Abstract
Rice false smut is heavily and increasingly occurring in subtropical zones in China in the past decades. The pathogen of the disease, Ustilaginoidea virens, can produce both chlamydospores and sclerotia, and the sclerotia seem to form frequently in temperate or high-altitude regions in China. Which of these structures play a dominant role in the pathogen’s life cycle in subtropical zones remains unclear. Here we found that Ustilaginoidea virens could produce a great number of sclerotia in subtropical zones and the maximal number of sclerotia could reach to 2.25 million per hectare. In the year with relatively low autumn temperatures, the disease severity and sclerotia numbers of U. virens increased significantly. Although there was a few sclerotia in subtropical zones capable of overwintering successfully, one individual sclerotium could produce large numbers of ascospores. In the rice-growing paddy field, the ascospores could be trapped in both temperate and subtropical zones in May–September, when rice was at the booting stage, the critical infection period of rice false smut. This suggested that the sclerotia of rice false smut in subtropical zone played an important role in the life cycle of Ustilaginoidea virens and acted as the primary inoculum. Experiments in the laboratory showed that mature sclerotia of rice false smut remained dormant for about 2–5 months, and that light was essential for fruiting body differentiation. As with ergot, the fruiting bodies of Ustilaginoidea virens secreted sticky droplets on the stromata that prevented the ascospores from dispersing into the air, implying that the transfer of ascospores of Ustilaginoidea virens to rice plants in paddy field needed an intermediary vector.
Similar content being viewed by others
References
Atia, M. M. M. (2004). Rice false smut (Ustilaginoidea virens) in Egypt. Journal of Plant Diseases and Protection, 111, 71–82.
Dong, K., & Fu, S. Y. (1989). Sprouting test on sclerotia of rice false smut. Journal of Shenyang Agriculture University, 20, 359–362.
Fan, R. H., Wang, Y. Q., Liu, B., Zhang, J. Z., & Hu, D. W. (2010). Asexual spore formation of Ustilaginodea virens in artificial medium and their germination features. Mycosystema, 29, 188–192 (In Chinese with English abstract).
Fan, J., Guo, X. Y., Huang, F., Li, Y., Liu, Y. F., Li, L., Xu, Y. J., Zhao, J. Q., Xiong, H., Yu, J. J., & Wang, W. M. (2014). Epiphytic colonzation of Ustilaginoidea virens on biotic and abiotic surfaces implies the widespread presence of primary inoculum for rice false smut disease. Plant Pathology, 63, 937–945.
Fan, L. L., Yong, M. L., Li, D. Y., Liu, Y. J., Lai, C. H., Chen, H. M., Cheng, F. M., & Hu, D. W. (2016). Effect of temperature on the development of sclerotia in Villosiclava virens. Journal of Integrative Agriculture. doi:10.1016/S2095-3119(16)61400-4.
Fujita, Y., Sonoda, R., & Yagashi, H. (1989). Inoculation with conidiospores of false smut fungus to rice panicles at the booting stage. Annals of the Phytopathological Society of Japan, 55, 629–634 (in Japanese with English summary).
Fujita, Y., Sonoda, R., & Yaegashi, H. (1990). The fruiting body formation in the sclerotia of Ustilaginoidea viren and the effect by light. Annual Report of the Society of Plant Protection of North Japan, 41, 205 (Abstract, in Japanese).
Haarmann, T., Rolke, Y., Giesbert, S., & Tudzynski, P. (2009). Ergot: From witchcraft to biotechnology. Molecular Plant Pathology, 10, 563–577.
Honkura, R., & Miura, Y. (1988). Some notes on the spore disperse and the period of infection of rice false smut pathogenic fungus. Annual Report of the Society of Plant Protection of North Japan, 39, 88–91 (in Japanese).
Hu, D. W., & Wang, S. (2012). Progress and perspectives in infection mechanism of Ustilaginoidea virens. Scientia Agricultura Sinica, 45, 4604–4611 (in Chinese with English abstract).
Hu, M. L., Luo, L. X., Wang, S., Liu, Y. F., & Li, J. Q. (2014). Infection processes of Ustilaginoidea virens during artificial inoculation of rice panicles. European Journal of Plant Pathology, 139, 67–77.
Ikegami, H. (1963). Studies on the false smut of rice. IX. Occurrence and development of sclerotia of the rice false smut fungus. Research Bulletin of the faculty of Agriculture, Gifu University, 18, 47–53.
Jin, M. Z., & Li, Y. (1987). Survey on the sclerotia of Ustilaginoidea virens in the paddy field. Zhejiang Agricultural Sciences, 5, 238–239 (in Chinese).
Li, Y. G., Kang, B. J., Zhang, B. L., Lan, Y. T., Zeng, H. L., Ma, H. K., Xie, K. X., & Li, T. F. (1986). Primary studies on rice false smut. Guangdong Agricultural Sciences, 4, 45–47 (in Chinese).
Li, D. Y., Deng, Q. D., Yong, M. L., Wang, H., Lai, C. H., Chen, H. M., He, W. M., & Hu, D. W. (2016). Screening of biocontrol fungi against sclerotia of Villosiclava virens and their mechanisms. Chinese Journal of Biological Control, 32(2), 258–264.
Liu, S. F., & Chen, Z. J. (1995). Studies on primary infection source and infection route of rice false smut. Tianjing Agricultural. Sciences, 1, 9–11 (in Chinese).
