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Published in: Archives of Virology 9/2016

Open Access 01-09-2016 | Original Article

The role of plasmodesma-located proteins in tubule-guided virus transport is limited to the plasmodesmata

Authors: P. W. den Hollander, S. N. Kieper, J. W. Borst, J. W. M. van Lent

Published in: Archives of Virology | Issue 9/2016

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Abstract

Intercellular spread of plant viruses involves passage of the viral genome or virion through a plasmodesma (PD). Some viruses severely modify the PD structure, as they assemble a virion carrying tubule composed of the viral movement protein (MP) inside the PD channel. Successful modulation of the host plant to allow infection requires an intimate interaction between viral proteins and both structural and regulatory host proteins. To date, however, very few host proteins are known to promote virus spread. Plasmodesmata-located proteins (PDLPs) localised in the PD have been shown to contribute to tubule formation in cauliflower mosaic virus and grapevine fanleaf virus infections. In this study, we have investigated the role of PDLPs in intercellular transport of another tubule-forming virus, cowpea mosaic virus. The MP of this virus was found to interact with PDLPs in the PD, as was shown for other tubule-forming viruses. Expression of PDLPs and MPs in protoplasts in the absence of a PD revealed that these proteins do not co-localise at the site of tubule initiation. Furthermore, we show that tubule assembly in protoplasts does not require an interaction with PDLPs at the base of the tubule, as has been observed in planta. These results suggest that a physical interaction between MPs and PDLPs is not required for assembly of the movement tubule and that the beneficial role of PDLPs in virus movement is confined to the structural context of the PD.
Literature
1.
go back to reference Kragler F (2013) Plasmodesmata: Intercellular tunnels facilitating transport of macromolecules in plants. Cell Tissue Res 352:49–58CrossRefPubMed Kragler F (2013) Plasmodesmata: Intercellular tunnels facilitating transport of macromolecules in plants. Cell Tissue Res 352:49–58CrossRefPubMed
3.
go back to reference Harries PA, Ding B (2011) Cellular factors in plant virus movement: at the leading edge of macromolecular trafficking in plants. Virology 411:237–243CrossRefPubMed Harries PA, Ding B (2011) Cellular factors in plant virus movement: at the leading edge of macromolecular trafficking in plants. Virology 411:237–243CrossRefPubMed
4.
go back to reference Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99CrossRefPubMed Niehl A, Heinlein M (2011) Cellular pathways for viral transport through plasmodesmata. Protoplasma 248:75–99CrossRefPubMed
5.
go back to reference van Lent JWM, Wellink J, Goldbach RW (1990) Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of Cowpea mosaic virus. J Gen Virol 71:219–223CrossRef van Lent JWM, Wellink J, Goldbach RW (1990) Evidence for the involvement of the 58K and 48K proteins in the intercellular movement of Cowpea mosaic virus. J Gen Virol 71:219–223CrossRef
6.
go back to reference Ritzenthaler C, Schmit AC, Michler P, Stussi-Garaud C, Pinck L (1995) Grapevine fanleaf nepovirus P38 putative movement protein is located on tubules in vivo. Mol Plant Microbe Interact 8:379–387CrossRef Ritzenthaler C, Schmit AC, Michler P, Stussi-Garaud C, Pinck L (1995) Grapevine fanleaf nepovirus P38 putative movement protein is located on tubules in vivo. Mol Plant Microbe Interact 8:379–387CrossRef
7.
go back to reference Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541–1555CrossRefPubMedPubMedCentral Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde JP, Lherminier J (2009) Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs Potato virus X movement. Plant Cell 21:1541–1555CrossRefPubMedPubMedCentral
8.
