Skip to main content
SpringerLink
Log in

Identification of host factors potentially involved in RTM-mediated resistance during potyvirus long distance movement

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The long distance movement of potyviruses is a poorly understood step of the viral cycle. Only factors inhibiting this process, referred to as “Restricted TEV Movement” (RTM), have been identified in Arabidopsis thaliana. On the virus side, the potyvirus coat protein (CP) displays determinants required for long-distance movement and for RTM-based resistance breaking. However, the potyvirus CP was previously shown not to interact with the RTM proteins. We undertook the identification of Arabidopsis factors which directly interact with either the RTM proteins or the CP of lettuce mosaic virus (LMV). An Arabidopsis cDNA library generated from companion cells was screened with LMV CP and RTM proteins using the yeast two-hybrid system. Fourteen interacting proteins were identified. Two of them were shown to interact with CP and the RTM proteins suggesting that a multiprotein complex could be formed between the RTM proteins and virions or viral ribonucleoprotein complexes. Co-localization experiments in Nicotiana benthamiana showed that most of the viral and cellular protein pairs co-localized at the periphery of chloroplasts which suggests a putative role for plastids in this process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Allison RF, Dougherty WG, Parks TD, Willis J, Johnston RE, Kelly ME, Armstrong FB (1985) Biochemical analysis of the capsid protein gene and capsid protein of tobacco etch virus: N-terminal amino acids are located on the virion’s surface. Virology 147:309–316

    Article  CAS  PubMed  Google Scholar 

  2. Andersen K, Johansen IE (1998) A single conserved amino acid in the coat protein gene of pea seed-borne mosaic potyvirus modulates the ability of the virus to move systemically in Chenopodium quinoa. Virology 241:304–311

    Article  CAS  PubMed  Google Scholar 

  3. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403:203–207

    Article  CAS  PubMed  Google Scholar 

  4. Cayla T, Batailler B, Le Hir R, Revers F, Anstead JA, Thompson GA, Grandjean O, Dinant S (2015) Live imaging of companion cells and sieve elements in arabidopsis leaves. PLoS One 10:e0118122

    Article  PubMed  PubMed Central  Google Scholar 

  5. Charon J, Theil S, Nicaise V, Michon T (2016) Protein intrinsic disorder within the Potyvirus genus: from proteome-wide analysis to functional annotation. Mol BioSyst 12:634–652

    Article  CAS  PubMed  Google Scholar 

  6. Chisholm J, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Chisholm ST, Mahajan SK, Whitham SA, Yamamoto ML, Carrington JC (2000) Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc Natl Acad Sci USA 97:489–494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chroboczek J, Hébrard E, Mäkinen K, Michon T, Rantalainen K (2012) Intrinsic disorder in genome-linked viral proteins VPgs of potyviruses. In: Uversky VN, Longhi S (eds) Flexible viruses: structural disorder in viral proteins. Wiley, Hoboken, pp 277–312

    Google Scholar 

  9. Cosson P, Sofer L, Le QH, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cosson P, Schurdi-Levraud V, Le QH, Sicard O, Caballero M, Roux F, Le Gall O, Candresse T, Revers F (2012) The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes. PLoS One 7:e39169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Decroocq V, Sicard O, Alamillo JM, Lansac M, Eyquard JP, García 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

    Article  CAS  PubMed  Google Scholar 

  12. Decroocq V, Salvador B, Sicard O, Glasa M, Cosson P, Svanella-Dumas L, Revers F, García 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

    Article  CAS  PubMed  Google Scholar 

  13. Dolja V, 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

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Dolja V, 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

    Article  CAS  PubMed  Google Scholar 

  15. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A (2004) A cysteine-rich plant protein potentiates Potyvirus movement through an interaction with the virus genome-linked protein VPg. J Virol 78:2301–2309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. English JJ, Davenport GF, Elmayan T, Vaucheret H, Baulcombe DC (1997) Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J 12:597–603

    Article  CAS  Google Scholar 

  17. Gámez-Arjona FM, de la Concepción JC, Raynaud S, Mérida Á (2014) Arabidopsis thaliana plastoglobule-associated fibrillin 1a interacts with fibrillin 1b in vivo. FEBS Lett 588:2800–2804

    Article  PubMed  Google Scholar 

  18. He Y, Chen B, Pang Q, Strul JM, Chen S (2010) Functional specification of Arabidopsis isopropylmalate isomerases in glucosinolate and leucine biosynthesis. Plant Cell Physiol 51:1480–1487

    Article  CAS  PubMed  Google Scholar 

  19. Hipper C, Brault V, Ziegler-Graff V, Revers F (2013) Viral and cellular factors involved in phloem transport of plant viruses. Front Plant Sci 4:154. doi:10.3389/fpls.2013.00154

