Transcriptional analysis of South African cassava mosaic virus-infected susceptible and tolerant landraces of cassava highlights differences in resistance, basal defense and cell wall associated genes during infection

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Allie, Farhahna ^a   Pierce, Erica J ^a   Okoniewski, Michal J ^b   Rey, Chrissie ^a  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^b ETH ZURICH   (Switzerland)

Author keywords

Cassava; Geminivirus; Next generation sequencing; South African cassava mosaic virus; Susceptibility; Tolerance; Transcriptome profiling

Indexed keywords

COMPLEMENTARY DNA; HISTONE; ORGANIC COMPOUND; PHENYLPROPANOID; PHYTOHORMONE; STARCH; SUCROSE; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG; VIRUS RNA; MESSENGER RNA; VEGETABLE PROTEIN;

ARTICLE; CASSAVA; CELL MEMBRANE; CELL NUCLEUS; CELL WALL; CONTROLLED STUDY; CULTIVAR; DNA LIBRARY; DNA METHYLATION; GENE EXPRESSION; HISTONE METHYLATION; IMMUNOLOGICAL TOLERANCE; INFECTION RESISTANCE; INFECTION SENSITIVITY; LANDRACE; METABOLISM; NEXT GENERATION SEQUENCING; NONHUMAN; PHENOTYPE; PLANT GENOME; PLANT VIRUS; RNA SEQUENCE; SIGNAL TRANSDUCTION; SOUTH AFRICAN CASSAVA MOSAIC VIRUS; VIRUS TRANSCRIPTION; ARABIDOPSIS; DISEASE RESISTANCE; DOWN REGULATION; GEMINIVIRIDAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; MANIHOT; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; SOUTH AFRICA; VIROLOGY;

ARABIDOPSIS; CELL WALL; DISEASE RESISTANCE; DOWN-REGULATION; GEMINIVIRIDAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; GENES, PLANT; MANIHOT; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE ANNOTATION; MOSAIC VIRUSES; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SOUTH AFRICA; TRANSCRIPTOME;

EID: 84965186450     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1006     Document Type: Article

References (158)

1. FAO: Cassava for Food and Energy Security. Rome: FAO Media Center; 2008. http://www.fao.org/Newsroom/en/news/2008/1000899/index.html. Accessed September 2012.
2. Blagbrough IS, Bayoumi SAL, Rowan MG, Beeching J: Cassava: An appraisal of its phytochemistry and its biotechnological prospects. Phytochemistry 2010, 71:1940-1951.
3. El-Sharkawy MA: Cassava biology and physiology. Plant Mol Biol 2004, 53:621-641.
4. Henry G: Global Cassava End Uses and Market, Production, Perspective and Future Prospects FAO Bulletin, Rome; 2000. 85:242.
5. Berry S, Rey MEC: Molecular evidence for diverse populations of cassava-infecting begomoviruses in southern Africa. Arch Virol 2001, 146:1795-1802.
6. Legg JP, Owor B, Sseruwagi P, Ndunguru J: Cassava mosaic virus disease in East and Central Africa: epidemiology and management of a regional pandemic. Adv Virus Res 2006, 67:355-418.
7. Berrie LC, Rybicki EP, Rey MEC: Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. J Gen Virol 2001, 82:53-58.
8. Bisaro DM: Silencing suppression by geminivirus proteins. Virology 2006, 344:158-168.
9. Dixon AGO, Whyte JBA, Mahungu NM, Ng SYC: Tackling the Cassava Mosaic Disease (CMD) Challenge in sub-Saharan Africa: The Role of Host-Plant Resistance and Germplasm Deployment. In Cassava, an Ancient Crop for Modern Times: Food, Health, Culture. Edited by Taylor NJ, Ogbe F, Fauquet CM. St. Louis, USA: Donald Danforth Plant sciences Center; 2001:S8-05.
10. Akano A, Dixon AGO, Mba C, Barrera E, Fregene M: Genetic mapping of a dominant gene conferring resistance to cassava mosaic disease. Theor Appl Genet 2002, 105:521-525.
11. Fregene M, Matsumura H, Akano A, Dixon A, Terauchi R: Serial analysis of gene expression (SAGE) of host-plant resistance to the cassava mosaic disease. Plant Mol Biol 2004, 56:563-571.
