European Journal of Plant Pathology

, Volume 137, Issue 4, pp 765–785 | Cite as

Transcriptional alterations in model host, Nicotiana benthamiana, in response to infection by South African cassava mosaic virus

  • F. Allie
  • M. E. C. ReyEmail author


Successful systemic infection by plant viruses is the outcome of complex molecular interactions between host and viral pathogen, leading to spatial and temporal alterations in plant gene expression. Results from a microarray study using the commercially available custom-made 60-mer oligo NimbleGen Platform (representing 13 014 ESTs) (Roche) revealed that expression levels of many transcripts were altered in response to SACMV at 21 dpi (representing full systemic infection), including encoded proteins involved in transcription networks, defence responses and plant hormone signalling. Approximately 4.7 % (611 of 13 014) of the transcripts were significantly altered in response to SACMV infection. Of these, 483 genes were found to be induced and 128 genes were suppressed. GOslim functional group analysis illustrated that differentially expressed genes in infected leaf tissue, compared to mock inoculated, were primarily overrepresented in the cellular component category for nuclear (19.92 %) and other cellular components (14 %), while categories corresponding to transferase activity (14.42 %) and other binding (13.43 %) were overrepresented for Molecular Function. Cellular processes (24.93 %) and other metabolic processes (18.05 %) were overrepresented for Biological Process. Notably from our data, we were able to detect transcript changes in several defence-related and sucrose/starch metabolic pathways. Collectively, alterations in genes associated with the cytoskeleton, cell wall and plasmodesmata, namely myosin heavy chain, beta-tubulin, Ras-GTPase (Rab6A), ß-1,3-glucanase, pectinesterase and pectate lyase, suggest possible roles in intracellular vesicle-assisted movement to the plasmamembrane and release into the adjacent cell via the plasmodesmata (Pd).


Microarray Geminivirus Gene expression Host-pathogen interaction 

Supplementary material

10658_2013_286_MOESM1_ESM.xlsx (100 kb)
Online Resource 1 (XLSX 100 kb)
10658_2013_286_MOESM2_ESM.xlsx (92 kb)
Online Resource 2 (XLSX 91.7 kb)
10658_2013_286_MOESM3_ESM.xlsx (67 kb)
Online Resource 3 (XLSX 67.2 kb)
10658_2013_286_MOESM4_ESM.xlsx (17 kb)
Online Resource 4 (XLSX 17.2 kb)
10658_2013_286_MOESM5_ESM.xlsx (62 kb)
Online Resource 5 (XLSX 61.9 kb)
10658_2013_286_MOESM6_ESM.xlsx (70 kb)
Online Resource 6 (XLSX 69.7 kb)


  1. Agudelo-Romero, P., Carbonell, P., Pérez-Amador, M. A., & Elena, S. F. (2008). Virus adaptation by manipulation of host’s gene expression. PLoS ONE, 3, e2397.PubMedGoogle Scholar
  2. Alba, R., Fei, Z., Payton, P., Liu, Y., Moore, S. L., Debbie, P., Cohn, J., D’Ascenzo, M., Gordon, J. S., Rose, J. K., et al. (2004). ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant Journal, 39, 697–714.PubMedGoogle Scholar
  3. Amin, I., Patil, B. L., Briddon, R. W., Mansoor, S., & Fauquet, C. M. (2011). Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virology Journal, 8, 238.PubMedGoogle Scholar
  4. Anaya-Lopez, J. L., Pérez-Mora, E., Torres-Pacheco, I., Muñoz-Sanchez, C. I., Guevara-Olvera, L., Gonzalez-Chavira, M. M., Ochoa-Alejo, N., Rivera-Bustamante, R. F., & Guevara-Gonzalez, R. G. (2005). Inducible gene expression by Pepper huasteco virus in Capsicum chinense plants with resistance to geminivirus infections. Canadian Journal of Plant Pathology, 27, 276–282.Google Scholar
