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

Plant Growth Regulation

Volumn 62, Issue 3, 2010, Pages 279-292

  Abdalla, Kamal Omer ^a,b   Baker, Bienyamien ^a   Rafudeen, Muhammad Suhail ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF GADARIF   (Sudan)

Author keywords

Chaperonin; Desiccation tolerance; Mass spectrometry; Nuclear proteins; Two dimensional electrophoresis; Xerophyta viscosa

Indexed keywords

SELAGINELLA PILIFERA; VELLOZIACEAE; XEROPHYTA VISCOSA;

EID: 78249232280     PISSN: 01676903     EISSN: 15735087     Source Type: Journal    
DOI: 10.1007/s10725-010-9497-2     Document Type: Article

References (103)

1. Abdalla K, Thomson JA, Rafudeen MS (2009) Protocols for nuclei isolation and nuclear protein extraction from the resurrection plant Xerophyta viscosa for proteomic studies. Anal Biochem 384(2): 365-367.
2. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209(9): 1575-1584.
3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol 55: 373-399.
4. Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36(5): 652-663.
5. Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum: a contribution to the study of drought tolerance at the molecular level. Plant Physiol 127: 1346-1353.
6. Bartels D, Phillips J, Chandler J (2007) Desiccation tolerance: gene expression, pathways, and regulation of gene expression. In: Jenks MA, Wood AJ (eds) Plant desiccation tolerance. Blackwell Publishing, Iowa, pp 115-148.
7. Belfort M, Derbyshire V, Parker M, Cousineau B, Lambowitz AM (2002) Mobile introns: pathways and proteins. In: Craig N, Craige R et al (eds) Mobile DNA II. ASM Press, Washington, pp 761-783.
8. Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Sci Res 16: 1-15.
9. Berlett BS, Levine RL, Stadtman ER (1996) Comparison of the effects of ozone on the modification of amino acid residues in glutamine synthetase and bovine serum albumin. J Biol Chem 271(8): 4177-4182.
10. Bernacchia G, Salamini F, Bartels D (1996) Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum. Plant Physiol 111(4): 1043-1050.
11. Blomstedt C, Neale A, Gianello R, Hamill J, Gaff DF (1998) Isolation and characterization of cDNAs associated with the onset of desiccation tolerance in the resurrection grass, Sporobolus stapfianus. Plant Growth Regul 24: 219-228.
12. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7): 1099-1111.
13. Bringaud F, Bartholomeu D, Blandin G, Delcher A, Baltz T, El-Sayed N, Ghedin E (2006) The Trypanosoma cruzi L1Tc and NARTc Non-LTR retrotransposons show relative site specificity for insertion. Mol Biol Evol 23(2): 411-420.
14. Caldas TD, El Yaagoubi A, Richarme G (1998) Chaperone properties of bacterial elongation factor EF-Tu. J Biol Chem 273(19): 11478-11482.
15. Calikowski TT, Meulia T, Meier I (2003) A proteomic study of the Arabidopsis nuclear matrix. J Cell Biochem 90(2): 361-378.
16. Capy P, Bazin C, Higuet D, Langin T (1998) Dynamics and evolution of transposable elements. Landes Bioscience, Austin.
17. Casacuberta JM, Santiago N (2003) Plant LTR-retrotransposons and MITEs: control of transposition and impact on the evolution of plant genes and genomes. Gene 311: 1-11.
18. Collett H, Shen A, Gardner M, Farrant JM, Denby KJ, 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. Physiol Plant 122(1): 39-53.
19. Colvis C, Garland D (2002) Posttranslational modification of human A-crystallin: correlation with electrophoretic migration. Arch Biochem Biophys 397(2): 319-323.
20. Cui X, Matsuura M, Wang Q, Ma H, Lambowitz AM (2004) A group II intron-encoded maturase functions preferentially in cis and requires both the reverse transcriptase and X domains to promote RNA splicing. J Mol Biol 340(2): 211-231.
