1932

Abstract

False smut of rice, caused by , has become one of the most important diseases in rice-growing regions worldwide. The disease causes a significant yield loss and imposes health threats to humans and animals by producing mycotoxins. In this review, we update our understanding of the pathogen, including the disease cycle and infection strategies, the decoding of the genome, comparative/functional genomics, and effector biology. Whereas the decoding of the genome unveils specific adaptations of the pathogen in successfully occupying rice flowers, progresses in comparative/functional genomics and effector biology have begun to uncover the molecular mechanisms underlying virulence and pathogenicity. We highlight the identification and characterization of the produced mycotoxins and their biosynthetic pathways in .The management strategies for this disease are also discussed. The flower-specific infection strategy makes the pathogen a unique tool to unveil novel mechanisms for the interactions between nonobligate biotrophic pathogens and their hosts.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-010820-012908
2020-08-25
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/phyto/58/1/annurev-phyto-010820-012908.html?itemId=/content/journals/10.1146/annurev-phyto-010820-012908&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ahonsi MO, Adeoti AYA. 2003. Evaluation of fungicides for the control of false smut of rice caused by Ustilaginoidea virens (Cooke) Tak. J. Agric. Res. 4:118–22
    [Google Scholar]
  2. 2.
    An J, Zeng T, Ji C, de Graaf S, Zheng Z et al. 2019. A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytol 224:396–408
    [Google Scholar]
  3. 3.
    Andargie M, Congyi Z, Yun Y, Li J 2017. Identification and evaluation of potential bio-control fungal endophytes against Ustilagonoidea virens on rice plants. World J. Microbiol. Biotechnol. 33:120
    [Google Scholar]
  4. 4.
    Andargie M, Li L, Feng A, Zhu X, Li J 2018. Mapping of the quantitative trait locus (QTL) conferring resistance to rice false smut disease. Curr. Plant Biol. 15:38–43
    [Google Scholar]
  5. 5.
    Ashizawa T, Kataoka Y. 2005. Detection of Ustilaginoidea virens in rice panicles before and after heading in the field using nested-PCR technique with species-specific primers. Jpn. J. Phytopathol. 71:16–19
    [Google Scholar]
  6. 6.
    Ashizawa T, Takahashi M, Arai M, Arie T 2012. Rice false smut pathogen, Ustilaginoidea virens, invades through small gap at the apex of a rice spikelet before heading. J. Gen. Plant Pathol. 78:255–59
    [Google Scholar]
  7. 7.
    Ashizawa T, Takahashi M, Moriwaki J, Hirayae K 2011. A refined inoculation method to evaluate false smut resistance in rice. J. Gen. Plant Pathol. 77:10–16
    [Google Scholar]
  8. 8.
    Atia M. 2004. Rice false smut (Ustilaginoidea virens) in Egypt. J. Plant Dis. Prot. 111:71–82
    [Google Scholar]
  9. 9.
    Brooks SA, Anders MM, Yeater KM 2009. Effect of cultural management practices on the severity of false smut and kernel smut of rice. Plant Dis 93:1202–8
    [Google Scholar]
  10. 10.
    Brooks SA, Anders MM, Yeater KM 2010. Effect of furrow irrigation on the severity of false smut in susceptible rice varieties. Plant Dis 94:570–74
    [Google Scholar]
  11. 11.
    Brooks SA, Anders MM, Yeater KM 2011. Influences from long-term crop rotation, soil tillage, and fertility on the severity of rice grain smuts. Plant Dis 95:990–96
    [Google Scholar]
  12. 12.
    Catanzariti A-M, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–56
    [Google Scholar]
  13. 13.
    Chanclud E, Morel J-B. 2016. Plant hormones: a fungal point of view. Mol. Plant Pathol. 17:1289–97
    [Google Scholar]
  14. 14.
    Chao J, Jin J, Wang D, Han R, Zhu R et al. 2014. Cytological and transcriptional dynamics analysis of host plant revealed stage-specific biological processes related to compatible rice–Ustilaginoidea virens interaction. PLOS ONE 9:e91391
    [Google Scholar]
  15. 15.
    Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–32
    [Google Scholar]
  16. 16.
    Chen X, Hai D, Tang J, Liu H, Huang J et al. 2020. UvCom1 is an important regulator for development and infection in the rice false smut fungus Ustilaginoidea virens. . Phytopathology 110:483–93
    [Google Scholar]
  17. 17.
