Abstract
Viruses profoundly depend on endogenous host transport system and interact with preexisting host cellular factors during movement. Potyviral movement is directed by several movement proteins that are HC-Pro, CP, VPg, and CI and newly discovered P3N-PIPO. CP and HC-Pro facilitate movement of virus by increasing size exclusion limit (SEL) of plasmodesmata (PD). These movement proteins serve many functions: binding the viral genome, transporting the viral genome to plasmodesmata, gating plasmodesmata, trafficking through plasmodesmata, and then transporting through phloem. TuMV P3N-PIPO is a PD-localized protein and mediates the targeting of CI to PD. The P3 protein was not previously associated with potyvirus movement, but it was known to interact with the P1 protein; it is co-localized with 6K2 vesicles (site of potyviral replication). This points out a link between virus replication complexes and intracellular movement. CP has the ability to increase SEL of PD and interact with host RTM factors and suppress RTM resistance of plants. HC-Pro is crucial for long-distance movement of potyvirus by suppressing gene silencing mechanism of host plant. Interaction with host factors and chaperones is also required for efficient spread of potyvirus; presumably interaction of the viral CP with a plant Dna J-like protein NtCPIP (capsid protein interacting proteins) provides a strong in vivo confirmation for the essential role of plant chaperones in potyvirus movement. In this chapter, we are concerned on potyvirus intracellular, intercellular, and long-distance movement, focusing on the host cellular factors’ interaction with movement proteins involved.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Atreya PL, Atreya CD, Pirone TP (1991) Amino acid substitutions in the coat protein result in loss of insect transmissibility of a plant virus. Proc Natl Acad Sci U S A 88:7887–7897
Bilgin DD, Liu Y, Schiff M, Dinesh-Kumar SP (2003) P58 (IPK), a plant ortholog of double-stranded RNA-dependent protein kinase PKR inhibitor, functions in viral pathogenesis. Dev Cell 4:651–661
Boevenik P, Oparka K (2005) Virus-host interactions during movement process. Plant Physiol 138:1815–1821
Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47:159–251
Carrington JC, Kasschau KD, Mahajan SK, Schaad MC (1996) Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8:1669–1681
Carrington JC, Jensen PE, Schaad MC (1998) Genetic evidence for an essential role for potyvirus CI protein in cell-to-cell movement. Plant J 14:393–400
Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:1667–1675
Chung BY, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105:5897–5902
Cosson P, Sofer L, Quang Hien Le, Leger V, Schurdi-Levraud V, Whitham SA, Yamamoto ML, Gopalan S, Le Gall O, Candresse T, Carrington JC, Revers F (2010) RTM3, which controls long-distance movement of potyviruses, is a member of a new plant gene family encoding a Meprin and TRAF homology domain-containing protein. Plant Physiol 154:222–232
Cotton S, Dufresne PJ, Thivierge K, Ide C, Fortin MG (2006) The VPgPro protein of Turnip mosaic virus: in vitro inhibition of translation from a ribonuclease activity. Virology 351:92–100
Cronin S, Verchot J, Haldeman-Cahill R, Schaad MC, Carrington JC (1995) Long-distance movement factor: a transport function of the potyvirus helper component-proteinase. Plant Cell 7:549–559
Cuevas JM, Delaunay A, Visser JC, Bellstedt DU, Jacquot E, Elena SF (2012) Phylogeography and molecular evolution of potato virus Y. PLoS One 7(5):e37853
Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A (2010) The tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397:56–63
Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, Garcia JA, Candresse T, Le Gall O, Revers F (2006) Multiple resistance traits control plum pox virus infection in Arabidopsis thaliana. Mol Plant Microbe Interact 19:541–549
Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, GarcĂa JA, Candresse T (2009) The determinant of potyvirus ability to overcome the RTM resistance of Arabidopsis thaliana maps to the N-terminal region of the coat protein. Mol Plant Microbe Interact 22:1302–1311
Dolja VV, Haldeman R, Robertson NL, Dougherty WG, Carrington JC (1994) Distinct functions of capsid protein in assembly and movement of tobacco etch potyvirus in plants. EMBO J 13:1482–1491
Dolja VV, Haldeman-Cahill R, Montgomery AE, VandenBosch KA, Carrington JC (1995) Capsid protein determinants involved in cell-to-cell and long distance movement of tobacco etch potyvirus. Virology 206:1007–1016