12. Rabbi IY, Kulembeka HP, Masumba E, Marri PR, Ferguson M: An EST-derived SNP and SSR genetic linkage map of cassava (Manihot esculenta Crantz). Theor Appl Genet 2012, 125:329-342.
13. Wang M-B, Masuta C, Neil A, Smith NA, Shimura H: RNA silencing and plant viral diseases. MPMI 2012, 25(10):1275-1285.
14. Raja P, Sanville BC, Buchmann RC, Bisaro DM: Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 2008, 82:8997-9007.
15. Góngora-Castillo E, Ibarra-Laclette E, Trejo-Saavedral DL, Rivera-Bustamante RF: Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virol J 2012, 9:295.
16. Rodríguez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF: RNA Silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 2009, 83:1332-1340.
17. Mysore KS, Ryu C: Nonhost resistance: how much do we know? Trends Plant Sci 2004, 9(2):97-104.
18. Whitham SA, Yang C, Goodin MM: Global impact: elucidating plant responses to viral infection. MPMI 2006, 19(11):1207-1215.
19. Agudelo-Romero P, Carbonell P, Perez-Amador MA, Elena SF: Virus adaptation by manipulation of Host's gene expression. PLoS ONE 2008, 3(6):e2397.
20. Pallas V, Garcia JA: How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol 2011, 92(12):2691-2705.
21. Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG: Molecular genetics of plant disease resistance. Science 1995, 268:661-667.
22. Feys BJ, Moisan LJ, Newman M, Parker JE: Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and Pad4. EMBO J 2001, 20(19):5400-5411.
23. Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
24. Bolton MD: Primary metabolism and plant defense-fuel for the fire. MPMI 2009, 22:487-497.
25. Durrant WE, Dong X: Systemic acquired resistance. Ann Rev Phytopathol 2004, 42:185-209.
26. Fagard M, Dellagi A, Roux C, Périno C, Rigault M, Boucher V, Shevchik VE, Expert D: Arabidopsis thaliana expresses multiple lines of defense to counterattack Erwinia chrysanthemi. MPMI 2007, 20:794-805.
27. Blomster T, Salojärvi J, Sipari N, Brosché M, Ahlfors R, Keinänen M, Overmyer Kangasjärvi J: Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol 2011, 157:1866-1883.
28. Abramovitch RB, Martin GB: Strategies used by bacterial pathogens to suppress plant defenses. Curr Opin Plant Biol 2004, 7:356-364.
29. Pavan S, Jacobsen E, Visser R, Bai Y: Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 2010, 25:1-12.
30. 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.
31. Ascencio-Ibáñez JT, Sozzani R, Lee T, Chu T, Wolfinger RD, Cella R, Hanley-Bowdoin L: Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 2008, 148:436-454.
32. Lozano-Duran R, Rosas-Diaz T, Luna AP, Bejarano ER: Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS One 2011, 6(7):e22383.
33. Babu M, Griffiths JS, Huang TS, Wang A: Altered gene expression changes in Arabidopsis leaf tissues and protoplasts in response to Plum pox virus infection. BMC Genomics 2008, 9:325.
34. Elena SF, Carrera J, Rodrigo G: A systems biology approach to the evolution of plant virus interactions. Curr Opin Plant Biol 2011, 14:372-377.
35. Postnikova O, Nemchinov L: Comparative analysis of microarray data in Arabidopsis transcriptome during compatible interactions with plant viruses. Virol J 2012, 9:101.
36. Carrington JC, Whitham SA: Viral invasion and host defence: strategies and counter-strategies. Curr Opin Plant Biol 1998, 1(4):336-341.
37. Maule A, Leh V, Lederer C: The dialogue between viruses and hosts in compatible interactions. Curr Opin Plant Biol 2002, 5(4):279-284.
38. Whitham SA, Wang Y: Roles for host factors in plant viral pathogenicity. Curr Opin Plant Biol 2004, 7:365-371.
39. Gutierrez C: Strategies of geminivirus DNA replication and cell cycle interference. Physiol Mol Biol Plants 2002, 60:19-230.
40. Jeske H: Geminiviruses. In Torque Teno Virus: the Still Elusive Human Pathogens. Edited by zur Hausen H, de Villiers EM. Berlin: Springer; 2009:185-226.
