The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen

New Phytologist

Volumn 164, Issue 1, 2004, Pages 123-136

  Smith, Caroline M ^a   Rodriguez Buey, Marisa ^b   Karlsson, Jan ^b   Campbell, Malcolm M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Microarray; Poplar Mosaic Virus; Populus; Transcription; Transcriptome; Wounding

Indexed keywords

PATHOGEN;

POPLAR MOSAIC VIRUS; POPULUS; POPULUS BEROLINENSIS;

EID: 4644337070     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2004.01151.x     Document Type: Article

References (79)

1. Ahn JH, Choi Y, Kwon YM, Kim SG, Choi YD, Lee JS. 1996. A novel extensin gene encoding a hydroxyproline-rich glycoprotein requires sucrose for its wound-inducible expression in transgenic plants. Plant Cell 8: 1477-1490.
2. Andersson A, Keskitalo J, Sjodin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P. 2004. A transcriptional timetable of autumn senescence. Genome Biology 5: R24.
3. Aranda MA, Maule AJ. 1998. Virus-induced host gene shutoff in animals and plants. Virology 243: 261-267.
4. Aranda MA, Escaler M, Wang D, Maule AJ. 1996. Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proceedings of the National Academy of Sciences, USA 93: 15289-15293.
5. Aranda MA, Escaler M, Thomas CL, Maule AJ. 1999. A heat shock transcription factor in pea is differentially controlled by heat and virus replication. Plant Journal 20: 153-161.
6. Atkinson MA, Cooper JI. 1976. Ultrastructural changes in leaf cells of poplar naturally infected with poplar mosaic virus. Annals of Applied Biology 83: 395-398.
7. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of Royal Statistical Society B 57: 289-300.
8. Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg et al. 2003. Gene expression in autumn leaves. Plant Physiology 131: 430-442.
9. Biddle PG, Tinsley TW. 1971a. Poplar mosaic virus. CMI/AAB Description of Plant Viruses 75: 1-3.
10. Biddle PG, Tinsley TW. 1971b. Poplar mosaic virus in Great Britain. New Phytologist 70: 61-66.
11. Biddle PG, Tinsley TW. 1971c. Some effects of poplar mosaic virus on the growth of poplar trees. New Phytologist 70: 67-75.
12. Bradshaw HD Jr, Stettler RF. 1995. Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139: 963-973.
13. Bradshaw HD, Villar M, Watson BD, Otto KG, Stewart S, Stettler RF. 1994. Molecular genetics of growth and development in Populus. 3. A genetic-linkage map of a hybrid poplar composed of RFLP, STS and RAPD markers. Theoretical and Applied Genetics 89: 167-178.
14. Brunner AM, Busov VB, Strauss SH. 2004. Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends in Plant Science 9: 49-56.
15. Brunt AA, Stace-Smith R, Leung E. 1976. Cytological evidence supporting the inclusion of poplar mosaic virus in the carlavirus group of plant viruses. Intervirology 7: 303-308.
16. Bucher GL, Tarina C, Heiniein M, Di Serio F, Meins FJ, Iglesias VA. 2001. Local expression of enzymatically active class I beta-1,3-glucanase enhances symptoms of TMV infection in tobacco. Plant Journal 28: 361-369.
17. Cervera MT, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, van Slycken J, van Montagu M, Boerjan W. 2001. Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigranna P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158: 787-809.
18. Chen M-H, Citovsky V. 2003. Systemic movement of a tobamovirus requires host cell pectin methylesterase. Plant Journal 35: 386-392.
19. Chen M-H, Sheng J, Hind G, Handa AK, 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.
20. Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129: 661-677.
21. Choi D, Kim HM, Yun HK, Park JA, Kim WT, Bok SH. 1996. Molecular cloning of a metallothionein-like gene from Nicotiana glutinosa L. and its induction by wounding and tobacco mosaic virus infection. Plant Physiology 112: 353-359.
22. Citovsky V, Ghoshroy S, Tsui F, Klessig D. 1998. Non-toxic concentrations of cadmium inhibit systemic movement of turnip vein clearing virus by a salicylic acid-dependent mechanism. Plant Journal 16: 13-20.
23. Cooper JI. 1993. Virus diseases of trees and shrubs, 2nd edn. London, UK: Chapman & Hall.
24. Cooper JI, Edwards ML. 1981. The distribution of poplar mosaic virus in hybrid poplars and virus detection by ELISA. Annals of Applied Biology 99: 53-61.
25. Cosgrove DJ. 1997. Assembly and enlargement of the primary cell wall in plants. Annual Review of Cell and Developmental Biology 13: 171-201.
26. Creelman RA, Tierney ML, Mullet JE. 1992. Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression. Proceedings of the National Academy of Sciences, USA 89: 4938-4941.
