Share This Article:

Rice False Smut Fungus, Ustilaginoidea virens, Inhibits Pollen Germination and Degrades the Integuments of Rice Ovule

Abstract Full-Text HTML XML Download Download as PDF (Size:515KB) PP. 2295-2304
DOI: 10.4236/ajps.2013.412284    4,975 Downloads   7,765 Views   Citations

ABSTRACT

Ustilaginoidea virens is a flower-infecting fungus that forms false smut balls in rice panicle. Rice false smut has long been considered a minor disease, but recently it occurred frequently and emerged as a major disease in rice production. In vitro co-cultivation of U. virens strain with young rice panicles showed that U. virens enters inside of spikelets from the apex and then grows downward to infect floral organs. In response to U. virens infection, rice host exhibits elevated ROS accumulation and enhanced callose deposition. The secreted compounds of U. virens can suppress rice pollen germination. Examination of sectioning slides of freshly collected smut balls demonstrated that both pistil and stamens of rice flower are infected by U. virens, hyphae degraded the contents of the pollen cells, and also invaded the filaments. In addition, U. virens entered rice ovary through the thin-walled papillary cells of the stigma, then decomposed the integuments and infected the ovary. The invaded pathogen could not penetrate the epidermis and other layers of the ovary. Transverse section of the pedicel just below the smut balls showed that there were no fungal hyphae observed in the vascular bundles of the pedicel, implicating that U. virens is not a systemic flower-infecting fungus.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

W. Li, L. Li, A. Feng, X. Zhu and J. Li, "Rice False Smut Fungus, Ustilaginoidea virens, Inhibits Pollen Germination and Degrades the Integuments of Rice Ovule," American Journal of Plant Sciences, Vol. 4 No. 12, 2013, pp. 2295-2304. doi: 10.4236/ajps.2013.412284.