  5. Aoki, K., Kragler, F., Xoconostle-Cazares, B., & Lucas, W. J. (2002). A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata. Proceedings of the National Academy of Sciences of the United States of America, 99, 16342–16347.PubMedGoogle Scholar
  6. Aparicio, F., Thomasm, C. L., Lederer, C., Niu, Y., Wang, D., & Maule, A. J. (2005). Virus induction of heat shock protein 70 reflects a general response to protein accumulation in the plant cytosol. Plant Physiology, 138, 529–536.PubMedGoogle Scholar
  7. Aranda, M., & Maule, A. (1998). Virus-induced host gene shutoff in animals and plants. Virology, 243, 261–267.PubMedGoogle Scholar
  8. Ascencio-Ibáñez, J. T., Sozzani, R., Lee, T., Chu, T., Wolfinger, R. D., Cella, R., & Hanley-Bowdoin, L. (2008). Global analysis of arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiology, 148, 436–454.PubMedGoogle Scholar
  9. Babu, M., Griffiths, J. S., Huang, T. S., & Wang, A. (2008). Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to Plum pox virus infection. BMC Genomics, 9, 325.PubMedGoogle Scholar
  10. Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Rudnev, D., Evangelista, C., Kim, I. F., Soboleva, A., Tomashevsky, M., & Edgar, R. (2007). NCBI GEO: mining tens of millions of expression profiles–database and tools update. Nucleic Acids Research, 35, D760–D765.PubMedGoogle Scholar
  11. Bazzini, A. A., Manacorda, C. A., Tohge, T., Conti, G., Rodriquez, M. C., Nunes-Nesi, A., Villanueva, S., Fernie, A. R., Carrari, F., & Asurmendi, S. (2011). Metabolic and miRNA profiling of TMV infected plants reveals biphasic temporal changes. PLoS ONE, 6(12), e28466.PubMedGoogle Scholar
  12. Berrie, L. C., Rybicki, E. P., & Rey, M. E. C. (2001). Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. Journal of General Virology, 82, 53–58.PubMedGoogle Scholar
  13. Bisaro, D. M. (2006). Silencing suppression by geminivirus proteins. Virology, 344, 158–168.PubMedGoogle Scholar
  14. Bolouri Moghaddam, M.R., & Van den Ende, W. (2012). Sugars and plant innate immunity. Journal of Experimental Botany, 63, 3989–3998.Google Scholar
  15. Bombarely, A., Rosli, H. G., Vrebalov, J., Moffett, P., Mueller, L., & Martin, G. (2012). A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Molecular Plant-Microbe Interactions, 25(12), 1523–1530.PubMedGoogle Scholar
  16. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55(4), 611–622.PubMedGoogle Scholar
  17. Carvalho, C. M., Fontenelle, M. R., Florentino, L. H., Santos, A. A., Zerbini, F. M., & Fontes, E. P. (2008a). A novel nucleocytoplasmic traffic GTPase identified as a functional target of the bipartite geminivirus nuclear shuttle protein. Plant Journal, 55, 869–880.PubMedGoogle Scholar
  18. Carvalho, C. M., Machado, J. P., Zerbini, F. M., & Fontes, E. P. (2008b). NSP-interacting GTPase: a cytosolic protein as cofactor for nuclear shuttle proteins. Plant Signalling and Behaviour, 3, 752–754.Google Scholar
  19. Castillo, A. G., Kong, L. J., Hanley-Bowdoin, L., & Bejarano, E. R. (2004). Interaction between a geminivirus replication protein and the plant sumoylation system. Journal of Virology, 78, 2758–2769.PubMedGoogle Scholar
