Morphological and Phylogenetic Characterization of Whip Smut on Commercial Sugarcane Cultivars and Assessing the Resistance to Sporisorium scitamineum

Document Type : Research Article

Authors

1 Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Iran

2 Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz

3 Biotechnology and Bioscience Research Center, Shahid Chamran University of Ahvaz, Iran

4 Plant Production & Genetics Department, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Iran

5 Iranian Sugarcane Research and Training Institute (ISCRTI), Ahvaz, Iran

Abstract

Whip smut, which is caused by Sporisorium scitamineum, is an important disease in areas where sugarcane is cultivated in Iran, particularly in the Khuzestan province. The pathogen significantly reduces sugarcane yield, and the use of resistant cultivars is the most cost-effective strategy for managing the disease. The present study characterized the S. scitamineum strains collected from five commercial sugarcane cultivars (CP69-1062, CP57-614, CP48-103, SP70-1143, and NCo310) based on their morphological and phylogenetic features. The sporidial cultures of the strains appeared in two growth forms: cottony colony and yeast-like. All strains were found to be identical based on the DNA sequences of ITS, COX3, GAPDH, and EF1α regions, and revealed that all strains were identical (100%) to the reference strain of S. scitamineum. The disease incidence of the cultivars varied from 5 to 43% during two consecutive years. Statistical analysis of the growth rates of the strains indicated significant differences. Combined analysis of variance (ANOVA) suggested that the effects of year, strain, cultivar, and the interaction effect of strain ´ cultivar were significant at a 1% probability level. Our results suggest that IRK310 was the most virulent among all cultivars, with different pathogenicity percentages, while the strain IRK70 had the lowest level of virulence among all strains. Among the tested cultivars, SP70-1143 and CP57-614 showed high resistance to smut. In this research, teliospore populations of whip smut were identified, and disease reactions of the cultivars were assayed. Screening and selecting smut-resistant cultivars can help reduce disease damage in cultivated areas and can serve as a basis for further research on plant disease management.

