Transcriptional profiling of the responses to infection by the false smut fungus Ustilaginoidea virens in resistant and susceptible rice varieties

References

• 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. 78:255–259. doi:10.1007/s10327-012-0389-3
   Web of Science ®Google Scholar
• 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. doi:10.1007/s10327-010-0279-5
   Web of Science ®Google Scholar
• Bagnaresi P, Biselli C, Orrù L, Urso S, Crispino L, Abbruscato P, Piffanelli P, Lupotto E, Cattivelli L, Valè G. 2012. Comparative transcriptome profiling of the early response to Magnaporthe oryzae in durable resistant vs susceptible rice (Oryza sativa L.) genotypes. PLoS One. 7:e51609. doi:10.1371/journal.pone.0051609
   Google Scholar
• Bari R, Jones JD. 2009. Role of plant hormones in plant defence responses. Plant Mol Biol. 69:473–488. doi:10.1007/s11103-008-9435-0
   PubMed Web of Science ®Google Scholar
• Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Ann Stat. 29:1165–1188.
   Web of Science ®Google Scholar
• Bischoff J, Sullivan R, Kjer K, White J. 2004. Phylogenetic placement of the anamorphic tribe Ustilaginoideae (Hypocreales, Ascomycota). Mycologia. 96:1088–1094. doi:10.2307/3762091
   PubMed Web of Science ®Google Scholar
• Campos ML, De Almeida M, Rossi ML, Martinelli AP, Junior CGL, Figueira A, Rampelotti-Ferreira FT, Vendramim JD, Benedito VA, Peres LEP. 2009. Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot. 60:4347–4361. doi:10.1093/jxb/erp270
   PubMed Web of Science ®Google Scholar
• Chao JQ, Jin J, Wang D, Han R, Zhu RS, Zhu YG, Li SQ. 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. doi:10.1371/journal.pone.0091391
   Google Scholar
• Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 21:3674–3676. doi:10.1093/bioinformatics/bti610
   PubMed Web of Science ®Google Scholar
• De Vleesschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi IR, Vera-Cruz C, Kikuchi S, Hofte M. 2012. Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol. 158:1833–1846. doi:10.1104/pp.112.193672
   PubMed Web of Science ®Google Scholar
• Ding X, Cao Y, Huang L, Zhao J, Xu C, Li X, Wang S. 2008. Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expans in expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell. 20:228–240. doi:10.1105/tpc.107.055657
   PubMed Web of Science ®Google Scholar
• Dixon RA, Paiva NL. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell. 7:1085–1097. doi:10.1105/tpc.7.7.1085
   PubMed Web of Science ®Google Scholar
• Domingo C, Andrés F, Tharreau D, Iglesias DJ, Talón M. 2009. Constitutive expression of OsGH3. 1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant–Microbe Interact. 22:201–210. doi:10.1094/MPMI-22-2-0201
   PubMed Web of Science ®Google Scholar
• Gao Y, Xu H, Shen Y, Wang J. 2013. Transcriptomic analysis of rice (Oryza sativa) endosperm using the RNA-Seq technique. Plant Mol Biol. 81:363–378. doi:10.1007/s11103-013-0009-4
   PubMed Web of Science ®Google Scholar
• Grant M, Jones JG. 2009. Hormone (dis) harmony moulds plant health and disease. Science. 324:750–752. doi:10.1126/science.1173771
   PubMed Web of Science ®Google Scholar
• Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J. 2001. Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell. 13:999–1010. doi:10.1105/tpc.13.5.999
   PubMed Web of Science ®Google Scholar
• Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M. 2005. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol. 15:1560–1565. doi:10.1016/j.cub.2005.07.023
   PubMed Web of Science ®Google Scholar
• Jones SI, Vodkin LO. 2013. Using RNA-Seq to profile soybean seed development from fertilization to maturity. PLoS One. 8:e59270. doi:10.1371/journal.pone.0059270
   PubMed Web of Science ®Google Scholar
• Kodama O, Miyakawa J, Akatsuka T, Kiyosawa S. 1992. Sakuranetin, a flavanone phytoalexin from ultraviolet-irradiated rice leaves. Phytochemistry. 31:3807–3809. doi:10.1016/S0031-9422(00)97532-0
   Web of Science ®Google Scholar
• Koiso Y, Li Y, Iwasaki S, Hanaka K, Kobayashi T, Sonoda R, Fujita Y, Yaegashi H, Sato Z. 1994. Ustiloxins, antimitotic cydic peptides from false smut balls on rice panicles caused by Ustilaginoidea virens.. J Antibiot. 47:765–773. doi:10.7164/antibiotics.47.765
   PubMed Web of Science ®Google Scholar
• Koiso Y, Morisaki N, Yamashita Y, Mitsui Y, Shirai R, Hashimoto Y, Iwasaki S. 1998. Isolation and structure of an antimitotic cyclic peptide, ustiloxin F: chemical interrelation with a homologous peptide, ustiloxin B. J Antibiot. 51:418–422. doi:10.7164/antibiotics.51.418
   PubMed Web of Science ®Google Scholar
• Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D, Grima-Pettenati J. 2001. Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry. 57:1187–1195. doi:10.1016/S0031-9422(01)00053-X
   PubMed Web of Science ®Google Scholar
• Lee F, Gunnell P. 1992. False smut. In: Webster RK, Gunnell PS, editors. Compendium of rice disease. St Paul (MN): APS Press; p. 21–24.
