15 research outputs found
Virus Adaptation by Manipulation of Host's Gene Expression
Viruses adapt to their hosts by evading defense mechanisms and taking over cellular metabolism for their own benefit. Alterations in cell metabolism as well as side-effects of antiviral responses contribute to symptoms development and virulence. Sometimes, a virus may spill over from its usual host species into a novel one, where usually will fail to successfully infect and further transmit to new host. However, in some cases, the virus transmits and persists after fixing beneficial mutations that allow for a better exploitation of the new host. This situation would represent a case for a new emerging virus. Here we report results from an evolution experiment in which a plant virus was allowed to infect and evolve on a naïve host. After 17 serial passages, the viral genome has accumulated only five changes, three of which were non-synonymous. An amino acid substitution in the viral VPg protein was responsible for the appearance of symptoms, whereas one substitution in the viral P3 protein the epistatically contributed to exacerbate severity. DNA microarray analyses show that the evolved and ancestral viruses affect the global patterns of host gene expression in radically different ways. A major difference is that genes involved in stress and pathogen response are not activated upon infection with the evolved virus, suggesting that selection has favored viral strategies to escape from host defenses
A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens
Understanding the mechanisms by which plants trigger host defenses in response to viruses has been a challenging problem owing to the multiplicity of factors and complexity of interactions involved. The advent of genomic techniques, however, has opened the possibility to grasp a global picture of the interaction. Here, we used Arabidopsis thaliana to identify and compare genes that are differentially regulated upon infection with seven distinct (+)ssRNA and one ssDNA plant viruses. In the first approach, we established lists of genes differentially affected by each virus and compared their involvement in biological functions and metabolic processes. We found that phylogenetically related viruses significantly alter the expression of similar genes and that viruses naturally infecting Brassicaceae display a greater overlap in the plant response. In the second approach, virus-regulated genes were contextualized using models of transcriptional and protein-protein interaction networks of A. thaliana. Our results confirm that host cells undergo significant reprogramming of their transcriptome during infection, which is possibly a central requirement for the mounting of host defenses. We uncovered a general mode of action in which perturbations preferentially affect genes that are highly connected, central and organized in modules. © 2012 Rodrigo et al.This work was supported by the Spanish Ministerio de Ciencia e Innovacion (MICINN) grants BFU2009-06993 (S. F. E.) and BIO2006-13107 (C. L.) and by Generalitat Valenciana grant PROMETEO2010/016 (S. F. E.). G. R. is supported by a graduate fellowship from the Generalitat Valenciana (BFPI2007-160) and J.C. by a contract from MICINN grant TIN2006-12860. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Rodrigo Tarrega, G.; Carrera Montesinos, J.; Ruiz-Ferrer, V.; Del Toro, F.; Llave, C.; Voinnet, O.; Elena Fito, SF. (2012). A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens. PLoS ONE. 7(7):40526-40526. https://doi.org/10.1371/journal.pone.0040526S405264052677Peng, X., Chan, E. Y., Li, Y., Diamond, D. L., Korth, M. J., & Katze, M. G. (2009). Virus–host interactions: from systems biology to translational research. Current Opinion in Microbiology, 12(4), 432-438. doi:10.1016/j.mib.2009.06.003Dodds, P. N., & Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant–pathogen interactions. Nature Reviews Genetics, 11(8), 539-548. doi:10.1038/nrg2812Maule, A., Leh, V., & Lederer, C. (2002). The dialogue between viruses and hosts in compatible interactions. Current Opinion in Plant Biology, 5(4), 279-284. doi:10.1016/s1369-5266(02)00272-8Whitham, S. A., Quan, S., Chang, H.