title: The tobamovirus Turnip Vein Clearing Virus 30-kilodalton movement protein localizes to novel nuclear filaments to enhance virus infection.
abstract: Plant viruses overcome the barrier of the plant cell wall by encoding cell-to-cell movement proteins (MPs), which direct newly replicated viral genomes to, and across, the wall. The paradigm for how a single MP regulates and coordinates these activities is the Tobacco mosaic virus (TMV) 30-kDa protein (MP(TMV)). Detailed studies demonstrate that TMV multiplies exclusively in the cytoplasm and have documented associations of MP(TMV) with endoplasmic reticulum (ER) membrane, microtubules, and plasmodesmata throughout the course of infection. As TMV poorly infects Arabidopsis thaliana, Turnip vein clearing virus (TVCV) is the tobamovirus of choice for studies in this model plant. A key problem, which has contributed to confusion in the field, is the unproven assumption that the TVCV and TMV life cycles are identical. We engineered an infectious TVCV replicon that expressed a functional fluorescence-tagged MP(TVCV) and report here the unexpected discovery that MP(TVCV), beyond localizing to ER membrane and plasmodesmata, targeted to the nucleus in a nuclear localization signal (NLS)-dependent manner, where it localized to novel F-actin-containing filaments that associated with chromatin. The MP(TVCV) NLS appeared to be conserved in the subgroup 3 tobamoviruses, and our mutational analyses showed that nuclear localization of MP(TVCV) was necessary for efficient TVCV cell-to-cell movement and systemic infection in Nicotiana benthamiana and Arabidopsis thaliana. Our studies identify a novel nuclear stage in TVCV infection and suggest that nuclear MP encoded by TVCV and other subgroup 3 tobamoviruses interacts with F-actin and chromatin to modulate host defenses or cellular physiology to favor virus movement and infection.
authors.affiliation: Cornell University, Department of Plant Pathology and Plant-Microbe Biology, Ithaca, New York, USA.
authors.forename: Amit
authors.initials: A
authors.lastname: Levy
authors.forename: Judy Y
authors.initials: JY
authors.lastname: Zheng
authors.forename: Sondra G
authors.initials: SG
authors.lastname: Lazarowitz
mesh_terms: D008841:Actin Cytoskeleton / Q000378:metabolism / Q000821:virology*; D000199:Actins / Q000378:metabolism; D017360:Arabidopsis / Q000378:metabolism / Q000821:virology*; D002467:Cell Nucleus / Q000378:metabolism / Q000821:virology*; D019913:Nuclear Localization Signals; D010935:Plant Diseases / Q000821:virology*; D053830:Plant Viral Movement Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D021381:Protein Transport; D014026:Nicotiana / Q000378:metabolism / Q000821:virology*; D017898:Tobamovirus / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
chemical_list: D000199:Actins; D019913:Nuclear Localization Signals; D053830:Plant Viral Movement Proteins
references.citation: Proc Natl Acad Sci U S A. 2010 Feb 9;107(6):2491-6
references.pmid: 20133785
references.citation: Plant Cell. 1999 Apr;11(4):535-48
references.pmid: 10213776
references.citation: Plant Cell. 1995 Dec;7(12):2101-14
references.pmid: 8718621
references.citation: Plant Mol Biol. 1996 Jan;30(1):191-7
references.pmid: 8616237
references.citation: Gene. 1994 Dec 30;151(1-2):119-23
references.pmid: 7828859
references.citation: Plant Physiol. 2007 Feb;143(2):801-11
references.pmid: 17189338
references.citation: Virology. 2011 Mar 15;411(2):237-43
references.pmid: 21239029
references.citation: Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1415-20
references.pmid: 14745003
references.citation: Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1433-7
references.pmid: 8108427
references.citation: Plant Signal Behav. 2010 May;5(5):518-22
references.pmid: 21228632
references.citation: Plant J. 1997 Oct;12(4):781-9
references.pmid: 9375392
references.citation: Science. 1987 Jul 24;237(4813):389-94
references.pmid: 17794341
references.citation: Plant J. 2007 Feb;49(4):669-82
references.pmid: 17270015
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19199-204