41. Mariano AC, Andrade MO, Santos AA, Carolino SMB, Oliveira ML, Baracat-Pereira MC, Brommonshenkel SH, Fontes EPB: Identification of a novel receptor-like protein kinase that interacts with a geminivirus nuclear shuttle protein. Virology 2004, 318:24-30.
42. Fontes EP, Santos AA, Luz DF, Waclawovsky AJ, Chory J: The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Gene Dev 2004, 18(20):2545-2556.
43. Selth LA, Dogra SC, Rasheed MS, Healy H, Randles JW, Rezaian MA: A NAC domain protein interacts with Tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell 2005, 17:311-325.
44. Whitham SA, Quan S, Chang HS, Cooper B, Estes B: Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J 2003, 33(2):271-283.
45. 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.
46. Schenk P, Kazan K, Wilson I, Anderson J, Richmond T, Somerville S, Manners J: Co-ordinated plant defense responses in Arabidopsis revealed in microarray analysis. PNAS 2000, 97:11655-11660.
47. Pierce EJ, Rey MEC: Assessing global transcriptome changes in response to South African cassava mosaic virus [ZA-99] infection in susceptible Arabidopsis thaliana. PLoS ONE 2013, 8:e67534.
48. Miozzi L, Napoli C, Sardo L, Accotto GP: Transcriptomics of the interaction between the monopartite phloem-limited geminivirus tomato yellow leaf curl Sardinia virus and Solanum lycopersicum highlights a role for plant hormones, autophagy and plant immune system fine tuning during infection. PLoS ONE 2014, 9(2):e8995.
49. Eybishtz A, Peretz Y, Sade D, Akad F, Czosnek H: Silencing of a single gene in tomato plants resistant to Tomato yellow leaf curl virus renders them susceptible to the virus. Plant Mol Biol 2009, 71:157-171.
50. Eybishtz A, Peretz Y, Sade D, Gorovits R, Czosnek H: Tomato yellow leaf curl virus infection of a resistant tomato line with a silenced sucrose transporter gene LeHT1 results in inhibition of growth, enhanced virus spread, and necrosis. Planta 2010, 231:537-548.
51. Sade D, Brothman Y, Eybishtz A, Cuadros-Inostroza A, Fernie AR, Willmitzer L, Czosnek H: Involvement of the hexose transporter gene LeHT1 and of sugars in resistance of tomato to tomato yellow leaf curl virus. Mol Plant 2013. doi:10.1093/mp/sst036.
52. Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2008, 10:57-63.
53. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, Sittka A, Chabas S, Reiche K, Hackermuller J, Reinhardt R, Stadler PF, Vogel J: The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 2010, 464:250-255.
54. Liu L, Li Y, Li S, He Y: Comparison of next-generation sequencing systems. J Biomed Biotechnol 2012, 2012:251364.
55. Dressman D, Yan H, Traverso G, Kinzler KW, Vogelstein B: Transforming single DNA molecules into fluorescent magnetic particles for detection and enumeration of genetic variations. PNAS 2003, 100:8817-8822.
56. Weber APM, Weber KL, Wilkerson C, Ohlrogge JB: Sampling the Arabidopsis transcriptome with massively parallel pyrosequencing. Plant Physiol 2007, 144:32-42.
57. Fedurco M, Romieu A, Williams S, Lawrence I, Turcatti G: BTA, a novel reagent for DNA attachment on glass and efficient generation of solid-phase amplified DNA colonies. Nucleic Acids Res 2006, 34(3):e22.
58. Anderson JV, Delseny M, Fregene MA, Jorge V, Mba C, Lopez C, Restrepo S, Soto S, Piegu B, Verdier V, Cooke R, Tohme J, Horvath DP: An EST resource for cassava and other species of Euphorbiaceae. Plant Mol Biol 2004, 56:527-539.
59. Lokko Y, Anderson JV, Rudd S, Raji A, Horvath D, Mikel MA, Kim R, Liu L, Hernandez A, Dixon AG, Ingelbrecht IL: Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Rep 2007, 26:1605-1618.