    Chen Y, Zhang Y, Yao J, Li YF, Yang X et al. 2013. Frequency distribution of sensitivity of Ustilaginoidea virens to four EBI fungicides, prochloraz, difenoconazole, propiconazole and tebuconazole, and their efficacy in controlling rice false smut in Anhui Province of China. Phytoparasitica 41:277–84
    [Google Scholar]
  18. 18.
    Choi W, Dean RA. 1997. The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9:1973–83
    [Google Scholar]
  19. 19.
    Cooke MC. 1878. Some extra-European fungi. Grevillea 7:13–15
    [Google Scholar]
  20. 20.
    Dalio RJD, Herlihy J, Oliveira TS, McDowell JM, Machado M 2018. Effector biology in focus: a primer for computational prediction and functional characterization. Mol. Plant-Microbe Interact. 31:22–33
    [Google Scholar]
  21. 21.
    Deng Q, Yong M, Li D, Lai C, Chen H et al. 2015. Survey and examination of the potential alternative hosts of Villosiclava virens, the pathogen of rice false smut, in China. J. Integr. Agric. 14:1332–37
    [Google Scholar]
  22. 22.
    Dhua U, Dhua SR, Sahu RK 2015. Precise disease severity assessment for false smut disease of rice. J. Phytopathol. 163:931–40
    [Google Scholar]
  23. 23.
    Dodan DS, Singh R. 1996. False smut of rice: present status. Agric. Rev. 17:227–40
    [Google Scholar]
  24. 24.
    Dong K, Fu S. 1989. Sprouting test on sclerotia of rice false smut. J. Shenyang Agric. Univ. 20:359–62
    [Google Scholar]
  25. 25.
    El-Naggar MM, Elsharkawy MM, Almalla RA, El-Kot GAN, Alwakil AM, Badr MM 2015. Control of Ustilaginoidea virens, the causal agent of rice false smut disease in Egypt. Egypt. J. Pest Control 25:555–64
    [Google Scholar]
  26. 26.
    Fan J, Du N, Li L, Li G, Wang Y et al. 2019. A core effector UV_1261 promotes Ustilaginoidea virens infection via spatiotemporally suppressing plant defense. Phytopathol. Res. 1:11
    [Google Scholar]
  27. 27.
    Fan J, Guo XY, Huang F, Li Y, Liu YF et al. 2014. Epiphytic colonization of Ustilaginoidea virens on biotic and abiotic surfaces implies the widespread presence of primary inoculum for rice false smut disease. Plant Pathol 63:937–45
    [Google Scholar]
  28. 28.
    Fan J, Guo XY, Li L, Huang F, Sun WX et al. 2015. Infection of Ustilaginoidea virens intercepts rice seed formation but activates grain-filling-related genes. J. Integr. Plant Biol. 57:577–90
    [Google Scholar]
  29. 29.
    Fan J, Liu J, Gong Z-Y, Xu P-Z, Hu X-H et al. 2020. The false smut pathogen Ustilaginoidea virens requires rice stamens for false smut ball formation. Environ. Microbiol. 22:646–59
    [Google Scholar]
  30. 30.
    Fan J, Yang J, Wang YQ, Li GB, Li Y et al. 2016. Current understanding on Villosiclava virens, a unique flower-infecting fungus causing rice false smut disease. Mol. Plant Pathol. 17:1321–30
    [Google Scholar]
  31. 31.
    Fan LL, Yong ML, Li DY, Liu YJ, Lai CH et al. 2016. Effect of temperature on the development of sclerotia in Villosiclava virens. J. Integr. . Agric 15:2550–55
    [Google Scholar]
  32. 32.
    Fan R, Wang Y, Liu B, Zhang J, Wang H, Hu D 2010. The process of asexual spore formation and examination of chlamydospore germination of Ustilaginoidea virens. . Mycosystema 29:188–92
    [Google Scholar]
  33. 33.
    Fang A, Gao H, Zhang N, Zheng X, Qiu S et al. 2019. A novel effector gene SCRE2 contributes to full virulence of Ustilaginoidea virens to rice. Front. Microbiol. 10:845
    [Google Scholar]
  34. 34.
    Fang A, Han Y, Zhang N, Zhang M, Liu L et al. 2016. Identification and characterization of plant cell death-inducing secreted proteins from Ustilaginoidea virens. Mol. . Plant-Microbe Interact 29:405–16
    [Google Scholar]
  35. 35.
    Fiorin GL, Sanchez-Vallet A, Thomazella DPD, do Prado PFV, do Nascimento LC et al. 2018. Suppression of plant immunity by fungal chitinase-like effectors. Curr. Biol. 28:3023–30
    [Google Scholar]
  36. 36.