references.pmid: 19052240
references.citation: Trends Biochem Sci. 2011 Oct;36(10):532-40
references.pmid: 21920760
references.citation: J Exp Bot. 2010 Sep;61(14):3839-45
references.pmid: 20624762
references.citation: Mol Cells. 2001 Aug 31;12(1):57-66
references.pmid: 11561731
references.citation: Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17594-9
references.pmid: 19805075
references.citation: Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):6291-6
references.pmid: 15079061
references.citation: Plant Physiol. 2003 Aug;132(4):1870-83
references.pmid: 12913144
references.citation: Traffic. 2007 Jan;8(1):21-31
references.pmid: 17132144
references.citation: Cold Spring Harb Perspect Biol. 2010 Apr;2(4):a000620
references.pmid: 20452941
references.citation: Nature. 2009 Sep 10;461(7261):193-8
references.pmid: 19741699
references.citation: Plant Cell. 1994 Jul;6(7):995-1006
references.pmid: 8069108
references.citation: Virology. 1991 Jan;180(1):318-26
references.pmid: 1984654
references.citation: Plant Physiol. 2006 Apr;140(4):1317-30
references.pmid: 16461385
references.citation: Virus Genes. 2012 Feb;44(1):131-40
references.pmid: 21948005
references.citation: Genes Dev. 2004 Oct 15;18(20):2545-56
references.pmid: 15489295
references.citation: Curr Biol. 2006 Apr 18;16(8):825-31
references.pmid: 16631592
references.citation: Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2122-7
references.pmid: 9122158
references.citation: Cell. 2011 Jan 7;144(1):158-158.e2
references.pmid: 21215376
references.citation: Plant Cell. 1992 Apr;4(4):397-411
references.pmid: 1379865
references.citation: Virology. 1990 Aug;177(2):553-8
references.pmid: 2371769
references.citation: Plant Cell. 1998 Jul;10(7):1107-20
references.pmid: 9668131
references.citation: J Cell Biol. 1999 Nov 29;147(5):945-58
references.pmid: 10579716
references.citation: Mol Plant Microbe Interact. 1995 Sep-Oct;8(5):666-73
references.pmid: 7579612
references.citation: Commun Integr Biol. 2011 Sep;4(5):582-3
references.pmid: 22046469
references.citation: J Cell Biol. 2007 Dec 17;179(6):1095-103
references.pmid: 18070915
references.citation: Mol Plant Microbe Interact. 2007 Jul;20(7):740-50
references.pmid: 17601162
references.citation: J Virol. 2004 Oct;78(20):11161-71
references.pmid: 15452236
references.citation: Arch Virol. 1999;144(5):957-71
references.pmid: 10416377
references.citation: Plant Cell. 2002 Jun;14(6):1207-22
references.pmid: 12084822
references.citation: Plant Physiol. 2005 Aug;138(4):1853-65
references.pmid: 16040646
references.citation: Arch Virol. 2004 Aug;149(8):1499-514
references.pmid: 15290376
references.citation: Immunol Rev. 2009 Jan;227(1):176-88
references.pmid: 19120484
references.citation: Mol Cell. 1998 Aug;2(2):241-5
references.pmid: 9734361
references.citation: Mol Plant. 2011 Sep;4(5):813-31
references.pmid: 21896501
references.citation: Genes Dev. 2011 May 1;25(9):946-58
references.pmid: 21536734
references.citation: Plant J. 1997 Sep;12(3):537-45
references.pmid: 9351241
references.citation: Cell Motil Cytoskeleton. 2007 Nov;64(11):822-32
references.pmid: 17685442
references.citation: Mol Plant Microbe Interact. 2010 Nov;23(11):1381-93
references.pmid: 20653412
references.citation: Mol Biol Evol. 1996 Dec;13(10):1327-38
references.pmid: 8952077
references.citation: Virology. 1995 Feb 20;207(1):191-204
references.pmid: 7871727
references.citation: Mol Plant Microbe Interact. 2001 Jul;14(7):895-904
references.pmid: 11437263
references.citation: J Virol. 2000 Apr;74(7):3330-7
references.pmid: 10708450
references.citation: Traffic. 2000 Jul;1(7):540-4
references.pmid: 11208141
references.citation: J Exp Bot. 2002 Jun;53(373):1531-2
references.pmid: 12021302
references.citation: Cell Microbiol. 2012 May;14(5):622-33
references.pmid: 22289128
references.citation: Cell. 2011 Jan 21;144(2):310.e1
references.pmid: 21241897
references.citation: Mol Plant Microbe Interact. 2010 Oct;23(10):1231-47
references.pmid: 20831404
references.citation: Plant J. 2009 Jul;59(1):150-62
references.pmid: 19309457