  20. Catoni, M., Miozzi, L., Fiorilli, V., Lanfranco, L., & Accotto, G. P. (2009). Comparative analysis of expression profiles in shoots and roots of tomato systemically infected by Tomato spotted wilt virus reveals organ-specific transcriptional responses. Molecular Plant-Microbe Interactions, 22, 1504–1513.PubMedGoogle Scholar
  21. Chan, A. P., Crabtree, J., Zhao, Q., et al. (2010). Draft genome sequence of the oilseed species Ricinus communis. Nature Biotechnology, 28(9), 951–956.PubMedGoogle Scholar
  22. Chen, M. H., & Citovsky, V. (2003). Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant Journal, 35, 386–392.PubMedGoogle Scholar
  23. Chen, M. H., Sheng, J., Hind, G., Handa, A., & Citovsky, V. (2000). Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO Journal, 19, 913–920.PubMedGoogle Scholar
  24. Culver, J. N., & Padmanabhan, M. S. (2007). Virus-induced disease: altering host physiology one interaction at a time. Annual Reviews in Phytopathology, 45, 221–243.Google Scholar
  25. Dardick, C. (2007). Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses. Molecular Plant-Microbe Interactions, 20(8), 1004–1017.PubMedGoogle Scholar
  26. De Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., et al. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions, 18(9), 923–937.PubMedGoogle Scholar
  27. Dorokhov, Y. L., Makinen, K., Frolova, O. Y., Merits, A., Saarinen, J., Kalkkinen, N., Atabekov, J. G., & Saarma, M. (1999). A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Letters, 461, 223–228.PubMedGoogle Scholar
  28. Dowd, C., Wilson, I. W., & McFadden, H. (2004). Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Molecular Plant-Microbe Interactions, 17, 654–667.PubMedGoogle Scholar
  29. Doyle, J. J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11–15.Google Scholar
  30. Edgar, R., Domrachev, M., & Lash, A. E. (2002). Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Research, 30(1), 207–210.PubMedGoogle Scholar
  31. Elena, S. F., & Rodrigo, G. (2012). Towards an integrated molecular model of plant-virus interactions. Current Opinion in Virology, 2, 719–724.PubMedGoogle Scholar
  32. Elena, S. F., Carrera, J., & Rodrigo, G. (2011). A systems biology approach to the evolution of plant virus interactions. Current Opinion in Plant Biology, 14, 372–377.PubMedGoogle Scholar
  33. Epel, B. L. (2009). Plant viruses spread by diffusion on ER-associated movement-protein-rafts through plasmodesmata gated by viral induced host β-1,3-glucanases. Seminars in Cell & Developmental Biology, 20, 1074–1081.Google Scholar
  34. Eybishtz, A., Peretz, Y., Sade, D., Akad, F., & Czosnek, H. (2009). Silencing of a single gene in tomato plants resistant to Tomato yellow leaf curl virus renders them susceptible to the virus. Plant Molecular Biology, 71, 157–171.Google Scholar
  35. Fauquet, C. M. & Fargette, D. (1988). Proceedings of the International Seminar: African Cassava Mosaic Disease and its Control. Ede, Netherlands: CTA/ORSTOM.Google Scholar
  36. Fernandez Calvino, L., Faulkner, C., & Maule, A. (2011). Plasmodesmata as active conduits for virus cell-to-cell movement. In C. Caranta, M.-A. Aranda, M. Tepfer, & J.-J. Lopez Moya (Eds.), Recent advances in plant virology (pp. 47–74). Norkfolk: Caister Academic Press.Google Scholar
  37. Feulner, G. E. (2008). The Modulation of Nicotiana benthamiana gene expression by red clover necrotic mosaic virus. Master’s thesis, North Carolina State University. (as of 11/19/09).
