalinková, T., Norphanphoun, C., Shaheen, S., Wang, Y., Wingfield, M. J., Wu, S. P., Wu, Y. M. and Yu J. Y. 2017. Fungal Systematics and Evolution: FUSE 3. Sydowia, 69: 229–264.
Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger data sets. Molecular Biology and Evolution, 33: 1870–1874.
Kuobi, T., Okazaki, K., Inotani, M., Sugino, M., Sadamura, T., Nakano, A., Kobayashi, S., Ota, A., Nishimura, K. and Yaguchi, T. 2016. A case of cutaneous Paecilomyces formosus infection in an extremely premature infant. Journal of Infection and Chemotherapy, 22: 339–341.
Liang, J., Li, G., Zhou, S., Zhao, M. and Cai, L. 2019. Myrothecium-like new species from turfgrasses and associated rhizosphere. MycoKeys, 51: 29–53.
Lombard, L., Houbraken, J., Decock, C., Samson, R. A., Meijer, M., Réblová, M., Groenewald, J. Z. and Crous, P. W. 2016. Generic hyper-diversity in Stachybotriaceae. Persoonia, 36: 156–246.
Matić, S., Gilardi, G., Gullino, M. L. and Garibaldi, A. 2019. Emergence of leaf spot disease on leafy vegetable and ornamental crops caused by Paramyrothecium and Albifimbria species. Phytopathology, 109: 1053–1061.
Mir, H. and Patel, V. B. 2018. Genetic engineering of temperate fruit crops. In: Rout, G. R. and Peter, K. V. (eds.), Genetic Engineering of Horticultural Crops. Elsevier Inc., UK. pp.89–119.
Mirabdollahi Shamsi, M., Akbarnia, M., Mirabolfathy, M., Manzari, S. and Ahmadikhah, A. 2019. Dieback and decline of wild almond (Amygdalus scoparia Spach) in the Harat protected forest of Yazd Province, Iran. Forest Pathology, 2019: e12538. Available from: https://doi.org/10.1111/efp.12538.
Moreira, D. C., Oliveira, M. M. and Borba, C. M. 2018. Human pathogenic Paecilomyces from food. Microorganisms, 6: 64. doi:10.3390/microorganisms6030064.
Page, R. D. 1996. Treeview, tree drawing software for Apple Macintosh and Microsoft Windows. Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, Scotland, UK.
Pelayo-Sánchez, G., Yáñez-Morales, M. J. and Solano-Vida, R. 2017. First report of leaf spot on Coffea arabica caused by Paramyrothecium roridum in Mexico. Plant Disease, 101(6): 1044.
Rennberger, G. 2018. Occurrence and pathogenicity of foliar pathogens on cucurbits in South Carolina with special emphasis on Stagonosporopsis and Stachybotriaceae on watermelon. Ph.D. Dissertation, Clemson University.
Sabernasab, M., Jamali, S., Marefat, A. and Abbasi, S. 2019. Molecular and pathogenic characteristics of Paecilomyces formosus, a new causal agent of oak tree dieback in Iran. Forest Science, 65(6):743-750.
Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4: 406–425.
Samson, R. A., Houbraken, J., Varga, J. and Frisvad, J. C. 2009. Polyphasic taxonomy of the heat resistant ascomycete genus Byssochlamys and its Paecilomyces anamorphs. Persoonia, 22: 14–27.
Schieber, E. and Zentmyer, G. A. 1968. Myrothecium stem necrosis and leaf spot: important coffee disease in Guatemala. Plant Disease Reporter, 52: 115–117.
Sikdar, P., Mazzola, M. and Xiao, C. L. 2019. Genetic and pathogenic characterization of Phacidiopycnis washingtonensis from apple and pacific Madrone from the Western United States. Phytopathology, 109(3): 469–479.
Sutton, T. B., Aldwinckle, H. S., Angello, M. A. and Walgenbach, J. F. 2014. Compendium of Apple and Pear Diseases and Pests, 2nd ed. APS Press, St. Paul, Minnesota, USA.
Swofford, D. L. 2002. PAUP, Phylogenetic analysis using parsimony (and other methods). Version 4.0b10. Sunderland, MA, USA.
Torabi, A., Shahidi Bonjar, G. H., Abdolshahi, R., Pournamdari, M., Saadoun, I. and Barka, E. A. 2019. Biological control of Paecilomyces formosus, the causal agent of dieback and canker disease of pistachio by two strains of Streptomyces misionensis. Biological Control, 137: 104029. doi:10.1016/j.biocontrol.2019.104029
Turechek, W. W. 2004. Apple diseases and their management. In: Naqvi, S. A. M. H. (ed.), Diseases of Fruits and Vegetables, Vol. I. Kluwer Academic Publishers, the Netherlands. pp.1–108.
Xiao, C. L. and Boal, R. J. 2005. A new canker and twig dieback disease of apple and crabapple trees caused by Sphaeropsis pyriputrescens in Washington State. Plant Disease, 89: 1130.
Zhao, Y. J., Li, B. J., Shi, Y. X. and Xie, X. W. 2010. First report of Myrothecium leaf spot of common bean in China caused by Myrotheciym roridum. Plant Disease, 94: 127.
Zhong, S. and Steffenson, B. J. 2001. Genetic and molecular characterization of mating type genes in Cochliobolus sativus. Mycologia, 93: 852–863.