    Frandsen RJ, Nielsen NJ, Maolanon N, Sørensen JC, Olsson S et al. 2006. The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol. Microbiol. 61:1069–80
    [Google Scholar]
  37. 37.
    Fu RT, Ding L, Zhu J, Li P, Zheng AP 2012. Morphological structure of propagules and electrophoretic karyotype analysis of false smut Villosiclava virens in rice. J. Microbiol. 50:263–69
    [Google Scholar]
  38. 38.
    Fu RT, Wang J, Lu D, Zhang H, Gong X et al. 2015. Resistance identification and influence factor of rice false smut. Chin. Agric. Sci. Bull. 31:266–72
    [Google Scholar]
  39. 39.
    Guo W, Gao Y, Yu Z, Xiao Y, Zhang Z, Zhang H 2019. The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens. Fungal Genet. Biol 129:65–73
    [Google Scholar]
  40. 40.
    Han Y, Song L, Peng C, Liu X, Liu L et al. 2019. A Magnaporthe chitinase interacts with a rice jacalin-related lectin to promote host colonization. Plant Physiol 179:1416–30
    [Google Scholar]
  41. 41.
    Han Y, Zhang K, Yang J, Zhang N, Fang A et al. 2015. Differential expression profiling of the early response to Ustilaginoidea virens between false smut resistant and susceptible rice varieties. BMC Genom 16:955
    [Google Scholar]
  42. 42.
    Honkura R, Kimura Y. 1988. Some notes on the spore disperse and the period of infection of rice false smut pathogenic fungus. Annu. Rep. Soc. Plant Prot. North Jpn. 39:88–91
    [Google Scholar]
  43. 43.
    Hu DW, Liang WS, Lai CH 2018. Advances in the occurrence of rice false smut and its control. Plant Prot 44:1–5
    [Google Scholar]
  44. 44.
    Hu M, Luo L, Wang S, Liu Y, Li J 2014. Infection processes of Ustilaginoidea virens during artificial inoculation of rice panicles. Eur. J. Plant Pathol. 139:67–77
    [Google Scholar]
  45. 45.
    Huang F, Li Y, Shi J, Fan J, Xu Y-J, Wang W-M 2016. Screening and polymorphism analysis of rice germplasms for resistance to false smut disease in Sichuan Province. Acta Phytotaxon. Sin. 46:247–57
    [Google Scholar]
  46. 46.
    Huang HC, Kokko EG, Erickson RS 1999. Infection of alfalfa pollen by Botrytis cinerea. Bot. Bull. Acad. Sin 40:101–6
    [Google Scholar]
  47. 47.
    Ikegami H. 1960. Studies on the false smut of rice, IV. Infection of the false smut due to inoculation with chlamydospores and ascospores at the booting stage of rice plants. Res. Bull. Fac. Agric. Gifu Univ. 12:45–51
    [Google Scholar]
  48. 48.
    Ikegami H. 1963. Studies on the false smut of rice, X. Invasion of chlamydospores and hyphae of the false smut fungus into rice plants. Res. Bull. Fac. Agric. Gifu Univ. 18:54–60
    [Google Scholar]
  49. 49.
    Jia Q, Lv B, Guo MY, Luo CX, Zheng L et al. 2015. Effect of rice growth stage, temperature, relative humidity and wetness duration on infection of rice panicles by Villosiclava virens. Eur. J. . Plant Pathol 141:15–25
    [Google Scholar]
  50. 50.
    Jiang C, Zhang X, Liu HQ, Xu JR 2018. Mitogen-activated protein kinase signaling in plant pathogenic fungi. PLOS Pathog 14:e1006875
    [Google Scholar]
  51. 51.
    Jin MZ, Li Y. 1987. Survey on the sclerotia of Ustilaginoidea virens in the paddy field. Zhejiang Agric. Sci. 5:238–39
    [Google Scholar]
  52. 52.
    Kämpe J, Kahmann R, Bölker M, Ma L-J, Brefort T et al. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. . Nature 444:97–101
    [Google Scholar]
  53. 53.
    Kaur Y, Lore JS, Pannu PPS 2015. Evaluation of rice genotypes for resistance against false smut. Plant Dis. Res. 30:46–49
    [Google Scholar]
  54. 54.
    Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL et al. 2011. Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. . PLOS Biol 9:e1001094
    [Google Scholar]
  55. 55.
    Khang CH, Park S, Lee Y, Kang S 2005. A dual selection based, targeted gene replacement tool for Magnaporthe grisea and Fusarium oxysporum. Fungal Genet. Biol 42:483–92
    [Google Scholar]
  56. 56.