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Abdou, Y. A., Moursy, M. A., Abdel-Fattah, M. N. D., & Mansour, I. M. (1990). Effect of temperature and certain cultural practices on longevity of teliospores of Ustilago scitaminea. Bulletin of the Faculty of Agriculture, University of Cairo, 41(2), 511-520. https://ejarc.journals.ekb.eg/journal/about
Abera, T. (1991). Characterization of Ustilago scitaminea Syd. isolates and evaluation of sugarcane (Saccharum officinarum L.) varieties for resistance to smut [Doctoral dissertation. Alemaya University].
Ahmadpour, S. A., Mehrabi-Koushki, M., Farokhinejad, R. (2017). Neodidymelliopsis farokhinejadii, a new fungal species from dead branches of trees in Iran. Sydowia, 69(171), 182. http://doi.org/10.12905/03-80.sydowia69-2017-0169
Ainsworth, G. C. (1965). Ustilago scitaminea. Descriptions of Fungi and Bacteria, 8. https://doi.org/10.1079/DFB/2005640008
Mansouri, M., Hassanzadeh, E. (2021). Policies and programs of Iranian governments in the sugar crisis in World War II. EcoSocial History studies, 9(2): 267-297. https://doi.org/10.30465/sehs.2021.34237.1658
Bhondave, T. S., Patil, S. A., Medhane, N., Jadhav, B. S. (1994). Effect of moist hot air treatment and fungicides on smut, yield and quality of sugarcane. Indian Sugar, 44(8), 653-656. https://typeset.io/journals/indian-sugar-2ja4j3gd
Bhuiyan, S. A., Croft, B. J., James, R. S., Cox, M. C. (2012). Laboratory and field evaluation of fungicides for the management of sugarcane smut caused by Sporisorium scitamineum in seedcane. Australasian Plant Pathology, 41(6), 591-599. https://doi.org/10.1007/s13313-012-0139-1
Bhuiyan, S. A., Croft, B. J., Stringer, J. K., Deomano, E. C., (2015). Pathogenic variation in spore populations of Sporisorium scitamineum, causal agent of sugarcane smut in Australia. Plant Disease, 99(1), 93-99. https://doi.org/10.1094/PDIS-12-13-1257-RE
Comstock, J. C., Croft, B. J., Saumtally, A. S. (2000). A guide to sugarcane diseases. CIRAD/ISSCT, Montpellier, France.
Croft, B. J., Braithwaite, K. S., (2006). Management of an incursion of sugarcane smut in Australia. Australasian Plant Pathology, 35(2), 113-122. https://doi.org/10.1071/AP05104
Darriba, D., Taboada, G. L., Doallo, R., Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9(8), 772-772. https://doi.org/10.1038/nmeth.2109
Deng, Q., Xu, G., Dou, Z., Shen, W. (2018). Identification of three Sporisorium scitamineum pathogenic races in mainland China. International Journal of Agriculture and Biology, 20(4), 799-802. http://doi.org/10.17957/IJAB/15.0566
Dotaniya, M. L., Datta, S. C., Biswas, D. R., Dotaniya, C. K., Meena, B. L., Rajendiran, S., ... & Lata, M. (2016). Use of sugarcane industrial by-products for improving sugarcane productivity and soil health. International Journal of Recycling of Organic Waste in Agriculture, 5(3), 185-194. https://doi.org/10.1007/s40093-016-0132-8
Edler, D., Klein, J., Antonelli, A., Silvestro, D. (2021). raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12(2), 373-377. https://doi.org/10.1111/2041-210X.13512
Ershad, D., Bani-Abbassi, N. (1971). The occurrence of the sugarcane smut in Iran, Iranian Journal Plant Pathology, 7, 19-22. https://www.ijpp.ir/?lang=en
Fauconnier, R. (1993). Sugar cane (The tropical agriculturist), Macmillan Press Ltd, London and Basingstoke.
Fereol, L. (1984). Inoculation of in vitro cultivated sugarcane with smut (Ustilago scitaminea). Canadian Journal of Botany, 62(10), 2043-2046. https://doi.org/10.1139/b84-278
Gravois, K., Viator, S., Reagan, T. E., Beuzelin, J. M., Griffin, J. L., Tubana, B. S., Hoy, J. W. (2014). Louisiana State University Agricultural Center Pub, 2859.
Hall, B. G. (2008). Phylogenetic trees made easy: a how-to manual. 3rd ed, Sinouer Associates, Sunderland, Massachusetts 125-141. ‏http://doi.org/10.1086/669273
Harlapur, S. I., Palakshappa, M, G., Chattannavar, S. N., Patil, R. S., Murthy TDK. (1992). Effect of hot water treatment against disease incidence in sugarcane. Current Research-University of Agricultural Sciences-Bangalore, 21(4), 6-9. https://doi.org/10.46429/jaupr.v46i2.12300
Hassin, M. A. A. (2016). Screening for Resistance to Smut Disease of Twenty-Seven Sugarcane Varieties. [Doctoral dissertation, Sudan University of Science and Technology].
Hoy, J. W., Jiaxie, Z., Grelen, L. B., Geaghan, J. P. (1993). Longevity of teliospores of Ustilago scitaminea in soil. Plant Disease, 77(4), 393-397. https://doi.org/10.1094/PD-77-0393
Huang, S. H. (2004). Progress of sugarcane disease research in China: recent developments. Sugar Tech, 6(4), 261-265. https://doi.org/10.1007/BF02942506
Izadi, M. B., Moosawi-Jorf, S, A. (2007). Isolation and identification of yeast-like and mycelial colonies of Ustilago scitaminea using specific primers. Asian Journal of Plant Sciences, 6(7), 1137-1142. http://doi.org/10.39-23/ajps.2007.1137.1142
Jacques-Edouard, Y. K., Didier, K. K., Gaston, K. K., Jean-Martial, K. K. F., N’guessan Aya Carine, E. E., Ghislain, C., Daouda, K., (2020). Structure of Sporisorium scitamineum isolates, the causative agent of sugarcane smut in Côte d’ivoire. International Journal of Science and Research, 9(3), 1376-1381. https://doi:10.21275/SR203070-72052
Kouamé, D. k., Péné, C. b., Zouzou, M., (2012). Response of some promising cane varieties under natural infections of sugarcane smut Sporisorium scitamineum in Ivory Coast. African Journal of Agricultural Research, 7(41), 5604-5610. https://doi: 10.5897/ AJAR12.1611
Mario, P. C., Raphaël, A., Marcelo, D. A. S., Celso, V. P., Antonio, P. D. C., Marcos, G. D. A. L., Maria, B. S. F. (1995). Sugarcane breeding: evaluation of clones obtained by hybridizations in 1980 and selected in Jau Region, State of Sao Paulo, Brazil. Bragantia, Campinas, 54(1), 95-102. https://doi.org/10.1590/S000687051995000100010