21. Demirevska K, Simova-Stoilova L, Vassileva V, Vaseva I, Grigorova B, Feller U (2008) Drought-induced leaf protein alterations in sensitive and tolerant wheat varieties. Gen Appl Plant Physiol 34(1-2): 79-102.
22. Di Michele M, Chiatante D, Plomion C, Scippa GS (2006) A proteomic analysis of Spanish broom (Spartium junceum L.) root growing on a slope condition. Plant Sci 170(5): 926-935.
23. Dreger M (2003) Proteome analysis at the level of subcellular structures. Eur J Biochem 270(4): 589-599.
24. Evans AR, Limp-Foster M, Kelley MR (2000) Going APE over ref-1. Mutat Res 461(2): 83-108.
25. Farrant JM (2007) Mechanisms of desiccation tolerance in angiosperm resurrection plants. In: Jenks MA, Wood AJ (eds) Plant desiccation tolerance. Blackwell, UK, pp 51-90.
26. Farrant JM, Sherwin HW (1998) Mechanisms of desiccation tolerance in seeds and resurrection plants. In: Taylor AG, Huang XL (eds) Progress in seed science research. Communication Services of the New York State Agricultural Experimental Station, New York, pp 109-120.
27. Feng O, Moran JV, Kazazian HH, Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87: 905-916.
28. Fink JL, Karunaratne S, Mittal A, Gardiner D, Hamilton N, Mahony D, Kai C, Suzuki H, Hayashizaki Y, Teasdale R (2008) Towards defining the nuclear proteome. Genome Biol 9(1): R15.
29. Finnegan DJ (1997) Transposable elements: how non-LTR retrotransposons do it. Curr Biol 7(4): 245-248.
30. Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127(3): 343-352.
31. Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO 16: 3599-3608.
32. Gaff DF (1971) Desiccation-tolerant flowering plants in Southern Africa. Science 174(4013): 1033-1034.
33. Gaff DF, Blomstedt CK, Neale AD, Le TN, Hamill JD, Ghasempour HR (2009) Sporobolus stapfianus, a model desiccation-tolerant grass. Funct Plant Biol 36: 589-599.
34. Galcheva-Gargova Z, Gangwani L, Konstantinov KN, Mikrut M, Theroux SJ, Enoch T, Davis RJ (1998) The cytoplasmic zinc finger protein ZPR1 accumulates in the nucleolus of proliferating cells. Mol Biol Cell 9(10): 2963-2971.
35. Gangwani L, Mikrut M, Galcheva-Gargova Z, Davis RJ (1998) Interaction of ZPR1 with translation elongation factor-1α in proliferating cells. J Cell Biol 143(6): 1471-1484.
36. Garwe D, Thomson JA, Mundree SG (2006) XVSAP1 from Xerophyta viscosa improves osmotic-, salinity- and high-temperature-stress tolerance in Arabidopsis. Biotechnol J 1(10): 1137-1146.
37. Georgieva K, Szigeti A, Sarvari E, Gaspar L, Maslenkova L, Peeva V, Peli E, Tuba Z (2007) Photosynthetic activity of homoiochlorophyllous desiccation tolerant plant Haberlea rhodopensis during dehydration and rehydration. Planta 225: 955-964.
38. Goff S, Ricke D, Lan T, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma HEA (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100.
39. Goldberg AL (1992) The mechanism and functions of ATP-dependent proteases in bacterial and animal cells. Eur J Biochem 203(1-2): 9-23.
40. Govender K (2006) Molecular and Biochemical characterisation of a type II Peroxiredoxin (XvPrx2) from the resurrection plant Xerophyta viscosa (Baker). Molecular and Cell Biology. PhD Thesis. University of Cape Town.
41. Grandbastien M (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3: 181-187.
42. Heazlewood JL, Whelan J, Millar AH (2003) The products of the mitochondrial orf25 and orfB genes are FO components in the plant F1FO ATP synthase. FEBS Lett 540(1-3): 201-205.
43. Henson I, Mahalakshmi V, Bidinger F, Alagarswamy G (1981) Genotypic variation in pearl millet (Pennisetum americanum L. leeka) in the ability to accumulate ABA in response to water stress. J Exp Bot 32: 899-904.
