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Moonlighting Cell Stress Proteins in Microbial Infections pp 173–187Cite as

Insect Symbiotic Bacterial GroEL (Chaperonin 60) and Plant Virus Transmission

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Part of the book series: Heat Shock Proteins ((HESP,volume 7))

Abstract

GroEL is a multifunctional protein belonging to the conspicuous family of chaperones active in prokaryotic and eukaryotic cells. GroEL of Escherichia coli is a heat shock-like protein (Hsp60). It is involved in the correct folding of newly synthesized proteins, and participates in protein aggregation and in repair of damaged proteins. GroEL is essential for the morphogenesis and the capsid assembly of a number of E. coli bacteriophages. In eukaryotic cells, HSPs were shown to promote virus replication and survival. GroEL homologues are produced not only by free living bacteria but also by bacteria living in total symbiosis with insects and located in specialized eukaryotic cells called bacteriocytes. Symbiosis, which occurred some 200 million years (MY) ago, has led to a reduction of the bacterial genome by two third, accompanied by the adaptation of the endosymbiotic bacteria to novel functions such as providing the host with essential amino acids and other nutrients. It seems that circulative plant viruses have taken advantage of the high production of GroEL by the endosymbionts to device a protective mechanism allowing viral particles to safely cross the haemolymph-filled body cavity of the insect, while translocating from the digestive tract to the salivary system. It seems that the relationship between chaperones and plant viruses, and the insects that vector them, have lasted for geological times (Fig. ). Here we analyze the relationship of endosymbiotic GroEL with viruses in a number of insect-circulative virus systems. Moreover, we show how we can exploit this relationship to devise diagnosis tests for a number of viruses and generate virus-resistant plants by expressing insect endosymbiotic GroEL proteins.

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References

  • Akad F, Dotan N, Czosnek H (2004) Trapping of Tomato yellow leaf curl virus (TYLCV) and other plant viruses with a GroEL homologue from the whitefly Bemisia tabaci. Arch Virol 149:1481–1497

    Article  PubMed  CAS  Google Scholar 

  • Akad F, Eybishtz A, Edelbaum D, Gorovits R, Dar-Issa O, Iraki N, Czosnek H (2007) Making a friend from a foe expressing a GroEL gene from the whitefly Bemisia tabaci in the phloem of tomato plants confers resistance to Tomato yellow leaf curl virus. Arch Virol 152:1323–1339

    Article  PubMed  CAS  Google Scholar 

  • Aparicio F, Thomas CL, Lederer C, Niu Y, Wang D, Maule AJ (2005) Virus induction of heat shock protein 70 reflects a general response to protein accumulation in the plant cytosol. Plant Physiol 138:529–536

    Article  PubMed  CAS  Google Scholar 

  • Aranda MA, Escaler M, Wang D, Maule AJ (1996) Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc Natl Acad Sci U S A 93:15289–15293

    Article  PubMed  CAS  Google Scholar 

  • Baumann P (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189

    Article  PubMed  CAS  Google Scholar 

  • Baumann P, Munson MA, Lai C-Y, Clark MA, Baumann L, Moran NA, Campbell BC (1993) Origin and properties of bacterial endosymbionts of aphids, whiteflies, and mealybugs. ASM News 5:21–24

    Google Scholar 

  • Bejarano ER, Khashoggi A, Witty M, Lichtenstein CP (1996) Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution. Proc Natl Acad Sci U S A 93:759–764

    Article  PubMed  CAS  Google Scholar 

  • Bouvaine S, Boonham N, Douglas AE (2011) Interactions between a luteovirus and the GroEL chaperonin protein of the symbiotic bacterium Buchnera aphidicola of aphids. J Gen Virol 92:1467–1674

    Article  PubMed  CAS  Google Scholar 

  • Braig K, Otwinowski Z, Hegde R, Boisvert DC, Joachimiak A, Horwich AL, Sigler P (1994) The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371:578–586

    Article  PubMed  CAS  Google Scholar 

  • Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66

    Article  Google Scholar 

  • Buchner P (1965) Endosymbionts of animals with plant micro-organisms. Wiley, New York, pp 210–332

