Proteome analysis of Physcomitrella patens exposed to progressive dehydration and rehydration

Journal of Experimental Botany

Volumn 63, Issue 2, 2012, Pages 711-726

  Cui, Suxia ^a   Hu, Jia ^a   Guo, Shilei ^a   Wang, Jie ^b   Cheng, Yali ^a   Dang, Xinxing ^a   Wu, Lili ^a   He, Yikun ^a  

^a CAPITAL NORMAL UNIVERSITY   (China)

^b NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

Author keywords

2D DIGE; dehydration tolerance; LEA proteins; moss; Physcomitrella patens; proteome profiling; rehydration

Indexed keywords

LATE EMBRYOGENESIS ABUNDANT PROTEIN, PLANT; PROTEOME; VEGETABLE PROTEIN; WATER;

ADAPTATION; ARTICLE; BRYOPSIDA; DEHYDRATION; DESICCATION; DOWN REGULATION; FLUID THERAPY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; PLANT LEAF; PLANT SEED; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UPREGULATION;

ADAPTATION, PHYSIOLOGICAL; BRYOPSIDA; DEHYDRATION; DESICCATION; DOWN-REGULATION; FLUID THERAPY; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; PLANT PROTEINS; PLANT SHOOTS; PROTEOME; PROTEOMICS; SEEDS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UP-REGULATION; WATER;

BRYOPHYTA; MAGNOLIOPHYTA; PHYSCOMITRELLA; PHYSCOMITRELLA PATENS;

EID: 84862970490     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err296     Document Type: Article

References (75)

1. Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE. 1998. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annual Review of Ecology and Systematics 29, 263-292. (Pubitemid 29033033)
2. Bevan M, Bancroft I, Bent E, et al. 1998. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391, 485-488. (Pubitemid 28086548)
3. Bogunovic B, Stojakovic M, Chen L, Maric M. 2008. An unexpected functional link between lysosomal thiol reductase and mitochondrial manganese superoxide dismutase. Journal of Biological Chemistry 283, 8855-8862.
4. Bray EA. 1994. Alteration in gene expression in response to water deficit. USA: Harwood Academic Publishers.
5. Brock BJ, Gold MH. 1996. 1,4-benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium: spectral and kinetic analysis. Archives of Biochemistry and Biophysics 331, 31-40. (Pubitemid 26230616)
6. Browne J, Tunnacliffe A, Burnell A. 2002. Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416, 38-38.
7. Buchanan BB, Gruissem W, Jones RL. 2000. Biochemistry and molecular biology of plants. Rockville: American Society of Plant Physiologists.
8. Campbell SA, Close TJ. 1997. Dehydrins: genes, proteins, and associations with phenotypic traits. New Phytologist 137, 61-74. (Pubitemid 27490833)
9. Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A. 2007. Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proceedings of the National Academy of Sciences, USA 104, 18073-18078. (Pubitemid 350210822)
10. Chen M, Zhao K, Sun YL, Cui SX, Zhang LF, Yang B, Wang J, Kuang TY, Huang F. 2010. Proteomic analysis of hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Journal of Proteome Research 9, 3854-3866.
11. Cho S, Hoang Q, Kim Y, Shin H, Ok S, Bae J, Shin J. 2006. Proteome analysis of gametophores identified a metallothionein involved in various abiotic stress responses in Physcomitrella patens. Plant Cell Reports 25, 475-488.
12. Choi G, Yi H, Lee J, Kwon Y-K, Soo Soh M, Shin B, Luka Z, Hahn T-R, Song P-S. 1999. Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401, 610-613.
13. Close TJ. 1996. Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiologia Plantarum 97, 795-803. (Pubitemid 27093675)
14. Close TJ. 1997. Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiologia Plantarum 100, 291-296. (Pubitemid 27274905)
15. Close TJ, Fenton RD, Yang A, Asghar R, DeMason DA, Crone DE, Meyer NC, Moonan F. 1993. Dehydrin: the protein. In: Close TJ, Bray EA, eds. Plant responses to cellular dehydration during environmental stress. USA: American Society of Plant Physiologists, 104-118.
16. Close TJ, Kortt AA, Chandler PM. 1989. A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Molecular Biology 13, 95-108.
17. Cui S, Hu J, Yang B, Shi L, Huang F, Tsai SN, Ngai SM, He Y, Zhang J. 2009. Proteomic characterization of Phragmites communis in ecotypes of swamp and desert dune. Proteomics 9, 3950-3967.
18. Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J. 2005. A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5, 3162-3172. (Pubitemid 41176484)
19. Cuming AC, Cho SH, Kamisugi Y, Graham H, Quatrano RS. 2007. Microarray analysis of transcriptional responses to abscisic acid and osmotic, salt, and drought stress in the moss. Physcomitrella patens. New Phytologist 176, 275-287. (Pubitemid 47480890)
20. Cuming AC. 1999. LEA proteins. Dordrecht, Netherlands: Kluwer Academic Publishers.
21. Dure L. 1993. A repeating 11-mer amino acid motif and plant desiccation. The Plant Journal 3, 363-369.
22. Dure L. 2001. Occurrence of a repeating 11-mer amino acid sequence motif in diverse organisms. Protein and Peptide Letters 8, 115-122.
23. Dure L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung ZR. 1989. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Molecular Biology 12, 475-486.
24. Eisenhaber B, Wildpaner M, Schultz CJ, Borner GHH, Dupree P, Eisenhaber F. 2003. Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence-and genome-wide studies for arabidopsis and rice. Plant Physiology 133, 1691-1701. (Pubitemid 38047300)
25. Ernster L, Estabrook RW, Hochstein P. 1987. DT diaphorase, a quinone reductase with special functions in cell metabolism and detoxification. Cambridge: Cambridge University Press.
26. Frank W, Ratnadewi D, Reski R. 2005. Physcomitrella patens is highly tolerant against drought, salt and osmotic stress. Planta 220, 384-394. (Pubitemid 40564240)
27. Frayne J, McMillen A, Love S, Hall L. 1998. Expression of phosphatidylethanolamine-binding protein in the male reproductive tract: immunolocalisation and expression in prepubertal and adult rat testes and epididymides. Molecular Reproduction and Development 49, 454-460. (Pubitemid 28114792)
28. Gal TZ, Glazer I, Koltai H. 2004. An LEA group 3 family member is involved in the survival of C. elegans during exposure to stress. FEBS Letters 577, 21-26. (Pubitemid 39456419)
29. Gornall AG, Bardawill CJ, David MM. 1949. Determination of serum proteins by means of the biuret reaction. Journal Biological Chemistry 177, 751-766.
30. Hartl FU. 1996. Molecular chaperones in cellular protein folding. Nature 381, 571-580. (Pubitemid 26177472)
31. Hedman H, Kallman T, Lagercrantz U. 2009. Early evolution of the MFT-like gene family in plants. Plant Molecular Biology 70, 359-369.
32. Hoang QT, Cho SH, McDaniel SF, Ok SH, Quatrano RS, Shin JS. 2009. An actinoporin plays a key role in water stress in the moss. Physcomitrella patens. New Phytologist 184, 502-510.
33. Hundertmark M, Hincha DK. 2008. LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9.
34. 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.
35. Khalifah RG. 1971. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. Journal Biological Chemistry 246, 2561-2573.
36. Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud PF, Pan A, Quatrano RS. 2010. Role of ABA and ABI3 in desiccation tolerance. Science 327, 546-546.
37. Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389, 33-39. (Pubitemid 27387682)
38. Lamport DTA, Kieliszewski MJ, Showalter AM. 2006. Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytologist 169, 479-492.
39. Lundstrom-Ljung J, Holmgren A. 1998. Prolyl hydroxylase, protein-disulfide isomerase and other structurally related proteins. New York: Dekker.
40. Matvienko M, Wojtowicz A, Wrobel R, Jamison D, Goldwasser Y, Yoder JI. 2001. Quinone oxidoreductase message levels are differentially regulated in parasitic and non-parasitic plants exposed to allelopathic quinones. The Plant Journal 25, 375-387. (Pubitemid 32235071)