27. Criqui MC, Durr A, Parmentier Y, Marbach J, Fleck J, Jamet E. 1992. How are photosynthetic gene repressed in freshly-isolated mesophyll protoplasts of Nicotiana sylvestris?. Plant Physiological Biochemistry 30: 597-601.
28. Dorokhov YL, Makinen K, Frolova OY, Merits A, Saarinen J, Kalkkinen N, Atabekov JG, 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.
29. Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDG. 2000. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963-977.
30. Ender F, Hallmann A, Amon P, Sumper M. 1999. Response to the sexual pheromone and wounding in the green alga Volvox: induction of an extracellular glycoprotein consisting almost exclusively of hydroxyproline. Journal of Biological Chemistry 274: 35023-35028.
31. Escaler M, Aranda MA, Thomas CL, Maule AJ. 2000. Pea embryonic tissues show common responses to the replication of a wide range of viruses. Virology 267: 318-325.
32. Frewen BE, Chen TH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD Jr. 2000. Quantitative trait loci and candidate gene mapping of bud set and bud flush in Pofulus. Genetics 154: 837-845.
33. Glotzer JB, Saltik M, Chiocca S, Michou A-I, Moseley P, Cotten M. 2000. Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407: 207-211.
34. Goujon T, Ferret V, Mila I, Pollet B, Ruel K, Burlat V, Joseleau J-P, Barriere Y, Lapierre C, Jouanin L. 2003. Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability. Planta 217: 218-228.
35. Haruta M, Major IT, Christopher MT, Patton JJ, Constabel CP. 2001. A kunitz trypsin inhibitor gene family from trembling aspen (Pofulus tremuloides Mischx): cloning, functional expression, and induction by wounding and herbivory. Plant Molecular Biology 46: 347-359.
36. Henderson J, Gibbs MJ, Edwards ML, Clarke VA, Gardner KA, Cooper JI. 1992. Partial nucleotide sequence of poplar mosaic virus RNA confirms its classification as a carlavirus. Journal of General Virology 73: 1887-1890.
37. Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhle M, Teeri TT, Lundeberg J, Sundberg B, Nilsson P, Sandberg G. 2001. A transcriptional roadmap to wood formation. Proceedings of the National Academy of Sciences, USA 98: 14732-14737.
38. Ihaka R, Gentleman R. 1996. R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5: 299-314.
39. Jones L, Ennos AR, Turner SR. 2001. Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant Journal 26: 205-216.
40. Kado CI, Agrawal HO. 1972. Principles and techniques in plant virology. New York, NY, USA: Van Nostrand Reinhold.
41. Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proceedings of the National Academy of Sciences, USA 98: 6511-6515.
42. von Kontzog H-G, Ebrahim-Nesbat F. 1992. Ermittlung und Bewertung quantitativer Virusresistenz von Pappeln nach Inokulation mit Pappelnmosaik-Virus (poplar mosaic virus, PopMV). European Journal of for Pathology 22: 193-203.
43. Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF. 2002. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130: 2129-2141.
44. Kuriyama H, Fukuda H. 2002. Developmental programmed cell death in plants. Current Opinion in Plant Biology 5: 568-573.
45. Lamb C, Dixon RA. 1997. The oxidative burst in plant disease resistance. Annual Review of Plant Physiological Plant Molecular Biology 48: 251-275.
46. Legionnet A, Muranty H, Lefevre F. 1999. Genetic variation of the riparian pioneer tree species Populus nigra. II. Variation in susceptibility to the foliar rust Melampsora larici-populina. Heredity 82: 318-327.
47. Li L, Li C, Howe GA. 2001. Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiology 127: 1414-1417.
48. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue. Physiological Plant 15: 473-497.
49. Newcombe G. 1996. The specificity of fungal pathogens of Populus. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM, eds. Biology of Populus and its implications for management and conservation. Ottawa, ON, Canada: NRC Research Press, 223-246.
50. Nienhaus F, Castello JD. 1989. Viruses in forest trees. Annual Review of Phytopathology 27: 165-186.
51. Osmark P, Boyle B, Brisson N. 1998. Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins. Plant Molecular Biology 38: 1243-1246.
52. Ostry ME, Ward KT. 2003. Field performance of Populus expressing somaclonal variation in resistance to Septoria musiva. Plant Science 164: 1-8.