44. Hilbricht T, Varotto S, Sgaramella V, Bartels D, Salamini F, Furini A (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol 179(3): 877-887.
45. Hoekstra FA, Golovina EA, Tetteroo FAA, Wolkers WF (2001) Induction of desiccation tolerance in plant somatic embryos: how exclusive is the protective role of sugars? Cryobiology 43: 140-150.
46. Iborra FJ, Jackson DA, Cook PR (2001) Coupled transcription and translation within nuclei of mammalian cells. Science 293(5532): 1139-1142.
47. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45(5): 771-787.
48. Ingle RA, Smith JA, Sweetlove LJ (2005) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. Biometals 18(6): 627-641.
49. Ingle RA, Schmidt UG, Farrant JM, Thomson JA, Mundree SG (2007a) Proteomic analysis of leaf proteins during dehydration of the resurrection plant Xerophyta viscosa. Plant Cell Environ 30(4): 435-446.
50. Ingle R, Collett H, Cooper K, Farrant JM, Illing N (2007b) Regulation of the reassembly of the photosynthetic complex by water and light in Xerophyta humilis. S Afr J Bot 73(3): 487-488.
51. Iyer R, Mundree SG, Rafudeen MS, Thomson JA (2007) A dessication tolerance gene with potential in crop improvement. In: Jenks MA, Wood AJ (eds) Plant dessication tolerance. Blackwell Publishing, Oxford, pp 283-296.
52. Jankowsky E, Fairman M (2007) RNA helicases-one fold for many functions. Curr Opin Struct Biol 17: 316-324.
53. Jiang XS, Dai J, Sheng QH, Zhang L, Xia QC, Wu JR, Zeng R (2005) A comparative proteomic strategy for subcellular proteome research: ICAT approach coupled with bioinformatics prediction to ascertain rat liver mitochondrial proteins and indication of mitochondrial localization for catalase. Mol Cell Proteomics 4(1): 12-34.
54. Jiang G, Wang Z, Shang H, Yang W, Hu Z, Phillips J, Deng X (2007) Proteome analysis of leaves from the resurrection plant Boea hygrometrica in response to dehydration and rehydration. Planta 225(6): 1405-1420.
55. Jin S, Chen C, Plant AL (2000) Regulation by ABA of osmotic-stress-induced changes in protein synthesis in tomato roots. Plant Cell Environ 23(1): 51-60.
56. Jung E, Heller M, Sanchez JC, Hochstrasser DF (2000) Proteomics meets cell biology: the establishment of subcellular proteomes. Electrophoresis 21(16): 3369-3377.
57. Khan MM, Komatsu S (2004) Rice proteomics: recent developments and analysis of nuclear proteins. Phytochemistry 65(12): 1671-1681.
58. Komatsu S, Tanaka N (2005) Rice proteome analysis: a step toward functional analysis of the rice genome. Proteomics 5(4): 938-949.
59. Komatsu M, Shimamoto K, Kyozuka J (2003) Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon karma. Plant Cell 15: 1934-1944.
60. Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, Clausen T (2008) Structural basis for the regulated protease and chaperone function of DegP. Nature 453(7197): 885-890.
61. Lillehoj EP, Salazar FH, Mervis RJ, Raum MG, Chan HW, Ahmad N, Venkatesan S (1988) Purification and structural characterization of the putative gag-pol protease of human immunodeficiency virus. J Virol 62(8): 3053-3058.
62. Michel F, Ferat JL (1995) Structure and activities of group II introns. Ann Rev Biochem 64: 435-461.
63. Mohr G, Lambowitz AM (2003) Putative proteins related to group II intron reverse transcriptase/maturases are encoded by nuclear genes in higher plants. Nucleic Acids Res 31(2): 647-652.
64. Molloy MP, Herbert BR, Walsh BJ, Tyler MI, Traini M, Sanchez JC, Hochstrasser DF, Williams KL, Gooley AA (1998) Extraction of membrane proteins by differential solubilization for separation using two-dimensional gel electrophoresis. Electrophoresis 19(5): 837-844.
65. Moran JV, Holmes SE, Naase TP, DeBerardinis RJ, Boeke JD, Kazazian HH (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87: 917-927.