   Google Scholar
• Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 25:1966–1967. doi:10.1093/bioinformatics/btp336
   PubMed Web of Science ®Google Scholar
• Li WL, Li LY, Feng AQ, Zhu X, Li JX. 2013. Rice false smut fungus, Ustilaginoidea virens, inhibits pollen germination and degrades the integuments of rice ovule. Am J Plant Sci. 4:2295–2304. doi:10.4236/ajps.2013.412284
   Google Scholar
• Li Y, Koiso Y, Kobayashi H, Hashimoto Y, Iwasaki S. 1995. Ustiloxins, new antimitotic cyclic peptides: interaction with porcine brain tubulin. Biochem Pharmacol. 49:1367–1372. doi:10.1016/0006-2952(95)00072-8
   PubMed Web of Science ®Google Scholar
• Li YS, Zhu Z, Zhang YD, Zhao L, Wang CL. 2008. Genetic analysis of rice false smut resistance using mixed major genes and polygenes inheritance model. Acta Agron Sin. 34:1728–1733. doi:10.1016/S1875-2780(09)60007-9
   Google Scholar
• Lin CY, Trinh NN, Fu SF, Hsiung YC, Chia LC, Lin CW, Huang HJ. 2013. Comparison of early transcriptome responses to copper and cadmium in rice roots. Plant Mol Biol. 81:507–522. doi:10.1007/s11103-013-0020-9
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT Method. Methods. 25:402–408. doi:10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Lu DH, Yang XQ, Mao JH, Ye H, Wang P, Chen YP, Chen F. 2009. Characterising the pathogenicity diversity of Ustilaginoidea virens in hybrid rice in China. J Plant Pathol. 91:443–451.
   Web of Science ®Google Scholar
• Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Li W, et al. 2010. Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res. 20:1238–1249. doi:10.1101/gr.106120.110
   PubMed Web of Science ®Google Scholar
• Ludueña RF, Roach MC, Prasad V, Banerjee M, Koiso Y, Li Y, Iwasaki S. 1994. Interaction of ustiloxin A with bovine brain tubulin. Biochem Pharmacol. 47:1593–1599. doi:10.1016/0006-2952(94)90537-1
   PubMed Web of Science ®Google Scholar
• Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BPHJ, Talbot NJ. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell. 24:322–335. doi:10.1105/tpc.111.092957
   PubMed Web of Science ®Google Scholar
• Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 320:1344–1349. doi:10.1126/science.1158441
   PubMed Web of Science ®Google Scholar
• Nakamura KI, Izumiyama N, Ohtsubo KI, Koiso Y, Iwasaki S, Sonoda R, Fujita Y, Yaegashi H, Sato Z. 1994. “Lupinosis”-Like lesions in mice caused by ustiloxin, produced by Ustilaginoieda virens: a morphological study. Nat Toxins. 2:22–28. doi:10.1002/nt.2620020106
   PubMedGoogle Scholar
• Narsai R, Wang C, Chen J, Wu J, Shou H, Whelan J. 2013. Antagonistic, overlapping and distinct responses to biotic stress in rice (Oryza sativa) and interactions with abiotic stress. BMC Genomic. 14:93. doi:10.1186/1471-2164-14-93
   PubMed Web of Science ®Google Scholar
• Nicholson RL, Hammerschmidt R. 1992. Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol. 30:369–389. doi:10.1146/annurev.py.30.090192.002101
   Web of Science ®Google Scholar
• Qin X, Liu JH, Zhao WS, Chen XJ, Guo ZJ, Peng YL. 2013. Gibberellin 20-oxidase gene OsGA20ox3 regulates plant stature and disease development in rice. Mol Plant-Microbe Interact. 26:227–239. doi:10.1094/MPMI-05-12-0138-R
   PubMed Web of Science ®Google Scholar
• Ride J. 1978. The role of cell wall alterations in resistance to fungi. Ann Appl Biol. 89:302–306.
