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A thioredoxin-like protein of Bemisia tabaci interacts with coat protein of begomoviruses

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Abstract

Bemisia tabaci (whitefly) is the sole vector of begomoviruses, which transmits them in a persistent and circulative manner from infected to healthy plants. During this process, begomoviruses interact with various proteins in the insect vector B. tabaci that would play a specific role in the virus transmission. Identification and characterization of such proteins are important to understand the complete process of virus transmission. Coat protein (CP) of begomoviruses is the only protein which is reported to interact with proteins of the insect vector B. tabaci. In this study, we performed yeast two-hybrid assay using CP of cotton leaf curl Rajasthan virus (CLCuV) and Tomato leaf curl New Delhi virus (ToLCNDV) as bait in separate experiments and cDNA prepared from total RNA of B. tabaci was used as prey. Yeast two-hybrid assay resulted in identification of a thioredoxin-like protein (TLP) from CLCuV yeast two-hybrid library. Later TLP was also found to interact with CP of ToLCNDV. In vitro pull-down assay showed TLP interaction with CP of both CLCuV and ToLCNDV. TLP was found to interact with ToLCNDV virus particles isolated from tomato leaves.

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References

  1. Gutierrez C (1999) Geminivirus DNA replication. Cell Mol Life Sci 56(3–4):313–329. https://doi.org/10.1007/s000180050433

    Article  CAS  PubMed  Google Scholar 

  2. Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Roumagnac P, Varsani A, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Geminiviridae. J Gen Virol 98:131–133. https://doi.org/10.1099/jgv.0.000738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11(11):777–788. https://doi.org/10.1038/nrmicro3117

    Article  CAS  PubMed  Google Scholar 

  4. Varsani A, Navas-Castillo J, Moriones E, Hernández-Zepeda C, Idris A, Brown JK, Zerbini FM, Martin DP (2014) Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. Arch Virol 159(8):2193–2203. https://doi.org/10.1007/s00705-014-2050-2

    Article  CAS  PubMed  Google Scholar 

  5. Varsani A, Roumagnac P, Fuchs M, Navas-Castillo J, Moriones E, Idris A, Briddon RW, Rivera-Bustamante R, Zerbini FM, Martin DP (2017) Capulavirus and Grablovirus: two new genera in the family Geminiviridae. Arch Virol 162(6):1819–1831. https://doi.org/10.1007/s00705-017-3268-6

    Article  CAS  PubMed  Google Scholar 

  6. Padidam M, Beachy RN, Fauquet CM (1995) Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol 76:25–35. https://doi.org/10.1099/0022-1317-76-1-25

    Article  CAS  PubMed  Google Scholar 

  7. Rana VS, Singh ST, Priya NG, Kumar J, Rajagopal R (2012) Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS ONE 7(8):e42168. https://doi.org/10.1371/journal.pone.0042168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sattar MN, Kvarnheden A, Saeed M, Briddon RW (2013) Cotton leaf curl disease—an emerging threat to cotton production worldwide. J Gen Virol 94(4):695–710. https://doi.org/10.1099/vir.0.049627-0

    Article  CAS  PubMed  Google Scholar 

  9. Chakraborty S, Pandey PK, Banerjee MK, Kallo G, Fauquet CM (2003) Tomato leaf curl Gujarat virus, a new begomovirus species causing a severe leaf curl disease of tomato in Varanasi, India. Phytopathology 93:1485–1495. https://doi.org/10.1094/PHYTO.2003.93.12.1485

    Article  CAS  PubMed  Google Scholar 

  10. Fortes MI, Sanchez-Campos S, Fiallo-Olive E, Diaz-Pendon JA, Navas-Castillo J, Moriones E (2016) A novel strain of Tomato leaf curl New Delhi virus has spread to the Mediterranean Basin. Viruses 8(11):307. https://doi.org/10.3390/v8110307

    Article  CAS  PubMed Central  Google Scholar 

  11. Pandey P, Mukhopadhya S, Naqvi AR, Mukherjee SK, Shekhawat GS, Choudhury NR (2010) Molecular characterization of two distinct monopartite begomoviruses infecting tomato in India. Virol J 7:337–346. https://doi.org/10.1186/1743-422X-7-337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394. https://doi.org/10.1146/annurev.phyto.43.040204.135939

    Article  CAS  PubMed  Google Scholar 

  13. Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359. https://doi.org/10.1146/annurev.phyto.022508.092135

    Article  CAS  PubMed  Google Scholar 

  14. Czosnek H, Ghanim M, Ghanim M (2002) The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci-insights from studies with Tomato yellow leaf curl virus. Ann Appl Biol 140(3):215–231. https://doi.org/10.1111/j.1744-7348.2002.tb00175.x

