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The genes involved in the protective effects of phytohormones in response to Verticillium dahliae infection in Gossypium hirsutum

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Abstract

Verticillium wilt disease caused by soil-borne fungus Verticillium dahliae (V. dahliae), is a serious threats to cotton growth worldwide. Endogenous phytohormones, such as salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and brassinosteroid (BR) have been reported to play important roles in defense response in plants. Based on highthroughput RNA sequencing analysis of resistant Gossypium hirsutum (G. hirsutum) variety Zhongzhimian KV-3, comparing the transcriptome with V. dahliae infection and non-infection, eight differentially expressed candidate genes functions indicated in SA (GhPUB17, GhTGA7 and GhPR1), JA (GhJAZ10 and GhbHLH18), ET (GhEBF1), cytokinine (GhE13L13) and BR (GhBZR1) signal pathways were investigated via virus-induced gene silencing (VIGS) using cotton leaf crumple virus (CLCrV) vector. The expression of eight genes was further validated through quantitative realtime PCR. The result showed that the expression level of GhPUB17, GhJAZ10, GhbHLH18, GhEBF1 and GhE13L13 increased faster in resistant variety Zhongzhimian KV-3 than in susceptible variety 86-1 upon V. dahliae infection. Silencing up-regulated genes GhPUB17, GhJAZ10, GhbHLH18 and GhEBF1 significantly enhanced resistant variety susceptibility to V. dahliae and silencing down-regulated genes GhTGA7 and GhBZR1 significantly increased susceptible variety resistance to V. dahliae. Taken together, these genes are important components in response to V. dahliae infection.

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References

  • Anderson JP, Badruzsaufari E, Schenk PM (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signal pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beyer EM (1979) Ethylene Metabolism during Leaf Abscission in Cotton. Plant Physiology 64:971–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brugiere N, Jiao S, Hantke S, Zinselmeier C, Roessler JA, Niu X, Jones RJ, Habben JE (2003). Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress. Plant Physiol 132:1228–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP (2004) Applications and advantages of virus-induced gene silencing for gene function studies in plants. Plant J 39:734–746

    Article  CAS  PubMed  Google Scholar 

  • Chae HS., Faure F, Kieber JJ. (2003). The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D (2011) The bHLH Transcription Factor MYC3 Interacts with the Jasmonate ZIM-Domain Proteins to Mediate Jasmonate Response in Arabidopsis. Mol Plant 4:279–288

    Article  CAS  PubMed  Google Scholar 

  • Chory J, Ecker JR, Briggs S, Caboche M, Coruzzi GM, Cook D, Dang J, Grant S, Guerinot ML, Henikoff S, Martienssen R, Okada K, Raikhel NV, Somerville CR, Weigel D (2000) National Science Foundation sponsored workshop report: ‘The 2010 Project’. Functional genomics and the virtual plant. A blueprint for understanding how plants are built and how to improve them. Plant Physiol 123:423–426

    CAS  Google Scholar 

  • Chung HS, Howe GA (2009) A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis. Plant Cell 21:131–145

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Demianski AJ, Chung KM, Kunkel BN (2012) Analysis of Arabidopsis JAZ gene expression during Pseudomonas syringae pathogenesis. Mol Plant Pathol 13:46–57

    Article  CAS  PubMed  Google Scholar 

  • Ekengren SK, Liu Y, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36:905–917

    Article  CAS  PubMed  Google Scholar 

  • Fradin EF, Thomma BP (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. alboatrum. Mol Plant Pathol 7:71–86

    Article  CAS  PubMed  Google Scholar 

  • Fulcher RG, McCully ME, Setterfield G, Sutherland J (1976) β-1,3- Glucans may be associated with cell Plate formation during cytokinesis. Can J Bot 54:459–542

    Article  Google Scholar 

  • Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ, Liu LL, Zhang XL (2013) Proteomic and Virus-induced Gene Silencing (VIGS) Analyses Reveal That Gossypol, Brassino- steroids, and Jasmonic acid Contribute to the Resistance of Cotton to Verticillium dahliae. Mol Cell Proteomics 12:3690–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L (2011) Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J 66:293–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotphic pathogens. Ann Rev Phytopathol 43:205–227

    Article  CAS  Google Scholar 

  • Gu Z, Huang C, Li F, Zhou X (2014) A versatile system for functional analysis of genes and microRNAs in cotton. Plant Biotechnol J 12:638–649

    Article  CAS  PubMed  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in post transcriptional gene silencing in plants. Science 286:950–952

    Article  CAS  PubMed  Google Scholar 

  • He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Q, McLellan H, Boevink PC, Sadanandom A, Xie C, Birch PR, Tian Z (2015) U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. J Exp Bot 66:3189–3199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hell M, Baldwin IT (2002) Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci 7:31–38

    Google Scholar 

  • Kesarwani M, Yoo JM, Dong XN (2007) Genetic Interactions of TGA Transcription Factors in the Regulation of Pathogenesis-Related Genes and Disease Resistance in Arabidopsis. Plant Physiol 144:336–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishna P (2003) Brassinosteroid-mediated stress response. Plant Growth Regul 22:289–297

    Article  CAS  Google Scholar 

  • Lee J, Bricker TM, Lefevre M, Pinson SR, Oard JH (2006) Proteomic and Genetic Approaches to Identifying Defence-related Proteins in rice Challenged with the Fungal Pathogen Rhizoctonia Solani. Mol Plant Pathol 7:405–416