60. Sakurai T, Plata G, Rodriguez-Zapata F, Seki M, Salcedo A, Toyoda A, Ishiwata A, Tohme J, Sakaki Y, Shinozaki K, Ishitani M: Sequencing analysis of 20,000 full-length cDNA clones from cassava reveals lineage specific expansions in gene families related to stress response. BMC Plant Biol 2007, 7:66.
61. Li YZ, Pan YH, Sun CB, Dong HT, Luo XL, Wang ZQ, Tang JL, Chen B: An ordered EST catalogue and gene expression profiles of cassava (Manihot esculenta) at key growth stages. Plant Mol Biol 2010, 74:573-90.
62. Reilly K, Bernal D, Cortes DF, Gomez-Vasquez R, Tohme J, Beeching JR: Towards identifying the full set of genes expressed during cassava post-harvest physiological deterioration. Plant Mol Biol 2007, 64:187-203.
63. Lopez C, Soto-Suarez M, Restrepo S, Piegu B, Cooke R, Delseny M, Tohme J, Verdier V: Global transcriptome analysis of cassava responses to Xanthomonas axonopodis pv.manihotis infection using a cassava cDNA microarray. Plant Mol Biol 2005, 57:393-410.
64. Utsumi Y, Tanaka M, Morosawa T, Kurotani A, Yoshida T, Mochida K, Matsui A, Umemura Y, Ishitani M, Shinozaki K, Sakurai T, Seki M: Transcriptome analysis using a high-density oligo microarray under drought stress in various genotypes of cassava, an important tropical crop. DNA Res 2012, 19(4):335-345.
65. Prochnik S, Marri PR, Desany B, Rabinowicz PD, Kodira C, Mohiuddin M, Rodriguez F, Fauquet C, Tohme J, Harkins T, Rokhsar DS, Rounsley S: The cassava genome: current progress, future directions. Trop Plant Biol 2012, 5(1):88-94.
66. Awoleye F, Duren M, Dolezel J, Novak FJ: Nuclear DNA content and in vitro induced somatic polyploidization cassava (Manihot esculenta Crantz) breeding. Euphytica 1994, 76:195-202.
67. Ayling S, Ferguson M, Rounsley S, Kulakow P: Information resources for cassava research and breeding. Tropl Plant Biol 2012, 5(1):140-15.
68. Liu J, Yang J, Bi H, Zhang P: Why mosaic? Gene expression profiling of African cassava mosaic virus infected cassava reveals the effect of chlorophyll degradation on symptom development. J Integr Plant Biol 2014, (2):122-132. doi:10.1111/jipb.12133.
69. Fauquet CM, Fargette D: Proceedings of the International Seminar: African Cassava Mosaic Disease and its Control. Ede, Netherlands: CTA/ORSTOM; 1988.
70. Allie F, Pierce EJ, Okoniewski MJ, Rey MEC: Monitoring comparative transcriptional changes in a susceptible and tolerant landrace of cassava infected with South African cassava mosaic virus using next-generation sequencing. 2014. NCBI Sequence Read Achive (SRA) database: http://www.ncbi.nlm.nih.gov/sra/?term=PRJNA255198.
71. Conti G, Rodriguez MC, Manacorda CA, Asurmendi S: Transgenic expression of Tobacco mosaic virus capsid and movement proteins modulate plant basal defense and biotic stress responses in Nicotiana tabacum. MPMI 2012, 25(10):1370-1384.
72. Larionov A, Krause A, Miller W: A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005, 6:62.
73. An D, Yang J, Zhang P: Transcriptome profiling of low temperaturetreated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genomics 2012, 13:64.
74. Lattanzio V, Lattanzio VMT, Cardinali A: Role of Polyphenols in the Resistance Mechanisms of Plants Against Fungal Pathogens and Insects. In Phytochemistry:Advances in Research. Edited by Imperato F. Trivandrum, Kerala, India: Research Signpost; 2006:23-67.
75. Zabala G, Zou J, Tuteja J, Gonzalez DO, Clough SJ, Vodkin LO: Transcriptome changes in the phenylpropanoid pathway of Glycine max in response to Pseudomonas syringae infection. BMC Plant Biol 2006, 6:26.
76. Hao Z, Wang L, He Y, Liang J, Tao R: Expression of defense genes and activities of antioxidant enzymes in rice resistance to rice stripe virus and small brown plant hopper. Plant Physiol Bioch 2011, 49:744-751.
