Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa

Plant, Cell and Environment

Volumn 30, Issue 4, 2007, Pages 435-446

  Ingle, Robert A ^a   Schmidt, Ulrike G ^b   Farrant, Jill M ^a   Thomson, Jennifer A ^a   Mundree, Sagadevan G ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Desiccation tolerance; Photosynthesis; Poikilochlorophylly; Proteome

Indexed keywords

ALCOHOL DEHYDROGENASE; ENOLASE; PHOSPHOPROTEIN PHOSPHATASE; RNA BINDING PROTEIN; VEGETABLE PROTEIN; WATER;

DEHYDRATION; DESICCATION; ELECTROKINESIS; MASS SPECTROMETRY; MONOCOTYLEDON; PHENOTYPE; PHOTOSYNTHESIS; PROTEIN; PROTEOMICS; QUANTITATIVE ANALYSIS; RNA;

ANGIOSPERM; ARTICLE; COMPARATIVE STUDY; CRATEROSTIGMA; DESICCATION; GENE EXPRESSION PROFILING; METABOLISM; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEOMICS; THYLAKOID;

ALCOHOL DEHYDROGENASE; ANGIOSPERMS; CRATEROSTIGMA; DESICCATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION PROFILING; OXIDATIVE STRESS; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPYRUVATE HYDRATASE; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PROTEOMICS; RNA-BINDING PROTEINS; THYLAKOIDS; WATER;

CRATEROSTIGMA; CRATEROSTIGMA PLANTAGINEUM; MAGNOLIOPHYTA; SELAGINELLA PILIFERA; XEROPHYTA VISCOSA;

EID: 33847206119     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2006.01631.x     Document Type: Article

References (70)