    Kim KW, Park EW. 2007. Ultrastructure of spined conidia and hyphae of the rice false smut fungus Ustilaginoidea virens. . Micron 38:626–31
    [Google Scholar]
  57. 57.
    Koiso Y, Li Y, Iwasaki S, Hanaoka K, Kobayashi T et al. 1994. Ustiloxins, antimitotic cyclic peptides from false smut balls on rice panicles caused by Ustilaginoidea virens. J. . Antibiot 47:765–73
    [Google Scholar]
  58. 58.
    Koiso Y, Morisaki N, Yamashita Y, Mitsui Y, Shirai R et al. 1998. Isolation and structure of an antimitotic cyclic peptide, ustiloxin F: chemical interrelation with a homologous peptide, ustiloxin B. J. Antibiot. 51:418–22
    [Google Scholar]
  59. 59.
    Koyama K, Natori S. 1988. Further characterization of seven bis(naphtho-γ-pyrone) congeners of ustilaginoidins, pigments of Claviceps virens (Ustilaginoidea virens). Chem. Pharm. Bull. 36:146–52
    [Google Scholar]
  60. 60.
    Koyama K, Ominato K, Natori S, Tashiro T, Tsuruo T 1988. Cytotoxicity and antitumor activities of fungal bis-(naphtho-γ-pyrone) derivatives. J. Pharmacobio-Dynamics 11:630–35
    [Google Scholar]
  61. 61.
    Kumari S, Kumar J. 2015. Evaluation of yield losses and management practices of false smut in rice (Oryza sativa). Indian Phytopathol 68:45–49
    [Google Scholar]
  62. 62.
    Ladhalakshmi D, Laha GS, Singh R, Karthikeyan A, Mangrauthia SK et al. 2012. Isolation and characterization of Ustilaginoidea virens and survey of false smut disease of rice in India. Phytoparasitica 40:171–76
    [Google Scholar]
  63. 63.
    Lai D, Meng J, Xu D, Zhang X, Liang Y et al. 2019. Determination of the absolute configurations of the stereogenic centers of ustilaginoidins by studying the biosynthetic monomers from a gene knockout mutant of Villosiclava virens. Sci. Rep 9:1855
    [Google Scholar]
  64. 64.
    Lai DW, Meng JJ, Zhang XP, Xu D, Dai JG, Zhou LG 2019. Ustilobisorbicillinol A, a cytotoxic sorbyl-containing aromatic polyketide from Ustilaginoidea virens. Org. . Lett 21:1311–14
    [Google Scholar]
  65. 65.
    Li T, Huang S, Zhou JH, Yang B 2013. Designer TAL effectors induce disease susceptibility and resistance to Xanthomonas oryzae pv. oryzae in rice. Mol. Plant 6:781–89
    [Google Scholar]
  66. 66.
    Li Y-S, Huang S-D, Yang J, Wang C-L 2011. Analysis of quantitative trait loci for resistance to rice false smut. Acta Agron. Sin. 37:778–83
    [Google Scholar]
  67. 67.
    Li Y-S, Zhu Z, Zhang Y-D, Zhao L, Wang C-L 2008. Genetic analysis of rice false smut resistance using mixed major genes and polygenes inheritance model. Acta Agron. Sin. 34:1728–33
    [Google Scholar]
  68. 68.
    Li Y, Wang M, Liu Z, Zhang K, Cui F, Sun W 2019. Towards understanding the biosynthetic pathway for ustilaginoidin mycotoxins in Ustilaginoidea virens. Environ. . Microbiol 21:2629–43
    [Google Scholar]
  69. 69.
    Liang Y, Zhang X, Li D, Huang F, Hu P, Peng Y 2014. Integrated approach to control false smut in hybrid rice in Sichuan Province, China. Rice Sci 21:354–60
    [Google Scholar]
  70. 70.
    Liang YF, Han Y, Wang CF, Jiang C, Xu JR 2018. Targeted deletion of the USTA and UvSLT2 genes efficiently in Ustilaginoidea virens with the CRISPR-Cas9 system. Front. Plant Sci. 9:699
    [Google Scholar]
  71. 71.
    Liu T, Song T, Zhang X, Yuan H, Su L et al. 2014. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686
    [Google Scholar]
  72. 72.
    Lore JS, Pannu PPS, Jain J, Hunjan MS, Kaur R, Mangat GS 2013. Susceptibility of rice hybrids and inbred cultivars to false smut under field conditions. Indian Phytopathol 66:397–99
    [Google Scholar]
  73. 73.
