title: Tomato yellow leaf curl Sardinia virus-resistant tomato plants expressing the multifunctional N-terminal domain of the replication-associated protein show transcriptional changes resembling stress-related responses.
abstract: The N-terminal domain (amino acids 1-130) of the replication-associated protein (Rep130 ) of Tomato yellow leaf curl Sardinia virus (TYLCSV) retains the ability of full-length Rep to localize to the nucleus and to down-regulate C1 transcription when ectopically expressed in plants, both functions being required to inhibit homologous viral replication. In this study, we analysed the effect of Rep130 expression on virus resistance and the plant transcriptome in the natural and agronomically important host species of TYLCSV, Solanum lycopersicum. Tomato plants accumulating high levels of Rep130 were generated and proved to be resistant to TYLCSV. Using an in vitro assay, we showed that plant-expressed Rep130 also retains the catalytic activity of Rep, thus supporting the notion that this protein domain is fully functional. Interestingly, Rep130 -expressing tomatoes were characterized by an altered transcriptional profile resembling stress-related responses. Notably, the serine-type protease inhibitor (Ser-PI) category was over-represented among the 20 up-regulated genes. The involvement of Rep130 in the alteration of host mRNA steady-state levels was confirmed using a distinct set of virus-resistant transgenic tomato plants expressing the same TYLCSV Rep130 , but from a different, synthetic, gene. Eight genes were found to be up-regulated in both types of transgenic tomato and two encoded Ser-PIs. Four of these eight genes were also up-regulated in TYLCSV-infected wild-type tomato plants. Implications with regard to the ability of this Rep domain to interfere with viral infections and to alter the host transcriptome are discussed.
authors.affiliation: Agenzia Nazionale per le Nuove Tecnologie, l'Energia e l'Ambiente (ENEA), UTAGRI-INN, C.R. Casaccia, Via Anguillarese 301, 00123, Rome, Italy.
authors.forename: Alessandra
authors.initials: A
authors.lastname: Lucioli
authors.forename: Alessandra
authors.initials: A
authors.lastname: Berardi
authors.forename: Francesca
authors.initials: F
authors.lastname: Gatti
authors.forename: Raffaela
authors.initials: R
authors.lastname: Tavazza
authors.forename: Daniele
authors.initials: D
authors.lastname: Pizzichini
authors.forename: Mario
authors.initials: M
authors.lastname: Tavazza
mesh_terms: D017360:Arabidopsis / Q000235:genetics; D001483:Base Sequence; D053839:Begomovirus / Q000502:physiology*; D016000:Cluster Analysis; D017124:Conserved Sequence / Q000235:genetics; D060467:Disease Resistance / Q000276:immunology*; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D018551:Solanum lycopersicum / Q000235:genetics* / Q000276:immunology / Q000821:virology*; D008969:Molecular Sequence Data; D010935:Plant Diseases / Q000235:genetics / Q000276:immunology / Q000821:virology; D030821:Plants, Genetically Modified; D017434:Protein Structure, Tertiary; D013312:Stress, Physiological / Q000235:genetics*; D014026:Nicotiana / Q000235:genetics; D014158:Transcription, Genetic; D015854:Up-Regulation / Q000235:genetics; D014764:Viral Proteins / Q000737:chemistry* / Q000378:metabolism
chemical_list: D014764:Viral Proteins
references.citation: Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5640-4
references.pmid: 7777563
references.citation: Plant Cell. 2005 Jan;17(1):311-25
references.pmid: 15608335
references.citation: J Virol. 1996 Oct;70(10):6790-5
references.pmid: 8794317
references.citation: J Virol. 2009 Jul;83(13):6769-78
references.pmid: 19369323
references.citation: Nucleic Acids Res. 2006;34(21):6362-77
references.pmid: 17142233
references.citation: Adv Bioinformatics. 2008;2008:420747
references.pmid: 19956698
references.citation: Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):9906-10
references.pmid: 8234334
references.citation: Curr Top Microbiol Immunol. 2009;331:185-226
references.pmid: 19230564
references.citation: EMBO J. 2000 Jul 3;19(13):3485-95
references.pmid: 10880461
references.citation: Plant Cell. 2011 Feb;23(2):499-514
references.pmid: 21343416
references.citation: Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9533-7
references.pmid: 8415736
references.citation: J Virol. 2004 Nov;78(21):11890-903
references.pmid: 15479830
references.citation: Plant Cell. 1995 Jun;7(6):705-19
references.pmid: 7647562
references.citation: Cell Mol Life Sci. 2012 Oct;69(19):3269-83
references.pmid: 22903295
references.citation: Plant Physiol. 2009 Dec;151(4):1758-68
references.pmid: 19819981
references.citation: J Biol Chem. 2000 Mar 3;275(9):6114-22
references.pmid: 10692401
references.citation: Plant J. 2007 Jul;51(1):127-39
references.pmid: 17559512