    Google Scholar 

  • Cabaleiro C, Segura A (1997) Field transmission of grapevine leafroll associated virus 3 (GLRaV-3) by the mealybug Planococcus citri. Plant Dis 81:283–287

    Article  Google Scholar 

  • Chen AYS, Walker GP, Carter D, Ng JCK (2011) A virus capsid component mediates virion retention and transmission by its insect vector. Proc Natl Acad Sci U S A 108:16777–16782

    Article  PubMed  Google Scholar 

  • Chiel E, Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Katzir N, Inbar M, Ghanim M (2007) Biotype-dependent secondary symbiont communities in sympatric populations of Bemisia tabaci. Bull Entomol Res 97:407–413

    Article  PubMed  CAS  Google Scholar 

  • Costa HS, Toscano NC, Henneberry TJ (1996) Mycetocyte inclusion in the oocytes of Bemisia argentifolii (Homoptera: Aleyrodidae). Ann Entomol Soc Am 89:694–699

    Google Scholar 

  • Czosnek H, Ghanim M, Rubinstein G, Morin S, Fridman V, Zeidan M (2001) Whiteflies: vectors – or victims ? – of geminiviruses. In: Maramorosch K (ed) Advances in virus research, vol 57. Academic Press, New York, pp 291–322

    Google Scholar 

  • De Barro PJ, Liu S-S, Boykin LM, Dinsdale AB (2010) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19

    Article  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37

    Article  PubMed  CAS  Google Scholar 

  • Edelbaum D, Gorovits R, Sasaki S, Ikegami M, Czosnek H (2009) Expressing a whitefly GroEL protein in Nicotiana benthamiana plants confers tolerance to Tomato yellow leaf curl virus (TYLCV) and Cucumber mosaic virus (CMV), but not to Grapevine virus A (GVA) and Tobacco mosaic virus (TMV). Arch Virol 154:399–407

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ, van der Vies SM (1991) Molecular chaperones. Annu Rev Biochem 60:321–347

    Article  PubMed  CAS  Google Scholar 

  • Escaler M, Aranda MA, Roberts IM, Thomas CL, Maule AJ (2000) A comparison between virus replication and abiotic stress (heat) as modifiers of host gene expression in pea. Mol Plant Pathol 1:159–167

    Article  PubMed  CAS  Google Scholar 

  • Fenton WA, Kashi Y, Furtak K, Horwich AL (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371:614–619

    Article  PubMed  CAS  Google Scholar 

  • Filichkin SA, Brumfield S, Filichkin TP, Young MJ (1997) In vitro interactions of the aphid endosymbiotic SymL chaperonin with Barley yellow dwarf virus. J Virol 71:569–577

    PubMed  CAS  Google Scholar 

  • Frohlich DR, Torres-Jerez I, Bedford ID, Markham PG, Brown JK (1999) A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Mol Ecol 8:1683–1691

    Article  PubMed  Google Scholar 

  • Gatehouse LN, Sutherland P, Forgie SA, Kaji R, Christeller JT (2012) Molecular and histological characterization of primary (Betaproteobacteria) and secondary (Gammaproteobacteria) endosymbionts of three mealybug species. Appl Environ Microbiol 78:1187–1197

    Article  PubMed  CAS  Google Scholar 

  • Gorovits R, Moshe A, Kolot M, Sobol I, Czosnek H (2012) Progressive aggregation of Tomato yellow leaf curl virus coat protein in systemically infected tomato plants, susceptible and resistant to the virus. Virus Res 171(1):33–43. doi:10.1016/j.virusres.2012.09.017

    Article  PubMed  Google Scholar 

  • Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M, Brumin N, Sobol I, Czosnek H, Vavre F, Fleury F, Ghanim M (2010) The transmission efficiency of Tomato yellow leaf curl virus is correlated with the presence of a specific symbiotic bacterium species. J Virol 84:9310–9317

    Article  PubMed  CAS  Google Scholar 

  • Götz M, Popovski S, Kollenberg M, Gorovitz R, Brown JK, Cicero J, Czosnek H, Winter S, Ghanim M (2012) Implication of Bemisia tabaci heat shock protein 70 in begomovirus – whitefly interactions. J Virol 86:13241–13252