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hruz TLO, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747

    Google Scholar 

  21. Izumi M, Tsunoda H, Suzuki Y, Makino A, Ishida H (2012) RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity. J Exp Bot 63:2159–2170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Karimi M, Inzé D, Depicker A (2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  Google Scholar 

  23. Knill T, Schuster J, Reichelt M, Gershenzon J, Binder S (2008) Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol 146:1028–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Krause-Sakate R, Le Gall O, Fakhfakh H, Peypelut M, Marrakchi M, Varveri C, Pavan MA, Souche S, Lot H, Zerbini FM, Candresse T (2002) Molecular characterization of Lettuce mosaic virus field isolates reveals a distinct and widespread type of resistance-breaking isolate: LMV-Most. Phytopathology 92:563–572

    Article  CAS  PubMed  Google Scholar 

  25. Krichevsky A, Zaltsman A, Kozlovsky SV, Tian GW, Citovsky V (2009) Regulation of root elongation by histone acetylation in Arabidopsis. J Mol Biol 385:45–50

    Article  CAS  PubMed  Google Scholar 

  26. Ksenofontov AL, Paalme V, Arutyunyan AM, Semenyuk PI, Fedorova NV, Rumvolt R, Baratova LA, Järvekülg L, Dobrov EN (2013) Partially disordered structure in intravirus coat protein of potyvirus potato virus A. PLoS One 8:e67830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kuusk S, Sohlberg JJ, Magnus Eklund D, Sundberg E (2006) Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J 47:99–111

    Article  CAS  PubMed  Google Scholar 

  28. Laizet Y, Pontier D, Mache R, Kuntz M (2004) Subfamily organization and phylogenetic origin of genes encoding plastid lipid-associated proteins of the fibrillin type. J Genome Sci Technol 3:19–28

    Article  CAS  Google Scholar 

  29. 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

    Article  CAS  PubMed  Google Scholar 

  30. Mahajan SK, Chisholm ST, Whitham SA, Carrington JC (1998) Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J 14:177–186

    Article  CAS  PubMed  Google Scholar 

  31. Nacir H, Bréhélin C (2013) When proteomics reveals unsuspected roles: the plastoglobule example. Front Plant Sci 4:114. doi:10.3389/fpls.2013.00114

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F, Westedt I, Staiger D, Alfano JR, Zipfel C (2013) Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J 32:701–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Revers F, Lot H, Souche S, Le Gall O, Candresse T, Dunez J (1997) Biological and molecular variability of lettuce mosaic virus isolates. Phytopathology 87:397–403

    Article  CAS  PubMed  Google Scholar 

  34. Revers F, Yang SJ, Walter J, Souche S, Lot H, Le Gall O, Candresse T, Dunez J (1997) Comparison of the complete nucleotide sequences of two isolates of lettuce mosaic virus differing in their biological properties. Virus Res 47:167–177

    Article  CAS  PubMed  Google Scholar 

  35. Revers F, van der Vlugt RA, Souche S, Lanneau M, Lot H, Candresse T, Le Gall O (1999) Nucleotide sequence of the 3′ terminal region of the genome of four lettuce mosaic virus isolates from Greece and Yemen. Arch Virol 144:1619–1626

    Article  CAS  PubMed  Google Scholar 

  36. Revers F, Guiraud T, Houvenaghel M-C, Mauduit T, Le Gall O, Candresse T (2003) Multiple resistance phenotypes to lettuce mosaic virus among Arabidopsis thaliana accessions. Mol Plant Microbe Interact 16:608–616

    Article  CAS  PubMed  Google Scholar 

  37. Revers F, García JA (2015) Molecular biology of potyviruses. Adv Virus Res 92:101–199

    Article  PubMed  Google Scholar 

  38. Rodriguez-Medina C, Boissinot S, Chapuis S, Gereige D, Rastegar M, Erdinger M, Revers F, Ziegler-Graff V, Brault V (2015) A protein kinase binds the C-terminal domain of the readthrough protein of Turnip yellows virus and regulates virus accumulation. Virology 486:44–53

    Article  CAS  PubMed  Google Scholar 

  39. Rybicki EP, Shukla DD (1992) Coat protein phylogeny and systematics of potyviruses. In: Barnett Jr O (ed) Potyvirus taxonomy. Springer, New York, pp 139–170

  40. Scharf K-D, Siddique M, Vierling E (2001) The expanding family of Arabidopsis thaliana small heat stress proteins and a new family of proteins containing α-crystallin domains (Acd proteins). Cell Stress Chaperones 6:225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Schuster J, Knill T, Reichelt M, Gershenzon J, Binder S (2006) BRANCHED-CHAIN AMINOTRANSFERASE4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18:2664–2679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Seibel NM, Eljouni J, Nalaskowski MM, Hampe W (2007) Nuclear localization of enhanced green fluorescent protein homomultimers. Anal Biochem 368:95–99