References

[1] G. S. Deng, “Present Status of Research on False Smut in China,” Plant Protection (Chinese), Vol. 15, No. 6, 1989, pp. 39-40.
[2] H. Yaegashi, Y. Fujita and R. Sonoda, “Severe Outbreak of False Smut of Rice in 1988,” Plant Protection (Tokyo), Vol. 43, No. 6, 1989, pp. 311-314.
[3] S. Savary, L. Willocquet, F. A. Elazegui, P. S. Teng, P. V. Du, D. F. Zhu, Q. Y. Tang, S. W. Huang, X. Q. Lin, H. M. Sing and R. K. Srivastave, “Rice Pest Constraints in Tropical Asia: Characterization of Injury Profiles in Relation to Production Situation,” Plant Disease, Vol. 84, No. 3, 2000, pp. 341-356.
http://dx.doi.org/10.1094/PDIS.2000.84.3.341
[4] T. Ashizawa, M. Takahashi, J. Moriwaki and H. Kazuyuki, “Quantification of the Rice False Smut Pathogen Ustilaginoidea virens from Soil in Japan Using Real-Time PCR,” European Journal of Plant Pathology, Vol. 128, No. 2, 2010, pp. 221-232.
http://dx.doi.org/10.1007/s10658-010-9647-4
[5] W. A. Orton, “Plant Diseases of 1906,” Year Book US Department of Agriculture. US Government Printing Office, Washington DC, pp. 499-508.
[6] M. C. Rush, A. K. M. Shahjahan and J. P. Jones, “Outbreak of False Smut of Rice in Louisiana,” Pant Disease, Vol. 84, No. 1, 2000, p. 100.
http://dx.doi.org/10.1094/PDIS.2000.84.1.100D
[7] Y. L. Zhou, Y. J. Pan, X. W. Xie, L. H. Zhu, J. L. Xu, S. Wang and Z. K. Li, “Genetic Diversity of Rice False Smut Fungus, Ustilaginoidea virens and Its Pronounced Differentiation of Populations in North China,” Journal of Phytopathology, Vol. 156, No. 9, 2008, pp. 559-564.
http://dx.doi.org/10.1111/j.1439-0434.2008.01387.x
[8] H. S. Chib, M. L. Tikoo, C. S. Kalha, B. R. Gupta, S. K. Sing and P. K. Raina, “Effect of False Smut on Yield of Rice,” Indian Journal of Mycology and Plant Pathology, Vol. 22, No, 3, 1992, pp. 278-280.
[9] D. H. Lu, X. Q. Yang, J. H. Mao, H. L. Ye, P. Wang, Y. P. Chen, Z. Q. He and F. Chen, “Characterising the Pathogenicity Diversity of Ustilaginoidea virens in Hybrid Rice in China,” Journal of Plant Pathology, Vol. 91, No. 2, 2009, pp. 443-451.
[10] T. Ashizawa, M. Takahashi, J. Moriwaki and K. Hirayae, “A Refined Inoculation Method to Evaluate False Smut Resistance in Rice,” Journal of General Plant Pathology, Vol. 77, No. 1, pp. 10-16.
http://dx.doi.org/10.1007/s10327-010-0279-5
[11] Y. X. Tang, J. Jin, D. W. Hu, M. L. Yong, Y. Xu and L. P. He, “Elucidation of the Infection Process of Ustilaginoidea virens (Teleomorph: Villosiclava virens) in Rice Spikelets,” Plant Pathology, Vol. 62, No. 1, 2013, pp. 1-8.
http://dx.doi.org/10.1111/j.1365-3059.2012.02629.x
[12] S. T. Chisholm, G. Coaker, B. Day and B. J. Staskawicz, “Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response,” Cell, Vol. 124, No. 4, pp. 803-814. http://dx.doi.org/10.1016/j.cell.2006.02.008
[13] J. D. G. Jones and J. L. Dangl, “The Plant Immune System,” Nature, Vol. 444, No. 7117, pp. 323-329.
http://dx.doi.org/10.1038/nature05286
[14] C. J. Baker and E. W. Orlandi, “Active Oxygen in Plant Pathogenesis,” Annual Review of Phytopathology,” Vol. 33, 1995, 299-321.
http://dx.doi.org/10.1146/annurev.py.33.090195.001503
[15] G. P. Bolwell, L. V. Bindschedler, K. A. Blee, V. S. Butt, D. R. Davies, S. L. Gardner, C. Gerrish and F. Minibayeva, “The Apoplastic Oxidative Burst in Response to Biotic Stress in Plants: A Three-Component System,” Journal Experimental Botany, Vol. 53, No. 372, 2002, pp. 1367-1376. http://dx.doi.org/10.1093/jexbot/53.372.1367
[16] R. Desikan, S. J. Neill and J. T. Hancock, “Hydrogen Peroxide-Induced Gene Expression in Arabidopsis thaliana,” Free Radical Biology and Medicine, Vol. 28, No. 5, 2000, pp. 773-778.
http://dx.doi.org/10.1016/S0891-5849(00)00157-X
[17] I. Apostol, P. F. Heinstein and P. S. Low, “Rapid Stimulation of an Oxidative Burst during Elicitation of Cultured Plant Cells: Role in Defense and Signal Transduction,” Plant Physiology, Vol. 90, No. 1, 1989, pp. 109-116.
http://dx.doi.org/10.1104/pp.90.1.109
[18] X. Qiu, C. Lei, L. Huang, X. Li, H. Hao, Z. Du, H. Wang, H. Ye, L. Beerhues and B. Liu, “Endogenous Hydrogen Peroxide Is a Key Factor in the Yeast Extract-Induced Activation of Biphenyl Biosynthesis in Cell Cultures of Sorbus aucupari,” Planta, Vol. 235, No.1, 2012, pp. 217-223. http://dx.doi.org/10.1007/s00425-011-1545-2