1. Alpert P. (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? Journal of Experimental Botany 209, 1575-1584.
2. Baier M. & Dietz K.-J. (1999) Protective function of chloroplast 2-cysteine peroxiredoxin in photosynthesis. Evidence from transgenic Arabidopsis. Plant Physiology 119, 1407-1414.
3. Baier M., Stroher E. & Dietz K.-J. (2004) The acceptor availability at photosystem I and ABA control nuclear expression of 2-Cys peroxiredoxin-A in Arabidopsis thaliana. Plant & Cell Physiology 45, 997-1006.
4. Bailey S., Thompson E., Nixon P.J., Horton P., Mullineaux C.W., Robinson C. & Mann N.H. (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. Journal of Biological Chemistry 277, 2006-2011.
5. Bailly C. (2004) Active oxygen species and antioxidants in seed biology. Seed Science Research 14, 93-107.
6. Bartels D., Schneider K., Terstappen G., Piatkowski D. & Salamini F. (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181, 27-34.
7. Bernacchia G. & Furini A. (2004) Biochemical and molecular responses to water stress in resurrection plants. Physiologia Plantarum 121, 175-181.
8. Bernacchia G., Salamini F. & Bartels D. (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiology 111, 1043-1050.
9. Bianchi G., Gamba A., Murelli C., Salamini F. & Bartels D. (1991) Novel carbohydrate metabolism in the resurrection plant Craterostigma plantagineum. The Plant Journal 1, 355-359.
10. Blomstedt C.K., Gianello R.D., Gaff D.F., Hamill J.D. & Neale A.D. (1998) Differential gene expression in desiccation-tolerant and desiccation-sensitive tissue of the resurrection grass, Sporobolus stapfianus. Australian Journal of Plant Physiology 25, 937-946.
11. Bockel C., Salamini F. & Bartels D. (1998) Isolation and characterization of genes expressed during early events of the dehydration process in the resurrection plant Craterostigma plantagineum. Journal of Plant Physiology 152, 158-166.
12. de Bruxelles G.L., Peacock W.J., Dennis E.S. & Dolferus R. (1996) Abscisic acid induces the alcohol dehydrogenase gene in Arabidopsis. Plant Physiology 111, 381-391.
13. Buitink J. & Leprince O. (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48, 215-228.
14. Collett H., Butowt R., Smith J., Farrant J. & Illing N. (2003) Photosynthetic genes are differentially transcribed during the dehydration-rehydration cycle in the resurrection plant, Xerophyta humilis. Journal of Experimental Botany 54, 2593-2595.
15. Collett H., Shen A., Gardner M., Farrant J.M., Denby K.J. & Illing N. (2004) Towards transcript profiling of desiccation tolerance in Xerophyta humilis: construction of a normalized 11 k X. humilis cDNA set and microarray expression analysis of 424 cDNAs in response to dehydration. Physiologia Plantarum 122, 39-53.
16. Cooper K. & Farrant J.M. (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. Journal of Experimental Botany 53, 1805-1813.
17. Dace H., Sherwin H.W., Illing N. & Farrant J.M. (1998) Use of metabolic inhibitors to elucidate mechanisms of recovery from desiccation stress in the resurrection plant Xerophyta humilis. Plant Growth Regulation 24, 171-177.
18. Dhindsa R. & Bewley J. (1978) Messenger RNA is conserved during drying of the drought-tolerant moss Tortula ruralis. Proceedings of the National Academy of Science USA 75, 842-846.
19. Emanuelsson O., Nielsen H. & von Heijne G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science 8, 978-984.
20. Farrant J.M. (2000) A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecology 151, 29-39.
21. Gaff D. (1971) Desiccation-tolerant plants in Southern Africa. Science 174, 1033-1034.
22. Gosti F., Beaudoin N., Serizet C., Webb A.A.R., Vartanian N. & Giraudat J. (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11, 1897-1910.
23. Gygi S.P., Rochon Y., Franza B.R. & Aebersold R. (1999) Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology 19, 1720-1730.
24. Hakala M., Tuominen I., Keranen M., Tyystjarvi T. & Tyystjarvi E. (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1706, 68-80.
25. Himmelbach A., Yang Y. & Grill E. (2003) Relay and control of abscisic acid signaling. Current Opinion in Plant Biology 6, 470-479.
26. Hoekstra F.A., Golovina E.A., Tetteroo F.A.A. & Wolkers W.F. (2001) Induction of desiccation tolerance in plant somatic embryos: how exclusive is the protective role of sugars? Cryobiology 43, 140-150.
27. Horling F., Lamkemeyer P., Konig J., Finkemeier I., Kandlbinder A., Baier M. & Dietz K.-J. (2003) Divergent light-, ascorbate-, and oxidative stress-dependent regulation of expression of the peroxiredoxin gene family in Arabidopsis. Plant Physiology 131, 317-325.
28. Ideker T., Thorsson V., Ranish J.A., Christmas R., Buhler J., Eng J.K., Bumgarner R., Goodlett D.R., Aebersold R. & Hood L. (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934.
29. Illing N., Denby K.J., Collett H., Shen A. & Farrant J.M. (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integrative & Comparative Biology 45, 771-787.
30. Ingle R., Smith J. & Sweetlove L. (2005) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. Biometals 18, 627-641.
31. Ingram J. & Bartels D. (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377-403.
32. Ingram J., Chandler J.W., Gallagher L., Salamini F. & Bartels D. (1997) Analysis of cDNA clones encoding sucrose-phosphate synthase in relation to sugar interconversions associated with dehydration in the resurrection plant Craterostigma plantagineum Hochst. Plant Physiology 115, 113-121.
33. Jannson S. (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends in Plant Science 4, 236-240.
34. Liepman A.H. & Olsen L.J. (2003) Alanine aminotransferase homologs catalyze the glutamate:glyoxylate aminotransferase reaction in peroxisomes of Arabidopsis. Plant Physiology 131, 215-227.
35. Meurer J., Plücken H., Kowallik K. & Westhoff P. (1998) A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. European Molecular Biology Organisation Journal 17, 5286-5297.