Miao, Q. M. (1994). Studies on the sclerotium of Ustilaginoidea virens (Cooke) Tak. Journal of Yunnan Agricultural University, 9(2), 101–104 (in Chinese).
Miklis, M., Consonni, C., Bhat, R. A., Lipka, V., Schulze-Lefert, P., & Panstruga, R. (2007). Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiology, 144, 1132–1143.
Padwick, G. W. (1950). Manual of Rice diseases. London: CAB Press.
Rush, M. C., Shahjahan, A. K. M., Jones, J. P., & Groth, D. E. (2000). Outbreak of false smut of rice in Louisiana. Plant Disease, 84, 100. (abstract).
Sakurai, M. (1934). On the causal fungus of rice false smut. Annals of the Phytopathological Society of Japan, 3(1), 70–71 (in Japanese Abstract).
Singh, R. A., & Dube, K. S. (1976). Occurrence of true sclerotia in Claviceps oryzae-sativae the causal organism of false smut of rice. Current Science, 45, 772–773.
Singh, R. A., & Dubey, K. S. (1980). Effect of different treatments on the dormancy of sclerotia of Claviceps Oryzae-sativae. Current Science, 49(03), 115–116.
Singh, A. K., & Pophaly, D. J. (2010). An unusual rice false smut epidemic reported in Raigarh District, Chhattisgarh, India. International Rice Research Notes, 35, 1–3.
Tanaka, E., Ashizawa, T., Sonoda, R., & Tanaka, C. (2008). Villosiclava virens gen. Nov., com. Nov., teleomorph of Ustilaginoidea virens, the causal agent of rice false smut. Mycotaxon, 106, 491–501.
Tang, Y. X., Jin, J., Hu, D. W., Yong, M. L., Xu, Y., & He, L. P. (2013). Elucidation of the infection process of Ustilaginoidea virens (teleomorph: Villosiclava virens) in rice spikelets. Plant Pathology, 62, 1–8.
Wang, S., Bai, Y. J., Zhou, Y. L., Yao, J. M., & Bai, J. K. (1998). The pathogen of false smut of rice. Acta Phytopathologica Sinica, 28(1), 19–24 (in Chinese).
Wang, Y. Q., Fan, R. H., Liu, B., Li, S. H., Zheng, D. W., Zhang, J. Z., & Hu, D. W. (2010). Preliminary analysis of rDNA-IGS of Ustilaginoidea virens isolates from different geographical regions in China. Acta Phytophylacica Sinica, 40(2), 214–216 (in Chinese with English abstract).
Whittaker, S. L., Shattock, R. C., & Shaw, D. S. (1991). Variation in DNA content of nuclei of Phytophthora infestans as measured by a microfluorimetric method using the fluorochrome DAPI. Mycological Research, 95, 602–610.
Willetts, H. J., & Bullock, S. (1992). Developmental biology of sclerotia. Mycological Research, 96, 801–816.
Yaegashi, H., Fujita, Y., & Sonoda, R. (1989). Severe outbreak of false smut of rice in 1988. Plant Protection Tokyo, 43, 311–314 (in Japanese).
Yamamoto, S., & Yoshino, J. (1955). Storage period of sclerotia of Ustilaginoidea virens. Annual Report of Kanto-Tosan Plant Protection Society, 2, 10 (In Japanese).
Yong, M. L., Fan, L. L., Li, D. Y., Liu, Y. J., Cheng, F. M., Xu, Y., Wang, Z. Y., & Hu, D. W. (2016). Villosiclava virens infects specifically rice and barley stamen filaments due to the unique host cell walls. Microscopy Research and Technique. doi:10.1002/jemt.22710.
Zhang, Y., Zhang, K., Fang, A. F., Han, Y. Q., Yang, J., Xue, M. F., Bao, J. D., Hu, D. W., Zhou, B., Sun, X. Y., Li, S. J., Wen, M., Yao, N., Ma, L. J., Liu, Y. F., Zhang, M., Huang, F., Luo, C. X., Zhou, L. G., Li, J. Q., Chen, Z. Y., Miao, J. K., Wang, S., Lai, J. S., Xu, J. R., Hsiang, T., Peng, Y. L., & Sun, W. X. (2014). Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nature Communications, 5. doi: 10.1038/ncomms4849.
Acknowledgments
This study was sponsored by the National Natural Science Foundation of China (31671969), the state key special program (2016YFD0300706), the Agricultural Technology Extension Funds of Zhejiang University and the San-nong-liu-fang Project of Zhejiang (CTZB-F160728AWZ-SNY1-30). We thank Dr. Xuanli Jiang at Guizhou University and Dr. Hua Zhao at Jinhua Science and Technology College for kindly providing some sclerotia collected in their regions. We are grateful to Dr. Tanaka with Ishikawa Prefectural University and Dr. Ikegami, a retired and honor professor at Gifu University in Japan for their advices. We also thank Miss Si-jia Hao for her help with sclerotial germination experiments.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Yong, M., Deng, Q., Fan, L. et al. The role of Ustilaginoidea virens sclerotia in increasing incidence of rice false smut disease in the subtropical zone in China. Eur J Plant Pathol 150, 669–677 (2018). https://doi.org/10.1007/s10658-017-1312-8
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-017-1312-8