Identification of Alternaria speIdentification of Alternaria Species from the Section Infectoriae associated with Wheat and Barley Black (Sooty) Head Mold in Irancies from the section Infectoriae associated with cereal sooty mold in Iran

Document Type : Original Article

Authors

1 M. S. Student of Plant Pathology, Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

2 Associate Professor, Department of Plant Protection, College of Agriculture, Urmia University, Urmia, Iran

3 Professor, Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

Abstract

Abstract
Black (sooty) head mold of wheat and barley, which is commonly characterized by black discoloration of their heads, is caused by different fungi colonizing the mature and senescent heads. It seems that black head mold develops more on plants when humid conditions occurs as the crop matures, or when harvest is delayed due to wet conditions and/or when portions of plants specially heads are died prematurely. During an investigation on fungal species associated with black head mold of wheat and barley in Golestan, Alborz and Qazvin provinces in the spring and summer of 2014 and 2015, a total of 133 Alternaria isolates with the characteristics of the section Infectoriae were collected. Based on the results obtained from morphological studies and data from nucleotide sequences of the two genomic loci, ITS–nrDNA and part of gelyceraldehyde–3–phosphate dehydrogenase (gpdh), four species Viz. Alternaria arbusti, A. ethzedia, A. incomplexa and A. triticimaculans were identified. All identified species in the case of this study are reported for the first time as Alternaria species associated with black head mold symptoms of wheat and barley in the world. Also, except for A. arbusti, which was previously reported from cabbage plants in Iran, the remaining three species are new records for mycobiota of Iran. The species are fully described here.