    Article  PubMed  Google Scholar 

  • Gupta RS (1995) Evolution of the chaperonin families (Hsp60, Hsp60 and TCP-1) of protein and the origin of eukaryotic cells. Mol Microbiol 15:1–11

    Article  PubMed  CAS  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–580

    Article  PubMed  CAS  Google Scholar 

  • Hogenhout SA, van der Wilk F, Verbeek M, Goldbach RW, van den Heuvel JFJM (2000) Identifying the determinants in the equatorial domain of Buchnera GroEL implicated in binding Potato leafroll virus. J Virol 74:4541–4548

    Article  PubMed  CAS  Google Scholar 

  • Hogenhout SA, Ammar E-D, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359

    Article  PubMed  CAS  Google Scholar 

  • Höhnle M, Höfer P, Bedford ID, Briddon RW, Markham PG, Frischmuth T (2001) Exchange of three amino acids in the coat protein results in efficient whitefly transmission of a nontransmissible Abutilon mosaic virus isolate. Virology 290:164–171

    Article  PubMed  Google Scholar 

  • Horwich AL, Low KB, Fanton WA, Hirshfield IN, Furtak K (1993) Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell 74:909–917

    Article  PubMed  CAS  Google Scholar 

  • Kunik T, Palanichelvam K, Czosnek H, Citovsky V, Gafni Y (1998) Nuclear import of a geminivirus capsid protein in plant and insect cells: implications for the viral nuclear entry. Plant J 13:121–129

    Article  Google Scholar 

  • Martin J, Larger T, Boteva R, Schramel A, Horwich AL, Hartl F-U (1991) Chaperonin-mediated protein folding at the surface of GroEL through a ‘molten-globule’-like intermediate. Nature 352:36–42

    Article  PubMed  CAS  Google Scholar 

  • Mayer MP (2005) Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev Physiol Biochem Pharmacol 153:1–46

    Article  PubMed  CAS  Google Scholar 

  • Miller WA, Rasochová L (1997) Barley yellow dwarf viruses. Annu Rev Phytopathol 35:167–190

    Article  PubMed  CAS  Google Scholar 

  • Mine A, Hyodo K, Tajima Y, Kusumanegara K, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T (2012) Differential roles of Hsp70 and Hsp90 in the assembly of the replicase complex of a positive-strand RNA plant virus. J Virol 86:12091–12104

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Baumann P (2000) Bacterial endosymbionts in animals. Curr Opin Microbiol 3:270–275

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Telang A (1998) Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. Bioscience 48:295–304

    Article  Google Scholar 

  • Morin S, Ghanim M, Zeidan M, Czosnek H, Verbeek M, van den Heuvel JFJM (1999) A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of Tomato yellow leaf curl virus. Virology 30:75–84

    Article  Google Scholar 

  • Morin S, Ghanim M, Sobol I, Czosnek H (2000) The GroEL protein of the whitefly Bemisia tabaci interacts with the coat protein of transmissible and non-transmissible begomoviruses in the yeast two-hybrid system. Virology 276:404–416

    Article  PubMed  CAS  Google Scholar 

  • Munson MA, Baumann P, Kinsey MG (1991) Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte associated, primary endosymbionts of aphids. Int J Syst Bacteriol 41:566–568

    Article  Google Scholar 

  • Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:247–266

    Article  PubMed  CAS  Google Scholar 

  • Pan H, Chu D, Yan W, Su Q, Liu B et al (2012) Rapid spread of Tomato yellow leaf curl virus in China is aided differentially by two invasive whiteflies. PLoS One 7:e34817

    Article  PubMed  CAS  Google Scholar 

  • Peremyslov VV, Hagiwara Y, Dolja VV (1999) HSP70 homolog functions in cell-to-cell movement of a plant virus. Proc Natl Acad Sci U S A 96:14771–14776

    Article  PubMed  CAS  Google Scholar 

  • Raccah B, Fereres A (2009) Plant virus transmission by insects. In: Encyclopedia of Life Sciences (ELS). Wiley, Chichester

    Google Scholar 

  • Raccah B, Gal-On A, Eastop V (1985) The role of flying aphid vectors in the transmission of cucumber Mosaic virus and potato virus y to peppers in Israel. Ann Appl Biol 106:451–460