-S., Cooper, B., Estes, B., Zhu, T., … Hou, Y.-M. (2003). Diverse RNA viruses elicit the expression of common sets of genes in susceptibleArabidopsis thalianaplants. The Plant Journal, 33(2), 271-283. doi:10.1046/j.1365-313x.2003.01625.xBailer, S., & Haas, J. (2009). Connecting viral with cellular interactomes. Current Opinion in Microbiology, 12(4), 453-459. doi:10.1016/j.mib.2009.06.004Whitham, S. A., Yang, C., & Goodin, M. M. (2006). Global Impact: Elucidating Plant Responses to Viral Infection. Molecular Plant-Microbe Interactions, 19(11), 1207-1215. doi:10.1094/mpmi-19-1207MacPherson, J. I., Dickerson, J. E., Pinney, J. W., & Robertson, D. L. (2010). Patterns of HIV-1 Protein Interaction Identify Perturbed Host-Cellular Subsystems. PLoS Computational Biology, 6(7), e1000863. doi:10.1371/journal.pcbi.1000863Jenner, R. G., & Young, R. A. (2005). Insights into host responses against pathogens from transcriptional profiling. Nature Reviews Microbiology, 3(4), 281-294. doi:10.1038/nrmicro1126Andeweg, A. C., Haagmans, B. L., & Osterhaus, A. D. (2008). Virogenomics: the virus–host interaction revisited. Current Opinion in Microbiology, 11(5), 461-466. doi:10.1016/j.mib.2008.09.010Elena, S. F., Carrera, J., & Rodrigo, G. (2011). A systems biology approach to the evolution of plant–virus interactions. Current Opinion in Plant Biology, 14(4), 372-377. doi:10.1016/j.pbi.2011.03.013Tan, S.-L., Ganji, G., Paeper, B., Proll, S., & Katze, M. G. (2007). Systems biology and the host response to viral infection. Nature Biotechnology, 25(12), 1383-1389. doi:10.1038/nbt1207-1383De la Fuente, A. (2010). From ‘differential expression’ to ‘differential networking’ – identification of dysfunctional regulatory networks in diseases. Trends in Genetics, 26(7), 326-333. doi:10.1016/j.tig.2010.05.001Albert, R. (2005). Scale-free networks in cell biology. Journal of Cell Science, 118(21), 4947-4957. doi:10.1242/jcs.02714Yu, H., Braun, P., Yildirim, M. A., Lemmens, I., Venkatesan, K., Sahalie, J., … Vidal, M. (2008). High-Quality Binary Protein Interaction Map of the Yeast Interactome Network. Science, 322(5898), 104-110. doi:10.1126/science.1158684Barabási, A.-L., & Oltvai, Z. N. (2004). Network biology: understanding the cell’s functional organization. Nature Reviews Genetics, 5(2), 101-113. doi:10.1038/nrg1272Albert, R., Jeong, H., & Barabási, A.-L. (2000). Error and attack tolerance of complex networks. Nature, 406(6794), 378-382. doi:10.1038/35019019Mukhtar, M. S., Carvunis, A.-R., Dreze, M., Epple, P., Steinbrenner, J., … Moore, J. (2011). Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network. Science, 333(6042), 596-601. doi:10.1126/science.1203659Calderwood, M. A., Venkatesan, K., Xing, L., Chase, M. R., Vazquez, A., Holthaus, A. M., … Johannsen, E. (2007). Epstein-Barr virus and virus human protein interaction maps. Proceedings of the National Academy of Sciences, 104(18), 7606-7611. doi:10.1073/pnas.0702332104De Chassey, B., Navratil, V., Tafforeau, L., Hiet, M. S., Aublin‐Gex, A., Agaugué, S., … Lotteau, V. (2008). Hepatitis C virus infection protein network. Molecular Systems Biology, 4(1), 230. doi:10.1038/msb.2008.66Shapira, S. D., Gat-Viks, I., Shum, B. O. V., Dricot, A., de Grace, M. M., Wu, L., … Hacohen, N. (2009). A Physical and Regulatory