Apoplast proteome reveals that extracellular matrix contributes to multistress response in poplar

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Pechanova, Olga ^a   Hsu, Chuan Yu ^a   Adams, Joshua P ^a   Pechan, Tibor ^b   Vandervelde, Lindsay ^a   Drnevich, Jenny ^c   Jawdy, Sara ^d   Adeli, Ardeshir ^e   Suttle, Jeffrey C ^e   Lawrence, Amanda M ^f   Tschaplinski, Timothy J ^d   Séguin, Armand ^g   Yuceer, Cetin ^a  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e AGRICULTURAL RESEARCH SERVICE   (United States)

^f MISSISSIPPI STATE UNIVERSITY   (United States)

^g LAURENTIAN FORESTRY CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PEROXIDASE; PROTEOME; STARCH; SUCROSE; ANTIOXIDANT; MESSENGER RNA; VEGETABLE PROTEIN; WATER;

APOPLAST; ARTICLE; ASPEN; CATABOLISM; EXTRACELLULAR MATRIX; FERMENTATION; GLYCOLYSIS; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PHYLOGENY; PLANT GROWTH; PLANT LEAF; PLANT ROOT; PLANT STEM; PLANT STRESS; PROTEIN ANALYSIS; PROTEIN PROCESSING; BIOLOGICAL MODEL; CELL WALL; CLUSTER ANALYSIS; DROUGHT; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HUMAN; INTRACELLULAR SPACE; METABOLISM; PHYSIOLOGICAL STRESS; PROTEOMICS; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

MELAMPSORA; POPULUS; POPULUS DELTOIDES;

ANTIOXIDANTS; CELL WALL; CLUSTER ANALYSIS; DROUGHTS; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; HUMANS; INTRACELLULAR SPACE; MODELS, BIOLOGICAL; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; POPULUS; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; WATER;

EID: 78649383919     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-674     Document Type: Article

References (142)

1. Braatne JH, Rood SB, Heilman PE. Life history, ecology, and conservation of riparian cottonwoods in north America. Biology of Populus 1996, 57-85. Ottawa, Canada: NRC Research Press, Stettler RF, Bradshaw Jr HD, Heilman PE, Hincley TM.
2. Parolin P. Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains. Ann Bot 2009, 103:359-376. 10.1093/aob/mcn216, 2707320, 19001429.
3. Rood SB, Braatne JH, Hughes FMR. Ecophysiology of riparian cottonwoods: stream flow dependency, water relations and restoration. Tree Physiol 2003, 23:1113-1124.
4. Rood SB, Patiño S, Coombs K, Tyree MT. Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees 2000, 14:248-257.
5. Smit BA. Selection of flood-resistant and susceptible seedlings of Populus trichocarpa Torr. & Gray. Can J For Res 1988, 18:271-275.
6. Sakurai N. Dynamic function and regulation of apoplast in the plant body. J Plant Res 1998, 111:133-148.
7. Dietz KJ. Functions and responses of the leaf apoplast under stress. Progress in Botany 1997, 58:221-254.
8. Haslam RP, Downie AL, Raveton M, Gallardo K, Job D, Pallett KE, John P, Parry MAJ, Coleman JOD. The assessment of enriched apoplastic extracts using proteomic approaches. Ann Appl Biol 2003, 143:81-91.
9. Alvarez S, Goodger JQD, Marsh EL, Chen S, Asirvatham VS, Schachtman DP. Characterization of the maize xylem sap proteome. J Proteome Res 2006, 5:963-972. 10.1021/pr050471q, 16602704.
10. Biles CL, Martyn RD, Wilson HD. Isozymes and general proteins from various watermelon cultivars and tissue types. HortScience 1989, 24:810-812.
11. Buhtz A, Kolasa A, Arlt K, Walz C, Kehr J. Xylem sap protein composition is conserved among different plant species. Planta 2004, 219:610-618. 10.1007/s00425-004-1259-9, 15064951.
12. Djordjevic MA, Oakes M, Li DX, Hwang CH, Hocart CH, Gresshoff PM. The Glycine max xylem sap and apoplast proteome. J Proteome Res 2007, 6:3771-3779. 10.1021/pr0606833, 17696379.
