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A novel plant protein-disulfide isomerase participates in resistance response against the TYLCV in tomato

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Abstract

Main conclusion

Overexpression or silencing of the SlPDI could increase plants resistance or sensitivity to TYLCV through enhancing or reducing the plant’s antioxidant capacity.

Abstract

Tomato yellow leaf curl virus (TYLCV), a plant virus that could infect a variety of crops, is particularly destructive to tomato growth. Protein disulfide isomerase (PDI) is a member of the thioredoxin (Trx) superfamily, is capable of catalyzing the formation and heterogeneity of protein disulfide bonds and inhibiting the aggregation of misfolded proteins. Studies have shown that PDI plays important roles in plant response to abiotic stress, there is no research report on the function of PDI in response to biotic stress, especially TYLCV infection. Here, we identified a tomato PDI gene, SlPDI, was involved in regulating tomato plants resistance to TYLCV. Subcellular localization results showed that SlPDI was located at the endoplasmic reticulum (ER), and its location remained unchanged after infection with TYLCV virus. Overexpression or silencing of SlPDI could increase plants resistance or sensitivity to TYLCV. Transgenic plants that overexpressing SlPDI exhibit enhanced antioxidant activity evidenced by lower hydrogen peroxide (H2O2) level and higher activity of superoxide dismutase (SOD) and peroxidase (POD) in comparison with WT plants, after infected by TYLCV. Moreover, the SlPDI-silencing plants showed opposite results. The promoter analyzes result showed that SlPDI was involved in response to salicylic acid (SA), and our experimental results also showed that the expression level of SlPDI was induced by SA. Taken together, our results indicated that SlPDI could regulate plant resistance to TYLCV through enhancing the protein folding function of ER and promoting the synthesis and conformation of antioxidant-related proteins.

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Abbreviations

DAB:

Diaminobenzidine;

ER:

Endoplasmic reticulum;

H2O2 :

Hydrogen peroxide;

MDA:

Malondialdehyde;

ORF:

Open reading frame;

PDI:

Protein disulfide isomerase;

POD:

Peroxidase;

RT-qPCR:

Quantitative real-time PCR;

ROS:

Reactive oxygen species;

SA:

Salicylic acid;

SOD:

Superoxide dismutase;

TYLCV:

Tomato yellow leaf curl virus;

VIGS:

Virus-induced gene silencing;

WT:

Wild type

References

  • Accotto GP, Bragaloni M, Luison D, Davino S, Davino M (2010) First report of tomato yellow leaf curl virus (TYLCV) in Italy. Plant Pathol 52:799–799

    Article  Google Scholar 

  • Anbinder I, Reuveni M, Azari R, Paran I, Nahon S, Shlomo H, Chen L, Lapidot M, Levin I (2009) Molecular dissection of Tomato leaf curl virus resistance in tomato line TY172 derived from Solanum peruvianum. Theor Appl Genet 119:519–530

    Article  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Apperizeller-Herzog C, Ellgaard L (2008) The human PDI family: versatility packed into a single fold. Bba-Mol Cell Res 1783:535–548

    Google Scholar 

  • Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313–20316

    Article  CAS  PubMed  Google Scholar 

  • Borg M, Brownfield L, Khatab H, Sidorova A, Lingaya M, Twell D (2011) The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23:534–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Pan YH, Wang SS, Ding YF, Yang WJ, Zhu C (2012) Overexpression of a protein disulfide isomerase-like protein from Methanothermobacter thermoautotrophicum enhances mercury tolerance in transgenic rice. Plant Sci 197:10–20

    Article  CAS  PubMed  Google Scholar 

  • Chen TZ, Lv YD, Zhao TM, Li N, Yang YW, Yu WG, He X, Liu TL, Zhang BL (2013) Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS ONE 8(11):e80816

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Darby NJ, Kemmink J, Creighton TE (1996) Identifying and characterizing a structural domain of protein disulfide isomerase. Biochemistry 35:10517–10528

    Article  CAS  PubMed  Google Scholar 

  • Deng X, Zhou S, Hu W, Feng J, Zhang F, Chen L, Huang C, Luo Q, He Y, Yang G, He G (2013) Ectopic expression of wheat TaCIPK14, encoding a calcineurin B-like protein-interacting protein kinase, confers salinity and cold tolerance in tobacco. Physiol Plant 149:367–377

    CAS  PubMed  Google Scholar 

  • Ellgaard L, Ruddock LW (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. Embo Rep 6:28–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiallo-Olive E, Rivera-Bustamante RF, Martinez-Zubiaur Y (2009) Tobacco yellow crinkle virus, a new bipartite begomovirus infecting tobacco and pepper in Cuba. Plant Pathol 58:785–785