  38. Fregene, M., Matsumura, H., Akano, A., Dixon, A., & Terauchi, R. (2004). Serial analysis of gene expression (SAGE) of host-plant resistance to the cassava mosaic disease. Plant Molecular Biology, 56, 563–571.PubMedGoogle Scholar
  39. García-Marcos, A., Pacheco, R., Martiáñez, J., González-Jara, P., Díaz-Ruíz, J. R., & Tenllado, F. (2009). Transcriptional changes and oxidative stress associated with the synergistic interaction between Potato virus X and Potato virus Y and their relationship with symptom expression. Molecular Plant-Microbe Interactions, 22, 1431–1444.PubMedGoogle Scholar
  40. Gilbertson, R. L., & Lucas, W. J. (1996). How do viruses traffic on the ‘vascular highway’? Trends in Plant Science, 1, 260–268.Google Scholar
  41. Golem, S., & Culver, J. N. (2003). Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 16, 681–688.PubMedGoogle Scholar
  42. Góngora-Castillo, E., Ibarra-Laclett, E., Diana, L., Trejo-Saavedra, D. L., & Rivera-Bustamante, R. F. (2012). Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virology Journal, 9, 295.PubMedGoogle Scholar
  43. Goodin, M. M., Zaitlin, Naidu, R. A., & Lommel, S. A. (2008). Nicotiana benthamiana: it’s history and future as a model for plant-pathogen interactions. Molecular Plant-Microbe Interactions, 21(8), 1015–1026.PubMedGoogle Scholar
  44. Grattapaglia, D., Silva-Junior, O. B., Kirst, M., de Lima, B. M., Faria, D. A., & Pappas, G. J. (2011). High-throughput SNP genotyping in the highly heterozygous genome of Eucalyptus: assay success, polymorphism and transferability across species. BMC Plant Biology, 11, 65.PubMedGoogle Scholar
  45. Gutierrez, C. (2002). Strategies of geminivirus DNA replication and cell cycle inerferance. Physiology and Molecular Biology of Plants, 60, 219–230.Google Scholar
  46. Gutierrez, C., Ramirez, P. E., Castellano, M. M., Sanz-Bugos, A. P., Luque, A., & Missich, R. (2004). Geminivirus DNA replication and cell cycle interactions. Veterinary Microbiology, 98, 111–119.PubMedGoogle Scholar
  47. Hanssen, I. M., Peter van Esse, H., Ballester, A. R., Hogewoning, S. W., Parra, N. O., et al. (2011). Differential tomato transcriptomic responses induced by Pepino mosaic virus isolates with differential aggressiveness. Plant Physiology, 156, 301–318.PubMedGoogle Scholar
  48. Harries, P. A., Park, J. W., Sasaki, N., Ballard, K. D., Maule, A. J., & Nelson, R. S. (2009). Differing requirements for actin and myosin by plant viruses for sustained intercellular movement. Proceedings of the National Academy of Sciences of the United States of America, 106, 17594–17599.PubMedGoogle Scholar
  49. Harries, P. A., Schoelz, J. E., & Nelson, R. S. (2010). Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Molecular Plant-Microbe Interactions, 2, 1381–1393.Google Scholar
  50. Heinlein, M. (2002). The spread of Tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cellular and Molecular Life Sciences, 59, 58–82.PubMedGoogle Scholar
  51. Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009a). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1), 44–57.Google Scholar
  52. Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009b). Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1), 1–13.Google Scholar
  53. Hückelhoven, R. (2007). Cell wall-associated mechanisms of disease resistance and susceptibility. Annual Reviews in Phytopathology, 45S, 101–127.Google Scholar
  54. Iglesias, V. A., & Meins, F. (2000). Movement of plant viruses is delayed in a β-1,3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant Journal, 21, 157–166.PubMedGoogle Scholar
  55. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., et al. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4(2), 249–264.PubMedGoogle Scholar