13. Floerl S, Druebert C, Majcherczyk A, Karlovsky P, Kues U, Polle A. Defence reactions in the apoplastic proteome of oilseed rape (Brassica napus var. napus) attenuate Verticillium longisporum growth but not disease symptoms. BMC Plant Biol 2008, 8:129. 10.1186/1471-2229-8-129, 2644697, 19094241.
14. Kehr J, Buhtz A, P G. Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol 2005, 21:5-11.
15. Masuda S, Kamada H, Satoh S. Chitinase in cucumber xylem sap. Biosci Biotechnol Biochem 2001, 65:1883-1885. 10.1271/bbb.65.1883, 11577735.
16. Masuda S, Sakuta C, Satoh S. cDNA cloning of a novel lectin-like xylem sap protein and its root-specific expression in cucumber. Plant Cell Physiol 1999, 40:1177-1181.
17. Rep M, Dekker HL, Vossen JH, de Boer A, Houterman PM, Speijer D, Back JW, de Koster CG, Cornelissen JC. Mass spectrometric identification of isoforms of PR proteins in xylem sap of fungus-infected tomato. Plant Physiol 2002, 130:904-917. 10.1104/pp.007427, 166617, 12376655.
18. Rep M, Dekker HL, Vossen JH, de Boer AD, Houterman PM, de Koster CG, Cornelissen BJC. A tomato xylem sap protein represents a new family of small cysteine-rich proteins with structural similarity to lipid transfer proteins. FEBS Lett 2003, 534:82-86. 10.1016/S0014-5793(02)03788-2, 12527365.
19. Satoh S, Iizuka C, Kikuchi A, Nakamura N, Fujii T. Proteins and carbohydrates in xylem sap from squash root. Plant Cell Physiol 1992, 33:841-847.
20. Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies G, Jauneau A, Esquerre-Tugaye M-T, Pont-Lezica R. Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: Identification by mass spectrometry and bioinformatics. Proteomics 2005, 5:212-221. 10.1002/pmic.200400882, 15593128.
21. Biles CL, Abeles FB. Xylem sap proteins. Plant Physiol 1991, 96:597-601. 10.1104/pp.96.2.597, 1080812, 16668227.
22. Dafoe NJ, Constabel CP. Proteomic analysis of hybrid poplar xylem sap. Phytochemistry 2009, 70:856-863. 10.1016/j.phytochem.2009.04.016, 19467552.
23. Diaz-Vivancos P, Rubio M, Mesonero V, Periago PM, Ros-Barcelo A, Martinez-Gomez P, Hernandez JA. The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 2006, 57:3813-3824. 10.1093/jxb/erl138, 17043083.
24. Gau AE, Koutb M, Piotrowski M, Kloppstech K. Accumulation of pathogenesis-related proteins in the apoplast of a susceptible cultivar of apple (Malus domestica cv. Elstar) after infection by Venturia inaequalis and constitutive expression of PR genes in the resistant cultivar Remo. Eur J Plant Pathol 2004, 110:703-711.
25. Giavalisco P, Kapitza K, Kolasa A, Buhtz A, Kehr J. Towards the proteome of Brassica napus phloem sap. Proteomics 2006, 6:896-909. 10.1002/pmic.200500155, 16400686.
26. Lin M-K, Lee Y-J, Lough TJ, Phinney BS, Lucas WJ. Analysis of the pumpkin phloem proteome provides functional insights into angiosperm sieve tube function. Mol Cell Proteomics 2009, 8:343-356.
27. Walz C, Giavalisco P, Schad M, Juenger M, Klose J, Kehr J. Proteomics of cucurbit phloem exudate reveals a network of defense proteins. Phytochemistry 2004, 65:1795-1804. 10.1016/j.phytochem.2004.04.006, 15276438.
28. Hartung W, Radin JW, Hendrix DL. Abscisic acid movement into the apoplastic solution of water-stressed cotton leaves. Plant Physiol 1988, 86:908-913. 10.1104/pp.86.3.908, 1054593, 16666007.