[19] A. Daudi, Z. Cheng and J. A. O’Brien, “The Apoplastic Oxidative Burst Peroxidase in Arabidopsis Is a Major Component of Pattern-Triggered Immunity,” Plant Cell, Vol. 24, No. 1, 2012, pp. 275-287.
http://dx.doi.org/10.1105/tpc.111.093039
[20] J. A. O’Brien, A. Daudi, P. Finch, V. S. Butt, J. P. Whitlegge, P. Souda, F. M. Ausubel and G. P. Bolwell, “A Peroxidase-dependent Apoplastic Oxidative Burst in Cultured Arabidopsis Cells Functions in MAMP-Elicited Defence,” Plant Physiology, Vol.158, No. 4, 2012, pp. 2013-2027. http://dx.doi.org/10.1104/pp.111.190140
[21] N. K. Clay, A. M. Adio, C. Denoux, G. Jander and F. M. Ausubel, “Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response,” Science, Vol. 323, No. 5910. pp. 95-101.
http://dx.doi.org/10.1126/science.1164627
[22] Y. A. Millet, C. H. Danna, N. K. Clay, W. Songnuan, M. D. Simon, D. Werck-Reichhart and F. M. Ausubel, “Innate Immune Responses Activated in Arabidopsis Roots by Microbe-Associated Molecular Patterns,” Plant Cell, Vol. 22, No. 3, 2010, pp. 973-990.
http://dx.doi.org/10.1105/tpc.109.069658
[23] M. E. Hood and H. D. Shew, “Applications of KOH-Aniline Blue Fluorescence in the Study of Plant-Fungal Interactions,” Phytopathoglogy, Vol. 86, No. 7, 1996, pp. 704-708. http://dx.doi.org/10.1094/Phyto-86-704
[24] T. Ashizawa, M. Takahashi, M. Arai and T. Arie, “Rice False Smut Pathogen, Ustilaginoidea virens, Invades Through Small Gap at the Apex of a Rice Spikelet Before Heading,” Journal of General Plant Pathology, Vol. 78, No. 4, 2012, pp. 255-259.
http://dx.doi.org/10.1007/s10327-012-0389-3
[25] K. Dong, B. Chen, Z. Y. Li, Y. Dong and H. L. Wang, “A Characterization of Rice Pests and Quantification of Yield Losses in the Japonica Rice Zone of Yunnan, China,” Crop Protection, Vol. 29, No. 6, 2010, pp. 603-611.
http://dx.doi.org/10.1016/j.cropro.2010.01.007
[26] G. L. Wang, “Studies on the Infection Period and the Infection Gate of the Chlamydospores of Ustilaginoidea virens (Cooke) Tak. on Rice,” Acta Phytophylacica Sinica, Vol. 19, No. 2, 1992, pp. 97-100.
[27] S. A. Kessler, H. Shimosato-Asano and N. F. Keinath, “Conserved Molecular Components for Pollen Tube Reception and Fungal Invasion,” Science, Vol. 330, No. 6006, 2010, pp. 968-971.
http://dx.doi.org/10.1126/science.1195211
[28] F. Govers and G. C. Angenent, “Fertility Goddesses as Trojan Horses,” Science, Vol. 330, No. 6006, 2010, 922-923. http://dx.doi.org/10.1126/science.1198347
[29] K. Koyama and S. Natori, “Further Characterization of Seven bis (naphtha-γ-pyrone) Congeners of Ustilaginoidins, Pigments of Claviceps virens (Ustilaginoidea virens),” Chemical and Pharmaceutical Bulletin, Vol. 36, No. 1, 1988, pp. 146-152.
http://dx.doi.org/10.1248/cpb.36.146
[30] Y. Koiso, Y. Li, S. Iwasaki, K. Hanaoka, T. Kobayashi, R. Sonoda, Y. Fujita, H. Yaegashi and Z. Sato, “Ustiloxins, Antimitotic Cyclic Peptides from False Smut Balls on Rice Panicles Caused by Ustilaginoidea virens,” Journal of Antibiotics (Tokyo), Vol. 47, No. 7, 1994, pp. 765-773.
http://dx.doi.org/10.7164/antibiotics.47.765
[31] Y. Koiso, N. Morisaki, Y. Yamashita, Y. Mitsui, R. Shirai, Y. Hashimoto and S. Iwasaki, “Isolation and Structure of an Antimitotic Cyclic Peptide, Ustiloxin F: Chemical Interrelation with a Homologous Peptide, Ustiloxin B,” Journal of Antibiotics (Tokyo), Vol. 51, No. 4, 1998, pp. 418-422.
http://dx.doi.org/10.7164/antibiotics.51.418
[32] Y. Li, Y. Koiso, H. Kobayashi, Y. Hashimoto and S. Iwasaki, “Ustiloxins, New Antimitotic Cyclic Peptides: Interaction with Porcine Brain Tubulin,” Biochemical Pharmacology, Vol. 49, No. 10, 1995, pp. 1367-1372.
http://dx.doi.org/10.1016/0006-2952(95)00072-8
[33] H. K. Ngugi and H. Scherm, “Biology of Flower-Infecting Fungi,” Annual Review of Phytopathology, Vol. 44, 2006, pp. 261-282.
http://dx.doi.org/10.1146/annurev.phyto.44.070505.143405

  
comments powered by Disqus

Copyright © 2018 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.