77. Chong J, Baltz R, Schmitt C, Beffa R, Fritig B, Saindrenan P: Downregulation of a pathogen-responsive tobacco UDP-Glc:phenylpropanoid glucosyltransferase reduces scopoletin accumulation, enhances oxidative stress, and weakens virus resistance. The Plant Cell 2002, 14:1093-1107.
78. O'Donnell PJ, Schmelz EA, Moussatche P, Lund ST, Jones JB, Klee HJ: Susceptible to intolerance-a range of hormonal actions in a susceptible Arabidopsis pathogen response. The Plant J 2003, 33:245-257.
79. Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW: Plant disease resistance genes: current status and future directions. Physiol Mol Plant P 2012, 78:51-65.
80. Bendahmane A, Kanyuka K, Baulcombe DC: The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 1999, 11:781-792.
81. Jennings DL: Breeding for resistance to African cassava geminivirus in East Africa. Trop Sci 1994, 34:110-122.
82. Fregene M, Matsumura H, Akano A, Dixon A, Terauchi R: Progress Towards Cloning the Single Dominant Gene Conferring Immunity to Cassava Mosaic Disease (CMD). In Cassava, an Ancient Crop for Modern Times: Food, Health, Culture. Edited by Taylor NJ, Ogbe F, Fauquet CM. St Louis, USA: Donald Danforth Plant Sciences Centre; 2001:S5-09.
83. Okogbenin E, Porto MCM, Egesi C, Mba C, Espinosa E, Santos LG, Ospina C, Marín J: Marker-assisted introgression of resistance to cassava mosaic disease into Latin American germplasm for the genetic improvement of cassava in Africa. Crop Sci 2007, 47:1895-1904.
84. Lokko Y, Danquah EY, Offei SK, Dixon AGO, Gedil MA: Molecular markers associated with a new source of resistance to the cassava mosaic disease. Afr J Biotechnol 2005, 4(9):873-881.
85. Gedil M, Kumar M, Igwe D: Isolation and characterization of resistant gene analogs in cassava, wild Manihot species, and castor bean (Ricinus communis). Afr J Biotechnol 2012, 11(85):15111-15123.
86. Patil BL, Fauquet CM: Cassava mosaic geminiviruses: actual knowledge and perspectives. Mol Plant Path 2009, 10:685-701.
87. Hagen C, Rojas MR, Kon T, Gilbertson RL: Recovery from Cucurbit leaf crumple virus (family Geminiviridae, genus Begomovirus) infection is an adaptive antiviral response associated with changes in viral small RNAs. Phytopath 2008, 98:1029-1037.
88. Aregger M, Borah BK, Seguin J, Rajeswaran R, Gubaeva EG: Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathog 2012, 8(9):e1002941. doi:10.1371/journal.ppat.1002941.
89. Ruiz-Ferrer V, Voinnet O: Roles of plant small RNAs in biotic stress responses. Ann Rev Plant Biol 2009, 60:485-510.
90. Sahu PP, Rai NK, Chakroborty S, Singh M, Chandrappa PH, Ramesh B, Chattopadhyay D, Prasad M: Tomato cultivar tolerant to tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol Plant Path 2010, 11(4):531-544.
91. Liu C, Lu F, Cui X, Cao X: Histone methylation in higher plants. Ann Rev Plant Biol 2010, 61:395-420. doi:10.1146/annurev. arplant.043008.091939.
92. Saze H, Tsugane K, Kanno T, Nishimura T: DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol 2012, 3(5):766-784.
93. Shen W, Hanley-Bowdoin L: Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1 and mammalian AMPK activating kinases. Plant Physiol 2006, 142:1642-1655.
94. McGarry RC, Barron YD, Carvalho MF, Hill JE, Gold D, Cheung E, Kraus WL, Lazarowitz SG: A novel Arabidopsis acetyltransferase interacts with the geminivirus movement protein NSP. Plant Cell 2003, 15:1605-1618.
95. Allie F, Rey MEC: Transcriptional alterations in model host, Nicotiana benthamiana, in response to infection by South African cassava mosaic virus. Eur J of Plant Path 2013, 137(4):765-785.