29. Ackerson RC. Synthesis and movement of abscisic acid in water-stressed cotton leaves. Plant Physiol 1982, 69:609-613. 10.1104/pp.69.3.609, 426263, 16662258.
30. Cornish K, Zeevaart JAD. Movement of abscisic acid into the apoplast in response to water stress in Xanthium strumarium L. Plant Physiol 1985, 78:623-626. 10.1104/pp.78.3.623, 1064787, 16664294.
31. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340:783-795. 10.1016/j.jmb.2004.05.028, 15223320.
32. Bendtsen JD, Kiemer L, Fausbøll A, Brunak S. Non-classical protein secretion in bacteria. BMC Microbiology 2005, 5:58. 10.1186/1471-2180-5-58, 1266369, 16212653.
33. Fujihara J, Yasuda T, Kunito T, Fujii Y, Takatsuka H, Moritani T, H T. Two N-linked glycosylation sites (Asn18 and Asn106) are both required for full enzymatic activity, thermal stability, and resistance to proteolysis in mammalian deoxyribonuclease I. Biosci Biotechnol Biochem 2008, 72:3197-3205. 10.1271/bbb.80376, 19060393.
34. Knudsen SK, Stensballe A, Franzmann M, Westergaard UB, Otzen DE. Effect of glycosylation on the extracellular domain of the Ag43 bacterial autotransporter: enhanced stability and reduced cellular aggregation. Biochem J 2008, 412:563-577. 10.1042/BJ20071497, 18341480.
35. Lige B, Ma S, van Huystee RB. The effects of the site-directed removal of N-glycosylation from cationic peanut peroxidase on its function. Arch Biochem Biophys 2001, 386:17-24. 10.1006/abbi.2000.2187, 11360996.
36. O'Neill HG, Redelinghuys P, Schwager SL, Sturrock ED. The role of glycosylation and domain interactions in the thermal stability of human angiotensin-converting enzyme. Biol Chem 2008, 389:1153-1161. 10.1515/BC.2008.131, 18713002.
37. Blom N, Gammeltoft S, Brunak S. Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 1999, 294:1351-1362. 10.1006/jmbi.1999.3310, 10600390.
38. Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 2009, 149:461-473. 10.1104/pp.108.125989, 2613732, 19005089.
39. Tripepi RR, Mitchell CA. Stem hypoxia and root respiration of flooded maple and birch seedlings. Physiol Plantarum 1984, 60:567-571.
40. Kimmerer TW, Stringer MA. Alcohol dehydrogenase and ethanol in the stems of trees: Evidence for anaerobic metabolism in the vascular cambium. Plant Physiol 1988, 87:693-697. 10.1104/pp.87.3.693, 1054822, 16666209.
41. Kreuzwieser J, Papadopoulou E, Rennenberg H. Interaction of flooding with carbon metabolism of forest trees. Plant Biol 2004, 6:299-306. 10.1055/s-2004-817882, 15143438.
42. Jaeger C, Gessler A, Biller S, Rennenberg H, Kreuzwieser J. Differences in C metabolism of ash species and provenances as a consequence of root oxygen deprivation by waterlogging. J Exp Bot 2009, 60:4335-4345. 10.1093/jxb/erp268, 19717531.
43. Kimmerer TW. Alcohol dehydrogenase and pyruvate decarboxylase activity in leaves and roots of eastern cottonwood (Populus deltoides Bartr.) and soybean (Glycine max L.). Plant Physiol 1987, 84:1210-1213. 10.1104/pp.84.4.1210, 1056753, 16665586.
44. Kreuzwieser J, Kuhnemann F, Martis A, Rennenberg H, Urban W. Diurnal pattern of acetaldehyde emission by flooded poplar trees. Physiol Plantarum 2000, 108:79-86.
45. Kreuzwieser J, Scheerer U, Rennenberg H. Metabolic origin of acetaldehyde emitted by poplar (Populus tremula x P. alba) trees. J Exp Bot 1999, 50:757-765.
46. MacDonald RC, Kimmerer TW. Metabolism of transpired ethanol by eastern cottonwood (Populus deltoides Bartr.). Plant Physiol 1993, 102:173-179. 158760, 12231807.