Map of Host-Influenza Interactions Reveals Pathways in H1N1 Infection. Cell, 139(7), 1255-1267. doi:10.1016/j.cell.2009.12.018Dyer, M. D., Murali, T. M., & Sobral, B. W. (2008). The Landscape of Human Proteins Interacting with Viruses and Other Pathogens. PLoS Pathogens, 4(2), e32. doi:10.1371/journal.ppat.0040032Golem, S., & Culver, J. N. (2003). Tobacco mosaic virusInduced Alterations in the Gene Expression Profile ofArabidopsis thaliana. Molecular Plant-Microbe Interactions, 16(8), 681-688. doi:10.1094/mpmi.2003.16.8.681Espinoza, C., Medina, C., Somerville, S., & Arce-Johnson, P. (2007). Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. Journal of Experimental Botany, 58(12), 3197-3212. doi:10.1093/jxb/erm165Yang, C., Guo, R., Jie, F., Nettleton, D., Peng, J., Carr, T., … Whitham, S. A. (2007). Spatial Analysis ofArabidopsis thalianaGene Expression in Response toTurnip mosaic virusInfection. Molecular Plant-Microbe Interactions, 20(4), 358-370. doi:10.1094/mpmi-20-4-0358Agudelo-Romero, P., Carbonell, P., de la Iglesia, F., Carrera, J., Rodrigo, G., Jaramillo, A., … Elena, S. F. (2008). Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virology Journal, 5(1), 92. doi:10.1186/1743-422x-5-92Agudelo-Romero, P., Carbonell, P., Perez-Amador, M. A., & Elena, S. F. (2008). Virus Adaptation by Manipulation of Host’s Gene Expression. PLoS ONE, 3(6), e2397. doi:10.1371/journal.pone.0002397Ascencio-Ibáñez, J. T., Sozzani, R., Lee, T.-J., Chu, T.-M., 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(1), 436-454. doi:10.1104/pp.108.121038Babu, 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(1), 325. doi:10.1186/1471-2164-9-325De Vienne, D. M., Giraud, T., & Martin, O. C. (2007). A congruence index for testing topological similarity between trees. Bioinformatics, 23(23), 3119-3124. doi:10.1093/bioinformatics/btm500Wise, R. P., Moscou, M. J., Bogdanove, A. J., & Whitham, S. A. (2007). Transcript Profiling in Host–Pathogen Interactions. Annual Review of Phytopathology, 45(1), 329-369. doi:10.1146/annurev.phyto.45.011107.143944Handford, M. G., & Carr, J. P. (2007). A defect in carbohydrate metabolism ameliorates symptom severity in virus-infected Arabidopsis thaliana. Journal of General Virology, 88(1), 337-341. doi:10.1099/vir.0.82376-0Hou, B., Lim, E.-K., Higgins, G. S., & Bowles, D. J. (2004). N-Glucosylation of Cytokinins by Glycosyltransferases ofArabidopsis thaliana. Journal of Biological Chemistry, 279(46), 47822-47832. doi:10.1074/jbc.m409569200Schwender, J., Goffman, F., Ohlrogge, J. B., & Shachar-Hill, Y. (2004). Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature, 432(7018), 779-782. doi:10.1038/nature03145Pagán, I., Alonso-Blanco, C., & García-Arenal, F. (2008). Host Responses in Life-History Traits and Tolerance to Virus Infection in Arabidopsis thaliana. PLoS Pathogens, 4(8), e1000124. doi:10.1371/journal.ppat.1000124Carrera, J., Rodrigo, G., Jaramillo, A., & Elena, S. F. (2009). Reverse-engineering the Arabidopsis thaliana transcriptional network under changing environmental conditions. Genome Biology, 10(9), R96. doi:10.1186/gb-2009-10-9-r96Geisler-Lee, J., O’Toole, N., Ammar, R., Provart, N. J., Millar, A. H., & Geisler, M. (2007). A Predicted Interactome for Arabidopsis. Plant Physiology, 145(2), 317-329. doi:10.1104/pp.107.103465Ma, S., Gong, Q., & Bohnert, H. J. (2007). An Arabidopsis gene network based on the graphical Gaussian model. Genome Research, 17(11), 1614-1625. doi:10.1101/gr.6911207Yamada, T., & Bork, P. (2009). Evolution of biomolecular networks — lessons from metabolic and protein interactions. Nature Reviews Molecular Cell Biology, 10(11), 791-803. doi:10.1038/nrm2787Humphries, M. D., & Gurney, K. (2008). Network ‘Small-World-Ness’: A Quantitative Method for Determining Canonical Network Equivalence. PLoS ONE, 3(4), e0002051. doi:10.1371/journal.pone.0002051Stumpf, M. P. H., & Ingram, P. J. (2005). Probability models for degree distributions of protein interaction networks. Europhysics Letters (EPL), 71(1), 152-158. doi:10.1209/epl/i2004-10531-8Khanin, R., & Wit, E. (2006). How Scale-Free Are Biological Networks. Journal of Computational Biology, 13(3), 810-818. doi:10.1089/cmb.2006.13.810Daudin, J.