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Virus-Induced Gene Silencing of a Putative Glutathione S-Transferase Gene Compromised Ol-1-Mediated Resistance against Powdery Mildew in Tomato

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Abstract

Previously, cDNA-amplified fragment length polymorphism analysis was used to profile differentially expressed transcript-derived fragments (DE-TDFs) of tomato between resistant and susceptible responses against the fungal pathogen Oidium neolycopersici. In the present study, we further investigated a DE-TDF annotated to a putative glutathione S-transferase (GST) that was more rapidly upregulated during the Ol-1-mediated resistance response than during the susceptible response. We used virus-induced gene silencing to knock-down expression of the putative GST gene (ShGST) in resistant tomato plants (Solanum habrochiates G1.1560) carrying the Ol-1 gene, and the ShGST-silenced plants showed a susceptible phenotype after inoculation with O. neolycopersici. Microscopic observation demonstrated that O. neolycopersici was able to complete its life cycle on silenced resistant plants and showed similar morphological characteristics to those of the fungus on susceptible tomato plants. The resistance against O. neolycopersici in G1.1560 was associated with hypersensitive response (HR); however, silencing of ShGST did not completely abolish the HR and hydrogen peroxide (H2O2) accumulation. These results indicate that ShGST is required for resistance against O. neolycopersici in tomato and that decreased HR and H2O2 accumulation may be insufficient for tomato to prevent sporulation of O. neolycopersici.

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References

  • Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, Davis RJ, Ronai Z (1999) Regulation of JNK signaling by GSTp. EMBO J 18:1321–1334

    Article  PubMed  CAS  Google Scholar 

  • Aswati Nair R, Kiran AG, Sivakumar KC, Thomas G (2010) Molecular characterization of an oomycete-responsive PR-5 protein gene from Zingiber zerumbet. Plant Mol Biol Report 28:128–135

    Article  Google Scholar 

  • Bai Y, van der Hulst R, Bonnema G, Marcel TC, Meijer-Dekens F, Niks RE, Lindhout P (2005) Tomato defense to Oidium neolycopersici: dominant Ol genes confer isolate-dependent resistance via a different mechanism than recessive ol-2. Mol Plant Microb Interact 18:354–362

    Article  CAS  Google Scholar 

  • Bi C, Chen F, Jackson L, Gill BS, Li WL (2011) Expression of lignin biosynthetic genes in wheat during development and upon infection by fungal pathogens. Plant Mol Biol Report 29:149–161

    Article  CAS  Google Scholar 

  • Chen S, Vaghchhipawala Z, Li W, Asard H, Dickman MB (2004) Tomato phospholipid hydroperoxide glutathione peroxidase inhibits cell death induced by bax and oxidative stresses in yeast and plants. Plant Physiol 135:1630–1641

    Article  PubMed  CAS  Google Scholar 

  • Cho SG, Lee YH, Park HS, Ryoo K, Kang KW, Park J, Eom SJ, Kim MJ, Chang TS, Choi SY, Shim J, Kim Y, Dong MS, Lee MJ, Kim SG, Ichijo H, Choi EJ (2001) Glutathione S-transferase mu modulates the stress-activated signals by suppressing apoptosis signal-regulating kinase 1. J Biol Chem 276:12749–12755

    Article  PubMed  CAS  Google Scholar 

  • Cumming RC, Lightfoot J, Beard K, Youssoufian H, O'Brien PJ, Buchwald M (2001) Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1. Nat Med 7:814–820

    Article  PubMed  CAS  Google Scholar 

  • Cummins I, Cole DJ, Edwards R (1999) A role for glutathione transferases functioning as glutathione peroxidases in resistance to multiple herbicides in black-grass. Plant J 18:285–292

    Article  PubMed  CAS  Google Scholar 

  • Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  PubMed  CAS  Google Scholar 

  • Diao GP, Wang YC, Wang C, Yang CP (2011) Cloning and functional characterization of a novel glutathione S-transferase gene from Limonium bicolor. Plant Mol Biol Report 29:77–87

    Article  CAS  Google Scholar 

  • Dong Y, Burch-Smith TM, Liu Y, Mamillapalli P, Dinesh-Kumar SP (2007) A ligation-independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and −2 in floral development. Plant Physiol 145:1161–1170

    Article  PubMed  CAS  Google Scholar 

  • Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Freialdenhoven A, Scherag B, Hollricher K, Collinge DB, Thordal-Christensen H, Schulze-Lefert P (1994) Nar-1 and Nar-2, two loci required for Mla12-specified race-specific resistance to powdery mildew in barley. Plant Cell 6:983–994

    Article  PubMed  CAS  Google Scholar 

  • Freialdenhoven A, Peterhansel C, Kurth J, Kreuzaler F, Schulze-Lefert P (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8:5–14

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Jones DA, Jones J (1994) Identification of two genes required in tomato for full Cf-9-dependent resistance to Cladosporium fulvum. Plant Cell 6:361–374