Matsuoka, S., Ferro, J., Arruda, P., (2009). The Brazilian experience of sugarcane ethanol industry. In Vitro Cellular & Developmental Biology-Plant, 45, 372-381. https://doi.org/10.1007/s11627-009-9220-z
McTaggart, A. R. (2010). Systematics of the Ustilago-Sporisorium-Macalpinomyces complex of smut fungi. [Doctoral dissertation, Queensland University of Technology]. https://eprints.qut.edu.au/47047/
Viswanathan, R., & Rao, G. P. (2011). Disease scenario and management of major sugarcane diseases in India. Sugar Tech13, 336-353. https://doi.org/10.1007/s12355-011-0102-4.
Pearse, T. L. (1989). Influence of roguing on the incidence of smut in Swaziland. Proceedings of the South African Sugar Technologists' Association, 63, 117-121. https://sasta.co.za/congress-proceedings/
Pereira, B. M. H. (2001). Study of genetic divergence in sugarcane varieties grown in Brazil using the parentage coefficient. International Sugar Journal, 103(1231), 294-295. https://internationalsugarjournal.com/
Raeder, U., Broda, P. (1985). Rapid preparation of DNA from filamentous fungi. Letters in Applied Microbiology, 1(1), 17-20. https://doi.org/10.1-111/j.1472765X.1985.tb01479.x
Rajput, M.A., Rajput, N. A., Syed, R. N., Lodhi, A. M., Que, Y. (2021). Sugarcane smut: current knowledge and the way forward for management. Journal of Fungi, 7(12), 1095. https://doi.org/10.3390/jof7121095
Ricaud, C., Egan, B. T., Gillaspie, A. G., Hughes, C. G. (2012). Diseases of sugarcane: major diseases. Elsevier Science.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic biology, 61(3), 539-542. https://doi.org/10.1093/sysbio/sys029
Sakaigaichi, T., Terajima, Y., Matsuoka, M., Irei, S., Fukuhara, S., Mitsunaga, T., Hayano, M. (2019). Evaluation of sugarcane smut resistance in wild sugarcane (Saccharum spontaneum L.) accessions collected in Japan. Plant Production Science, 22(2), 327-332. https:-//doi.org/10.1080/1343943X.2018.1535834
SAS. (2002). SAS software, Version 9.1 of the SAS system for windows. Cary: SAS Institute Inc.
Scortecci, K. C., Creste, S., Calsa Jr, T., Xavier, M. A., Landell, M.G., Figueira, A., Benedito, V. A. (2012). Challenges, opportunities and recent advances in sugarcane breeding. Plant Breeding, 1, 267-296. http://doi.org/10.5772/28606
Singh, N., Somai, B. M., Pillay, D. (2005a). In vitro screening of sugarcane to evaluate smut susceptibility. Plant cell, tissue and organ culture, 80, 259-266. https://www.springer.com/journal/11240
Singh, N., Somai, B. M., Pillay, D. (2005b). Molecular profiling demonstrates limited diversity amongst geographically separate strains of Ustilago scitaminea. FEMS Microbiology Letters, 247(1), 7-15. https://doi.org/10.1016/j.femsle.2005.04.022
Singh, P., Kumar, B., Jindal, M. M., Rani, R. (2014). Management of sugarcane smut (Ustilago scitaminea) with fungicides and bio-agents. African Journal of Microbiology Research, 8(51), 3954-3959. https://academicjournals.org/journal/AJMR
Sundar, A. R., Barnabas, E. L., Malathi, P., Viswanathan, R., Sundar, A. R., Barnabas, E. L. (2012). A mini-review on smut disease of sugarcane caused by Sporisorium scitamineum. Botany, 2014, 108- 228. https://doi.org/10.5772/34116
Suzuki, S., Maffia, L. A., Cruz Filho, J. (1994). Survival of teliospores of Ustilago scitaminea in the soil. Fitopatologia Brasileira (Brazil). 19 (3): 442-448. https://www.scielo.br/j/fb/
Syed, A., Fahmy, Z., El-Samman, M., Mostafa, M. H. (2015). Phylogenetic diversity among some isolates of Ustilago scitaminae Sydow the causal agent of whip smut of sugarcane in Egypt. American International Journal of Research in Formal, Applied and Natural Science, 10(1), 46-55. http://www.iasir.net.
Tafesse, A., Zekarias, Y., Yirefu, F., Mengistu, L. (2009). Handbook for sugarcane pest management in Ethiopia. Wonji, Ethiopia.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 272-2729.https://doi.org/10.1093/molbev/mst197
Thokoane, L. N., Rutherford, R. S. (2001). cDNA-AFLP differential display of sugarcane (Saccharum spp, hybrids) genes induced by challenge with the fungal pathogen Ustilago scitaminea (sugarcane smut). South African Sugar Technologists' Association, 75,104-107. https://sasta.co.za/
Tiwari, A. K., Singh, A., Singh, S. P, Dagar, A., Kumari, K., Kumar, D., Kumar, P. (2017). An overview of major fungal diseases of sugarcane in India: detection and management strategies. In: Singh, B.P., Gupta, V.K. (eds) Molecular Markers in Mycology. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-34106-4_14
Wada, A. C., Iwo, G. A. (1997). Evaluation of some sugarcane accessions for their reactions to smut disease (Ustilago scitaminea Syd) in Nigeria. African journal of Natural Sciences, 1(1), 93-95. https://www.ajns.org.ng/
Wada, A.C., Mian, M. A. W., Anaso, A. B., Busari, L. D., Kwon-Ndung, E. H. (1999). Control of sugarcane smut (Ustilago scitaminea Syd) disease in Nigeria and suggestions for an integrated pest management approach. Sugar Technology, 1(3), 48-53. https://www.springer.com/journal/12355
Toju, H., Tanabe, A. S., Yamamoto, S., Sato, H. (2012). High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS One, 7(7), e40863. https://doi.org/10.1371/journal.pone.0040863
Xu, L. P., Chen, R.K. (2000). Current status and prospects of smut and smut resistance breeding in sugarcane. Journal of Fujian Agricultural Science, 15(2), 26-31. http://edit.fjnyxb.cn/EN/1008-0384/home.shtml Zekarias, Y., Dejene, M., Tegegn, G., Yirefu F. (2013). Study on cultural and pathogenic variability of Ustilago scitaminea isolates in the sugarcane plantations of Ethiopia. Proceedings of Ethiopian Sugar Industry Biennial Conference, 2, 111-120.