title: Long-distance movement of Cauliflower mosaic virus and host defence responses in Arabidopsis follow a predictable pattern that is determined by the leaf orthostichy.
abstract: Long-distance virus transport takes place through the vascular system and is dependent on the movement of photoassimilates. Here, patterns of symptom development, virus movement and gene expression were analysed in Arabidopsis following inoculation with Cauliflower mosaic virus (CaMV) on a single leaf. Virus accumulation and expression of markers for the salicylic acid (SA) and ethylene/jasmonate (Et/JA) defence pathways, PR-1 and PDF1.2, were analysed on a leaf-by-leaf basis by real-time reverse transcription polymerase chain reaction (qRT-PCR). Virus spread followed a strictly defined pattern identical to that of a source-sink relationship. This was exploited to study differences between local and systemic defence responses in a developmental and spatial manner. In infected plants, PR-1 transcripts accumulated primarily but not exclusively in leaves with a direct vascular connection to the inoculated leaf. Abundances fell significantly as virus accumulated. By contrast, PDF1.2 transcripts were significantly lower than in controls in all leaves at early stages of infection, but recovered as virus accumulated. Virus and PR-1 transcript abundances are negatively correlated, and SA- and Et/JA-mediated signalling of gene expression occurs independently of the presence of virus. Although SA-dependent signalling responses were mainly linked to the orthostichy, Et/JA-dependent responses were independent of vascular connections.
authors: Plant Science Group, Division of Biochemistry & Molecular Biology, Institute of Biomedical and Life Sciences, Glasgow University, Glasgow G12 8QQ, UK.|School of Biological Sciences, University of Wales - Bangor, Memorial Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, UK.
authors: Karen
authors: K
authors: Roberts
authors: Plant Science Group, Division of Biochemistry & Molecular Biology, Institute of Biomedical and Life Sciences, Glasgow University, Glasgow G12 8QQ, UK.
authors: Andrew J
authors: AJ
authors: Love
authors: Plant Science Group, Division of Biochemistry & Molecular Biology, Institute of Biomedical and Life Sciences, Glasgow University, Glasgow G12 8QQ, UK.
authors: Valérie
authors: V
authors: Laval
authors: Plant Science Group, Division of Biochemistry & Molecular Biology, Institute of Biomedical and Life Sciences, Glasgow University, Glasgow G12 8QQ, UK.
authors: Janet
authors: J
authors: Laird
authors: School of Biological Sciences, University of Wales - Bangor, Memorial Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, UK.
authors: A Deri
authors: AD
authors: Tomos
authors: School of Biological Sciences, University of Wales - Bangor, Memorial Building, Deiniol Road, Bangor, Gwynedd LL57 2UW, UK.
authors: Mark A
authors: MA
authors: Hooks
authors: Plant Science Group, Division of Biochemistry & Molecular Biology, Institute of Biomedical and Life Sciences, Glasgow University, Glasgow G12 8QQ, UK.
authors: Joel J
authors: JJ
authors: Milner
mesh_terms: D017360:Arabidopsis / Q000033:anatomy & histology / Q000378:metabolism* / Q000821:virology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D001692:Biological Transport; D017796:Caulimovirus / Q000502:physiology*; D023082:Defensins / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D015967:Gene Expression Regulation, Viral; D018515:Plant Leaves / Q000033:anatomy & histology* / Q000378:metabolism / Q000821:virology*
chemical_list: D029681:Arabidopsis Proteins; D023082:Defensins; C487542:At5g44420 protein, Arabidopsis; C077262:PR-1 protein, Arabidopsis
references: Al Kaff NS, Covey SN. 1995. Biological diversity of cauliflower mosaic-virus isolates expressed in two brassica species. Plant Pathology 44: 516-526.
references: Allan AC, Lapidot M, Culver JN, Fluhr R. 2001. An early tobacco mosaic virus-induced oxidative burst in tobacco indicates extracellular perception of the virus coat protein. Plant Physiology 126: 97-108.
references: Aranda MA, Escaler M, Wang DW, Maule AJ. 1996. Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proceedings of the National Academy of Sciences, USA 93: 15289-15293.