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Lu XY, Zhao JT, Chen JK, Dai XM, Xiao W, Chen YP, Chen YF, Huang XL (2010) MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Mol Biol Report 28:309–316

    Article  CAS  Google Scholar 

  • Kilili KG, Atanassova N, Vardanyan A, Clatot N, Al-Sabarna K, Kanellopoulos PN, Makris AM, Kampranis SC (2004) Differential roles of tau class glutathione S-transferases in oxidative stress. J Biol Chem 279:24540–24551

    Article  PubMed  CAS  Google Scholar 

  • Leng XD, Xiao BG, Wang S, Gui YJ, Wang Y, Lu XP, Xie JH, Li YP, Fan LJ (2010) Identification of NBS-type resistance gene homologs in tobacco genome. Plant Mol Biol Report 28:152–161

    Article  CAS  Google Scholar 

  • Li C (2005) Transcriptional, microscopic and macroscopic investigations into monogenic and polygenic interactions of tomato and powdery mildew. Dissertation, Wageningen Uinversity

    Google Scholar 

  • Li C, Bai Y, Jacobsen E, Visser R, Lindhout P, Bonnema G (2006) Tomato defense to the powdery mildew fungus: differences in expression of genes in susceptible, monogenic- and polygenic resistance responses are mainly in timing. Plant Mol Biol 62:127–140

    Article  PubMed  CAS  Google Scholar 

  • Li C, Bonnema G, Che D, Dong L, Lindhout P, Visser R, Bai Y (2007) Biochemical and molecular mechanisms involved in monogenic resistance responses to tomato powdery mildew. Mol Plant Microb Interact 20:1161–1172

    Article  CAS  Google Scholar 

  • Li CW, Pei DL, Wang WJ, Ma YS, Wang L, Wang F (2008) First report of powdery mildew caused by Oidium neolycopersici on tomato in China. Plant Dis 92:1370–1370

    Google Scholar 

  • Li DM, Staehelin C, Wang WT, Peng SL (2010) Molecular cloning and characterization of a chitinase-homologous gene from Mikania micrantha infected by Cuscuta campestris. Plant Mol Biol Report 28:90–101

    Article  CAS  Google Scholar 

  • Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30:415–429

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Mackey D, Holt BF 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Ohmiya A, Hagen G, Guilfoyle T (1995) The soybean GH2/4 gene that encodes a glutathione S-transferase has a promoter that is activated by a wide range of chemical agents. Plant Physiol 108:919–927

    Article  PubMed  CAS  Google Scholar 

  • Yang B, Rahman MH, Liang Y, Shah S, Kav NNV (2010) Characterization of defense signaling pathways of Brassica napus and Brassica carinata in response to Sclerotinia sclerotiorum challenge. Plant Mol Biol Report 28:253–263

    Article  CAS  Google Scholar 

  • Zhang LY, Zhang YY, Chen RG, Zhang JH, Wang TT, Li HX, Ye ZB (2010) Ectopic expression of the tomato Mi-1 gene confers resistance to root knot nematodes in lettuce (Lactuca sativa). Plant Mol Biol Report 28:204–211

    Article  CAS  Google Scholar 

  • Zhao F, Cai ZJ, Hu TZ, Yao HG, Wang L, Dong N, Wang B, Ru ZG, Zhai WX (2010) Genetic analysis and molecular mapping of a novel gene conferring resistance to rice stripe virus. Plant Mol Biol Report 28:512–518

    Article  Google Scholar 

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Acknowledgments

We thank Professor David Baulcombe and Professor Liu Yule for providing the VIGS vectors and Dr. Bai Yuling for the seeds of wild-type tomato. This research was supported by National Natural Science Foundation of China Projects (Grant No. 31071807, 30600413), Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry (Grant No. 20071108), Key Project of Chinese Ministry of Education (Grant No. 207064) to CL and Natural Science Foundation of Henan Province ( Grant No. 082300430320) to DL.

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Authors and Affiliations

  1. College of Agromony, Henan Agricultural University, Zhengzhou, 450002, China

    Dongli Pei, Hongzhen Ma, Jianyu Wu & Chengwei Li

  2. Department of Life Science, Shangqiu Normal University, Shangqiu, 476000, China

    Dongli Pei, Yuansong Ma, Wenjing Wang, Huixia Geng & Chengwei Li

  3. Key Laboratory of Plant Genetics and Molecular Breeding, Zhoukou Normal University, Zhoukou, 466001, China

    Yi Zhang & Chengwei Li

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  1. Dongli Pei
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  2. Hongzhen Ma
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  3. Yi Zhang
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  4. Yuansong Ma
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  5. Wenjing Wang
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  7. Jianyu Wu
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  8. Chengwei Li
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Correspondence to Chengwei Li.

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Pei, D., Ma, H., Zhang, Y. et al. Virus-Induced Gene Silencing of a Putative Glutathione S-Transferase Gene Compromised Ol-1-Mediated Resistance against Powdery Mildew in Tomato. Plant Mol Biol Rep 29, 972–978 (2011). https://doi.org/10.1007/s11105-011-0331-4

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