references.citation: Plant Cell. 2010 Apr;22(4):1313-32
references.pmid: 20418496
references.citation: Virology. 2005 Jul 5;337(2):273-83
references.pmid: 15913696
references.citation: Cell Death Differ. 2011 Aug;18(8):1289-97
references.pmid: 21546909
references.citation: J Biol Chem. 1994 Mar 18;269(11):8459-65
references.pmid: 8132573
references.citation: Nucleic Acids Res. 1992 Jul 11;20(13):3279-85
references.pmid: 1630899
references.citation: Virology. 2001 Jan 20;279(2):570-6
references.pmid: 11162812
references.citation: Planta. 2001 Jan;212(2):222-30
references.pmid: 11216843
references.citation: Plant Cell. 2001 Jun;13(6):1437-52
references.pmid: 11402171
references.citation: Arch Biochem Biophys. 1982 Feb;213(2):463-72
references.pmid: 7041827
references.citation: Proc Natl Acad Sci U S A. 1990 Nov;87(21):8560-4
references.pmid: 2236066
references.citation: Plant Mol Biol. 1994 Oct;26(2):553-6
references.pmid: 7948911
references.citation: Funct Integr Genomics. 2009 Nov;9(4):433-46
references.pmid: 19633874
references.citation: Nature. 2011 Oct 13;478(7368):264-8
references.pmid: 21964330
references.citation: Bioinformatics. 2004 Aug 4;20 Suppl 1:i31-9
references.pmid: 15262778
references.citation: Virology. 2008 Oct 10;380(1):75-83
references.pmid: 18703212
references.citation: Mol Plant. 2011 Jul;4(4):607-15
references.pmid: 21357647
references.citation: Mol Plant Pathol. 2004 Mar 1;5(2):149-56
references.pmid: 20565592
references.citation: J Virol. 2006 Nov;80(22):11322-30
references.pmid: 16943286
references.citation: J Virol. 2003 Mar;77(5):2972-80
references.pmid: 12584322
references.citation: Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3879-83
references.pmid: 7732000
references.citation: Curr Protein Pept Sci. 2011 Aug;12(5):374-85
references.pmid: 21418020
references.citation: Mol Plant. 2008 May;1(3):482-95
references.pmid: 19825555
references.citation: Plant Cell. 2001 Jan;13(1):179-91
references.pmid: 11158538
references.citation: Plant Physiol. 1997 Sep;115(1):137-49
references.pmid: 9306697
references.citation: J Virol. 2011 Oct;85(19):9789-800
references.pmid: 21775461
references.citation: Mol Plant Pathol. 2008 Jan;9(1):73-83
references.pmid: 18705886
references.citation: Plant J. 2006 Apr;46(1):34-53
references.pmid: 16553894
references.citation: Arch Virol. 2008;153(4):783-821
references.pmid: 18256781
references.citation: Plant Physiol. 2007 Sep;145(1):119-34
references.pmid: 17644626
references.citation: Arch Virol. 2001 Aug;146(8):1465-85
references.pmid: 11676411
references.citation: Planta. 1986 Nov;169(3):399-405
references.pmid: 24232653
references.citation: Plant Sci. 2012 Jul;190:9-15
references.pmid: 22608515
references.citation: Plant J. 1999 May;18(3):265-76
references.pmid: 10377992
references.citation: PLoS One. 2011;6(7):e22383
references.pmid: 21818318
references.citation: Plant Cell. 2002 Dec;14(12):3225-36
references.pmid: 12468739
references.citation: J Virol. 2005 Feb;79(4):2517-27
references.pmid: 15681452
references.citation: Nat Rev Drug Discov. 2008 Sep;7(9):747-58
references.pmid: 18758472
references.citation: Plant J. 2006 Aug;47(4):652-63
references.pmid: 16856987
references.citation: Plant J. 2009 Mar;57(5):905-17
references.pmid: 19000158
references.citation: Virus Res. 2000 Nov;71(1-2):123-34
references.pmid: 11137167
references.citation: Science. 1972 Feb 18;175(4023):776-7
references.pmid: 17836138
references.citation: Curr Biol. 2007 Jul 3;17(13):1116-22
references.pmid: 17583510
references.citation: Nucleic Acids Res. 1991 Mar 25;19(6):1349
references.pmid: 2030957
references.citation: Nucleic Acids Res. 1991 May 11;19(9):2325-30
references.pmid: 2041773
references.citation: Physiol Plant. 2010 Apr;138(4):414-29
references.pmid: 20002601
references.citation: Mol Plant Microbe Interact. 1991 May-Jun;4(3):284-92
references.pmid: 1932815
references.citation: PLoS One. 2012;7(7):e40526
references.pmid: 22808182
references.citation: Virology. 2003 Aug 1;312(2):381-94
references.pmid: 12919743
references.citation: Nucleic Acids Res. 1988 Jul 25;16(14B):7043-60
references.pmid: 3405758
references.citation: Plant Physiol. 2008 Sep;148(1):436-54
references.pmid: 18650403
references.citation: J Gen Virol. 2011 Jan;92(Pt 1):204-9
references.pmid: 20943892
references.citation: Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8029-33
references.pmid: 1896448
references.citation: J Virol. 2003 Jun;77(12):6785-98
references.pmid: 12767999
references.citation: Nat Biotechnol. 2008 Jun;26(6):617-9
references.pmid: 18536679
references.citation: Plant Cell. 1994 Aug;6(8):1157-70
references.pmid: 7919985
references.citation: J Virol. 2004 Mar;78(6):2758-69
references.pmid: 14990696
references.citation: J Biol Chem. 2003 Feb 28;278(9):6862-72
references.pmid: 12482876