  56. Itaya, A., Matsuda, Y., Gonzales, R. A., Nelson, R. S., & Ding, B. (2002). Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Molecular Plant-Microbe Interactions, 15, 990–999.PubMedGoogle Scholar
  57. Jaillon, O., Aury, J. M., Noel, B., et al. (2007). The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature, 449(7161), 463–467.PubMedGoogle Scholar
  58. Jeske, H. (2009). Geminiviruses. In H. zur Hausen & E. M. de Villiers (Eds.), Torque Teno virus: The still elusive human pathogens (pp. 185–226). Berlin: Springer.Google Scholar
  59. Jia, M. A., Li, Y., Lei, L., Di, D., Miao, H., & Fan, Z. (2012). Alteration of gene expression profile in maize infected with a double-stranded RNA fijivirus associated with symptom development. Molecular Plant Pathology, 13, 251–262.PubMedGoogle Scholar
  60. Krenz, B., Windeisen, V., Wege, C., Jeske, H., & Kleinow, T. (2010). A plastid-targeted heat shock cognate 70 kDa protein interacts with the Abutilon mosaic virus movement protein. Virology, 401, 6–17.PubMedGoogle Scholar
  61. Lazarowitz, S. G., & Beachy, R. N. (1999). Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell, 11, 535–548.PubMedGoogle Scholar
  62. Lee, Y. R., & Liu, B. (2004). Cytoskeletal motors in Arabidopsis: sixty-one kinesins and seventeen myosins. Plant Physiology, 136, 877–3883.Google Scholar
  63. Levy, A., Guenoune-Gelbart, D., & Epel, B. L. (2007). β-1,3-Glucanases: plasmodesmal gate keepers for intercellular communication. Plant Signalling and Behavior, 2, 404–407.Google Scholar
  64. Lewis, J. D., & Lazarowitz, S. G. (2010). Arabidopsis synaptotagmin AtSYTA regulates early endosome formation and virus movement protein cell-to-cell transport. Proceedings of the National Academy of Sciences of the United States of America, 107, 2491–2496.PubMedGoogle Scholar
  65. Li, Y. Q., Mareck, A., Faleri, C., Moscatelli, A., Liu, Q. A., & Cresti, M. (2002). Detection and localization of pectin methylesterase isoforms in pollen tubes of Nicotiana tabacum L. Planta, 214, 734–740.PubMedGoogle Scholar
  66. Liu, J. Z., Blancaflor, E. B., & Nelson, R. S. (2005). The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiology, 138, 1853–1865.PubMedGoogle Scholar
  67. Love, A. J., Yun, B. W., Laval, V., Loake, G. J., & Milner, J. J. (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.PubMedGoogle Scholar
  68. Lucas, W. J. (2006). Plant viral movement proteins, agents for cell-to-cell trafficking of viral genomes. Virology, 344, 169–184.PubMedGoogle Scholar
  69. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H., & Dinesh-Kumar, S. P. (2004). Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Molecular Biology, 55, 501–520.PubMedGoogle Scholar
  70. Maule, A. J. (1991). Virus movement in infected plants. Critical Reviews in Plant Sciences, 9, 457–473.Google Scholar
  71. McGarry, R. C., Barron, Y. D., Carvalho, M. F., Hill, J. E., Gold, D., et al. (2003). A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell, 15, 1605–1618.PubMedGoogle Scholar
  72. Melcher, U. (2000). The ‘30K’ superfamily of viral movement proteins. Journal of General Virology, 81, 257–266.PubMedGoogle Scholar
  73. Min, B. E., Martin, K., Wang, R., Tafelmeyer, P., Bridges, M., & Goodin, M. (2010). A host-factor interaction and localization map for a plant-adapted rhabdovirus implicates cytoplasm-tethered transcription activators in cell-to-cell movement. Molecular Plant Microbe Interactions, 23, 1420–1432.PubMedGoogle Scholar