    Lu MH, Liu WC, Zhu F 2018. Epidemic law and control technique of rice false smut in recent years. China Plant Prot 38:44–47
    [Google Scholar]
  74. 74.
    Lu S, Sun W, Meng J, Wang A, Wang X et al. 2015. Bioactive bis-naphtho-λ-pyrones from rice false smut pathogen Ustilaginoidea virens. J. Agric. Food Chem 63:3501–8
    [Google Scholar]
  75. 75.
    Lv B, Zheng L, Liu H, Tang JT, Hsiang T, Huang JB 2016. Use of random T-DNA mutagenesis in identification of gene UvPRO1, a regulator of conidiation, stress response, and virulence in Ustilaginoidea virens. Front. Microbiol 7:2086
    [Google Scholar]
  76. 76.
    Meng J, Gu G, Dang P, Zhang X, Wang W et al. 2019. Sorbicillinoids from the fungus Ustilaginoidea virens and their phytotoxic, cytotoxic, and antimicrobial activities. Front. Chem. 7:435
    [Google Scholar]
  77. 77.
    Meng J, Sun W, Mao Z, Xu D, Wang X et al. 2015. Main ustilaginoidins and their distribution in rice false smut balls. Toxins 7:4023–34
    [Google Scholar]
  78. 78.
    Meng J, Zhao S, Dang P, Zhou Z, Lai D, Zhou L 2019. Ustilaginoidin M1, a new bis-naphtho-γ-pyrone from the fungus Villosiclava virens. . Nat. Prod. Res https://doi.org/10.1080/14786419.2019.1652289
    [Crossref] [Google Scholar]
  79. 79.
    Miao QM. 1994. Studies on the sclerotium of Ustilaginoidea virens (Cooke) Tak. J. Yunnan Agric. Univ. 9:101–4
    [Google Scholar]
  80. 80.
    Muniraju KM, Pramesh D, Mallesh SB, Mallikarjun K, Guruprasad GS 2017. Novel fungicides for the management of false smut disease of rice caused by Ustilaginoidea virens. Int. J. Curr. Microbiol. Appl. Sci 6:2664–69
    [Google Scholar]
  81. 81.
    Nakamura K, Izumiyama N, Ohtsubo K, Koiso Y, Iwasaki S et al. 1994. “Lupinosis”-like lesions in mice caused by ustiloxin, produced by Ustilaginoidea virens: a morphological study. Nat. Toxins 2:22–28
    [Google Scholar]
  82. 82.
    NCBI (Natl. Cent. Biotechnol. Inf.) 2019. Ustilaginoidea virens. Genome Assembly Annot. Rep., NCBI Bethesda, MD: https://www.ncbi.nlm.nih.gov/genome/genomes/31935
    [Google Scholar]
  83. 83.
    Ngugi HK, Scherm H. 2006. Biology of flower-infecting fungi. Annu. Rev. Phytopathol. 44:261–82
    [Google Scholar]
  84. 84.
    Prakobsub K, Ashizawa T. 2017. Intercellular invasion of rice roots at the seedling stage by the rice false smut pathogen. Villosiclava virens. J. Gen. Plant Pathol. 83:358–61
    [Google Scholar]
  85. 85.
    Rong N, Yong M, Ying XU, Hu DW 2017. Relationship between ultrastructure of cell walls of rice spikelets and infection specificity of Villosiclava virens. Acta Bot. . Boreali-Occidentalia Sin 37:1–7
    [Google Scholar]
  86. 86.
    Rush MCA, Shahjahan KM, Jones JP 2000. Outbreak of false smut of rice in Louisiana. Plant Dis 84:100
    [Google Scholar]
  87. 87.
    Sander JD, Joung JK. 2014. CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32:347–55
    [Google Scholar]
  88. 88.
    Schroud P, TeBeest DO. 2005. Germination and infection of rice roots by spores of Ustilaginoidea virens. AAES Res. . Ser 540:143–51
    [Google Scholar]
  89. 89.
    Schuler D, Wahl R, Wippel K, Vranes M, Münsterkötter M et al. 2015. Hxt1, a monosaccharide transporter and sensor required for virulence of the maize pathogen Ustilago maydis. . New Phytol 206:1086–100
    [Google Scholar]
  90. 90.
    Shetty SA, Shetty HS. 1985. An alternative host for Ustilaginodea virens (Cooke) Takahashi. IRRI Newslett 10:11
    [Google Scholar]
  91. 91.