Keywords


Andersen, B. and Hollensted, M. (2008) Metabolite production by different Ulocladium species. International Journal of Food Microbiology 126(1): 172-179.
Andersen, B. and Thrane, U. (1996) Differentiation of Altemaria infectoria and Alternaria alternata based on morphology, metabolite profiles, and cultural characteristics. Canadian Journal of Microbiology 42(7): 685-689.
Andersen, B., Dongo, A. and Pryor, B. M. (2008) Secondary metabolite profiling of Alternaria dauci, A. porri, A. solani and A. tomatophila. MycologicalResearch 112(2): 241-250.
Andersen, B., Krøger, E. and Roberts, R. G. (2002) Chemical and morphological segregation of Alternaria arborescens, A. infectoria and A. tenuissima species–groups. Mycological Research 106(2): 170-182.
Andersen, B., Sørensen, J. L., Nielsen, K. F., van den Ende, B. G. and de Hoog, S. (2009) A polyphasic approach to the taxonomy of the Alternaria infectoria species-group. FungalGeneticsandBiology 46(9): 642-656.
Ardestani, S. T., Sharifnabi, B., Zare, R. and Moghadam, A. A. (2010) New Alternaria species associated with potato leaf spot in various potato growing regions of Iran. Iranian Journal of Plant Pathology 45: 83-86 (in Persian).
Bagherabadi, S., Zafari, D. and Soleimani, M. J. (2015) A report on the Alternaria species and its similar genera in Hamedan province. Taxonomy and Biosystematics 7(24): 95-112 (in Persian).
Bensassi, F., Zid, M., Rhouma, A., Bacha, H. and Hajlaoui, M. R. (2009) First report of Alternaria species associated with black point of wheat in Tunisia. Annals of Microbiology 59(3): 465-467.
Berbee, M. L., Pirseyedi, M. and Hubbard, S. (1999) Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde–3–phosphate dehydrogenase gene sequences. Mycologia 91(6): 964-977.
Christensen, K. B., Van Klink, J. W., Weavers, R. T., Larsen, T. O., Andersen, B. and Phipps, R. K. (2005) Novel chemotaxonomic markers of the Alternaria infectoria species–group. Journal of Agricultural and Food Chemistry 53(24): 9431-9435.
Crous, P. W., Wingfield, M. J., Richardson, D. M., Le Roux, J. J., Strasberg, D., Edwards, J. and et al. (2016) Fungal planet description sheets: 400-468. Persoonia36: 316-458.
Dexter, J. E. and Matsuo, R. R. (1982) Effect of smudge and black point, mildewed kernels, and ergot on durum wheat quality. Cereal Chemistry 59(1): 63-69.
Dugan, F. M. and Peever, T. L. (2002) Morphological and cultural differentiation of described species of Alternaria from Poaceae. Mycotaxon 83: 229-264.
Farr, D. F., Bills, G. F., Chamuris, G. P. and Rossman, A. Y. (1989) Fungi on plants and plant products in the United States. APS press, St. Paul, MN, USA.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4): 783-791.
Frisvad, J. C. (1983) A selective and indicative medium for groups of Penicillium viridicatum producing different mycotoxins in cereals. Journal of Applied Bacteriology 54(3): 409-416.
Gannibal, P. B. and Lawrence, D. P. (2016) Distribution of Alternaria species among sections. 3. Sections Infectoriae and Pseudoalternaria. Mycotaxon 131(4): 781-790.
Ghosta, Y., Ershad, D., Zare, R. and Goltapeh, E. M. (2003) A taxonomic study on Alternaria species in Iran (2). Rostaniha 4(3/4): 31-56 (in Persian).
Ghosta, Y., Ershad, D., Zare, R. and Mohammadi, G. E. (2004) A taxonomic study on Alternaria species in Iran. Iranian Journal of Plant Pathology 49(3): 101-104 (in Persian).
Hajipour Jarchelou, Z., Ghosta, Y. and Rezaee, S. (2012) An identification and pathogenicity study of Alternaria spp. of tomato and potato in West Azerbaijan Province. Iranian Journal of Plant Protection Science 43(1): 155-163 (in Persian).
Hajipour Jarchelou, Z., Ghosta, Y. and Rezaee, S. (2013) Identification and pathogenicity study of Alternaria spp. on potato in West Azerbaijan Province (1). Iranian Journal of Plant Pathology 49(3): 101-104.
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.
Hershman, D. E. (2011) Black “sooty” head mold of wheat. Plant Pathology Fact Sheet, PPFS–AG–SG–07, 2 pp.
Hong, S. G., Cramer, R. A., Lawrence, C. B. and Pryor, B. M. (2005) Alt a 1 allergen homologs from Alternaria and related taxa: analysis of phylogenetic content and secondary structure. Fungal Genetics and Biology 42(2): 119-129.
Katoh, K. and Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4): 772-780.
Lawrence, D. P., Gannibal, P. B., Dugan, F. M. and Pryor, B. M. (2014) Characterization of Alternaria isolates from the infectoria species–group and a new taxon from Arrhenatherum, Pseudoalternaria arrhenatheria sp. nov. Mycological Progress 13(2): 257-276.
Lawrence, D. P., Gannibal, P. B., Peever, T. L. and Pryor, B. M. (2013) The sections of Alternaria: formalizing species-group concepts. Mycologia 105(3): 530-546.
Lawrence, D. P., Park, M. S. and Pryor, B. M. (2012) Nimbya and Embellisia revisited, with nov. comb. for Alternaria celosiae and A. perpunctulata. Mycological Progress 11(3): 799-815.
Lawrence, D. P., Rotondo, F. and Gannibal, P. B. (2016) Biodiversity and taxonomy of the pleomorphic genus Alternaria. Mycological Progress 15(1): 1-22.