-J., Picard, F., & Robin, S. (2007). A mixture model for random graphs. Statistics and Computing, 18(2), 173-183. doi:10.1007/s11222-007-9046-7Uetz, P. (2006). Herpesviral Protein Networks and Their Interaction with the Human Proteome. Science, 311(5758), 239-242. doi:10.1126/science.1116804Choi, I.-R., Stenger, D. C., & French, R. (2000). Multiple Interactions among Proteins Encoded by the Mite-Transmitted Wheat Streak Mosaic Tritimovirus. Virology, 267(2), 185-198. doi:10.1006/viro.1999.0117Guo, D., Saarma, M., Rajamäki, M.-L., & Valkonen, J. P. T. (2001). Towards a protein interaction map of potyviruses: protein interaction matrixes of two potyviruses based on the yeast two-hybrid system. Journal of General Virology, 82(4), 935-939. doi:10.1099/0022-1317-82-4-935Lin, L., Shi, Y., Luo, Z., Lu, Y., Zheng, H., Yan, F., … Wu, Y. (2009). Protein–protein interactions in two potyviruses using the yeast two-hybrid system. Virus Research, 142(1-2), 36-40. doi:10.1016/j.virusres.2009.01.006Shen, W., Wang, M., Yan, P., Gao, L., & Zhou, P. (2010). Protein interaction matrix of Papaya ringspot virus type P based on a yeast two-hybrid system. Acta Virologica, 54(1), 49-54. doi:10.4149/av_2010_01_49Redner, S. (2008). Teasing out the missing links. Nature, 453(7191), 47-48. doi:10.1038/453047aIrizarry, R. A. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4(2), 249-264. doi:10.1093/biostatistics/4.2.249Smyth, G. K. (2004). Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments. Statistical Applications in Genetics and Molecular Biology, 3(1), 1-25. doi:10.2202/1544-6115.1027Allemeersch, J., Durinck, S., Vanderhaeghen, R., Alard, P., Maes, R., Seeuws, K., … Kuiper, M. T. R. (2005). Benchmarking the CATMA Microarray. A Novel Tool forArabidopsis Transcriptome Analysis. Plant Physiology, 137(2), 588-601. doi:10.1104/pp.104.051300Cleveland, W. S. (1979). Robust Locally Weighted Regression and Smoothing Scatterplots. Journal of the American Statistical Association, 74(368), 829-836. doi:10.1080/01621459.1979.10481038Tarraga, J., Medina, I., Carbonell, J., Huerta-Cepas, J., Minguez, P., Alloza, E., … Dopazo, J. (2008). GEPAS, a web-based tool for microarray data analysis and interpretation. Nucleic Acids Research, 36(Web Server), W308-W314. doi:10.1093/nar/gkn303Al-Shahrour, F., Minguez, P., Vaquerizas, J. M., Conde, L., & Dopazo, J. (2005). BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Research, 33(Web Server), W460-W464. doi:10.1093/nar/gki456Al-Shahrour, F., Minguez, P., Tárraga, J., Medina, I., Alloza, E., Montaner, D., & Dopazo, J. (2007). FatiGO +: a functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments. Nucleic Acids Research, 35(suppl_2), W91-W96. doi:10.1093/nar/gkm260Mueller, L. A., Zhang, P., & Rhee, S. Y. (2003). AraCyc: A Biochemical Pathway Database for Arabidopsis. Plant Physiology, 132(2), 453-460. doi:10.1104/pp.102.017236Navratil, V., de Chassey, B., Combe, C., & Lotteau, V. (2011). When the human viral infectome and diseasome networks collide: towards a systems biology platform for the aetiology of human diseases. BMC Systems Biology, 5(1), 13. doi:10.1186/1752-0509-5-13Shannon, C. E. (1948). A Mathematical Theory of Communication. Bell System Technical Journal, 27(3), 379-423. doi:10.1002/j.1538-7305.1948.tb01338.