    Shibata S, Ogihara Y. 1963. Metabolic products of fungi. XXIII. On ustilaginoidins. 3. The structure of ustilaginoidins B and C. Chem. Pharm. Bull. 11:1576–78
    [Google Scholar]
  92. 92.
    Shibata S, Ogihara Y, Ohta A 1963. Metabolic products of fungi. XXII. On ustilaginoidins. 2. The structure of ustilaginoidin A. Chem. Pharm. Bull. 11:1179–82
    [Google Scholar]
  93. 93.
    Singh RA, Dubey KS. 1980. Effect of different treatments on the dormancy of sclerotia of Claviceps oryzae-sativae. Curr. . Sci 49:115–16
    [Google Scholar]
  94. 94.
    Solomon PS, Oliver RP. 2001. The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. . Planta 213:241–49
    [Google Scholar]
  95. 95.
    Solomon PS, Oliver RP. 2002. Evidence that γ-aminobutyric acid is a major nitrogen source during Cladosporium fulvum infection of tomato. Planta 214:414–20
    [Google Scholar]
  96. 96.
    Song JH, Wei W, Lv B, Lin Y, Yin WX et al. 2016. Rice false smut fungus hijacks the rice nutrients supply by blocking and mimicking the fertilization of rice ovary. Environ. Microbiol. 18:3840–49
    [Google Scholar]
  97. 97.
    Sun WB, Wang A, Xu D, Wang WX, Meng JJ et al. 2017. New ustilaginoidins from rice false smut balls caused by Villosiclava virens and their phytotoxic and cytotoxic activities. J. Agric. Food Chem. 65:5151–60
    [Google Scholar]
  98. 98.
    Tanaka E, Ashizawa T, Sonoda R, Tanaka C 2008. Villosiclava virens gen. nov., comb. nov., teleomorph of Ustilaginoidea virens, the causal agent of rice false smut. Mycotaxon 106:491–501
    [Google Scholar]
  99. 99.
    Tanaka E, Kumagawa T, Ito N, Nakanishi A, Ohta Y et al. 2017. Colonization of the vegetative stage of rice plants by the false smut fungus Villosiclava virens, as revealed by a combination of species-specific detection methods. Plant Pathol 66:56–66
    [Google Scholar]
  100. 100.
    Tang J, Bai J, Chen X, Zheng L, Liu H, Huang J 2020. Two protein kinases UvPmk1 and UvCDC2 with significant functions in conidiation, stress response and pathogenicity of rice false smut fungus Ustilaginoidea virens. Curr. . Genet 66:409–20
    [Google Scholar]
  101. 101.
    Tang YX, Jin J, Hu DW, Yong ML, Xu Y, He LP 2013. Elucidation of the infection process of Ustilaginoidea virens (teleomorph: Villosiclava virens) in rice spikelets. Plant Pathol 62:1–8
    [Google Scholar]
  102. 102.
    Toruño TY, Stergiopoulos I, Coaker G 2016. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54:419–41
    [Google Scholar]
  103. 103.
    Tsuchiya T, Sekita S, Koyama K, Natori S, Takahashi A 1987. Effect of chaetochromin A, chaetochromin D, and ustilaginoidin A, bis(naphtho-γ-pyrone) derivatives, on the mouse embryo limb bud and midbrain cells in culture. Congenit. Anom. 247:245–50
    [Google Scholar]
  104. 104.
    Tsuda M, Sasahara M, Ohara T, Kato S 2006. Optimal application timing of simeconazole granules for control of rice kernel smut and false smut. J. Gen. Plant Pathol. 72:301–4
    [Google Scholar]
  105. 105.
    Tsukui T, Nagano N, Umemura M, Kumagai T, Terai G et al. 2015. Ustiloxins, fungal cyclic peptides, are ribosomally synthesized in Ustilaginoidea virens. . Bioinformatics 31:981–85
    [Google Scholar]
  106. 106.
    Tudzynski P, Scheffer J. 2004. Claviceps purpurea: molecular aspects of a unique pathogenic lifestyle. Mol. Plant Pathol. 5:377–88
    [Google Scholar]
  107. 107.
    Voegele RT, Struck C, Hahn M, Mendgen K 2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. . PNAS 98:8133–38
    [Google Scholar]
  108. 108.
    Wahl R, Wippel K, Goos S, Kamper J, Sauer N 2010. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. . PLOS Biol 8:e1000303
    [Google Scholar]
  109. 109.
    Wang G. 1995. The sexual stage of Ustilaginoidea virens and the infection process of ascospores on rice. J. Zhejiang Wanli Univ. Z1:3–9
    [Google Scholar]
  110. 110.