47. Telewski FW, Aloni R, Sauter JJ. Physiology of secondary tissues of Populus. Biology of Populus 1996, 57-85. Ottawa, Canada: NRC Research Press, Stettler RF, Bradshaw Jr HD, Heilman PE, Hincley TM.
48. Heizmann U, Kreuzwieser J, Schnitzler JP, Bruggemann N, Rennenberg H. Assimilate transport in the xylem sap of pedunculate oak (Quercus robur) saplings. Plant Biol 2001, 3:132-138.
49. Coleman HD, Yan J, Mansfield SD. Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci USA 2009, 106:13118-13123. 10.1073/pnas.0900188106, 2722352, 19625620.
50. Gravatt DA, Kirby CJ. Patterns of photosynthesis and starch allocation in seedlings of four bottomland hardwood tree species subjected to flooding. Tree Physiol 1998, 18:411-417.
51. Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B. Biosynthesis of cellulose-enriched tension wood in Populus: Global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 2006, 45:144-165. 10.1111/j.1365-313X.2005.02584.x, 16367961.
52. Ricard B, Rivoal J, Spiteri A, Pradet A. Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol 1991, 95:669-674. 10.1104/pp.95.3.669, 1077589, 16668037.
53. Albrecht G, Mustroph A. Localization of sucrose synthase in wheat roots: increased in situ activity of sucrose synthase correlates with cell wall thickening by cellulose deposition under hypoxia. Planta 2003, 217:252-260.
54. Biemelt S, Hajirezaei MR, Melzer M, Albrecht G, Sonnewald U. Sucrose synthase activity does not restrict glycolysis in roots of transgenic potato plants under hypoxic conditions. Planta 1999, 210:41-49. 10.1007/s004250050652, 10592031.
55. Akihiro T, Umezawa T, Ueki C, Lobna BM, Mizuno K, Ohta M, Fujimura T. Genomic wide cDNA-AFLP analysis of genes rapidly induced by combined sucrose and ABA treatment in rice cultured cells. FEBS Lett 2006, 580:5947-5952. 10.1016/j.febslet.2006.09.065, 17046759.
56. Tang T, Xie H, Wang Y, Lu B, Liang J. The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.). J Exp Bot 2009, 60:2641-2652. 10.1093/jxb/erp114, 19401410.
57. Wang YT, Yang CY, Chen Y-T, Lin Y, Shaw J-F. Characterization of senescence-associated proteases in postharvest broccoli florets. Plant Physiol Biochem 2004, 42:663-670. 10.1016/j.plaphy.2004.06.003, 15331096.
58. Schaller A, Stintzi A. Enzymes in jasmonate biosynthesis - Structure, function, regulation. Phytochemistry 2009, 70:1532-1538. 10.1016/j.phytochem.2009.07.032, 19703696.
59. Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Thiec DL, Fluch S, Martin F, et al. Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiol 2007, 144:347-366. 10.1104/pp.106.094987, 1913798, 17400708.
60. Azaiez A, Boyle B, Levée V, A S. Transcriptome profiling in hybrid poplar following interactions with Melampsora rust fungi. Mol Plant-Microbe Interact 2009, 22:190-200. 10.1094/MPMI-22-2-0190, 19132871.
61. Bowles DJ. Defense-related proteins in higher plants. Ann Rev Biochem 1992, 59:873-907.
62. Leah R, Tommerup H, Svendsen I, Mundy J. Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J Biol Chem 1991, 266:1564-1573.
63. Mauch F, Mauch-Mani B, Boller T. Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and b-1,3-glucanase. Plant Physiol 1988, 88:936-942. 10.1104/pp.88.3.936, 1055685, 16666407.
64. Schlumbaum A, Mauch F, Vogeli U, Boller T. Plant chitinases are potent inhibitors of fungal growth. Nature 1986, 324:365-367.
65. Doxey AC, Yaish MWF, Moffatt BA, Griffith M, McConkey BJ. Functional divergence in the Arabidopsis b-1,3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Mol Biol Evol 2007, 24:1045-1055. 10.1093/molbev/msm024, 17272678.