    Article  Google Scholar 

  • 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:e42168

    Article  PubMed  CAS  Google Scholar 

  • Roseman AM, Chen SX, White H, Braig K, Saibil HR (1996) The chaperonin ATPase cycle: mechanism of allosteric switching and movements of substrate-binding domains in GroEL. Cell 87:241–251

    Article  PubMed  CAS  Google Scholar 

  • Rubinstein G, Czosnek H (1997) Long-term association of tomato yellow leaf curl virus (TYLCV) with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. J Gen Virol 78:2683–2689

    PubMed  CAS  Google Scholar 

  • Russell JA, Latorre A, Sabater-Muňoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond Aphidoidea. Mol Ecol 12:1061–1075

    Article  PubMed  CAS  Google Scholar 

  • Schlee D (1970) Verwandtschaftsforschung an fossilen und rezenten Aleyrodina (Insectas, Hemiptera). Stuttgarter Beiträge zur Naturkunde 213:1–74

    Google Scholar 

  • Sigler PB, Xu Z, Rye HS, Burston SG, Fenton WA, Horwich AL (1998) Structure and function in GroEL-mediated protein folding. Annu Rev Biochem 67:581–608

    Article  PubMed  CAS  Google Scholar 

  • Silva FJ, Latorre A, Moya A (2001) Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17:615–618

    Article  PubMed  CAS  Google Scholar 

  • Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 8:986–989

    Article  PubMed  CAS  Google Scholar 

  • Thao ML, Baumann P (2004) Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol 70:3401–3406

    Article  PubMed  CAS  Google Scholar 

  • van den Heuvel JFJM, Verbeek M, van der Wilk F (1994) Endosymbiotic bacteria associated with circulative transmission of potato leafroll virus by Myzus persicae. J Gen Virol 75:2559–2565

    Article  PubMed  Google Scholar 

  • van Ham RCHJ, Kamerbeek J, Palacios C, Rausell C, Abscal F, Bastolla U, Fernandez JM, Jimenez L, Postigo M, Silva FJ, Tamames J, Viguera E, Latorre A, Valencia A, Moran F, Moya A (2003) Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100:581–586

    Article  PubMed  Google Scholar 

  • von Dohlen CD, Kohler S, Alsop ST, McManus WR (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature 412:433–436

    Article  Google Scholar 

  • Whitfield AE, Ullman DE, German TL (2005) Tospovirus-thrips interactions. Annu Rev Phytopathol 43:459–489

    Article  PubMed  CAS  Google Scholar 

  • Wintermantel WM, Wisler GC (2006) Vector specificity, host range, and genetic diversity of Tomato chlorosis virus. Plant Dis 90:814–819

    Article  CAS  Google Scholar 

  • Zchori-Fein E, Brown JK (2002) Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Entomol Soc Am 95:711–718

    Article  Google Scholar 

  • Zeilstra-Ryalls J, Fayet O, Georgopoulos C (1991) The universally conserved GroE chaperonins. Annu Rev Microbiol 31:301–325

    Article  Google Scholar 

  • Zhu H-Y, Ling K-S, Goszczynski DE, McFerson JR, Gonsalves D (1998) Nucleotide sequence and genome organization of Grapevine leafroll-associated virus-2 are similar to beet yellows virus, the closterovirus type member. J Gen Virol 79:1289–1298

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Otto Warburg Minerva Center for Agricultural Biotechnology and Institute of Plant Science and Genetics in Agriculture, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Rena Gorovits & Henryk Czosnek

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  1. Rena Gorovits
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  2. Henryk Czosnek
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Correspondence to Henryk Czosnek .

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  1. Eastman Dental Institute, Div. Microbial Diseases, University College, London, Gray's Inn Road 256, London, WC1X 8LD, United Kingdom

    Brian Henderson

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Gorovits, R., Czosnek, H. (2013). Insect Symbiotic Bacterial GroEL (Chaperonin 60) and Plant Virus Transmission. In: Henderson, B. (eds) Moonlighting Cell Stress Proteins in Microbial Infections. Heat Shock Proteins, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6787-4_11

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