    Article  CAS  PubMed  Google Scholar 

  43. Shukla DD, Strike PM, Tracy SL, Gough KH, Ward CW (1988) The N and C termini of the coat proteins of potyviruses are surface-located and the N-terminus contains the major virus-specific epitopes. J Gen Virol 69:1497–1508

    Article  CAS  Google Scholar 

  44. Singh DK, McNellis TW (2011) Fibrillin protein function: the tip of the iceberg? Trends Plant Sci 16:432–441

    Article  CAS  PubMed  Google Scholar 

  45. Tanaka Y, Nakamura S, Kawamukai M, Koizumi N, Nakagawa T (2011) Development of a series of gateway binary vectors possessing a tunicamycin resistance gene as a marker for the transformation of Arabidopsis thaliana. Biosci Biotechnol Biochem 75:804–807

    Article  CAS  PubMed  Google Scholar 

  46. Wei T, Huang T-S, McNeil J, Laliberté J-F, Hong J, Nelson RS, Wang A (2010) Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. J Virol 84:799–809

    Article  CAS  PubMed  Google Scholar 

  47. Whitham SA, Yamamoto ML, Carrington JC (1999) Selectable viruses and altered susceptibility mutants in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:772–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yang Y, Sulpice R, Himmelbach A, Meinhard M, Christmann A, Grill E (2006) Fibrillin expression is regulated by abscisic acid response regulators and is involved in abscisic acid-mediated photoprotection. Proc Natl Acad Sci USA 103:6061–6066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhan G-M, Li R-J, Hu Z-Y, Liu J, Deng L-B, Lu S-Y, Hua W (2014) Cosuppression of RBCS3B in Arabidopsis leads to severe photoinhibition caused by ROS accumulation. Plant Cell Rep 33:1091–1108

    Article  CAS  PubMed  Google Scholar 

  51. Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers EP (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138:803–818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Thierry Mauduit, Marylin Roncoroni and Aurélie Bailly for the production and maintenance of Arabidopsis plants, Sixue Chen (University of Florida) for the atleud1 mutant, Brigitte Batailler and Lysiane Brocard (BIC, Bordeaux) for technical help with the confocal microscopy, Valérie Nicaise (Virology team, INRA, Bordeaux) for advice with the Western blotting experiments. The microscopy was done in the Bordeaux Imaging Center, a service unit of the CNRS-INSERM and Bordeaux University, a member of the national infrastructure, France BioImaging.

Author information

Author notes

  1. Frédéric Revers

    Present address: BIOGECO, INRA, University of Bordeaux, 33615, Pessac, France

  2. Daniel Garcia Cabanillas

    Present address: Institut National de la Recherche Scientifique-Institut Armand-Frappier, Laval, QC, H7V 1B7, Canada

  3. Jérôme Pouzoulet

    Present address: Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

  4. Marie Ducousso

    Present address: UMR 0385 BGPI, Virus Insecte Plante, INRA, Campus international de Bailllarguet, Montpellier, France

Authors and Affiliations

  1. BFP, INRA, University of Bordeaux, 33140, Villenave d’Ornon, France

    Luc Sofer, Daniel Garcia Cabanillas, Mathieu Gayral, Rachèle Téplier, Jérôme Pouzoulet, Marie Ducousso, Laurène Dufin & Frédéric Revers

  2. UMR 5200, Laboratory of Membrane Biogenesis, CNRS, University of Bordeaux, 33140, Villenave d’Ornon, France

    Claire Bréhélin

  3. Institut de Biologie Moléculaire des Plantes, Laboratoire propre du CNRS conventionné avec l’Université de Strasbourg, 12 rue du Général Zimmer, 67084, Strasbourg, France

    Véronique Ziegler-Graff

  4. SVQV, INRA, 28 rue de Herrlisheim, 68021, Colmar, France

    Véronique Brault

Authors
  1. Luc Sofer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Garcia Cabanillas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mathieu Gayral
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachèle Téplier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jérôme Pouzoulet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marie Ducousso
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Laurène Dufin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Claire Bréhélin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Véronique Ziegler-Graff
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Véronique Brault
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Frédéric Revers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frédéric Revers.

Ethics declarations

Funding

This study was funded by the French National Research Agency (ANR) in the frame of the ViroMouv project (ANR-08-GENM-016-001).

Conflict of interest

Authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sofer, L., Cabanillas, D.G., Gayral, M. et al. Identification of host factors potentially involved in RTM-mediated resistance during potyvirus long distance movement. Arch Virol 162, 1855–1865 (2017). https://doi.org/10.1007/s00705-017-3292-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3292-6

Keywords

Search

Navigation