66. Kästner B, Tenhaken R, Kauss H. Chitinase in cucumber hypocotyls is induced by germinating fungal spores and by fungal elicitor in synergism with inducers of acquired resistance. Plant J 1998, 13:447-454.
67. Mauch F, Staehelin A. Functional implications of the subcellular localization of ethylene-induced chitinase and b-1,3-glucanase in bean leaves. Plant Cell 1989, 1:447-457. 10.1105/tpc.1.4.447, 159776, 12359894.
68. Salzer P, Hebe G, Reith A, Zitterell-Haid B, Stransky H, Gaschler K, Hager A. Rapid reaction of spruce cells to elicitors released from ectomycorrhizal fungus Hebeloma crustuliniforme, and inactivation of these elicitors by extracellular spruce cell inzymes. Planta 1996, 198:118-126.
69. Grenier J, Potvin C, Trudel J, Asselin A. Some thaumatin-like proteins hydrolyse polymeric β-1,3-glucans. Plant J 1999, 19:4473-4480.
70. Trudel J, Grenier J, Potvin C, Asselin A. Several thaumatin-like proteins bind to β-1,3-glucans. Plant Physiol 1998, 118:1431-1438. 10.1104/pp.118.4.1431, 34760, 9847118.
71. Bokma E, Rozeboom HJ, Sibbald M, Dijkstra BW, Beintema JJ. Expression and characterization of active site mutants of hevamine, a chitinase from the rubber tree Hevea brasiliensis. Eur J Biochem 2002, 269:893-901. 10.1046/j.0014-2956.2001.02721.x, 11846790.
72. Broglie KE, Gaynor JJ, Broglie RM. Ethylene-regulated gene expression: molecular cloning of the genes encoding an endochitinase from Phaseolus vulgaris. Proc Natl Acad Sci USA 1986, 83:6820-6824. 10.1073/pnas.83.18.6820, 386601, 2428042.
73. Petruzzelli L, Kunz C, Waldvogel R, Meins FJ, Leubner-Metzger G. Distinct ethylene- and tissue-specific regulation of β-1,3-glucanases and chitinases during pea seed germination. Planta 1999, 209:195-201. 10.1007/s004250050622, 10436221.
74. Vorwerk S, Somerville S, Somerville C. The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 2004, 9:203-209. 10.1016/j.tplants.2004.02.005, 15063871.
75. Bae E-K, Lee H, Lee J-S, Noh E-W, Han M-S, Choi Y-I. Molecular cloning of a peroxidase gene from poplar and its differential expression in response to stress. Tree Physiol 2006, 26:1405-1412.
76. Chittoor JM, Leach JE, White FF. Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact 1997, 10:861-871. 10.1094/MPMI.1997.10.7.861, 9304860.
77. Choi HW, YJ K, Lee SC, Hong JK, Hwang BK. Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 2007, 145:890-904. 10.1104/pp.107.103325, 2048806, 17905862.
78. Delannoy E, Jalloul A, Assigbetse K, Marmey P, Geiger JP, Lherminier J, Daniel JF, Martinez C, Nicole M. Activity of class III peroxidases in the defense of cotton to bacterial blight. Mol Plant-Microbe Interact 2003, 16:1030-1038. 10.1094/MPMI.2003.16.11.1030, 14601671.
79. Kim Y-H, Yang K-S, Kim CY, Ryu S-H, Song W-K, Kwon S-Y, Lee H-S, Bang J-W, Kwak S-S. Molecular cloning of peroxidase cDNAs from dehydration-treated fibrous roots of sweetpotato and their differential expression in response to stress. J Biochem Mol Biol 2007, 41:259-265.
80. Hilaire E, A S, Young SA, Willard LH, McGee JD, Sweat T, Chittoor JM, Guikema JA, Leach JE. Vascular defense responses in rice: Peroxidase accumulation in xylem parenchyma cells and xylem wall thickening. Mol Plant-Microbe Interact 2001, 14:1411-1419. 10.1094/MPMI.2001.14.12.1411, 11768536.