  74. Moreno, I., Gruissem, W., & Vanderschuren, H. (2011). Reference genes for reliable potyvirus quantitation in cassava and analysis of Cassava brown streak virus load in host varieties. Journal of Virological Methods, 177, 49–54.PubMedGoogle Scholar
  75. Nairn, C. J., Lewandowski, D. J., & Burns, J. K. (1998). Genetics and expression of two pectinesterase genes in Valencia orange. Plant Physiology, 102, 226–235.Google Scholar
  76. Okinaka, Y., Yang, C. H., Perna, N. T., & Keen, N. T. (2002). Microarray profiling of Erwinia chrysanthemi 3937 genes that are regulated during plant infection. Molecular Plant-Microbe Interactions, 15, 619–629.PubMedGoogle Scholar
  77. Oparka, K. J. (2004). Getting the message across: how do plant cells exchange macromolecular complexes? Trends in Plant Sciences, 9, 33–41.Google Scholar
  78. Pallas, V., & Garcia, J. A. (2011). How do plant viruses induce disease? Interactions and interference with host components. Journal of General Virology, 92, 2691–2705.PubMedGoogle Scholar
  79. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-timeRT-PCR. Nucleic Acid Research, 29(9), e45.Google Scholar
  80. Pierce, E. J., & Rey, M. E. C. (2013). Assessing global transcriptome changes in response to South African cassava mosaic virus [ZA-99] infection in susceptible Arabidopsis thaliana. PLoS ONE, 8(6), e67534.PubMedGoogle Scholar
  81. Pompe-Novak, M., Gruden, K., Baebler, S., Krecic-Stres, H., Kovac, M., Jongsma, M., & Ravnikar, M. (2006). Potato virus Y induced changes in the gene expression of potato (Solanum tuberosum L.). Physiological and Molecular Plant Pathology, 67, 237–247.Google Scholar
  82. Postnikova, O., & Nemchinov, L. (2012). Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses. Virology Journal, 9, 101.PubMedGoogle Scholar
  83. Prochnik, S., Marri, P. R., Desany, B., Rabinowicz, P. D., Kodira, C., Mohiuddin, M., Rodriguez, F., Fauquet, C., Tohme, J., Harkins, T., Rokhsar, D. S., & Rounsley, S. (2012). The cassava genome: current progress, future directions. Tropical Plant Biology, 5(1), 88–94.PubMedGoogle Scholar
  84. Prokhnevsky, A. I., Peremyslov, V. V., Napuli, A. J., & Dolja, V. V. (2002). Interaction between long-distance transport factor and Hsp70-related movement protein of Beet yellows virus. Journal of Virology, 76, 11003–11011.PubMedGoogle Scholar
  85. Raja, P., Sanville, B. C., Buchmann, R. C., & Bisaro, D. M. (2008). Viral genome methylation as an epigenetic defense against geminiviruses. Journal of Virology, 82, 8997–9007.PubMedGoogle Scholar
  86. Rensink, W. A., & Buell, C. (2005). Microarray expression profiling for plant genomes. Trends in Plant Sciences, 10(12), 603–609.Google Scholar
  87. Rojas, M. R., Noueiry, A. O., Lucas, W. J., & Gilbertson, R. L. (1998). Bean dwarf mosaic geminivirus movement proteins recognize DNA in a form- and size-specific manner. Cell, 95, 105–113.PubMedGoogle Scholar
  88. Rom, M. Y., Antignus, Y., Gidoni, D., Pilowskyand, M., & Cohen, S. (1993). Accumulation of Tomato yellow leaf curl virus DNA in tolerant and susceptible tomato lines. Plant Disease, 77, 253–257.Google Scholar
  89. Sánchez-Durán, M. A., Dallas, M. B., Ascencio-Ibañez, J. T., Reyes, M. I., Arroyo-Mateos, M., Ruiz-Albert, J., Hanley-Bowdoin, L., Bejarano, E. R., et al. (2011). Interaction between geminivirus replication protein and the SUMO-conjugating enzyme is required for viral infection. Journal of Virology, 85, 9789–9800.PubMedGoogle Scholar
  90. Senthil, G., Liu, H., Puram, V. G., Clark, A., Stromberg, A., & Goodin, M. M. (2005). Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped viruses. Journal of General Virology, 86, 2615–2625.PubMedGoogle Scholar