96. Xie AD, Zilberman D, Jacobsen SE, Carrington JC: Genetic and functional diversification of small RNA path-ways in plants. PLoS Biol 2004, 2:E104.
97. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC: RNA polymerase IV directs silencing of endogenous DNA. Science 2005, 308:118-120.
98. Springer NM, Kaeppler SM: Evolutionary divergence of monocot and dicot methyl-CpG-binding domain proteins. Plant Physiol 2005, 138:92-104.
99. Zemach A, Grafi G: Methyl-CpG-binding domain proteins in plants: interpreters of DNA methylation. Trends Plant Sci 2007, 12(2):80-5.
100. Cheong YH, Chang HS, Gupta R, Wang X, Luan S: Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 2002, 129(2):661-77.
101. Golem S, Culver JN: Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. MPMI 2003, 16:681-688.
102. Pompe-Novak M, Gruden K, Baebler S, Krecic-Stres H, Kovac M, Jongsma M, Ravnikar M: Potato virus Y induced changes in the gene expression of potato (Solanum tuberosum L.). Physiol Mol Plant Pathol 2006, 67:237-247.
103. Koornneef A, Pieterse CMJ: Cross-talk in defense signaling. Plant Physiol 2008, 146:839-844.
104. Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardóczy V, Teige M, Koncz C, Peck S, Bögre L: The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 2006, 48:485-498.
105. Innes RW: Mapping out the roles of MAP kinases in plant defense. Trends Plant Sci 2001, 6:392-394.
106. Pitzschke A, Schikora A, Hirt H: MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 2009, 12:421-426.
107. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J: MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 2002, 415:977-983.
108. Yang K-Y, Liu Y, Zhang S: Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. PNAS 2001, 98:741-746.
109. Menke FL, van Pelt JA, Pieterse CM, Klessig DF: Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 2004, 16:897-907.
110. Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U: Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 2009, 21:944-953.
111. Meldau S, Ullman-Zeunert L, Govind G, Bartram S, Baldwin IT: MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biol 2012, 12:213.
112. Brodersen P, Petersen M: Arabidopsis MAP kinase 4 regulates salicylic acid-and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J 2006, 47:532-546.
113. Liu Y, Schiff M, Dinesh-Kumar SP: Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 2004, 38:800-809.
114. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y: Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. PNAS 2003, 100(13):8024-8029.
115. Ishihama N, Yoshioka H: Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 2012, 15:431-437.
116. Li J, Brader G, Palva ET: The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 2004, 16:319-331.
117. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman M, Nielsen HB, Hirt H, Somssich I, Mattsson O, Mundy J: The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 2005, 24:2579-2589.
118. Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C: Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 2008, 18(7):756-67.
119. Culver JN, Padmanabhan MS: Virus-induced disease: Altering host physiology one interaction at a time. Ann Rev Phytopath 2007, 45:221-243.
120. Dempsey DA, Shah J, Klessig DF: Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 1999, 18:547-575.
121. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC: Networking by small-molecule hormones in plant immunity. Nat Chem Biol 2009, 5(5):308-316.
122. Ballare CL: Jasmonate-induced defences: a tale of intelligence, collaborators and rascals. Trends Plant Sci 2011, 16(5):249-257.
123. Chico JM, Chini A, Fonseca S, Solano R: JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 2008, 11:486-494.
124. Lorenzo O, Solano R: Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol 2005, 8:532-540.
125. Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M: Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 2000, 12:393-404.
126. Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH: Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 2001, 13:1035-1046.
127. Love AJ, Yun BW, Laval V, Loake GJ, Milner JJ: Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defence signalling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 2005, 139:935-948.
128. Shimizu T, Satoh K, Kikuchi S, Omura T: The repression of cell wall-and plastid-related genes and the induction of defense-related genes in rice plants infected with Rice dwarf virus. MPMI 2007, 20:247-254.
129. Chou HM, Bundock N, Rolfe SA, Scholes JD: Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol Plant Path 2000, 1:99-113.
130. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE: The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 2003, 132:821-829.
131. Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T: Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 2004, 122:419-428.
132. Swarbrick PJ, Schulze-Lefert P, Scholes JD: Metabolic consequences of susceptibility and resistance in barley leaves challenged with powdery mildew. Plant Cell Environ 2006, 29:1061-1076.