81. Reimers PJ, Guo A, Leach JK. Increased activity of a cationic peroxidase associated with an incompatible interaction between Xanthomonas oryzae pv oryzae and Rice (Oryza sativa). Plant Physiol 1992, 99:1044-1050. 10.1104/pp.99.3.1044, 1080582, 16668969.
82. Young SA, Cuo A, Cuikema JA, White FF, Leach JE. Rice cationic peroxidase accumulates in xylem vessels during incompatible interactions with Xanthomonas oryzae pv oryzae. Plant Physiol 1995, 107:1333-1341. 10.1104/pp.107.4.1333, 157268, 7770527.
83. Christensen JH, Bauw G, Welinder KG, Van Montagu M, Boerjan W. Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol 1998, 118:125-135. 10.1104/pp.118.1.125, 34849, 9733532.
84. Christensen JH, Overney S, Rohde A, Diaz WA, Bauw G, Simon P, Van Montagu M, Boerjan W. The syringaldazine-oxidizing peroxidase PXP 3-4 from poplar xylem: cDNA isolation, characterization and expression. Plant Mol Biol 2001, 47:581-593. 10.1023/A:1012271729285, 11725944.
85. Li Y, Kajita S, Kawai S, Katayama Y, Morohoshi M. Down regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. J Plant Res 2003, 116:175-182. 10.1007/s10265-003-0087-5, 12836039.
86. Osakabe K, Koyama H, Kawai S, Katayama Y, Morohoshi N. Molecular cloning and the nucleotide sequences of two novel cDNAs that encode anionic peroxidases of Populus kitakamiensis. Plant Sci 1994, 103:167-175.
87. Osakabe K, Koyama H, Kawai S, Katayama Y, Morohoshi N. Molecular cloning of two tandemly arranged peroxidase genes from Populus kitakamiensis and their differential regulation in the stem. Plant Mol Biol 1995, 28:677-689. 10.1007/BF00021193, 7647300.
88. Sasaki S, Baba K, Nishida T, Tsutsumi Y, Kondo R. The cationic cell-wall-peroxidase having oxidation ability for polymeric substrate participates in the late stage of lignification of Populus alba L. Plant Mol Biol 2006, 62:797-807. 10.1007/s11103-006-9057-3, 17004015.
89. Sasaki S, Nishida T, Tsutsumi Y, Kondo R. Lignin dehydrogenative polymerization mechanism: a poplar cell wall peroxidase directly oxidizes polymer lignin and produces in vitro dehydrogenative polymer rich in b-O-4 linkage. FEBS Lett 2004, 562:197-201. 10.1016/S0014-5793(04)00224-8, 15044025.
90. Sasaki S, Shimizu M, Wariishi H, Tsutsumi Y, Kondo R. Transcriptional and translational analyses of poplar anionic peroxidase isoenzymes. J Wood Sci 2007, 53:427-435.
91. Takeuchi M, Takabe K, Minoru Fujita M. Immunolocalization of an anionic peroxidase in differentiating poplar xylem. J Wood Sci 2005, 51:317-322.
92. Bernards MA, Fleming WD, Llewellyn DB, Priefer R, Yang X, Sabatino A, Plourde GL. Biochemical characterization of the suberization-associated anionic peroxidase of potato. Plant Physiol 1999, 121:135-145. 10.1104/pp.121.1.135, 59361, 10482668.
93. Czaninski Y, Sachot RM, Catesson AM. Cytochemical localization of hydrogen peroxide in lignifying cell walls. Ann Bot 1993, 72:547-550.
94. Ros Barcelo A. Hydrogen peroxide production is a general property of the lignifying xylem from vascular plants. Ann Bot 1998, 82:97-103.
95. Ros Barcelo A. Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. Planta 2005, 220:747-756. 10.1007/s00425-004-1394-3, 15747145.
96. Ros Barcelo A, Gomez-Ros LV, Ferrer MA, Hernandez JA. The apoplastic antioxidant enzymatic system in the wood-forming tissues of trees. Trees 2006, 20:145-156.
97. Bolwell GP, Wojtaszek P. Mechanisms for the generation of reactive oxygen species in plant defence - a broad perspective. Physiol Mol Plant Pathol 1997, 51:347-366.