A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by Prunus necrotic ringspot virus and Peach latent mosaic viroid
[EN] Background: Microarray profiling is a powerful technique to investigate expression changes of large amounts of
genes in response to specific environmental conditions. The majority of the studies investigating gene expression
changes in virus-infected plants are limited to interactions between a virus and a model host plant, which usually is
Arabidopsis thaliana or Nicotiana benthamiana. In the present work, we performed microarray profiling to explore
changes in the expression profile of field-grown Prunus persica (peach) originating from Chile upon single and
double infection with Prunus necrotic ringspot virus (PNRSV) and Peach latent mosaic viroid (PLMVd), worldwide
natural pathogens of peach trees.
Results: Upon single PLMVd or PNRSV infection, the number of statistically significant gene expression changes
was relatively low. By contrast, doubly-infected fruits presented a high number of differentially regulated genes.
Among these, down-regulated genes were prevalent. Functional categorization of the gene expression changes
upon double PLMVd and PNRSV infection revealed protein modification and degradation as the functional category
with the highest percentage of repressed genes whereas induced genes encoded mainly proteins related to
phosphate, C-compound and carbohydrate metabolism and also protein modification. Overrepresentation analysis
upon double infection with PLMVd and PNRSV revealed specific functional categories over- and underrepresented
among the repressed genes indicating active counter-defense mechanisms of the pathogens during infection.
Conclusions: Our results identify a novel synergistic effect of PLMVd and PNRSV on the transcriptome of peach
fruits. We demonstrate that mixed infections, which occur frequently in field conditions, result in a more complex
transcriptional response than that observed in single infections. Thus, our data demonstrate for the first time that
the simultaneous infection of a viroid and a plant virus synergistically affect the host transcriptome in infected
peach fruits. These field studies can help to fully understand plant-pathogen interactions and to develop
appropriate crop protection strategies.We thank Drs M.A. Perez-Amador y J. Gadea for helping in the result analysis. This work was supported by grant BIO2011-25018 from the Spanish granting agency Direccion General de Investigacion Cientifica for the transcriptomic analyses and from the grant 2009CL0020 from the bilateral project INIA-Chile/CSIC-Spain for the phytosanitary evaluation. MC Herranz was the recipient of a contract from the Juan de la Cierva program of the Ministerio de Educacion y Ciencia of Spain.Herranz Gordo, MDC.; Niehl, A.; Rosales, M.; Fiore, N.; Zamorano, A.; Granell Richart, A.; Pallás Benet, V. (2013). A remarkable synergistic effect at the transcriptomic level in peach fruits doubly infected by Prunus necrotic ringspot virus and Peach latent mosaic viroid. Virology Journal. 10:11-15. https://doi.org/10.1186/1743-422X-10-164S111510Pallas V, Garcia JA: How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol 2011, 92: 2691-2705.Whitham SA, Yang C, Goodin MM: Global impact: elucidating plant responses to viral infection. Mol Plant Microbe Interact 2006, 19: 1207-1215.Havelda Z, Varallyay E, Valoczi A, Burgyan J: Plant virus infection-induced persistent host gene downregulation in systemically infected leaves. Plant J 2008, 55: 278-288.Aranda M, Maule A: Virus-induced host gene shutoff in animals and plants. Virology 1998, 243: 261-267.Whitham SA, Quan S, Chang HS, Cooper B, Estes B, Zhu T, Wang X, Hou YM: Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 2003, 33: 271-283.Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S: Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 2007, 51: 941-954.Hadidi A, Barba M: Economic impact of pome and stone fruit viruses and viroids. In Virus and Virus Like Diseases of Pome and Stone Fruits. Edited by: Hadidi A, Barba M, Candresse T, Jelkmann W. St Paul, MN: American Phytopathological Society; 2011:1-8.Flores R, Delgado S, Rodio ME, Ambros S, Hernandez C, Serio FD: Peach latent mosaic viroid: not so latent. Mol Plant Pathol 2006, 7: 209-221.Pallas V, Aparicio F, Herranz MC, Amari K, Sanchez-Pina MA, Myrta A, Sanchez-Navarro JA: Ilarviruses of Prunus spp.: A continued concern for fruit trees. Phytopathology 2012,102(12):1108-1120.Rowland O, Jones JD: Unraveling regulatory networks in plant defense using microarrays. Genome Biol 2001,2(1):1001.1-1001.3.Trinks D, Rajeswaran R, Shivaprasad PV, Akbergenov R, Oakeley EJ, Veluthambi K, Hohn T, Pooggin MM: Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 2005, 79: 2517-2527.Senthil G, Liu H, Puram VG, Clark A, Stromberg A, Goodin MM: Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped viruses. J Gen Virol 2005, 86: 2615-2625.Marathe R, Guan Z, Anandalakshmi R, Zhao H, Dinesh-Kumar SP: Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol 2004, 55: 501-520.Agudelo-Romero P, Carbonell P, de la Iglesia F, Carrera J, Rodrigo G, Jaramillo A, Perez-Amador MA, Elena SF: Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virol J 2008, 5: 92.Itaya A, Matsuda Y, Gonzales RA, Nelson RS, Ding B: Potato spindle tuber viroid strains of different pathogenicity induces and suppresses expression of common and unique genes in infected tomato. Mol Plant Microbe Interact 2002, 15: 990-999.Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA: Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 2005, 137: 1147-1159.Rizza S, Conesa A, Juarez J, Catara A, Navarro L, Duran-Vila N, Ancillo G: Microarray analysis of Etrog citron (Citrus medica L.) reveals changes in chloroplast, cell wall, peroxidase and symporter activities in response to viroid infection. Mol Plant Pathol 2012,13(8):852-864.Golem S, Culver JN: Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Mol Plant Microbe Interact 2003, 16: 681-688.Dardick C: Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses. Mol Plant Microbe Interact 2007, 20: 1004-1017.Hull R: In Matthews’ Plant Virology. London: Edited by Academic Press; 2002.Gonzalez-Jara P, Tenllado F, Martinez-Garcia B, Atencio FA, Barajas D, Vargas M, Diaz-Ruiz J, Diaz-Ruiz JR: Host-dependent differences during synergistic infection by Potyviruses with potato virus X. Mol Plant Pathol 2004, 5: 29-35.Gonzalez-Jara P, Atencio FA, Martinez-Garcia B, Barajas D, Tenllado F, Diaz-Ruiz JR: A Single Amino Acid Mutation in the Plum pox virus Helper Component-Proteinase Gene Abolishes Both Synergistic and RNA Silencing Suppression Activities. Phytopathology 2005, 95: 894-901.Vance VB: Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology 1991, 182: 486-494.Garcia-Marcos A, Pacheco R, Martianez J, Gonzalez-Jara P, Diaz-Ruiz JR, Tenllado F: Transcriptional changes and oxidative stress associated with the synergistic interaction between Potato virus X and Potato virus Y and their relationship with symptom expression. Mol Plant Microbe Interact 2009, 22: 1431-1444.Postnikova OA, Nemchinov LG: Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses. Virol J 2012, 9: 101.Zanchin A, Bonghi C, Casadoro G, Ramina A, Rascio N: Cell enlargement and cell separation during peach fruit development. International Journal of Plant Science 1994, 155: 49-56.Herranz MC, Sanchez-Navarro JA, Aparicio F, Pallas V: Simultaneous detection of six stone fruit viruses by non-isotopic molecular hybridization using a unique riboprobe or ‘polyprobe’. J Virol Methods 2005, 124: 49-55.Pallas V, Mas P, Sanchez-Navarro JA: Detection of plant RNA viruses by nonisotopic dot-blot hybridization. Methods Mol Biol 1998, 81: 461-468.Lilly ST, Drummond RS, Pearson