36. Millar A.H., Sweetlove L.J., Giege P. & Leaver C.J. (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiology 127, 1711-1727.
37. Mittler R., Merquiol E., Hallak-Herr E., Rachmilevitch S., Kaplan A. & Cohen M. (2001) Living under a 'dormant' canopy: a molecular acclimation mechanism of the desert plant Retama raetam. The Plant Journal 25, 407-416.
38. Moore J., Westall K., Ravenscroft N., Farrant J., Lindsey G. & Brandt W. (2005) The predominant polyphenol in the leaves of the resurrection plant Myrothamnus flabellifolius, 3,4,5 tri-Ogalloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochemical Journal 385, 301-308.
39. Moore J.P., Nguema-Ona E., Chevalier L., Lindsey G.G., Brandt W.F., Lerouge P., Farrant J.M. & Driouich A. (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiology 141, 651-662.
40. Mowla S.B., Thomson J.A., Farrant J.M. & Mundree S.G. (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa Baker. Planta 215, 716-726.
41. Müller J., Boller T. & Wiemken A. (1995) Trehalose and trehalase in plants: recent developments. Plant Science 112, 1-9.
42. Mundree S.G. & Farrant J.M. (2000) Some physiological and molecular insights into the mechanisms of desiccation tolerance in the resurrection plant Xerophyta viscosa Baker. In Plant Tolerance to Abiotic Stresses in Agriculture: Role of Genetic Engineering (ed. J. Cherry), pp. 201-222. Kluwer Academic Publishers, Dordrecht, the Netherlands.
43. Mundree S.G., Whittaker A., Thomson J.A. & Farrant J.M. (2000) An aldose reductase homolog from the resurrection plant Xerophyta viscosa Baker. Planta 211, 693-700.
44. Nakamura T., Ohta M., Sugiura M. & Sugita M. (2001) Chloroplast ribonucleoproteins function as a stabilizing factor of ribosome-free mRNAs in the stroma. Journal of Biological Chemistry 276, 147-152.
45. Neale A.D., Blomstedt C.K., Bronson P., Le T.N., Guthridge K., Evans J., Gaff D.F. & Hamill J.D. (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant, Cell & Environment 23, 265-277.
46. Niyogi K.K., Li X.-P., Rosenberg V. & Jung H.-S. (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? Journal of Experimental Botany 56, 375-382.
47. Ohnishi N., Allakhverdiev S.I., Takahashi S., Higashi S., Watanabe M., Nishiyama Y. & Murata N. (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44, 8494-8499.
48. Oliver M.J. & Bewley J. (1984) Plant desiccation and protein synthesis: VI. Changes in protein synthesis elicited by desiccation of the moss Tortula ruralis are effected at the translational level. Plant Physiology 74, 923-927.
49. Oliver M.J. & Bewley J. (1997) Desiccation tolerance of plant tissues: a mechanistic overview. Horticultural Reviews 18, 171-214.
50. Oliver M.J., Tuba Z. & Mishler B. (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecology 151, 85-100.
51. Oliver M.J., Dowd S.E., Zaragoza J., Mauget S.A. & Payton P.R. (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5, 89.
52. Ostersetzer O. & Adam Z. (1997) Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell 9, 957-965.
53. Panchuk I., Zentgraf U. & Volkov R. (2005) Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana. Planta 222, 926-932.
54. Röhrig H., Schmidt J., Colby T., Brautigam A., Hufnagel P. & Bartels D. (2006) Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation. Plant, Cell & Environment 29, 1606-1617.
55. Sakamoto W., Zaltsman A., Adam Z. & Takahashi Y. (2003) Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15, 2843-2855.
56. Sherwin H.W. & Farrant J.M. (1996) Differences in rehydration of three desiccation-tolerant angiosperm species. Annals of Botany 78, 703-710.
57. Sherwin H.W. & Farrant J.M. (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regulation 24, 203-210.
58. Smirnoff N. (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125, 27-58.
59. Suzuki I., Simon W.J. & Slabas A.R. (2006) The heat shock response of Synechocystis sp. PCC 6803 analysed by transcriptomics and proteomics. Journal of Experimental Botany 57, 1573-1578.
60. Vander Willigen C., Pammenter N.W., Mundree S.G. & Farrant J.M. (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartmentalization of subcellular components and metabolites play a role? Journal of Experimental Botany 55, 651-661.
61. Vicré M., Farrant J.M. & Driouich A. (2004a) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant, Cell & Environment 27, 1329-1340.
62. Vicré M., Lerouxel O., Farrant J.M., Lerouge P. & Driouich A. (2004b) Composition and desiccation-induced alterations of the cell wall in the resurrection plant Craterostigma wilmsii. Physiologia Plantarum 120, 229-239.
63. Wang S.Y., Jiao H.J. & Faust M. (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron-induced bud break of apple. Physiologia Plantarum 82, 231-236.
64. Whittaker A., Bochicchio A., Vazzana C., Lindsey G. & Farrant J. (2001) Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. Journal of Experimental Botany 52, 961-969.
65. Wolucka B.A. & Van Montagu M. (2003) GDP-mannose 3′,5′- epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. Journal of Biological Chemistry 278, 47483-47490.
66. Wolucka B.A., Persiau G., Van Doorsselaere J., Davey M.W., Demol H., Vandekerckhove J., Van Montagu M., Zabeau M. & Boerjan W. (2001) Partial purification and identification of GDP-mannose 3,′5′-epimerase of Arabidopsis thaliana, a key enzyme of the plant vitamin C pathway. Proceedings of the National Academy of Science USA 98, 14843-14848.
67. Wolucka B.A., Goossens A. & Inze D. (2005) Methyl jasmonate stimulates the de novo biosynthesis of vitamin C in plant cell suspensions. Journal of Experimental Botany 56, 2527-2538.
68. Wood A.J., Duff R.J. & Oliver M.J. (1999) Expressed sequence tags (ESTs) from desiccated Tortula ruralis identify a large number of novel plant genes. Plant & Cell Physiology 40, 361-368.
69. Yu F., Park S. & Rodermel S.R. (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. The Plant Journal 37, 864-876.
70. Zaltsman A., Ori N. & Adam Z. (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17, 2782-2790.