    Google Scholar 

  • Freedman RB, Hirst TR, Tuite MF (1994) Protein disulphide isomerase: building bridges in protein folding. Trends Biochem Sci 19:331–336

    Article  CAS  PubMed  Google Scholar 

  • Ghanim M, Czosnek H (2000) Tomato yellow leaf curl geminivirus (TYLCV-Is) is transmitted among whiteflies (Bemisia tabaci) in a sex-related manner. J Virol 74:4738–4745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao H, Teng H, Guan Z, Xin W, Xu R (2018) Preliminary identification of tomato yellow leaf curl virus in Yuncheng Shanxi Province. Mol Plant Breed 16(5):1558–1565

    Google Scholar 

  • Hatahet F, Ruddock LW (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Sign 11:2807–2850

    Article  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general-method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Houston NL, Fan C, Xiang JQ, Schulze JM, Jung R, Boston RS (2005) Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol 137:762–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang DJ, Chen HJ, Lin YH (2005) Isolation and expression of protein disulfide isomerase cDNA from sweet potato [Ipomoea batatas (L.) Lam ‘Tainong 57’] storage roots. Plant Sci 169:776–784

    Article  CAS  Google Scholar 

  • Huang Y, Ma HY, Huang W, Wang F, Xu ZS, Xiong AS (2016) Comparative proteomic analysis provides novel insight into the interaction between resistant vs. susceptible tomato cultivars and TYLCV infection. Bmc Plant Biol 16(1):162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang Y, Li T, Xu ZS, Wang F, Xiong AS (2017) Six NAC transcription factors involved in response to TYLCV infection in resistant and susceptible tomato cultivars. Plant Physiol Biochem 120:61–74

    Article  CAS  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  CAS  PubMed  Google Scholar 

  • Ji Y, Schuster DJ, Scott JW (2007) Ty-3, a begomovirus resistance locus near the tomato yellow leaf curl virus resistance locus Ty-1 on chromosome 6 of tomato. Mol Breeding 20:271–284

    Article  CAS  Google Scholar 

  • Ji YF, Scott JW, Schuster DJ (2009a) Toward fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato. HortScience 44:614–618

    Article  Google Scholar 

  • Ji YF, Scott JW, Schuster DJ, Maxwell DP (2009b) Molecular mapping of Ty-4, a new tomato yellow leaf curl virus resistance locus on chromosome 3 of tomato. J Am Soc Hortic Sci 134:281–288

    Article  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kayum MA, Park JI, Nath UK, Saha G, Biswas MK, Kim HT, Nou IS (2017) Genome-wide characterization and expression profiling of PDI family gene reveals function as abiotic and biotic stress tolerance in Chinese cabbage (Brassica rapa ssp pekinensis). Bmc Genomics 18(1):885

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kessmann H, Staub T, Ligon J, Oostendorp M, Ryals J (1994) Activation of systemic acquired disease resistance in plants. Eur J Plant Pathol 100:359–369

    Article  Google Scholar 

  • Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7(12):1013–1030

    Article  CAS  PubMed  Google Scholar 

  • Koornneef A, Pieterse CM (2008) Cross talk in defense signaling. Plant Physiol 146:839–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lapidot M, Friedmann M, Pilowsky M, Ben-Joseph R, Cohen S (2001) Effect of host plant resistance to tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector. Phytopathology 91:1209–1213

    Article  CAS  PubMed  Google Scholar 

  • Li JB, Luan YS, Jin H (2012) The tomato SlWRKY gene plays an important role in the regulation of defense responses in tobacco. Biochem Bioph Res Co 427:671–676

    Article  CAS  Google Scholar 

  • Li JB, Luan YS, Liu Z (2015) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. Plant Cell Tiss Org 123:67–81

    Article  CAS  Google Scholar 

  • Li MY, Xu ZS, Tian C, Huang Y, Wang F, Xiong AS (2016) Genomic identification of WRKY transcription factors in carrot (Daucus carota) and analysis of evolution and homologous groups for plants. Sci Rep 6:23101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li KQ, Xing CH, Yao ZH, Huang XS (2017) PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotechnol J 15:1186–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Zhang XY, Huang Y, Xu ZS, Wang F, Xiong AS (2018) An R2R3-MYB transcription factor, SlMYB28, involved in the regulation of TYLCV infection in tomato. Sci Hortic (Amsterdam) 237:192–200

    Article  CAS  Google Scholar 

  • Li T, Huang Y, Xu ZS, Wang F, Xiong AS (2019) Salicylic acid-induced differential resistance to the Tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biol 19:173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YL, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Luan YS, Li JB, Yin YL (2016) Expression of a tomato MYB gene in transgenic tobacco increases resistance to Fusarium oxysporum and Botrytis cinerea. Eur J Plant Pathol 144:607–617