53. Pozueta-Romero J, Klein M, Houlne G, Schantz M-L, Meyer B, Shantz R. 1995. Characterisation of a family of gene encoding a fruit-specific wound-stimulated protein of Bell pepper (Capsicum annuum): identification of a new family of transposable elements. Plant Molecular Biology 28: 1011-1025.
54. Preston CA, Lewandowski C, Enyedi AJ, Baldwin IT. 1999. Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209: 87-95.
55. Qi X, Behrens BX, West PR, Mort AJ. 1995. Solubilization and partial characterisation of extensin fragments from cell walls of cotton suspension cultures. Plant Physiology 108: 1691-1701.
56. Reinbothe S, Reinbothe C, Porthier B. 1993. Methyl jasmonate-regulated translation of nuclear-encoded chloroplast proteins in barley (Hordeum vulgare L. cv. Salome). Journal of Biological Chemistry 268: 10606-10611.
57. Reymond P, Weber H, Damond M, Farmer EE. 2000. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12: 707-720.
58. Rhee Y, Tzfira T, Chen M-H, Waigmann E, Citovsky V. 2000. Cell-to-cell movement of tobacco mosaic virus: enigmas and explanations. Molecular Plant Pathology 1: 33-39.
59. Royle DJ, Ostry ME. 1995. Disease and pest control in the bioenergy crops poplar and willow. Biomass and Bioenergy 9: 69-79.
60. Scheme PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM. 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences, USA 97: 11655-11660.
61. Showalter AM. 1993. Structure and function of plant cell wall proteins. Plant Cell 5: 9-23.
62. Smith CM, Campbell MM. 2004a. Complete genome sequence of Poplar mosaic virus. Archives of Virology. (In press).
63. Smith CM, Campbell MM. 2004b. Populus genotypes differ in infection and systematic spread of Poplar mosaic virus (PopMV). Plant Pathology. (In press).
64. Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Bhalerao R, Larsson M, Villarroel R, van Montagu M, Sandberg G, Olsson O, Teeri TT, Boerjan W, Gustafsson P, Uhlen M, Sundberg B, Lundeberg J. 1998. Gene discovery in the wood-forming tissues of poplar: analysis of 5692 expressed sequence tags. Proceedings of the National Academy of Sciences, USA 95: 13330-13335.
65. Sugimoto K, Takeda S, Hirochika H. 2000. MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Ttol and defense-related genes. Plant Cell 12: 2511-2528.
66. Sugimoto K, Takeda S, Hirochika H. 2003. Transcriptional activation mediated by binding of a plant GATA-type zinc finger protein AGP1 to the AG-motif (AGATCCAA) of the wound-inducible Myb gene NtMyb2. Plant Journal 36: 550-564.
67. Suh MC, Choi D, Liu JR. 1998. Cadmium resistance in transgenic tobacco plants expressing the Nicotiana glutinosa L. metallothionein-like gene. Molecular Cells 8: 678-684.
68. Tainter FH, Baker FA. 1996. Principles of forest pathology. New York, NY, USA: John Wiley.
69. 2+-binding protein in wheat cultured cells. Plant Molecular Biology 42: 807-817.
70. Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, Han B, Zhu T, Zou G, Katagiri F. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317-330.
71. Titarenko E, Rojo E, Leon J, Sanchez-Serrano JJ. 1997. Jasmonic acid-dependent and -independent signaling pathways control wound-induced gene activation m Arabidopsis thaliana. Plant Physiology 115: 817-826.
72. Ueki S, Citovsky V. 2002. The systemic movement of a tobamovirus is inhibited by a cadmium-ion-induced glycine-rich protein. Nature Cell Biology 4: 478-485.
73. van der Meer FA, Maat DZ, Vink J. 1980. Poplar mosaic virus: purification, antiserum preparation, and detection in poplars with the enzyme-linked immunosorbent assay (ELISA) and with infectivity tests on Nicotiana megalosiphon. Netherlands Journal of Plant Pathology 86: 99-110.
74. Villar M, Lefevre F, Bradshaw HD Jr, Teissier du Cros E. 1996. Molecular genetics of rust resistance in poplars (Melampsora larici-populina Kleb/ Populus sp.) by bulked segregant analysis in a 2 x 2 factorial mating design. Genetics 143: 531-536.
75. Whitham SA, Quan S, Chang H-S, 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.
76. Wojtaszek P. 1997. Oxidative burst: an early plant response to pathogen infection. Biochemistry and Journal 322: 681-692.
77. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Research 30: e15.
78. You HJ, Oh DH, Choi CY, Lie DG, Hahm KS, Moon AR, Jeong HG. 2002. Protective effect of metallothionein-III on DNA damage in response to reactive oxygen species. Biochemica Kophysica Acta 1573: 33-38.
79. Zhou L, Thornburg R. 1999. Wound-inducible genes in plants. In: Reynolds PHS, ed. Inducible Gene expression. Wallingford, UK: CAB International, 127-156.