98. Kotchoni S, Gachomo EW. The reactive oxygen species network pathways: an essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. J Biosci 2006, 31:389-404. 10.1007/BF02704112, 17006022.
99. Levine A, Tenhaken R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 1994, 79:583-593. 10.1016/0092-8674(94)90544-4, 7954825.
100. Mellersh DG, Foulds IV, Higgins VJ, CM H. H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J 2002, 29:257-268. 10.1046/j.0960-7412.2001.01215.x, 11844104.
101. Vanacker H, Harbinson J, Ruisch J, Carver TLW, Foyer CH. Antioxidant defences of the apoplast. Protoplasma 1998, 205:129-140.
102. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002, 7:405-410. 10.1016/S1360-1385(02)02312-9, 12234732.
103. Moller IM, Jensen PE, Hansson A. Oxidative modification to cellular components in plants. Annu Rev Plant Biol 2007, 58:459-481. 10.1146/annurev.arplant.58.032806.103946, 17288534.
104. Pavet V, Olmos E, Kiddle G, Mowla S, Kumar S, Antoniw J, Alvarez ME, Foyer CH. Ascorbic acid deficiency activates cell death and disease resistance responses in Arabidopsis. Plant Physiol 2005, 139:1291-1303. 10.1104/pp.105.067686, 1283766, 16244149.
105. Montricharda F, Alkhalfiouib F, Yano F, Vensel WH, Hurkman WJ, Buchanan BB. Thioredoxin targets in plants: The first 30 years. J Proteomics 2009, 72:452-474. 10.1016/j.jprot.2008.12.002, 19135183.
106. Ishikawa T, Shigeoka S. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosysnthesizing organisms. Biosci Biotechnol Biochem 2008, 72:1143-1154. 10.1271/bbb.80062, 18460785.
107. Pignocchi C, Foyer CH. Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Curr Opin Plant Biol 2003, 6:379-389. 10.1016/S1369-5266(03)00069-4, 12873534.
108. Plomion C, Lalanne C, Claverol S, Meddour H, Kohler A, Bogeat-Triboulot M-B, Barre A, Le Provost G, Dumazet H, Jacob D, et al. Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 2006, 6:6509-6527. 10.1002/pmic.200600362, 17163438.
109. Srivastava V, Schinkel H, Witzell J, Hertzberg M, Torp M, Srivastava MK, Karpinska B, Melzer M, Wingsle G. Downregulation of high-isoelectric-point extracellular superoxide dismutase mediates alterations in the metabolism of reactive oxygen species and developmental disturbances in hybrid aspen. Plant J 2006, 49:135-148.
110. Thornalley PJ. The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 1990, 269:1-11. 1131522, 2198020.
111. Yadav SK, Singla-Pareek SL, Ray M, Reddy MK, Sopory SK. Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophysical Res Com 2005, 337:61-67.
112. Edwards R, Dixon DP, Walbot V. Plant glutathione S-transferases: enzymes with multiple functions in sickness and health. Trends Plant Sci 2000, 5:193-198. 10.1016/S1360-1385(00)01601-0, 10785664.
113. Jiang L, Yang H. Prometryne-induced oxidative stress and impact on antioxidant enzymes in wheat. Ecotoxicol Environ Saf 2009, 72:1687-1693. 10.1016/j.ecoenv.2009.04.025, 19473703.
114. Yin XL, Jiang L, Song NH, Yang H. Toxic reactivity of wheat (Triticum aestivum) plants to herbicide isoproturon. J Agric Food Chem 2008, 56:4825-4831. 10.1021/jf800795v, 18522406.
115. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 2000, 290:2110-2113. 10.1126/science.290.5499.2110, 11118138.
116. Kehr J, Rep M. Protein extraction from xylem and phloem sap. Plant Proteomics Methods and Protocols 2007, 355:27-35. Totowa, New Jersey: Humana Press, Thiellement H, Zivy M, Damerval C, Méchin V.
117. Hurkman WJ, Tanaka CK. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 1986, 81:802-806. 10.1104/pp.81.3.802, 1075430, 16664906.