Dufresne PJ, Thivierge K, Cotton S, Beauchemin C, Ide C, Ubalijoro E, Laliberte JF, Fortin MG (2008) Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology 374:217–227
Eduardo I, Chietera G, Pirona R, Pacheco I, Troggio M, Banchi E, Bassi D, Rossini L, Vecchietti A, Pozzi C (2012) Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps. Tree Genetics Genomes 9(1):189–204. http://link.springer.com/journal/11295
Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340:245–246
Gao Z, Johansen E, Eyers S, Thomas CL, Noel Ellis TH, Maule AJ (2004) The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J 40:376–385
Govier DA, Kassanis B (1974) A virus-induced component of plant sap needed when aphids acquire potato virus Y from purified preparations. Virology 61:420–426
Greber UF, Way M (2006) A superhighway to virus infection. Cell 124:741–754
Hofius D, Maier AT, Dietrich C, Jungkunz I, Bo¨rnke F, Maiss E, Sonnewald U (2007) Capsid protein-mediated recruitment of host DnaJ-Like proteins is required for Potato Virus Y infection in tobacco plants. J Virol 81:11870–11880
Huang M, Zhang L (1999) Association of the movement protein of alfalfa mosaic virus with the endoplasmic reticulum and its trafficking in epidermal cells of onion bulb scales. Mol Plant Microbe Interact 12:680–690
Huang Z, Han Y, Howell SH (2000) Formation of surface tubules and fluorescent foci in Arabidopsis thaliana protoplasts expressing a fusion between the green fluorescent protein and the Cauliflower mosaic virus movement protein. Virology 271:58–64
Huet H, Gal-on A, Meir E, Lecoq H, Raccah B (1994) Mutations in the helper component protease gene of zucchini yellow mosaic virus affect its ability to mediate aphid transmissibility. J Gen Virol 75:1407–1414
Ivanov KI, Puustinen P, Merits A, Saarma M, Mäkinen K (2001) Phosphorylation down-regulates the RNA binding function of the coat protein of potato virus A. J Biol Chem 276:13530–13540
Ivanov KI, Puustinen P, Gabrenaite R, Vihinen H, Rönnstrand L, Valmu L, Kalkkinen N, Mäkinen K (2003) Phosphorylation of the potyvirus capsid protein by protein kinase CK2 and its relevance for virus infection. Plant Cell 15:2124–2139
Kasschau KD, Carrington JC (1995) Requirement for HC-Pro processing during genome amplification of tobacco etch potyvirus. Virology 209:268–273
Kasschau KD, Cronin S, Carrington JC (1997) Genome amplification and long-distance movement functions associated with the central domain of tobacco etch potyvirus helper component-proteinase. Virology 228:251–262
Kasschau KD, Xie ZX, Llave AE, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217
Kelley WL (1998) The J-domain family and the recruitment of chaperone power. Trends Biochem Sci 23:222–227
Klein PG, Klein RR, RodrõÂguez-Cerezo E, Hunt AG, Shaw JG (1994) Mutational analysis of the tobacco vein mottling virus genome. Virology 204:759–769
Langenberg WG (1986) Virus protein association with cylindrical inclusion of two viruses that infect wheat. J Gen Virol 67:1161–1168
Langford GM (1995) Actin- and microtubule-dependant organelle motors: interrelationships between the two motility systems. Curr Opin Cell Biol 7:82–88
Laporte C, Vetter G, Loudes AM, Robinson DG, Hillmer S et al (2003) Involvement of the secretory pathway and the cytoskeleton in intracellular targeting and tubule assembly of grapevine fanleaf virus movement protein in tobacco BY-2 cells. Plant Cell 15:2058–2075
Lellis AD, Kasschau KD, Whitham SA, Carrington JC (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr Biol 12:1046–1051
Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberte JF (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J Virol 74:7730–7737
Léonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberté JF (2004) Interaction of VPg-Pro of turnip mosaic virus with the translation initiation factor 4E and the poly (A)-binding protein in planta. J Gen Virol 85:1055–1063
Li XH, Valdez P, Olvera RE, Carrington JC (1997) Functions of the tobacco etch virus RNA polymerase (NIb): subcellular transport and protein-protein interaction with VPg/proteinase (NIa). J Virol 71:1598–1607
Lopez-Moya JJ, Pirone TP (1998) Charge changes near the N terminus of the coat protein of two potyviruses affect virus movement. J Gen Virol 79:161–165
Maia IG, Bernardi F (1996) Nucleic acid-binding properties of a bacterially expressed potato virus Y helper component-proteinase. J Gen Virol 77:869–877
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684
Merits A, Guo D, Järvekülg L, Saarma M (1998) Biochemical and genetic evidence for interactions between potato a potyvirus-encoded proteins P1 and P3 and proteins of the putative replication complex. Virology 263:15–22