Mak, Y., Willows, R. D., Roberts, T. H., Wrigley, C. W., Sharp, P. J. and Copeland, L. E. S. (2006) Black point is associated with reduced levels of stress, disease‐and defense‐related proteins in wheat grain. Molecular Plant Pathology 7(3): 177-189.
Nees von Esenbeck, C. G. (1816) Das System derPilze und Schwamme. StahelscheBuchhandlung, Wurzburg.
Oviedo, M. S., Sturm, M. E., Reynoso, M. M., Chulze, S. N. and Ramirez, M. L. (2013) Toxigenic profile and AFLP variability of Alternaria alternata and Alternaria infectoria occurring on wheat. Brazilian Journal of Microbiology 44(2): 447-455.
Perelló, A., Cordo, C. and Simón, M. R. (1996) A new disease of wheat caused by Alternaria triticimaculans in Argentina. Agronomie-Sciences des Productions Vegetales et de l'Environnement 16(2): 107-112.
Perelló, A., Moreno, M. and Sisterna, M. (2008) Alternaria infectoria species‐group associated with black point of wheat in Argentina. Plant Pathology 57(2): 379-379.
Poursafar, A., Ghosta, Y., Orina, A. S., Gannibal, P. B., Javan–Nikkhah, M. and Lawrence, D. P. (2017) Taxonomic study on Alternaria sections Infectoriae and Pseudoalternaria associated with black (sooty) head mold of wheat and barley in Iran. Mycological Progress 17(3): 343-356.
Prescott, J. M., Burnett, P. A., Saari, E. E., Ransom, J., Bowman, J., de Milliano, W., Singh, R. P. and Bekele, G. (1985) Wheat diseases and pests: a guide for field identification. CIMMYT, Mexico.
Pryor, B. M. and Bigelow, D. M. (2003) Molecular characterization of Embellisia and Nimbya species and their relationship to Alternaria, Ulocladium and Stemphylium. Mycologia 95(6): 1141-1154.
Pryor, B. M. and Michailides, T. J. (2002) Morphological, pathogenic, and molecular characterization of Alternaria isolates associated with Alternaria late blight of pistachio. Phytopathology 92(4): 406-416.
Rahimlou, T. and Ghosta, Y. (2015) The occurrence of Alternaria species on cabbage in Iran. Zemdirbyste-Agriculture 102(3): 343-350.
Roberts, R. G., Reymond, S. T. and Andersen, B. (2000) RAPD fragment pattern analysis and morphological segregation of small–spored Alternaria species and species groups. Mycological Research 104(02): 151-160.
Runa, F., Park, M. S. and Pryor, B. M. (2009) Ulocladium systematics revisited: phylogeny and taxonomic status. Mycological Progress 8(1): 35-47.
Schubert, K., Groenewald, J. Z., Braun, U., Dijksterhuis, J., Starink, M., Hill, C. F., Zalar, P., de Hoog, G. S. and Crous, P. W. (2007) Biodiversity in the Cladosporium herbarum complex (Davidiellaceae, Capnodiales), with standardisation of methods for Cladosporium taxonomy and diagnostics. Studies in Mycology 58: 105-156.
Simmons, E. G. (1986) Alternaria themes and variations (17-21). Mycotaxon 25(1): 203-216.
Simmons, E. G. (1992) Alternaria taxonomy: current status, viewpoint, challenge. In: Alternaria: biology, plant diseases, and metabolites (Eds. Chelkowski, J. and Visconti, A.) 1-35. Elsevier, Amsterdam.
Simmons, E. G. (1993) Alternaria themes and variations (63-72). Mycotaxon 68: 91-107.
Simmons, E. G. (1994) Alternaria themes and variations (106-111). Mycotaxon 50: 409-427.
Simmons, E. G. (1996) Alternaria themes and variations (145-149). Mycotaxon 57: 391-409.
Simmons, E. G. (2007) Alternaria. An identification manual. CBS Biodiversity Series 6. CBS Fungal Biodiversity Centre, Utrecht.
Sisterna, M. and Sarandón, S. (2010) Wheat grain discoloration in Argentina: current status. American Journal of Biochemistry and Biotechnology 3(Special Issue 1): 54-64.
Spurlock, T., Faske, T., Kirkpatrick, T., Mills, G. and Kelley, J. (2015) Important wheat diseases in Arkansas and their management. Arkansas Plant Disease Control Products Guide 7: 1-14.
Srivastava, J., Kushwaha, G. and Shukla, D. (2014) Black point disease of wheat and its implications on seed quality. Crop Research 47: 21-23.
Swofford, D. L. (1999) PAUP, Phylogenetic analysis using parsimony, version 4.0b2. Sinauer Associates, Inc, Sunderland.
Thambugala, K. M., Wanasinghe, D. N., Phillips, A. J. L., Camporesi, E., Bulgakov, T. S., Phukhamsakda, C., Ariyawansa, H. A., Goonasekara, I. D., Phookamsak, R., Dissanayake, A., Tennakoon, D. S., Tibpromma, S., Chen, Y. Y., Liu, Z. Y. and Hyde, K. D. (2017) Mycosphere notes 1-50: grass (Poaceae) inhabiting Dothideomycetes. Mycosphere 8(4): 697-796.
Tymon, L. S., Peever, T. L. and Johnson, D. A. (2016) Identification and enumeration of small-spored Alternaria species associated with potato in the US Northwest. Plant Disease 100(2): 465-472.
White, T. J., Bruns, T. D., Lee, S. B. and Taylor, J. W. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications (Eds. Innis, M. A., Gelfand, D. H., Sninsky, J. J. and White, T. J.) 315-322. Academic Press, London.
Woudenberg, J. H. C., Groenewald, J. Z., Binder, M. and Crous, P. W. (2013) Alternaria redefined. Studies in Mycology 75: 171-212.
Woudenberg, J. H. C., Truter, M., Groenewald, J. Z. and Crous, P. W. (2014) Large-spored Alternaria pathogens in section Porri disentangled. Studies in Mycology 79: 1-47.
Zhong, S. and Steffenson, B. J. (2001) Genetic and molecular characterization of mating type genes in Cochliobolus sativus. Mycologia 93(5): 852-863.