    Article  Google Scholar 

  15. Ghanim M, Rosell RC, Campbell LR, Czosnek H, Brown JK, Ullman DE (2001) Digestive, salivary, and reproductive organs of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) B Type. J Morphol 248(1):22–40. https://doi.org/10.1002/jmor.1018

    Article  CAS  PubMed  Google Scholar 

  16. Briddon RW, Pinner MS, Stanley J, Markham PG (1990) Geminivirus coat protein gene replacement alters insect specificity. J Virol 177(1):85–94. https://doi.org/10.1016/0042-6822(90)90462-Z

    Article  CAS  Google Scholar 

  17. Höfer P, Bedford ID, Markham PG, Jeske H, Frischmuth T (1997) Coat protein gene replacement results in whitefly transmission of an insect nontransmissible geminivirus isolate. Virology 236(2):288–295. https://doi.org/10.1006/viro.1997.8751

    Article  PubMed  Google Scholar 

  18. Noris E, Vaira AM, Caciagli P, Masenga V, Gronenborn B, Accotto GP (1998) Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. J Virol 72:10050–10057

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Götz M, Popovski S, Kollenberg M, Gorovitz R, Brown JK, Cicero JM, Czosnek H, Winter S, Ghanim M (2012) Implication of Bemisia tabaci heat shock protein 70 in begomovirus-whitefly interactions. J Virol 86:13241–13252. https://doi.org/10.1128/JVI.00880-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ohnesorge S, Bejarano ER (2009) Begomovirus coat protein interacts with a small heat-shock protein of its transmission vector (Bemisia tabaci). Insect Mol Biol 18(6):693–703. https://doi.org/10.1111/j.1365-2583.2009.00906.x

    Article  CAS  PubMed  Google Scholar 

  21. Rana VS, Popli S, Saurav GK, Raina HS, Chaubey R, Ramamurthy VV, Rajagopal R (2016) A Bemisia tabaci midgut protein interacts with begomoviruses and plays a role in virus transmission. Cell Microbiol 18(5):663–678. https://doi.org/10.1111/cmi.12538

    Article  CAS  PubMed  Google Scholar 

  22. Kanakala S, Ghanim M (2016) Implication of the whitefly Bemisia tabaci cyclophilin B protein in the transmission of Tomato yellow leaf curl virus. Front Plant Sci 7:1702. https://doi.org/10.3389/fpls.2016.01702

    Article  PubMed  PubMed Central  Google Scholar 

  23. Shalev AH, Sobol I, Ghanim M, Liu S-S, Czosnek H (2016) The whitefly Bemisia tabaci knottin-1 gene is implicated in regulating the quantity of Tomato Yellow Leaf Curl Virus ingested and transmitted by the insect. Viruses 8(7):205. https://doi.org/10.3390/v8070205

    Article  CAS  Google Scholar 

  24. Wang Z-Z, Shi M, Huang Y-C, Wang X-W, Stanley D, Chen X-X (2016) A peptidoglycan recognition protein acts in whitefly (Bemisia tabaci) immunity and involves in Begomovirus acquisition. Sci Rep 6:37806. https://doi.org/10.1038/srep37806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pan L-L, Chen Q-F, Zhao J-J, Guo T, Wang X-W, Hariton-Shalev A, Czosnek H, Liu S-S (2017) Clathrin-mediated endocytosis is involved in Tomato yellow leaf curl virus transport across the midgut barrier of its whitefly vector. Virology 502:152–159. https://doi.org/10.1016/j.virol.2016.12.029

    Article  CAS  PubMed  Google Scholar 

  26. Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin M, Sobol I, Czosnek H, Vavre F, Fleury F, Ghanim M (2010) The transmission efficiency of Tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317. https://doi.org/10.1128/JVI.00423-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  28. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Morgulis AG, Raytselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24(16):1757–1764. https://doi.org/10.1093/bioinformatics/btn322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214. https://doi.org/10.1089/10665270050081478

    Article  CAS  PubMed  Google Scholar 

  31. Chou K-C, Shen H-B (2008) ProtIdent: a web server for identifying proteases and their types by fusing functional domain and sequential evolution information. Biochem Biophys Res Commun 376(2):321–325. https://doi.org/10.1016/j.bbrc.2008.08.125

    Article  CAS  PubMed  Google Scholar 

  32. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. https://doi.org/10.1038/nmeth.1701

    Article  CAS  PubMed  Google Scholar 

  33. Källberg M, Wang H, Wang S, Peng J, Wang Z, Lu H, Xu J (2012) Template-based protein structure modeling using the RaptorX web server. Nat Protoc 7:1511–1522. https://doi.org/10.1038/nprot.2012.085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rana VS (2013) Identification of receptor candidates of Begomovirus in B. tabaci. PhD Thesis, University of Delhi, Delhi