   Web of Science ®Google Scholar
• Snyder BA, Nicholson RL. 1990. Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science. 248:1637–1639. doi:10.1126/science.248.4963.1637
   PubMed Web of Science ®Google Scholar
• Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W. 2005. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 17:616–627. doi:10.1105/tpc.104.026690
   PubMed Web of Science ®Google Scholar
• Tanaka N, Matsuoka M, Kitano H, Asano T, Kaku H, Komatsu S. 2006. gid1, a gibberellin-insensitive dwarf mutant, shows altered regulation of probenazole-inducible protein (PBZ1) in response to cold stress and pathogen attack. Plant Cell Environ. 29:619–631. doi:10.1111/j.1365-3040.2005.01441.x
   PubMed Web of Science ®Google Scholar
• Tang CS, Gao JZ, Cao GP, Huang SX, Liu EM, Liu CL. 2001. Study and application of the classification standard of rice false smut. Plant Prot. Feb; 27:18–21. Chinese.
   Google Scholar
• 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. doi:10.1111/j.1365-3059.2012.02629.x
   Web of Science ®Google Scholar
• Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. 2004. MapMan: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37:914–939. doi:10.1111/j.1365-313X.2004.02016.x
   PubMed Web of Science ®Google Scholar
• Tronchet M, Balaguã C, Kroj T, Jouanin L, Roby D. 2010. Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol Plant Pathol. 11:83–92. doi:10.1111/j.1364-3703.2009.00578.x
   PubMed Web of Science ®Google Scholar
• Varin L, Deluca V, Ibrahim RK, Brisson N. 1992. Molecular characterization of two plant flavonol sulfotransferases. Proc Natl Acad Sci USA. 89:1286–1290. doi:10.1073/pnas.89.4.1286
   PubMed Web of Science ®Google Scholar
• Wang D, Wang S, Fu J. 2004. Research advance on false smut of rice. Liaoning Agri Sci. 1:21–24.
   Google Scholar
• Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature. 456:470–476. doi:10.1038/nature07509
   PubMed Web of Science ®Google Scholar
• Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 10:57–63. doi:10.1038/nrg2484
   PubMed Web of Science ®Google Scholar
• Wei T, Ou B, Li J, Zhao Y, Guo D, Zhu Y, Chen ZL, Gu HY, Li CY, Qin GJ, Qu LJ. 2013. Transcriptional profiling of rice early response to Magnaporthe oryzae identified OsWRKYs as important regulators in rice blast resistance. PLoS One. 8:e59720.
   PubMed Web of Science ®Google Scholar
• Weng JK, Chapple C. 2010. The origin and evolution of lignin biosynthesis. New Phytol. 187:273–285. doi:10.1111/j.1469-8137.2010.03327.x
   PubMed Web of Science ®Google Scholar
• Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM. 2004. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 23:2903–2913. doi:10.1038/sj.emboj.7600290
   PubMed Web of Science ®Google Scholar
• Yang DL, Li Q, Deng YW, Lou YG, Wang MY, Zhou GX, Zhang YY, He ZH. 2008. Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol Plant. 1:528–537. doi:10.1093/mp/ssn021
   PubMed Web of Science ®Google Scholar
• Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li ST, Li RQ, Bolund L, Wang J. 2006. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 34:W293–W297. doi:10.1093/nar/gkl031
   PubMed Web of Science ®Google Scholar
• Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, et al. 2006. ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell. 18:442–456. doi:10.1105/tpc.105.038455
   PubMed Web of Science ®Google Scholar