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Macadam JW, Nelson CJ, Sharp RE (1992) Peroxidase activity in the leaf elongation zone of tall fescue : I. Spatial distribution of ionically bound peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiol 99:872–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meiri E, Levitan A, Guo F, Christopher DA, Schaefer D, Zryd JP, Danon A (2002) Characterization of three PDI-like genes in Physcomitrella patens and construction of knock-out mutants. Mol Genet Genom 267:231–240

    Article  CAS  Google Scholar 

  • Meng YL, Zhang Q, Zhang MX, Gu B, Huang GY, Wang QH, Shan WX (2015) The protein disulfide isomerase 1 of Phytophthora parasitica (PpPDI1) is associated with the haustoria-like structures and contributes to plant infection. Front Plant Sci 6:632

    PubMed  PubMed Central  Google Scholar 

  • Navot N, Pichersky E, Zeidan M, Zamir D, Czosnek H (1991) Tomato yellow leaf curl virus: a whitefly-transmitted geminivirus with a single genomic component. Virology 185:151–161

    Article  CAS  PubMed  Google Scholar 

  • Ondzighi CA, Christopher DA, Cho EJ, Chang SC, Staehelin LA (2008) Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205–2220

    Article  CAS  Google Scholar 

  • Ou W, Silver J (2006) Role of protein disulfide isomerase and other thiol-reactive proteins in HIV-1 envelope protein-mediated fusion. Virology 350:406–417

    Article  CAS  PubMed  Google Scholar 

  • Park JM, Park CJLee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-Typetranscription factor enhances resistance against pathogen attack andosmotic stress in tobacco. Plant Cell 13:1035–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radonic A, Thulke S, Mackay IM, Landt O, Siegert W, Nitsche A (2004) Guideline to reference gene selection for quantitative real-time PCR. Biochem Bioph Res Co 313:856–862

    Article  CAS  Google Scholar 

  • Sade D, Shriki O, Cuadros-Inostroza A, Tohge T, Semel Y, Haviv Y, Willmitzer L, Fernie AR, Czosnek H, Brotman Y (2015) Comparative metabolomics and transcriptomics of plant response to Tomato yellow leaf curl virus infection in resistant and susceptible tomato cultivars. Metabolomics 11:81–97

    Article  CAS  Google Scholar 

  • Shan TL, Rong W, Xu HJ, Du LP, Liu X, Zhang ZY (2016) The wheat R2R3-MYB transcription factor TaRIM1 participates in resistance response against the pathogen Rhizoctonia cerealis infection through regulating defense genes. Sci Rep 6:28777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi W, Hao L, Li J, Liu D, Guo X, Li H (2014) The Gossypium hirsutum WRKY gene GhWRKY39-1 promotes pathogen infection defense responses and mediates salt stress tolerance in transgenic Nicotiana benthamiana. Plant Cell Rep 33:483–498

    Article  CAS  PubMed  Google Scholar 

  • Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290:1571–1574

    Article  CAS  PubMed  Google Scholar 

  • Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylidès C, Roby D (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA 99:10179–10184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Verlaan MG, Szinay D, Hutton SF, de Jong H, Kormelink R, Visser RGF, Scott JW, Bai YL (2011) Chromosomal rearrangements between tomato and Solanum chilense hamper mapping and breeding of the TYLCV resistance gene Ty-1. Plant J 68:1093–1103

    Article  CAS  PubMed  Google Scholar 

  • Walker KW, Lyles MM, Gilbert HF (1996) Catalysis of oxidative protein folding by mutants of protein disulfide isomerase with a single active-site cysteine. Biochemistry 35:1972–1980

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Sun PP, Chen CL, Wang Y, Fu XZ, Liu JH (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. J Exp Bot 62:2899–2914

    Article  CAS  PubMed  Google Scholar 

  • Wei X, Shan T, Hong Y, Xu H, Liu X, Zhang Z (2017) TaPIMP2, a pathogen-induced MYB protein in wheat, contributes to host resistance to common root rot caused by Bipolaris sorokiniana. Sci Rep 7:1754

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkinson B, Gilbert HF (2004) Protein disulfide isomerase. Biochim Biophys Acta 1699:35–44

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Sankar S, Neamati N (2014) Protein disulfide isomerase: a promising target for cancer therapy. Drug Discov Today 19:222–240

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The research was supported by New Century Excellent Talents in University (NCET-11-0670), Jiangsu Natural Science Foundation (BK20130027), and Priority Academic Program Development of Jiangsu Higher Education Institutions Project (PAPD).

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Correspondence to Ai-Sheng Xiong.

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Communicated by Anastasios Melis.

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Li, T., Wang, YH., Huang, Y. et al. A novel plant protein-disulfide isomerase participates in resistance response against the TYLCV in tomato. Planta 252, 25 (2020). https://doi.org/10.1007/s00425-020-03430-1

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