Proteomic analysis of β-aminobutyric acid priming and abscisic Acid - Induction of drought resistance in crabapple (Malus pumila): Effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes

Plant, Cell and Environment

Volumn 32, Issue 11, 2009, Pages 1612-1631

  MacArisin, Dumitru ^a   Wisniewski, Michael E ^a   Bassett, Carole ^a   Thannhauser, Theodore W ^b  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Drought stress; Lignin biosynthesis; Pectin methylesterase; Rosaceae; Woody plants

Indexed keywords

ABSCISIC ACID; DECIDUOUS TREE; DROUGHT RESISTANCE; ELECTROKINESIS; ENZYME ACTIVITY; FRUIT; LIGNIN; METABOLISM; PHYTOCHEMISTRY; PROTEIN; PROTEOMICS; SEEDLING; WOODY PLANT;

MALUS PUMILA; MALUS X DOMESTICA; ROSACEAE;

EID: 70349858123     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2009.02025.x     Document Type: Article

References (86)

1. Abernethy G.A. McManus M.T. (1998) Biochemical responses to an imposed water deficit in mature leaf tissue of Festuca arundinacea. Environmental and Experimental Botany 40, 17 28.
2. Al-Qsous S., Carpentier E., Klein-Eude D., Burel C., Mareck A., Dauchel H., Gomord V. Balange A.P. (2004) Identification and isolation of a pectin methylesterase isoform that could be involved in flax cell wall stiffening. Planta 219, 369 378.
3. Alvarez S., Marsh E., Schroeder S. Schachtman D. (2008) Metabolomic and proteomic changes in the xylem sap of maize under drought. Plant, Cell & Envrionment 31, 325 340.
4. Amzalek E. Cohen Y. (2007) Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology 97, 179 186.
5. Arakawa K., Mizuno K., Kishitani S. Takabe T. (1992) Immunological studies of betaine aldehyde dehydrogenase in barley. Plant & Cell Physiology 33, 833 840.
6. Bosch M., Cheung A.Y. Hepler P.K. (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiology 138, 1334 1346.
7. Bray E.A., Bailey-Serres J. Weretilnyk E. (2000) Responses to abiotic stresses Biochemistry and Molecular Biology of Plants (eds W. Gruissem, B. Buchannan R. Jones pp. 1158 1249. American Society of Plant Physiologists, Rockville, MD, USA.
8. Chang S., Puryear J.D., Dias M.A.D.L., Funkhouser E.A., Newton R.J. Cairney J. (1995) Gene expression under water deficit in loblolly pine (Pinus taeda L.): isolation and characterization of cDNA clones. Physiologia Plantarum 95, 1 10.
9. Conrath U., Beckers J., Flors V., et al. (2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062 1071.
10. Derbyshire P., McCann M.C. Roberts K. (2007) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biology 7, 31.
11. Dixon R. Paiva N.L. (1995) Stress-induced phenylpropanoid metabolism. The Plant Cell 7, 1085 1097.
12. Espartero J., Pintor-Toro J.A. Pardo J.M. (1994) Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Molecular Biology 25, 217 227.
13. Flexas J., Bota J., Cifre J., et al. (2004) Understanding down-regulation of photosynthesis under water stress: future prospects and searching for physiological tools for irrigation management. Annals of Applied Biology 144, 273 283.
14. Gao X.P., Pan Q.H., Li M.J., Zhang L.Y., Wang X.F., Shen Y.Y., Lu Y.F., Chen S.W., Liang Z. Zhang D.P. (2004) Abscisic acid is involved in the water stress-induced betaine accumulation in pear leaves. Plant & Cell Physiology 45, 742 750. (Pubitemid 38893498)
15. Grant G.T., Morris E.R., Rees D.A., Smith P.J.C. Thorn D. (1973) Biological interactions between polysaccharides and divalent cations: the egg-box model. FEBS Letters 32, 195 198.
16. Griffith M. Ewart K.V. (1995) Antifreeze proteins and their potential use in frozen foods. Biotechnology Advances 13, 375 402.
17. Hamiduzzaman M.M., Jakab G., Barnavon L., Neuhaus J.-M. Mauch-Mani B. (2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Molecular Plant-Microbe Interactions 18, 819 829.
18. Hasunuma T., Fukusaki E. Kobayashi A. (2004) Expression of a fungal pectin methylesterase in transgenic tobacco leads to alteration in cell wall metabolism and a dwarf phenotype. Journal of Biotechnology 111, 241 251.