MN, MacDiarmid RM: Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana. Mol Plant Microbe Interact 2011, 24: 294-304.Cosgrove JD: Expansive growth of plant cell walls. Plant Physiol Biochem 2000,38(1–2):109-124.Tessitori M, Maria G, Capasso C, Catara G, Rizza S, De Luca V, Catara A, Capasso A, Carginale V: Differential display analysis of gene expression in Etrog citron leaves infected by Citrus viroid III. Biochim Biophys Acta 2007, 1769: 228-235.Rizza S, Capasso C, Catara A, Capasso A, Conte E, Catara A Proceedings of the 17th Conference of the International Organization of Citrus Virologists-IOCV, pp. XVII. In Transcriptional response of Troyer citrange, sour orange and alemow rootstocks to Citrus viroid IIIb (CVd-IIIb) infection. Adana, Turkey: Conference of the International Organization of Citrus Virologists; 2010:142-149. http://www.ivia.es/iocv/Owens RA, Tech KB, Shao JY, Sano T, Baker CJ: Global analysis of tomato gene expression during Potato spindle tuber viroid infection reveals a complex array of changes affecting hormone signaling. Mol Plant Microbe Interact 2012, 25: 582-598.Ogundiwin EA, Marti C, Forment J, Pons C, Granell A, Gradziel TM, Peace CP, Crisosto CH: Development of ChillPeach genomic tools and identification of cold-responsive genes in peach fruit. Plant Mol Biol 2008, 68: 379-397.Sánchez-Navarro JA FA, Rowhani A, Pallás V: Comparative analysis of ELISA, nonradioactive molecular hybridization and PCR for the detection of Prunus necrotic ringspot virus in herbaceous and prunus host. Plant Pathol 1998, 47: 780-786.Astruc N, Marcos JF, Macquaire G, Candresse T, Pallas V: Studies on the diagnosis of hop stunt viroid in fruit trees: Identification of new hosts and application of a nucleic acid extraction procedure based on non-organic solvents. Eur J Plant Pathol 1996, 102: 837-846.Myrta A, Di Terlizzi B, Pallas V, Savino V: Viruses and viroids of apricot in the Mediterranean: incidence and biodiversity. Acta Horticulturae 2006, 701: 409-417.Bouzayen M, Latché A, Nath P, Pech JC: Mechanism of fruit ripening. In Plant Developmental Biology- Biotechnological Perspectives: Volume I Edited by: Pua EC, Darvey MR. 2010, 319-339. Chapter 16Trainotti L, Bonghi C, Ziliotto F, Zanin D, Rasori A, Casadoro G, Ramina A, T P: The use of microarray mPEACH 1.0 to investigate transcriptome changes during transition from pre-climateric to climacteric phase in peach fruit. Plant Sci 2006, 170: 606-613.Lombardo VA, Osorio S, Borsani J, Lauxmann MA, Bustamante CA, Budde CO, Andreo CS, Lara MV, Fernie AR MFD: Metabolic profiling during peach fruit development and ripening reveals the metabolic networks that underpin each developmental stage. Plant Physiol 2011,157(4):1696-1710.Manganaris GA RA, Bassi D, Geuna F, Ramina A, Tonutti P, Bonghi C: Comparative transcript profiling of apricot (Prunus armeniaca L.) fruit development and on-tree ripening. Tree Genet Genomes 2011, 7: 609-616.Uyemoto JK, Scott SW: Important diseases of Prunus caused by viruses and other graft-transmissible pathogens in California and South Carolina. Plant Dis 1992, 76: 5-11.Li J, Yang H, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, et al.: Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 2005, 310: 121-125.Paponov IA, Paponov M, Teale W, Menges M, Chakrabortee S, Murray JA, Palme K: Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 2008, 1: 321-337.Padmanabhan MS, Goregaoker SP, Golem S, Shiferaw H, Culver JN: Interaction of the tobacco mosaic virus replicase protein with the Aux/IAA protein PAP1/IAA26 is associated with disease development. J Virol 2005, 79: 2549-2558.Padmanabhan MS, Shiferaw H, Culver JN: The Tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol Plant Microbe Interact 2006, 19: 864-873.Padmanabhan MS, Kramer SR, Wang X, Culver JN: Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. J Virol 2008, 82: 2477-2485.Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI: The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol 2006, 140: 127-139.Whenham RJ, Fraser RSS, Brown LP, Payne JA: Tobacco-mosaic-virus-induced increase in abscisic-acid concentration in tobacco leaves: Intracellular location in light and dark-green areas, and relationship to symptom development. Planta 1986, 168: 592-598.Bari R, Jones JD: Role of plant hormones in plant defence responses. Plant Mol Biol 2009, 69: 473-488.Kotchoni SO, Kuhns C, Ditzer A, Kirch HH, Bartels D: Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 2006, 29: 1033-1048.Mowla SB, Cuypers A, Driscoll SP, Kiddle G, Thomson J, Foyer CH, Theodoulou FL: Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant (LEA)-like protein in oxidative stress tolerance. Plant J 2006, 48: 743-756.Amari K, Diaz-Vivancos P, Pallas V, Sanchez-Pina MA, Hernandez JA: Oxidative stress induction by Prunus necrotic ringspot virus infection in apricot seeds. Physiol Plant 2007, 131: 302-310.Gilroy EM, Hein I, van der Hoorn R, Boevink PC, Venter E, McLellan H, Kaffarnik F, Hrubikova K, Shaw J, Holeva M, et al.: Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 2007, 52: 1-13.Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD: A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 2002, 296: 744-747.Bernoux M, Timmers T, Jauneau A, Briere C, De Wit PJ, Marco Y, Deslandes L: RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 2008, 20: 2252-2264.Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RA: Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 2008, 20: 1169-1183.Van Esse HP, Van’t Klooster JW, Bolton MD, Yadeta KA, Van Baarlen P, Boeren S, Vervoort J, De Wit PJ, Thomma BP: The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 2008, 20: 1948-1963.Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RA, Kamoun S: Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci U S A 2009, 106: 1654-1659.Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S: A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 2007, 143: 364-377.Rooney H, Van’t Klooster J, Van der Hoorn R, Joosten M, Jones J: Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 2005, 308: 1783-1786.Auger AJ: Tomato ringspot virus associated with brownline disease on prune trees in Chile. Acta Horticulturae 1989, 235: 197-204.Herrera G: Enfermedades causadas por virus en frutales en Chile. Santiago, Chile: Instituto de Investigación Agropecuaria; 2001. Boletín INIA N°52. 65pFiore N, Abou Ghanem-Sabanadzovic N, Infante R, Myrta A, Pallás V: Detection of Peach latent mosaic viroid in stone fruits from Chile. In Option Méditerranéennes, Sér. B/n°45 –Virus ad virus-like disease of stone fruits, with particular reference to the Mediterranean region Edited by: Myrta A, Di Terlizzi B, Savino V. 2003, 143-145.Torres H, Gómez G, Pallás V, Stamo B, Shalaby A, Aouane B, Gavriel I, Kominek P, Caglayan K, Sipahioglu M, et al.: Detection by tissue printing of stone fruit viroids, from europe, the mediterranean and north and south America. Acta Horticulturae 2004, 657: 379-383.Peiró A, Pallás V, Sánchez-Navarro JA: Simultaneous detection of eight viruses and two viroids affecting stone fruit trees by using a unique polyprobe. Eur J Plant Pathol 2012,132(4):469-475.Meisel L, Fonseca B, Gonzalez S, Baeza-Yates R, Cambiazo V, Campos R, Gonzalez M, Orellana A, Retamales J, Silva H: A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 2005, 38: 83-88.Van Gelder RN, Von Zastrow ME, Yool A, Dement WC, Barchas JD JHE: Amplified RNA synthesized from limited quantities of heterogeneous cDNA. Proc Natl Acad Sci U S A 1990,87(5):1663-1667.Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98: 5116-5121.Sanchez-Navarro JA, Canizares MC, Cano EA, Pallas V: Simultaneous detection of five carnation viruses by non-isotopic molecular hybridization. J Virol Methods 1999, 82: 167-175