references: Baulcombe D. 2004. RNA silencing in plants. Nature 431: 356-363.
references: Busse JS, Evert RF. 1999. Vascular differentiation and transition in the seedling of Arabidopsis thaliana (Brassicaceae). International Journal of Plant Sciences 160: 241-251.
references: Callaway A, Liu WN, Andrianov V, Stenzler L, Zhao JM, Wettlaufer S, Jayakumar P, Howell SH. 1996. Characterization of cauliflower mosaic virus (CaMV) resistance in virus-resistant ecotypes of Arabidopsis. Molecular Plant-Microbe Interactions 9: 810-818.
references: Callos JD, Medford JI. 1994. Organ positions and pattern-formation in the shoot apex. Plant Journal 6: 1-7.
references: Cameron RK, Paiva NL, Lamb CJ, Dixon RA. 1999. Accumulation of salicylic acid and PR-1 gene transcripts in relation to the systemic acquired resistance (SAR) response induced by Pseudomonas syringae pv. tomato in Arabidopsis. Physiological and Molecular Plant Pathology 55: 121-130.
references: Cecchini E, Al Kaff NS, Bannister A, Giannakou ME, McCallum DG, Maule AJ, Milner JJ, Covey SN. 1998. Pathogenic interactions between variants of cauliflower mosaic virus and Arabidopsis thaliana. Journal of Experimental Botany 49: 731-737.
references: Covey SN, McCallum DG, Turner DS, Al Kaff NS, Dale P, Cecchini E, Milner JJ. 2000. Pararetrovirus-crucifer interactions: attack and defence or modus vivendi. Molecular Plant Pathology 1: 77-86.
references: Dempsey DA, Pathirana MS, Wobbe KK, Klessig DF. 1997. Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. Plant Journal 11: 301-311.
references: Dempsey DA, Wobbe KK, Klessig DF. 1993. Resistance and susceptible responses of Arabidopsis thaliana to turnip crinkle virus. Phytopathology 83: 1021-1029.
references: Dewdney J, Reuber TL, Wildermuth MC, Devoto A, Cui JP, Stutius LM, Drummond EP, Ausubel FM. 2000. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant Journal 24: 205-218.
references: French CJ, Elder M. 1999. Virus particles in guttate and xylem of infected cucumber (Cucumis sativus L.). Annals of Applied Biology 134: 81-87.
references: Geri C, Cecchini E, Giannakou ME, Covey SN, Milner JJ. 1999. Altered patterns of gene expression in Arabidopsis elicited by cauliflower mosaic virus (CaMV) infection and by a CaMV gene VI transgene. Molecular Plant-Microbe Interactions 12: 377-384.
references: Geri C, Love AJ, Cecchini E, Barrett SJ, Laird J, Covey SN, Milner JJ. 2004. Arabidopsis mutants that suppress the phenotype induced by transgene-mediated expression of cauliflower mosaic virus (CaMV) gene VI are less susceptible to CaMV-infection and show reduced ethylene sensitivity. Plant Molecular Biology 56: 111-124.
references: Haas M, Bureau M, Geldreich A, Yot P, Keller M. 2002. Cauliflower mosaic virus: still in the news. Molecular Plant Pathology 3: 419-429.
references: Haritatos E, Medville R, Turgeon R. 2000. Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211: 105-111.
references: Havelda Z, Maule AJ. 2000. Complex spatial responses to cucumber mosaic virus infection in susceptible Cucurbita pepo cotyledons. Plant Cell 12: 1975-1985.
references: Hull R. 2001. Matthews plant virology, 4th edn. New York, NY, UAS: Academic Press.
references: Ji LH, Ding SW. 2001. The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Molecular Plant-Microbe Interactions 14: 715-724.
references: Kang J, Tang J, Donnelly P, Dengler N. 2003. Primary vascular pattern and expression of ATHB-8 in shoots of Arabidopsis. New Phytologist 158: 443-454.
references: Kiefer IW, Slusarenko AJ. 2003. The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiology 132: 840-847.