    Article  CAS  PubMed  Google Scholar 

  • Li F, Fan G, Wang K, Sun F, Yuan Y, Song G, Li Q, Ma Z, Lu C, Zou C, Chen W, Liang X, Shang H, Liu W, Shi C, Xiao G, Gou C, Ye W, Xu X, Zhang X, Wei H, Li Z, Zhang G8, Wang J, Liu K, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu S (2014) Genome sequence of the cultivated cotton Gossypium arboretum. Nat Genet 46:567–574

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) Jasmonateinsensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu R, Martin-Hernandez AM, Peart JR, Malcuit I, Baulcombe DC (2003) Virus-induced gene silencing in plants. Methods 30:296–303

    Article  CAS  PubMed  Google Scholar 

  • McDowell JM, Dangl JL. (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79–82

    Article  CAS  PubMed  Google Scholar 

  • Mersmann S, Bourdais G, Rietz S (2010) Ethylene Signal Regulates Accumulation of the FLS2 Receptor and Is Required for the Oxidative Burst Contributing to Plant Immunity. Plant Physiol 154:391–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279:415–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takatsuto S, Yamaguchi I, Yoshida S (2003) Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J 33:887–898

    Article  CAS  PubMed  Google Scholar 

  • Niu Y, Figueroa P, Browse J (2011) Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62:2143–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohashi Y, Matsuoka M (1987) Induction and secretion of pathogenesisrelated proteins by salicylate or plant hormones in tobacco suspension cultures. Plant Cell Physiol 28:573–580

    CAS  Google Scholar 

  • Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CM, van Wees SC, Hoffland E, van Pelt JA, van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-Dependent Regulation of Plant Ethylene Hormone Signaling by Two Arabidopsis F-Box Proteins: EBF1 and EBF2. Cell 115:679–689

    Article  CAS  PubMed  Google Scholar 

  • Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Wu D, Guo H, Xie D (2013) The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development. PLoS Genet 9:e1003653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006). Cytokinin and auxin inhibit abscisic acid-induced stomatal closureby enhancing ethylene production in Arabidopsis. J Exp Bot 57:2259–2266

    Article  CAS  PubMed  Google Scholar 

  • Tuttle JR, Idris AM, Brown JK, Haigler CH, Robertson D (2008) Geminivirus-Mediated Gene Silencing from Cotton Leaf Crumple Virus Is Enhanced by Low Temperature in Cotton. Plant Physiol 148:41–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umemoto N, Kakitani M, Iwamatsu A, Yoshikawa M, Yamaoka N, Ishida I (1997) The structure and function of a soybean betaglucan-elicitor-binding protein. Proc Nat Acad Sci USA 94:1029–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Veronese P, Narasimhan ML, Stevenson RA, Zhu JK, Weller SC, Subbarao KV, Bressan RA (2003) Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. TPlant J 35:574–587

    Article  CAS  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic Acid, a Multifaceted Hormone to Combat Disease. Annu Rev Phytopathol 47:177–206

    Article  CAS  PubMed  Google Scholar 

  • Wang FX, Ma YP, Yang CL, Zhao PM, Yao Y, Jian GL, Luo YM, Xia GX (2011) Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 114:296–309

    Google Scholar 

  • Wang K, Wang Z, Li F, Ye W, Wang J, Song G, Yue Z, Cong L, Shang H, Zhu S, Zou C, Li Q, Yuan Y, Lu C, Wei H, Gou C, Zheng Z, Yin Y, Zhang X, Liu K, Wang B, Song C, Shi N, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu S (2012) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44:1098–1103

    Article  CAS  PubMed  Google Scholar 

  • Xia XJ, Chen Z, Yu JQ (2010) ROS mediate brassinosteroids-induced plant stress responses. Plant Signal Behav 5:532–534

    Article  CAS  PubMed  Google Scholar 

  • Yadeta KA, Valkenburg DJ, Hanemian M, Marco Y, Thomma BP (2014) The Brassicaceae-Specific EWR1 Gene Provides Resistance to Vascular Wilt Pathogens. PLoS ONE 9:e88230

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q et al. (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537

    Article  CAS  PubMed  Google Scholar 

  • Zhang WW, Jian GL, Jiang TF, Wang SZ, Qi FJ, Xu SC (2012) Cotton gene expression profiles in resistant Gossypium hirsutum cv. Zhongzhimian KV1 responding to Verticillium dahliae strain V991 infection. Mol Biol Rep 39:9765–9774

    CAS  PubMed  Google Scholar 

  • Zhang WW, Jiang TF, Cui X, Qi FJ, Jian GL (2013) Colonization in cotton plants by a green fluorescent protein labeled strain of Verticillium dahliae. Eur J Plant Pathol 135:867–876

    Article  CAS  Google Scholar 

  • Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL, Li ZK, Wu LQ, Zhang GY, Ma ZY (2013) Transcriptome profiling of Gossypium barbadense inoculated with Verticillium dahliae provides a resource for cotton improvement. BMC Genomics 14:637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Wenwei Zhang.

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Zhang, H., Zhang, W., Jian, G. et al. The genes involved in the protective effects of phytohormones in response to Verticillium dahliae infection in Gossypium hirsutum . J. Plant Biol. 59, 194–202 (2016). https://doi.org/10.1007/s12374-016-0568-4

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