Peña EJ, Heinlein M (2012) RNA transport during TMV cell-to-cell movement. Front Plant Sci 3:193
Pouwels J, Van Der Krogt GNM, Van Lent J, Bisseling T, Wellink J (2002) The cytoskeleton and the secretory pathway are not involved in targeting the cowpea mosaic virus movement protein to the cell periphery. Virology 297:48–56
Radtke AL, O’Riordan MXD (2006) Intracellular innate resistance to bacterial pathogens. Cell Microbiol 8:1720–1729. doi:10.1111/j.1462-5822.2006.00795.x
Rajamaki M-L, Valkonen JPT (2002) Viral genome-linked protein (VPg) controls accumulation and phloem-loading of a potyvirus in inoculated potato leaves. Mol Plant-Microbe Interact 15:138–149
Roberts IM, Wang D, Findaly K, Maule AJ (1998) Ultrastructural and temporal observations of the potyvirus cylindrical inclusions (CIs) show that the CI protein acts transiently in aiding virus movement. Virology 244:173–181
Rojas MR, Zerbini FM, Allison RF, Gilbertson RL, Lucas WJ (1997) Capsid protein and helper component-proteinase function as potyvirus cell-to-cell movement proteins. Virology 237:283–295
Roudet-Tavert G, Michon T, Walter J, Delaunay T, Redondo E, Le Gall O (2007) Central domain of a potyvirus VPg is involved in the interaction with the host translation initiation factor eIF4E and the viral protein HcPro. J Gen Virol 88:1029–1033
Santa Cruz S (1999) Perspective: phloem transport of viruses and macromolecules-what goes in must come out. Trends Microbiol 7:237–241
Schaad MC, Haldeman-Cahill R, Cronin S, Carrington JC (1996) Analysis of the VPg-proteinase (NIa) encoded by tobacco etch potyvirus: effects of mutations on subcellular transport, proteolytic processing, and genome amplification. J Virol 70:7039–7048
Schaad MC, Jensen PE, Carrington JC (1997) Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J 16:4049–4059
Serva S, Nagy PD (2006) Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J Virol 80:2162–2169
Shahabuddin M, Shaw JG, Rhoads RE (1988) Mapping of the tobacco vein mottling virus VPg cistron. Virology 163:635–637
Shukla DD, Ward CW, Brunt AA (1994) The Potyviridae. CAB International, Oxford
Silva MS, Wellink J, Goldbach RW, van Lent JWM (2002) Phloem loading and unloading of Cowpea mosaic virus in Vigna unguiculata. J Gen Virol 83:1493–1504
Spetz C, Jari PT (2004) Valkonen potyviral 6K2 protein long-distance movement and symptom-induction functions are independent and host-specific. Mol Plant-Microbe Interact 17:502–510
Vijayapalani P, Maeshima M, Nagasaki-Takekuchi N, Miller WA (2012) Interaction of the trans-frame potyvirus protein P3N-PIPO with host protein PCaP1 facilitates potyvirus movement. PLoS Pathog 8(4): e1002639. doi:10.1371/journal.ppat.1002639
Wei T, Wang A (2008) Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at the endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J Virol 82:12252–12264
Wei T, Zhang C, Hong J, Xiong R, Kasschau KD, Zhou XP, Carrington JC, Wang AM (2010a) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6:e1000962
Wei TY, Huang TS, McNeil J, Laliberte JF, Jong J, Nelson RS, Wang AM (2010b) Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J Virol 84:799–809
Wen RH, Hajimorad MR (2010) Mutational analysis of the putative PIPO of soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400:1–7
Whitham S, Wang Y (2004) Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 7:1–7
Whitham SA, Anderberg RJ, Chisholm ST, Carrington JC (2000) Arabidopsis RTM2 gene is necessary for specific restriction of tobacco etch virus and encodes an unusual small heat shock-like protein. Plant Cell 12:569–582
Yasuyuki Yamaji, Kensaku Maejima, Ken Komatsu, Takuya Shiraishi, Yukari Okano, Misako Himeno, Kyoko Sugawara, Yutaro Neriya, Nami Minato, Chihiro Miura, Masayoshi Hashimoto, Shigetou Namba (2012) Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell 24:778–793
Acknowledgement
The authors are thankful to Department of Biotechnology, New Delhi, India for providing the financial support (ref no. BT/PR14902/BRB/10/889/2010) during this study.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer India
About this chapter
Cite this chapter
Verma, R.K., Mishra, R., Sharma, P., Choudhary, D.K., Gaur, R.K. (2014). Systemic Infection of Potyvirus: A Compatible Interaction Between Host and Viral Proteins. In: Gaur, R., Sharma, P. (eds) Approaches to Plant Stress and their Management. Springer, New Delhi. https://doi.org/10.1007/978-81-322-1620-9_20
Download citation
DOI: https://doi.org/10.1007/978-81-322-1620-9_20
Published:
Publisher Name: Springer, New Delhi
Print ISBN: 978-81-322-1619-3
Online ISBN: 978-81-322-1620-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)