    Wang WM, Fan J, Jeyakumar JMJ 2019. Rice false smut: an increasing threat to grain yield and quality. Protecting Rice Grains in the Post-Genomic Era Y Jia 89–108 London: IntechOpen
    [Google Scholar]
  111. 111.
    Wang X, Fu X, Lin F, Sun W, Meng J et al. 2016. The contents of ustiloxins A and B along with their distribution in rice false smut balls. Toxins 8:262
    [Google Scholar]
  112. 112.
    Wang XH, Wang J, Lai DW, Wang WX, Dai JG et al. 2017. Ustiloxin G, a new cyclopeptide mycotoxin from rice false smut balls. Toxins 9:54
    [Google Scholar]
  113. 113.
    Wang Y, Wang Y. 2018. Phytophthora sojae effectors orchestrate warfare with host immunity. Curr. Opin. Microbiol. 46:7–13
    [Google Scholar]
  114. 114.
    Wang YQ, Li GB, Gong ZY, Li Y, Huang F et al. 2016. Stachyose is a preferential carbon source utilized by the rice false smut pathogen. Villosiclava virens. Physiol. Mol. Plant Pathol. 96:69–76
    [Google Scholar]
  115. 115.
    Wang Z, Gu Y, Gao Y 1994. Structure of rachillae and its changes during flower opening and closure in rice. J. Jiangsu Agric. Coll. 15:1–10
    [Google Scholar]
  116. 116.
    Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23
    [Google Scholar]
  117. 117.
    Win J, Chaparro-Garcia A, Belhaj K, Saunders DGO, Yoshida K et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235–47
    [Google Scholar]
  118. 118.
    Xie S, Wang Y, Wei W, Li C, Liu Y et al. 2019. The Bax inhibitor UvBI-1, a negative regulator of mycelial growth and conidiation, mediates stress response and is critical for pathogenicity of the rice false smut fungus Ustilaginoidea virens. Curr. . Genet 65:1185–97
    [Google Scholar]
  119. 119.
    Xu J, Xue Q, Luo L, Li Z 2002. Preliminary report on quantitative trait loci mapping of false smut resistance using near-isogenic introgression lines in rice. Acta Agric. Zhejiangensis 14:14–19
    [Google Scholar]
  120. 120.
    Xu Z, Xu X, Gong Q, Li Z, Li Y et al. 2019. Engineering broad-spectrum bacterial blight resistance by simultaneously disrupting variable TALE-binding elements of multiple susceptibility genes in rice. Mol. Plant 12:111434–46
    [Google Scholar]
  121. 121.
    Xue M, Yang J, Li Z, Hu S, Yao N et al. 2012. Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae. . PLOS Genet 8:e1002869
    [Google Scholar]
  122. 122.
    Yang C, Li L, Feng A, Zhu X, Li J 2014. Transcriptional profiling of the responses to infection by the false smut fungus Ustilaginoidea virens in resistant and susceptible rice varieties. Can. J. Plant Pathol. 36:377–88
    [Google Scholar]
  123. 123.
    Yang C, Yu Y, Huang J, Meng F, Pang J et al. 2019. Binding of the Magnaporthe oryzae chitinase MoChia1 by a rice tetratricopeptide repeat protein allows free chitin to trigger immune responses. Plant Cell 31:172–88
    [Google Scholar]
  124. 124.
    Ye Y, Minami A, Igarashi Y, Izumikawa M, Umemura M et al. 2016. Unveiling the biosynthetic pathway of the ribosomally synthesized and post-translationally modified peptide ustiloxin B in filamentous fungi. Angew. Chem. Int. Ed. Engl. 55:8072–75
    [Google Scholar]
  125. 125.
    Yong ML, Deng QD, Fan LL, Miao JK, Lai CH et al. 2018. The role of Ustilaginoidea virens sclerotia in increasing incidence of rice false smut disease in the subtropical zone in China. Eur. J. Plant Pathol. 150:669–77
    [Google Scholar]
  126. 126.
    Yong ML, Fan LL, Li DY, Liu YJ, Cheng FM et al. 2016. Villosiclava virens infects specifically rice and barley stamen filaments due to the unique host cell walls. Microsc. Res. Tech. 79:838–44
    [Google Scholar]
  127. 127.
    Yong ML, Liu YJ, Chen TQ, Fan LL, Wang ZY, Hu DW 2018. Cytological studies on the infection of rice root by Ustilaginoidea virens. Microsc. Res. Tech 81:389–96
    [Google Scholar]
  128. 128.