  35. Bock KR, Guthrie EJ, Meredith G (1978) Distribution host range, properties and purification of cassava latent virus, a geminivirus. Ann Appl Biol 90(3):361–367. https://doi.org/10.1111/j.1744-7348.1978.tb02644.x

    Article  CAS  Google Scholar 

  36. Ohnishi J, Kitamura T, Terami F, Honda K (2009) A selective barrier in the midgut epithelial cell membrane of the nonvector whitefly Trialeurodes vaporariorum to Tomato yellow leaf curl virus uptake. J Gen Plant Pathol 75(2):131–139. https://doi.org/10.1007/s10327-009-0147-3

    Article  Google Scholar 

  37. Ohta A, Nishiyama Y (2011) Mitochondria and viruses. Mitochondrion 11(1):1–12. https://doi.org/10.1016/j.mito.2010.08.006

    Article  CAS  PubMed  Google Scholar 

  38. Li J-M, Ruan Y-M, Li F-F, Liu S-S, Wang X-W (2011) Gene expression profiling of the whitefly (Bemisia tabaci) Middle East—Asia Minor 1 feeding on healthy and Tomato yellow leaf curl China virus-infected tobacco. Insect Sci 18(1):11–22. https://doi.org/10.1111/j.1744-7917.2010.01386.x

    Article  CAS  Google Scholar 

  39. Arnér ESJ, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109. https://doi.org/10.1046/j.1432-1327.2000.01701.x

    Article  PubMed  Google Scholar 

  40. Chibani K, Wingsle G, Jacquot J-P, Gelhaye E, Rouhier N (2009) Comparative genomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol Plant 2(2):308–322. https://doi.org/10.1093/mp/ssn076

    Article  CAS  PubMed  Google Scholar 

  41. Åslund F, Beckwith J (1999) The thioredoxin superfamily: redundancy, specificity and gray-Area Genomics. J Bacteriol 181:1375–1379

    PubMed  PubMed Central  Google Scholar 

  42. Liu Q, Liu H, Gong Y, Tao Y, Jiang L, Zuo W, Yang Q, Ye J, Lai J, Wu J, Lübberstedt T, Xu M (2017) An atypical thioredoxin imparts early resistance to Sugarcane mosaic virus in maize. Mol Plant 10(3):483–497. https://doi.org/10.1016/j.molp.2017.02.002

    Article  CAS  PubMed  Google Scholar 

  43. Russel M, Model P (1986) The role thioredoxin in filamentous phage assembly. Construction, isolation and characterization of mutant thioredoxins. J Biol Chem 261:14997–15005

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Dr. V. G. Malthi for providing ToLCNDV infectious clone. We thank Dr. N. C. Naveen and Dr. V. V. Ramamurthy of Division of Entomology, Indian Agriculture Research Institute (IARI), New Delhi for their scientific help in this work. We also thank Ashok Kumar and Ravi Singh for their excellent lab assistance. This work was funded by Indian Council of Agricultural Research-National Agricultural Science Fund (ICAR-NASF). GD was provided research fellowship by Council of Scientific and Industrial Research (CSIR). VSR was provided Research Fellowship by University Grants Commission-Dr. D. S. Kothari Postdoctoral Fellowship Scheme (UGC-DSKPDF).

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Authors and Affiliations

  1. Gut Biology Laboratory, Department of Zoology, University of Delhi, Room No. 117, Delhi, 110007, India

    Gunjan Kumar Saurav, Vipin Singh Rana, Sonam Popli, Guisuibou Daimei & Raman Rajagopal

  2. Dr. B. R. Ambedkar Center for Biomedical Research, University of Delhi, Delhi, 110007, India

    Vipin Singh Rana

  3. Department of Immunology and Microbiology, The Scripps Research Institute, Jupiter, FL, USA

    Sonam Popli

  4. Department of Zoology, United College, Chandel, Manipur, 795127, India

    Guisuibou Daimei

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  1. Gunjan Kumar Saurav
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Contributions

Conceived and designed the experiments: RR, GKS. Performed the experiments: GKS, VSR, SP, GD. Analyzed the data: GKS, VSR, RR. Wrote the paper: GKS, RR. Read and approved: GKS, VSR, SP, GD, RR.

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Correspondence to Raman Rajagopal.

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Communicated by A. Lorena Passarelli.

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Saurav, G.K., Rana, V.S., Popli, S. et al. A thioredoxin-like protein of Bemisia tabaci interacts with coat protein of begomoviruses. Virus Genes 55, 356–367 (2019). https://doi.org/10.1007/s11262-019-01657-z

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