41. Mayaba N, Beckett RP, Csintalan Z, Tuba Z. 2001. ABA increases the desiccation tolerance of photosynthesis in the afromontane understorey moss Atrichum androgynum. Annals of Botany 88, 1093-1100. (Pubitemid 34115568)
42. Mayaba N, Minibayeva F, Beckett RP. 2002. An oxidative burst of hydrogen peroxide during rehydration following desiccation in the moss Atrichum androgynum. New Phytologist 155, 275-283. (Pubitemid 34838055)
43. Moore C, Perry AC, Love S, Hall L. 1996. Sequence analysis and immunolocalisation of phosphatidylethanolamine binding protein (PBP) in human brain tissue. Molecular Brain Research 37, 74-78. (Pubitemid 26147976)
44. Moore JP, Le NT, Brandt WF, Driouich A, Farrant JM. 2009. Towards a systems-based understanding of plant desiccation tolerance. Trends in Plant Science 14, 110-117.
45. Moriarty-Craige SE, Jones DP. 2004. Extracellular thiols and thiol/disulfide redox in metabolism. Annual Review of Nutrition 24, 481-509. (Pubitemid 38938801)
46. Moroney JV, Bartlett SG, Samuelsson G. 2001. Carbonic anhydrases in plants and algae. Plant, Cell and Environment 24, 141-153.
47. Munnik T, Meijerter Riet HJG, ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A. 2000. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. The Plant Journal 22, 147-154.
48. Nishiyama T, Hiwatashi Y, Sakakibara K, Kato M, Hasebe M. 2000. Tagged mutagenesis and gene-trap in the moss Physcomitrella patens by shuttle mutagenesis. DNA Research 7, 9-17.
49. Nylander M, Svensson J, Palva ET, Welin BV. 2001. Stress-induced accumulation and tissue-specific localization of dehydrins in. Arabidopsis thaliana. Plant Molecular Biology 45, 263-279. (Pubitemid 32235166)
50. Oldenhof H, Wolkers WF, Bowman JL, Tablin F, Crowe JH. 2006. Freezing and desiccation tolerance in the moss Physcomitrella patens: an in situ Fourier transform infrared spectroscopic study. Biochimica et Biophysica Acta 1760, 1226-1234. (Pubitemid 43928258)
51. Oliver MJ. 1991. Influence of protoplasmic water loss on the control of protein synthesis in the desiccation-tolerant moss Tortula ruralis: ramifications for a repair-based mechanism of desiccation tolerance. Plant Physiology 97, 1501-1511. (Pubitemid 21914394)
52. Oliver MJ, Bewley JD. 1997. Desiccation-tolerance of plant tissues: a mechanistic overview: John Wiley & Sons, Inc.
53. Oliver MJ, Velten J, Mishler BD. 2005. Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integrative and Comparative Biology 45, 788-799. (Pubitemid 43098211)
54. Proctor MCF, Ligrone R, Duckett JG. 2007. Desiccation tolerance in the moss Polytrichum formosum: physiological and fine-structural changes during desiccation and recovery. Annals of Botany 99, 75-93. (Pubitemid 47355455)
55. Qiu YL, Li LB, Wang B, et al. 2006. The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences, USA 103, 15511-15516. (Pubitemid 44625623)
56. Rensing SA, Lang D, Zimmer AD, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64-69.
57. Rinne PLH, Kaikuranta PLM, van der Plas LHW, van der Schoot C. 1999. Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209, 377-388.
58. Robertson M, Chandler PM. 1994. A dehydrin cognate protein from pea (Pisum sativum L.) with an atypical pattern of expression. Plant Molecular Biology 26, 805-816.
59. Ruelland E, Cantrel C, Gawer M, Kader JC, Zachowski A. 2002. Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiology 130, 999-1007. (Pubitemid 35224799)
60. Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S. 2006. A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. The Plant Journal 45, 237-249. (Pubitemid 43382056)
61. Sanchez-Ballesta MT, Rodrigo MJ, LaFuente MT, Granell A, Zacarias L. 2004. Dehydrin from citrus, which confers in vitro dehydration and freezing protection activity, is constitutive and highly expressed in the flavedo of fruit but responsive to cold and water stress in leaves. Journal of Agricultural and Food Chemistry 52, 1950-1957.
62. Sarnighausen E, Wurtz V, Heintz D, Van Dorsselaer A, Reski R. 2004. Mapping of the Physcomitrella patens proteome. Phytochemistry 65, 1589-1607. (Pubitemid 38969940)
63. Schultz CJ, Johnson KL, Currie G, Bacic A. 2000. The classical arabinogalactan protein gene family of arabidopsis. The Plant Cell 12, 1751-1767.
64. Seitz M, Park CK, Wong JY, Israelachvili JN. 1999. Study of the fusion process between solid and soft-supported phospholipid bilayers with the surface forces apparatus. In: Manne S, Warr GG, eds. Supramolecular structure in confined geometries, Vol. 736. American Chemical Society, 215-230. (Pubitemid 129557972)
65. Shih MD, Hoekstra FA, Hsing YIC. 2008. Late embryogenesis abundant proteins. Advances in Botanical Research 48, 211-255.
66. Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P, Manon S, Teyssier E, Payet N, Avelange-Macherel M-H, Macherel D. 2007. Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. The Plant Cell 19, 1580-1589. (Pubitemid 47025378)
67. Tunnacliffe A, Lapinski J, McGee B. 2005. A putative LEA protein, but no trehalose, is present in anhydrobiotic Bdelloid Rotifers. Hydrobiologia 546, 315-321. (Pubitemid 41239968)
68. Volker U, Engelmann S, Maul B, Riethdorf S, Volker A, Schmid R, Mach H, Hecker M. 1994. Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology 140, 741-752. (Pubitemid 24124644)
69. Wang W, Meng B, Chen W, Ge X, Liu S, Yu J. 2007. A proteomic study on postdiapaused embryonic development of brine shrimp (Artemia franciscana). Proteomics 7, 3580-3591. (Pubitemid 47597679)
70. Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Pei ZM, Shen SH, He YK. 2009. Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiology 149, 1739-1750.
71. Wang YX, Xiang YH, Qiang H. 2009. Study on protein determination experiment based on instrumental method. Experimental Technology and Management 26, 31-32.
72. Wickner S, Maurizi MR, Gottesman S. 1999. Posttranslational quality control: folding, refolding, and degrading proteins. Science 286, 1888-1893. (Pubitemid 129515889)
73. Wood AJ, Oliver MJ. 2004. Molecular biology and genomics of the desiccation tolerant moss Tortula ruralis. In: Wood AJ, Oliver MJ, Cove Dj, eds. New frontiers in bryology. Kluwer Academic Publishers, 71-89.
74. Xi W, Liu C, Hou X, Yu H. 2010. MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. The Plant Cell 22, 1733-1748.
75. Zhang Y, Wang X, Xiang Z, Li H, Qiu J, Sun Q, Wan T, Li N, Cao X, Wang J. 2007. Promotion of cellular migration and apoptosis resistance by a mouse eye-specific phosphatidylethanolamine-binding protein. International Journal of Molecular Medicine 19, 55-63.