133. Roitsch T, Balibrea ME, Hofman M, Proels R, Sinha AK: Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 2003, 54:513-524.
134. Truernit E, Schmid J, Epple P, Illig J, Sauer N: The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 1996, 8:2169-2182.
135. Bolouri-Moghaddam MR, Van den Ende W: Sugars and plant innate immunity. J Exp Bot 2012, 63(11):3989-98.
136. Gómez-Ariza J, Campo S, Rufat M, Estopà M, Messeguer J, San Segundo B, Coca M: Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. MPMI 2007, 20:832-842.
137. Herbers K, Takahata Y, Melzer M, Mock HP, Hajirezaei M, Sonnewald U: Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco. Mol Plant Path 2000, 1:51-59.
138. Harries PA, Schoelz JE, Nelson RS: Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. MPMI 2010, 23:1381-1393.
139. Ghoshroy S, Lartey R, Sheng JS, Citovsky V: Transport of proteins and nucleic acids through plasmodesmata. Annu Rev Plant Physiol Plant Mol Biol 1997, 48:25-48.
140. Lazarowitz SG, Beachy RN: Viral movement proteins as probes for intracellular and intercellular trafficking in plants. Plant Cell 1999, 11:535-548.
141. Boevink P, Oparka KJ: Virus-host interactions during movement processes. Plant Physiol 2005, 138(4):1815-21.
142. Heinlein M, Epel BL, Padgett HS, Beachy RN: Interaction of tobamovirus movement proteins with the plant cytoskeleton. Science 1995, 270:1983-1985.
143. Heinlein M, Padgett HS, Gens JS, Pickard BG, Casper SJ, Epel BL, Beachy RN: Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 1998, 10:1107-1120.
144. Kahn TW, Lapidot M, Heinlein M, Reichel C, Cooper B, Gafny R, Beachy RN: Domains of the TMV movement protein involved in subcellular localization. Plant J 1998, 15:15-25.
145. Lucas WJ: Plant viral movement proteins, Agents for cell-to-cell trafficking of viral genomes. Virology 2006, 344:169-184.
146. McLean BG, Zupan J, Zambryski P: Tobacco mosaic virus movement protein associates with the cytoskeleton in tobacco plants. Plant Cell 1995, 7:2101-2114.
147. Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang X-C, Yuan M: Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. The Plant Cell 2010, 22:1373-1387.
148. Chen MH, Sheng J, Hind G, Handa A, Citovsky V: Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 2000, 19:913-920.
149. Dorokhov YL, Makinen K, Frolova OY, Merits A, Saarinen J, Kalkkinen N, Atabekov JG, Saarma M: A novel function for a ubiquitous plant enzyme pectin methylesterase: the host-cell receptor for the tobacco mosaic virus movement protein. FEBS Lett 1999, 461:223-228.
150. Heinlein M: The spread of Tobacco mosaic virus infection: insights into the cellular mechanism of RNA transport. Cell Mol Life Sci 2002, 59:58-82.
151. Pérez-Quintero AL, Quintero A, Urrego O, Vanegas P, López C: Bioinformatic identification of cassava miRNAs differentially expressed in response to infection by Xanthomonas axonopodis pv. Manihotis. BMC Plant Biol 2012, 12:29.
152. Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco cultures. Plant Physiol 1962, 15:473-497.
153. Hayes RL, Brough CL, Prince VE, Coutts RHA, Buck KW: Infection of Nicotiana benthamiana with uncut cloned tandem dimers of tomato golden mosaic virus DNA. J Gen Virol 1988, 69:209-218.
154. Doyle JJ, Doyle JL: A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 1987, 19:11-15.
155. Moreno I, Gruissem W, Vanderschuren H: Reference genes for reliable potyvirus quantitation in cassava and analysis of Cassava brown streak virus load in host varieties. J Virol Methods 2011, 177:49-54.
156. Gehrig HH, Winter K, Cushman J, Borland A, Taybi T: An improved RNA isolation method for succulent plant species rich in polyphenols and polysaccharides. Plant Mol Biol Rep 2000, 18:369-376.
157. Lesniewska A, Okoniewski MJ: rnaSeqMap: a Bioconductor package for RNA sequencing data exploration. BMC Bioinformatics 2011, 12:200.
158. Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. doi:10.1186/gb-2010-11-10-r106.