118. Pechanova O, Stone WD, Monroe W, Nebeker TE, Klepzig KD, Yuceer C. Global and comparative protein profiles of the pronotum of the southern pine beetle, Dendroctonus frontalis. Insect Mol Biol 2008, 17:261-277. 10.1111/j.1365-2583.2008.00801.x, 18477241.
119. Nanduri B, Lawrence ML, Vanguri S, Pechan T, Burgess SC. Proteomic analysis using an unfinished bacterial genome: the effect of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 2005, 5:4852-4863. 10.1002/pmic.200500112, 16247735.
120. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene Ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29. 10.1038/75556, 10802651.
121. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 1997, 10:1-6. 10.1093/protein/10.1.1, 9051728.
122. Yuceer C, Land SB, Kubiske ME, Harkess RL. Shoot morphogenesis associated with flowering in Populus deltoides (SALICACEAE). Amer J Bot 2003, 90:196-206.
123. Wan CY, Wilkins TA. A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 1994, 223:7-12. 10.1006/abio.1994.1538, 7535022.
124. R Development Core Team R: A language and environment for statistical computing. 2008, Vienna, Austria: R Foundation for Statistical Computing, R Development Core Team.
125. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
126. MacDonald JW. Affycoretools: Functions useful for those doing repetitive analyses with Affymetrix GeneChips. R package version 1141 2005,
127. Wu Z, Irizarry RA. Stochastic models inspired by hybridization theory for short oligonucleotide arrays. J Comput Biol 2005, 12:882-893. 10.1089/cmb.2005.12.882, 16108723.
128. Smyth GK. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
129. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statist Appl in Gen Mol Biology 2004, 3(1):Article 3.
130. Langfelder P, Zhang B, Horvath S. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut library for R. Bioinformatics 2008, 24:719-720. 10.1093/bioinformatics/btm563, 18024473.
131. Hsu C-Y, Liu Y, Luthe DS, Yuceer C. Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 2006, 18:1846-1861. 10.1105/tpc.106.041038, 1533980, 16844908.
132. Larson PR, Isebrands JG. The plastochron index as applied to developmental studies of cottonwood. Can J For Res 1971, 1:1-11.
133. Boyle B, Levée V, Hamel L-P, Nicole M-C, Séguin A. Molecular and histochemical characterization of two distinct poplar Melampsora leaf rust pathosystems. Plant Biology 2010, 12:364-376. 10.1111/j.1438-8677.2009.00310.x, 20398242.
134. Rutledge RG, Stewart D. A kinetic-based sigmoidal model for the polymerase chain reaction and its application to high-capacity absolute quantitative real-time PCR. BMC Biotechnol 2008, 8:47. 10.1186/1472-6750-8-47, 2397388, 18466619.
135. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and 2-DDCt method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
136. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:research 0034.
137. Destefano-Beltrán L, Knauber D, Huckle L, Suttle JC. Effects of postharvest storage and dormancy status on ABA content, metabolism, and expression of genes involved in ABA biosynthesis and metabolism in potato tuber tissues. Plant Mol Biol 2006, 61:687-697. 10.1007/s11103-006-0042-7, 16897484.
138. Srivastava LM. Plant Growth and Development. Hormones and Environment. 2002, San Diego, CA, USA: Academic Press.
139. Magneschi L, Perata P. Rice germination and seedling growth in the absence of oxygen. Ann Bot 2009, 103:181-196. 10.1093/aob/mcn121, 2707302, 18660495.
140. Narsai R, Howell KA, Carroll A, Ivanova A, Millar AH, Whelan J. Defining core metabolic and transcriptomic responses to oxygen availability in rice embryos and young seedlings. Plant Physiol 2009, 151:306-322. 10.1104/pp.109.142026, 2736006, 19571305.
141. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP. The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Microbe Interact 2007, 20:816-831. 10.1094/MPMI-20-7-0816, 17601169.
142. Street NR, Skogstrom O, Sjodin A, Tucker J, Rodri{dotless}guez-Acosta R, Nilsson P, Jansson S, Taylor G. The genetics and genomics of the drought response in Populus. Plant J 2006, 48:321-341. 10.1111/j.1365-313X.2006.02864.x, 17005011.