19. Heil M. (2002) Ecological costs of induced resistance. Current Opinions in Plant Biology 5, 345 350.
20. Holmstrom K.O., Mantyla E., Welin B., Mandal A., Palva E.T., Tunnela O.E. Londesborough J. (1996) Drought tolerance in tobacco. Nature 379, 683 684.
21. Humphreys J.M. Chapple C. (2002) Rewriting the lignin roadmap. Current Opinions in Plant Biology 5, 224 229.
22. Husaini A.M. Abdin M.Z. (2008) Development of transgenic strawberry (Fragaria × ananassa Duch.) plants tolerant to salt stress. Plant Science 174, 446 455.
23. Ifuku K., Yamamoto Y., Ono T.A., Ishihara S. Sato F. (2005) PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. Plant Physiology 139, 1175 1184.
24. Ingram J. Bartels D. (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology & Molecular Biology 47, 377 403.
25. Ishitani M., Nakamura T., Youn-Han S. Takabe T. (1995) Expression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Molecular Biology 27, 307 315.
26. Jagendorf A.T. Takabe T. (2001) Inducers of glycinebetaine synthesis in barley. Plant Physiology 127, 1827 1835.
27. Jakab G., Cottier V., Toquin V., Rigoli G., Zimmerli L., Metraux J.P. Mauch-Mani B. (2001) β-Aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology 107, 29 37.
28. Jakab G., Ton J., Flors V., Zimmerli L., Metraux J.P. Mauch-Mani B. (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology 139, 267 274.
29. Jarvis M.C. (1984) Structure and properties of pectin gels in plant cell walls. Plant, Cell & Environment 7, 153 164.
30. Jarvis M.C., Briggs S.P.H. Knox J.P. (2003) Intercellular adhesion and cell separation in plants. Plant, Cell & Environment 26, 977 989.
31. Jolivet Y., Larher F. Hamelin J. (1982) Osmoregulation in halophytic higher plants: the protective effect of glycinebetaine against the heat destabilization of membranes. Plant Science Letters 25, 193 201.
32. Jorge I., Navarro R.M., Lenz C., Ariza D. Jorrín J. (2006) Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress. Proteomics 6, S207 S214.
33. Kang H.M. Saltveit M.E. (2002) Chilling tolerance of maize, cucumber and reice seeling leaves and roots are differentially affected by salicylic acid. Physiologia Plantarum 115, 571 576.
34. Kawalleck P., Plesch G., Hahlbrock K. Somssich E. (1992) Induction by fungal elicitor of S-adenosyl-l-methionine synthetase and S-adenosyl-l- homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proceedings of the National Academy of Sciences of the United States of America 89, 4713 4717.
35. Lee B.-K., Jung W.-J, Lee B.-H., Avice J.-C., Ourry A. Kim T.-H. (2008) Kinetics of drought-induced pathogenesis-related proteins and its physiological significance in white clover leaves. Physiologia Plantarum 132, 329 337.
36. Mathesius U., Keijzers G., Natera S., Weinman J., Djordjevic M. Rolfe B. (2001) Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 1, 1424 1440.
37. Maury S., Geoffroy P. Legrand M. (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoylcoenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiology 121, 215 223.
38. Micheli F. (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends in Plant Science 6, 414 419.
39. Murata N., Mohanty P.S., Hayashi H. Papageorgiou G.C. (1992) Glycine betaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Letters 296, 187 189.
40. Nakamura T., Nomura M., Mori H., Jagendorf A.T., Ueda A. Takabe T. (2001) An isozyme of betaine aldehyde dehydrogenase in barley. Plant & Cell Physiology 42, 1088 1092.
41. Papageorgiou C. Murata N. (1995) The unusually strong stabilizing effects of glycinebetaine on the structure and function in the oxygen-evolving photosystem II complex. Photosynthesis Research 44, 243 252.
42. Peleman J., Boerjan W., Engler G.J., Seurinck J., Botterman J., Alliote T., Van Montagu M. Inzé D. (1989) Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. The Plant Cell 1, 81 93.
43. Phan T., Bo W., West G., Lycett G. Tucker G. (2007) Silencing of the major salt-dependent isoform of pectinesterase in tomato alters fruit softening. Plant Physiology 144, 1960 1967.