  91. Seo, Y. S., Jeon, J. S., Rojas, M. R., & Gilbertson, R. L. (2007). Characterization of a novel Toll/interleukin-1 receptor (TIT)-TIR gene differentially expressed in common bean (Phaseolus vulgaris cv. Othello) undergoing a defence response to the geminivirus Bean dwarf mosaic virus. Molecular Plant Pathology, 8, 151–162.PubMedGoogle Scholar
  92. Shalitin, D., & Wolf, S. (2000). Cucumber mosaic virus infection affects sugar transport in melon plants. Plant Physiology, 123, 597–604.PubMedGoogle Scholar
  93. Shen, W., & Hanley-Bowdoin, L. (2006). Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1 and mammalian AMPK activating kinases. Plant Physiology, 142, 1642–1655.PubMedGoogle Scholar
  94. Smith, B. H. (1999). Sucrose synthase and the fruit of its labor. Plant Cell, 11, 2261–2262.PubMedGoogle Scholar
  95. Takai, Y., Sasaki, T., & Matozaki, T. (2001). Small GTP-binding proteins. Physiological Reviews, 81, 153–208.PubMedGoogle Scholar
  96. Taliansky, M., Torrance, L., & Kalinina, N. O. (2008). Role of plant virus movement proteins. Methods in Molecular Biology, 451, 33–54.PubMedGoogle Scholar
  97. Tecsi, L. I., Maule, A. J., Smith, A. M., & Leegood, R. C. (1996). A spatial analysis of physiological changes associated with infection of cotyledons of marrow plants with cucumber mosaic virus. Plant Physiology, 111, 975–985.PubMedGoogle Scholar
  98. The Tomato Genome Consortium. (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature, 485(7400), 635–641.Google Scholar
  99. Trinks, D., Rajeswaran, R., Shivaprasad, P. V., Akbergenov, R., Oakeley, E. J., Veluthambi, K., Hohn, T., Pooggin, M. M., et al. (2005). Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. Journal of Virology, 79(4), 2517–2527.PubMedGoogle Scholar
  100. Ventelon-Debout, M., Delalande, F., Brizard, J. P., Diemer, H., Van Dorsselaer, A., & Brugidou, C. (2004). Proteome analysis of cultivar-specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing rice yellow mottle virus infection. Proteomics, 4, 216–225.PubMedGoogle Scholar
  101. Verchot, J. (2012). Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Frontiers in Plant Science, 3, 275.PubMedGoogle Scholar
  102. Wan, J. G., Dunning, F. M., & Bent, A. F. (2002). Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays. Functional & Integrative Genomics, 2, 259–273.Google Scholar
  103. Whitham, S. A., Quan, S., Chang, H.-R., Cooper, B., Estes, B., Zhu, T., Wang, X., & Hou, Y.-M. (2003). Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant Journal, 33, 271–283.PubMedGoogle Scholar
  104. Whitman, S. A., Yang, C., & Goodin, M. M. (2006). Global impact: elucidating plant responses to viral infection. Molecular Plant-Microbe Interactions, 19(11), 1207–1215.Google Scholar
  105. Woollard, A. A. D., & Moore, I. (2008). The functions of Rab GTPases in plant membrane traffic. Current Opinion in Plant Biology, 11, 610–619.PubMedGoogle Scholar
  106. Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P., Zhang, G., Yang, S., et al. (2011). Genome sequence and analysis of the tuber crop potato. Nature, 475(7355), 189–195.PubMedGoogle Scholar
  107. Yang, C., Guo, R., Jie, F., Nettleton, D., Peng, J., Carr, T., Yeakley, J. M., Fan, J. B., & Whitham, S. A. (2007). Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Molecular Plant-Microbe Interactions, 20(4), 359–370.Google Scholar
  108. Zhou, Y., Rojas, M. R., Park, M. R., Seo, Y. S., Lucas, W. J., & Gilbertson, R. L. (2011). Histone H3 interacts and colocalizes with the nuclear shuttle protein and the movement protein of a geminivirus. 85(22), 11821–32.Google Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  1. 1.School of Molecular and Cell BiologyUniversity of the WitwatersrandJohannesburgSouth Africa

Personalised recommendations