    Yu JJ, Sun WX, Yu MN, Yin XL, Meng XK et al. 2015. Characterization of mating-type loci in rice false smut fungus Villosiclava virens. . FEMS Microbiol. Lett 362:fnv014
    [Google Scholar]
  129. 129.
    Yu JJ, Yu MN, Song TQ, Cao HJ, Pan XY et al. 2019. A homeobox transcription factor UvHOX2 regulates chlamydospore formation, conidiogenesis, and pathogenicity in Ustilaginoidea virens. Front. . Microbiol 10:1071
    [Google Scholar]
  130. 130.
    Yu M, Yu J, Hu J, Huang L, Wang Y et al. 2015. Identification of pathogenicity-related genes in the rice pathogen Ustilaginoidea virens through random insertional mutagenesis. Fungal Genet. Biol. 76:10–19
    [Google Scholar]
  131. 131.
    Zhang HF, Liu KY, Zhang X, Tang W, Wang JS et al. 2011. Two phosphodiesterase genes, PDEL and PDEH, regulate development and pathogenicity by modulating intracellular cyclic AMP levels in Magnaporthe oryzae. . PLOS ONE 6:e17241
    [Google Scholar]
  132. 132.
    Zhang K, Li Y, Li T, Li Z-G, Hsiang T et al. 2017. Pathogenicity genes in Ustilaginoidea virens revealed by a predicted protein–protein interaction network. J. Proteome Res. 16:1193–206
    [Google Scholar]
  133. 133.
    Zhang N, Yang J, Fang AF, Wang J, Li D et al. 2019. The essential effector SCRE1 in Ustilaginoidea virens suppresses rice immunity via a small peptide region. Mol. Plant Pathol. In press
    [Google Scholar]
  134. 134.
    Zhang Y, Zhang K, Fang A, Han Y, Yang J et al. 2014. Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nat. Commun. 5:3849
    [Google Scholar]
  135. 135.
    Zhang Z, Du X, Chai R, Wang J, Qiu H et al. 2008. Cloning of a homologous gene of Magnaporthe grisea PMK1 type MAPK from Ustilaginoidea virens and functional identification by complement in Magnaporthe grisea corresponding mutant. Acta Microbiol. Sin. 48:1473–78
    [Google Scholar]
  136. 136.
    Zheng D, Yi W, Yu H, Xu JR, Wang C 2016. UvHOG1 is important for hyphal growth and stress responses in the rice false smut fungus Ustilaginoidea virens. . Sci. Rep 6:24824
    [Google Scholar]
  137. 137.
    Zheng MT, Ding H, Huang L, Wang YH, Yu MN et al. 2017. Low-affinity iron transport protein Uvt3277 is important for pathogenesis in the rice false smut fungus Ustilaginoidea virens. Curr. . Genet 63:131–44
    [Google Scholar]
  138. 138.
    Zhou J, Wang X-S. 2011. Field efficacy of 27.12% cuproxat SC against rice false smut Ustilaginoidea oryzae. . Agrochem. Res. Appl 15:21–22
    [Google Scholar]
  139. 139.
    Zhou L, Lu S, Shan T, Wang P, Sun W et al. 2012. Chemistry and biology of mycotoxins from rice false smut pathogen. In Mycotoxins: Properties. Applications and Hazards BJ Melborn, JC Greene 109–30 New York: Nova Sci. Publ.
    [Google Scholar]
  140. 140.
    Zhou YL, Xie XW, Wang S, Pan YJ, Liu XZ et al. 2006. Detection of Ustilaginoidea virens from rice field and plants by nested PCR. J. Agric. Biotechnol. 14:542–45
    [Google Scholar]
  141. 141.
    Zhou YL, Xie XW, Zhang F, Wang S, Liu XZ et al. 2014. Detection of quantitative resistance loci associated with resistance to rice false smut (Ustilaginoidea virens) using introgression lines. Plant Pathol 63:365–72
    [Google Scholar]
  142. 142.
    Zhou YX, Yu JJ, Pan XY, Yu MN, Du Y et al. 2019. Characterization of propiconazole field-resistant isolates of Ustilaginoidea virens. Pestic. Biochem. . Physiol 153:144–51
    [Google Scholar]
  143. 143.
    Zhu L. 2015. Changes of vigor, physiology, biochemistry and storability during hybrid rice seeds maturity and the effect of dehydrating agent application PhD Thesis, Zhejiang Univ Zhejiang, China:
    [Google Scholar]
/content/journals/10.1146/annurev-phyto-010820-012908
Loading
/content/journals/10.1146/annurev-phyto-010820-012908
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error