44. Pichler F., Walton E., Davy M., Triggs C., Janssen B., Wünsche J., Putterill J. Schaffer R. (2007) Relative developmental, environmental, and tree-to-tree variability in buds from field-grown apple trees. Tree Genetics & Genomes 3, 329 339.
45. Pilling J., Willmitzer L., Bucking H. Fisahn J. (2004) Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta 219, 32 40.
46. Plomion C., Lalanne C., Claverol S., et al. (2006) Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 6, 6509 6527.
47. Rajashekar C.B., Zhou H., Marcum K.B. Prakash O. (1999) Glycine betaine accumulation and induction of cold tolerance in strawberry plants. Plant Science 148, 175 183.
48. Renaut J., Hausman J.-F., Bassett C., Artlip T., Cauchie H.-M., Witters E. Wisniewski M. (2008) Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genetics & Genomes 4, 589 600.
49. Rezzonico E., Flury N., Meins F. Beffa R. (1998) Transcriptional down-regulation by abscisic acid of pathogenesis-related β-1,3-glucanase genes in tobacco cell cultures. Plant Physiology 117, 585 592.
50. Riccardi F., Gazeau P., de Vienne D. Zivy M. (1998) Protein changes in response to progressive water deficit in maize. Quantitative variation and polypeptide identification. Plant Physiology 117, 1253 1263.
51. Roeckner E. (1992) Past, present and future levels of greenhouse gases in the atmosphere and model projections of related climatic changes. Journal of Experimental Botany 43, 1097 1109.
52. Saher S., Piqueras A., Hellin E. Olmos E. (2005) Pectin methyl esterases and pectins in normal and hyperhydric shoots of carnation cultured in vitro. Plant Physiology & Biochemistry 43, 155 159.
53. Saneoka H., Ishiguro S. Moghaieb R.E.A. (2001) Effect of salinity and abscisic acid on accumulation of glycinebetaine and betaine aldehyde dehydrogenase mRNA in sorghum leaves. Journal of Plant Physiology 158, 853 859.
54. Saravanan R. Rose J.K.C. (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4, 2522 2532.
55. Schmitt D., Pakusch A.E. Matern U. (1991) Molecular cloning, induction, and taxonomic distribution of caffeoyl-CoA 3-O-methyltransferase, an enzyme involved in disease resistance. Journal of Biological Chemistry 266, 17416 17423.
56. Shakirova F.M., Sakhabutdinova A.R., Bezrukova M.V., Fatkhutdinova R.A. Fatkhutdinova D.R. (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Science 164, 317 322.
57. Shinozaki K. Yamaguchi-Shinozaki K. (2007) Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221 227.
58. Siedlecka A., Wiklund S., Péronne M.-A., Micheli F., Lesniewska J., Sethson I., Edlund U., Richard L., Sundberg B. Mellerowicz E. (2008) Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiology 146, 554 565.
59. Sircelj H., Tausz M., Grill D. Batic F. (2007) Detecting different levels of drought stress in apple trees (Malus domestica Borkh.) with selected biochemical and physiological parameters. Scientia Horticulturae 113, 362 369.
60. Sjodin A., Bylesjo M., Skogstro O., Eriksson D., Nilsson P., Ryde P., Jansson S. Karlsson J. (2006) UPSC-BASE - Populus transcriptomics online. The Plant Journal 48, 806 817.
61. Skynner H.A., Rosahl T.W., Knowles M.R., Salim K., Reid L., Cothliff R., McAllister G. Guest P.C. (2002) Alterations of stress related proteins in genetically altered mice revealed by two-dimensional differential in-gel electrophoresis analysis. Proteomics 2, 1018 1025.
62. Sobry S., Havelange A. Van Cutsem P. (2005) Immunocytochemistry of pectins in shoot apical meristems: consequences for intercellular adhesion. Protoplasma 225, 15 22.
63. Tabuchi T., Kawaguchi Y., Azuma T., Nanmori T. Yasuda T. (2005) Similar regulation patterns of choline monooxygenase, phosphoethanolamine N-methyltransferase and S-adenosyl-L-methionine synthetase in leaves of the halophyte Atriplex nummularia L. Plant & Cell Physiology 46, 505 513.
64. Ton J. Mauch-Mani B. (2004) Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. The Plant Journal 38, 119 130.