references: Kisslaszlo Z, Blanc S, Hohn T. 1995. Splicing of cauliflower mosaic virus 35S RNA is essential for viral infectivity. EMBO Journal 14: 3552-3562.
references: Kunkel BN, Brooks DM. 2002. Cross talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5: 325-331.
references: Laird J, Armengaud P, Giuntini P, Laval V, Milner JJ. 2004. Inappropriate annotation of a key defence marker in Arabidopsis: will the real PR-1 please stand up? Planta 219: 1089-1092.
references: Lartey RT, Ghoshroy S, Citovsky V. 1998. Identification of an Arabidopsis thaliana mutation (vsm1) that restricts systemic movement of tobamoviruses. Molecular Plant-Microbe Interactions 11: 706-709.
references: Leisner SM, Howell SH. 1992. Symptom variation in different Arabidopsis thaliana ecotypes produced by cauliflower mosaic-virus. Phytopathology 82: 1042-1046.
references: Leisner S, Turgeon R. 1993. Movement of virus and photoassimilate in the phloem - a comparative-analysis. Bioessays 15: 741-748.
references: Love AJ, Laval V, Geri C, Laird J, Tomos AD, Hooks MA, Milner JJ. 2007. Components of Arabidopsis defense- and ethylene-signaling pathways regulate susceptibility to Cauliflower mosaic virus by restricting long-distance movement. Molecular Plant-Microbe Interactions 20: 659-670.
references: Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ. 2005. Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defence signalling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiology 139: 935-948.
references: 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 Journal 14: 177-186.
references: Maule A, Leh V, Lederer C. 2002. The dialogue between viruses and hosts in compatible interactions. Current Opinion in Plant Biology 5: 279-284.
references: Melcher UK. 1989. Symptoms of cauliflower mosaic virus infection in Arabidopsis thaliana and turnips. Botanical Gazette 150: 139-147.
references: Mitter N, Kazan K, Way HM, Broekaert WF, Manners JM. 1998. Systemic induction of an Arabidopsis plant defensin gene promoter by tobacco mosaic virus and jasmonic acid in transgenic tobacco. Plant Science 136: 169-180.
references: Murray SL, Thomson C, Chini A, Read ND, Loake GJ. 2002. Characterization of a novel, defense-related Arabidopsis mutant, cir1, isolated by luciferase imaging. Molecular Plant-Microbe Interactions 15: 557-566.
references: Penninckx IAMA, Eggermont K, Schenk PM, Van Den Ackerveken G, Cammue BPA, Thomma BPHJ. 2003. The Arabidopsis mutant iop1 exhibits induced over-expression of the plant defensin gene PDF1.2 and enhanced pathogen resistance. Molecular Plant Pathology 4: 479-486.
references: Penninckx IAMA, Thomma BPHJ, Buchala A, Metraux JP, Broekaert WF. 1998. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10: 2103-2113.
references: Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M. 2007. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proceedings of the National Academy of Sciences, USA 104: 1075-1080.
references: Turgeon R. 1989. The sink_source transition in leaves. Annual Review of Plant Physiology and Plant Molecular Biology 40: 119-138.
references: Van Bel AJE, Gaupels F. 2004. Pathogen-induced resistance and alarm signals in the phloem. Molecular Plant Pathology 5: 495-504.
references: Voinnet O. 2005. Induction and suppression of RNA silencing: Insights from viral infections. Nature Reviews Genetics 6: 206-202U1.
references: Volko SM, Boller T, Ausubel FM. 1998. Isolation of new Arabidopsis mutants with enhanced disease susceptibility to Pseudomonas syringae by direct screening. Genetics 149: 537-548.
references: Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J. 2004. Proteomics of curcurbit phloem exudate reveals a network of defence proteins. Phytochemistry 65: 1795-1804.
references: Wang DW, Maule AJ. 1995. Inhibition of host gene expression associated with plant-virus replication. Science 267: 229-231.
references: Whitham SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM. 2003. Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant Journal 33: 271-283.
references: Wiermer M, Feys BJ, Parker JE. 2005. Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8: 383-389.