go back to reference Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61:131–142CrossRefPubMed Zavaliev R, Sagi G, Gera A, Epel BL (2010) The constitutive expression of arabidopsis plasmodesmal-associated class 1 reversibly glycosylated polypeptide impairs plant development and virus spread. J Exp Bot 61:131–142CrossRefPubMed
10.
go back to reference Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS biol 6:e7CrossRefPubMedPubMedCentral Thomas CL, Bayer EM, Ritzenthaler C, Fernandez-Calvino L, Maule AJ (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS biol 6:e7CrossRefPubMedPubMedCentral
11.
go back to reference Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6:301–311CrossRefPubMed Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6:301–311CrossRefPubMed
12.
go back to reference Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6:e1001119CrossRefPubMedPubMedCentral Amari K, Boutant E, Hofmann C, Schmitt-Keichinger C, Fernandez-Calvino L, Didier P, Lerich A, Mutterer J, Thomas CL (2010) A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6:e1001119CrossRefPubMedPubMedCentral
13.
go back to reference Amari K, Lerich A, Schmitt-Keichinger C, Dolja VV, Ritzenthaler C (2011) Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog 7:e1002327CrossRefPubMedPubMedCentral Amari K, Lerich A, Schmitt-Keichinger C, Dolja VV, Ritzenthaler C (2011) Tubule-guided cell-to-cell movement of a plant virus requires class XI myosin motors. PLoS Pathog 7:e1002327CrossRefPubMedPubMedCentral
14.
go back to reference Liebrand TW, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JH, America AH, Sklenar J, Jones AM, Robatzek S (2012) Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol 159:1819–1833CrossRefPubMedPubMedCentral Liebrand TW, Smit P, Abd-El-Haliem A, de Jonge R, Cordewener JH, America AH, Sklenar J, Jones AM, Robatzek S (2012) Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol 159:1819–1833CrossRefPubMedPubMedCentral
15.
go back to reference Pouwels J, van der Krogt GN, 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 297:48–56CrossRefPubMed Pouwels J, van der Krogt GN, 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 297:48–56CrossRefPubMed
16.
go back to reference Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94:2122–2127CrossRefPubMedPubMedCentral Haseloff J, Siemering KR, Prasher DC, Hodge S (1997) Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci USA 94:2122–2127CrossRefPubMedPubMedCentral
17.
go back to reference de Ronde D, Butterbach P, Lohuis D, Hedil M, van Lent JWM, Kormelink R (2013) Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol Plant Pathol 14:405–415CrossRefPubMed de Ronde D, Butterbach P, Lohuis D, Hedil M, van Lent JWM, Kormelink R (2013) Tsw gene-based resistance is triggered by a functional RNA silencing suppressor protein of the Tomato spotted wilt virus. Mol Plant Pathol 14:405–415CrossRefPubMed
18.
go back to reference van Bokhoven H, Verver J, Wellink J, van Kammen A (1993) Protoplasts transiently expressing the 200K coding sequence of Cowpea mosaic virus B-RNA support replication of M-RNA. J Gen Virol 74:2233–2241CrossRefPubMed van Bokhoven H, Verver J, Wellink J, van Kammen A (1993) Protoplasts transiently expressing the 200K coding sequence of Cowpea mosaic virus B-RNA support replication of M-RNA. J Gen Virol 74:2233–2241CrossRefPubMed
19.
go back to reference Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS (2009) Tape-arabidopsis sandwich—a simpler arabidopsis protoplast isolation method. Plant Methods 5:16CrossRefPubMedPubMedCentral Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS (2009) Tape-arabidopsis sandwich—a simpler arabidopsis protoplast isolation method. Plant Methods 5:16CrossRefPubMedPubMedCentral
20.
go back to reference Truong K, Ikura M (2001) The use of FRET imaging microscopy to detect protein–protein interactions and protein conformational changes in vivo. Curr Opin Struct Biol 11:573–578CrossRefPubMed Truong K, Ikura M (2001) The use of FRET imaging microscopy to detect protein–protein interactions and protein conformational changes in vivo. Curr Opin Struct Biol 11:573–578CrossRefPubMed