65. Ton J., Jakab G., Toquin V., Flors V., Iavicoli A., Maeder M., Metraux J.P. Mauch-Mani B. (2005) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. The Plant Cell 17, 987 999.
66. Toquin V., Grausem B., Geoffroy P. Legrand M. (2003) Structure of the tobacco caffeic acid O-methyltransferase (COMT) II gene: identification of promoter sequences involved in gene inducibility by various stimuli. Plant Molecular Biology 52, 495 509.
67. Umezawa T., Fujita M., Fujita Y., Yamaguchi-Shinozaki K. Shinozaki K. (2006) Engineering drought tolerance in plants: discovering and tailoring genes unlock the future. Current Opinions in Biotechnology 17, 113 122.
68. Vincent D., Lapierre C., Pollet B., Cornic G., Negroni L. Zivy M. (2005) Water deficits affect caffeate o-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiology 137, 949 960.
69. Wang W., Scali M., Vignani R., Spadafora A., Sensi E., Mazzuca S. Cresti M. (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24, 2369 2375.
70. Wang Y., Wisniewski M., Meilan R., Cui M. Fuchigami L. (2006) Transgenic tomato (Lycopersicon esculentum) overexpressing cAPX exhibits enhanced tolerance to UV-B and heat stress. Journal of Applied Horticulture 8, 87 90.
71. Wang Y., Meilan R., Wisniewski M., Uratsu S.L., Cui M., Dandekar A. Fuchigami L. (2007) Ectopic expression of Mn-SOD in Lycopersicon esculentum leads to enhanced tolerance to salt and oxidative stress. Journal of Applied Horticulture 9, 3 8.
72. Wen F., Zhu Y. Hawes M. (1999) Effect of pectin methylesterase gene expression on pea root development. The Plant Cell 11, 1129 1140.
73. Wen X.P., Pang X.M., Matsuda N., Kita M., Inoue H., Hao Y.J., Honda C. Moriguchi T. (2008) Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Research 17, 251 263.
74. Wisniewski M., Bassett C. Arora R. (2004) Distribution and partial characterization of seasonally expressed proteins in different aged shoots and roots of 'Loring' peach (Prunus persica L. Batsch). Tree Physiology 24, 339 345.
75. Wisniewski M., Bassett C., Norelli J., Macarisin D., Artlip T., Gasic K. Korban S. (2008) Expressed sequence tag analysis of the response of apple (Malus domestica'Royal Gala') to low temperature and water deficit. Physiologia Plantarum 133, 298 317.
76. Wyn J. (1984) Phytochemical aspects of osmotic adaptation. Recent Advances in Phytochemistry 18, 55 78.
77. Xing W.B. Rajashekar C.B. (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Enviromental and Experimental Botany 46, 21 28.
78. Yang Y., Thannhauser T.W., Li L. Zhang S. (2007) Development of an integrated approach for evaluation of 2-D gel image analysis: impact of multiple proteins in single spots on comparative proteomics in conventional 2-D gel/MALDI workflow. Electrophoresis 28, 2080 2094.
79. Yeh S., Moffatt B.A., Griffith M., et al. (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiology 124, 1251 1264.
80. Zhang J.Z., Creelman R.A. Zhu J.K. (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiology 135, 615 621.
81. Zhao Y., Aspinall D. Paleg L.G. (1992) Protection of membrane integrity in Medicago sativa L. by glycinebetaine against the effects of freezing. Journal of Plant Physiology 140, 541 543.
82. Zimmerli L., Jakab G., Metraux J.P. Mauch-Mani B. (2000) Potentiation of pathogen-specific defence mechanisms in Arabidopsis by beta-aminobutyric acid. Proceedings of the National Academy of Sciences of the United States of America. 97, 12920 12925.
83. Zimmerli L., Metraux J.P. Mauch-Mani B. (2001) Beta-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiology. 126, 517 523.
84. Zimmerli L., Hou B.-H., Tsai C.-H., Jakab G., Mauch-Mani B. Somerville S. (2008) The xenobiotic β-aminobutyric acid enhances Arabidopsis thermotolerance. The Plant Journal 53, 144 156.
85. Zimmermann P., Hirsch-Hoffmann M., Hennig L. Gruissem W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621 2632.
86. Zubieta C., He X.Z., Dixon R.A. Noel J.P. (2001) Structures of two natural product methyltransferases reveal the basis for substrate specificity in plant O-methyltransferases. Nature Structural and Molecular Biology 8, 271 279.