21.
go back to reference Borst JW, Visser AJWG (2010) Fluorescence lifetime imaging microscopy in life sciences. Meas Sci Technol 21:102002CrossRef Borst JW, Visser AJWG (2010) Fluorescence lifetime imaging microscopy in life sciences. Meas Sci Technol 21:102002CrossRef
22.
go back to reference Bücherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH, Aker J, van Hoek A, Albrecht C, Borst JW (2013) Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol 162:1911–1925CrossRefPubMedPubMedCentral Bücherl CA, van Esse GW, Kruis A, Luchtenberg J, Westphal AH, Aker J, van Hoek A, Albrecht C, Borst JW (2013) Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling. Plant Physiol 162:1911–1925CrossRefPubMedPubMedCentral
23.
go back to reference Gopinath K, Bertens P, Pouwels J, Marks H, van Lent JWM, Wellink J, van Kammen A (2003) Intracellular distribution of Cowpea mosaic virus movement protein as visualised by green fluorescent protein fusions. Arch Virol 148:2099–2114CrossRefPubMed Gopinath K, Bertens P, Pouwels J, Marks H, van Lent JWM, Wellink J, van Kammen A (2003) Intracellular distribution of Cowpea mosaic virus movement protein as visualised by green fluorescent protein fusions. Arch Virol 148:2099–2114CrossRefPubMed
24.
go back to reference Storms MM, Kormelink R, Peters D, van Lent JWM, Goldbach RW (1995) The nonstructural NSm protein of Tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485–493CrossRefPubMed Storms MM, Kormelink R, Peters D, van Lent JWM, Goldbach RW (1995) The nonstructural NSm protein of Tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214:485–493CrossRefPubMed
25.
go back to reference Kasteel DTJ, van der Wel NN, Jansen KA, Goldbach RW, van Lent JWM (1997) Tubule-forming capacity of the movement proteins of Alfalfa mosaic virus and Brome mosaic virus. J Gen Virol 78:2089–2093CrossRefPubMed Kasteel DTJ, van der Wel NN, Jansen KA, Goldbach RW, van Lent JWM (1997) Tubule-forming capacity of the movement proteins of Alfalfa mosaic virus and Brome mosaic virus. J Gen Virol 78:2089–2093CrossRefPubMed
26.
27.
go back to reference den Hollander PW, de Sousa Geraldino Duarte P, Bloksma H, Boeren S, Van Lent JWM (2016) Proteomic analysis of the plasma membrane-movement tubule complex of cowpea mosaic virus. Arch Virol 161:1309–1314CrossRef den Hollander PW, de Sousa Geraldino Duarte P, Bloksma H, Boeren S, Van Lent JWM (2016) Proteomic analysis of the plasma membrane-movement tubule complex of cowpea mosaic virus. Arch Virol 161:1309–1314CrossRef
28.
go back to reference Pouwels J, van der Velden T, Willemse J, Borst JW, van Lent JWM, Bisseling T, Wellink J (2004) Studies on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85:3787–3796CrossRefPubMed Pouwels J, van der Velden T, Willemse J, Borst JW, van Lent JWM, Bisseling T, Wellink J (2004) Studies on the origin and structure of tubules made by the movement protein of Cowpea mosaic virus. J Gen Virol 85:3787–3796CrossRefPubMed
29.
go back to reference Kasteel DTJ, Perbal MC, Boyer JC, Wellink J, Goldbach RW, Maule AJ, Van Lent JWM (1996) The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77:2857–2864CrossRefPubMed Kasteel DTJ, Perbal MC, Boyer JC, Wellink J, Goldbach RW, Maule AJ, Van Lent JWM (1996) The movement proteins of cowpea mosaic virus and cauliflower mosaic virus induce tubular structures in plant and insect cells. J Gen Virol 77:2857–2864CrossRefPubMed
Metadata
Title
The role of plasmodesma-located proteins in tubule-guided virus transport is limited to the plasmodesmata
Authors
P. W. den Hollander
S. N. Kieper
J. W. Borst
J. W. M. van Lent
Publication date
01-09-2016
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2016
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-2936-2

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