66. Moriguchi K, Suzuki T, Ito Y, Yamazaki Y, Niwa Y, Kurata N (2005) Functional isolation of novel nuclear proteins showing a variety of subnuclear localizations. Plant Cell 17(2): 389-403.
67. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, Taccioli GE, Batzer MA, Moran JV (2002) DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet 31(2): 159-165.
68. Mundree SG, Baker B, Mowla S, Peters S, Marais S, Vander Willigen C, Govender K, Maredza A, Muyanga S, Farrant JM, Thomson JA (2002) Physiological and molecular insights into drought tolerance. Afr J Biotechnol 1: 28-38.
69. Mundree SG, Iyer R, Baker B, Conrad N, Davis E, Govender K, Maredza A, Thomson JA (2006) Prospects for using genetic modification to engineer drought tolerance in crops. In: Halford N (ed) Plant biotechnology. Wiley, Hoboken, pp 193-205.
70. Narberhaus F (2002) Alpha-crystallin-type heat shock proteins: socializing minichaperones in the context of a multichaperone network. Microbiol Mol Biol Rev 66(1): 64-93.
71. Neale AD, Blomstedt CK, Bronson P, Le TN, Guthridge K, Evans J, Gaff DF, Hamill JD (2000) The isolation of genes from the resurrection grass Sporobolus stapfianus which are induced during severe drought stress. Plant Cell Environ 23: 265-277.
72. Olivares M, Lopez M, Garcia-Perez J, Briones P, Pulgar M, Thomas M (2003) The endonuclease NL1Tc encoded by the LINE L1Tc from Trypanosoma cruzi protects parasites from daunorubicin DNA damage. Biochim Biophys Acta 1626: 25-32.
73. Oliver MJ (2007) In: Jenks MA, Wood AJ (eds) Plant desiccation tolerance. Blackwell Publishing, Oxford, p 11.
74. Oliver MJ, Tuba Z, Mishler B (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol 151: 85-100.
75. Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5: 1-19.
76. Otto T, Zoitan T, Scott P (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci 176(2): 187-199.
77. Pandey A, Choudhary MK, Bhushan D, Chattopadhyay A, Chakraborty S, Datta A, Chakraborty N (2006) The nuclear proteome of chickpea (Cicer arietinum L.) reveals predicted and unexpected proteins. J Proteome Res 5(12): 3301-3311.
78. Pandey A, Chakraborty S, Datta A, Chakraborty N (2008) Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol Cell Proteomics 7(1): 88-107.
79. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu Rev Genet 27: 437-496.
80. Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581(19): 3592-3597.
81. Rahman I (2003) Oxidative stress, chromatin remodeling and gene transcription in inflammation and chronic lung diseases. J Biochem Mol Biol 36(1): 95-109.
82. Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25(2): 141-151.
83. Repetto O, Rogniaux H, Firnhaber C, Zuber H, Küster H, Larré C, Thompson R, Gallardo K (2008) Exploring the nuclear proteome of Medicago truncatula at the switch towards seed filling. Plant J 56(3): 398-410.
84. 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 Environ 29: 1606-1617.
85. Shaw P, Doonan J (2005) The nucleolus. Playing by different rules? Cell cycle 4(1): 102-105.
86. Sherwin HW, Farrant JM (1996) Differences in rehydration of three desiccation-tolerant angiosperm species. Ann Bot 78: 703-710.
87. Sherwin HW, Farrant JM (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul 24: 203-210.
88. Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779(11): 743-748.
89. Sørensen J, Kristensen T, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6: 1025-1037.
90. Talapatra S, Wagner JD, Thompson CB (2002) Elongation factor-1 alpha is a selective regulator of growth factor withdrawal and ER stress-induced apoptosis. Cell Death Differ 9(8): 856-861.
91. Tuba Z, Lichtenthaler HK, Csintalan Z, P′ocs T (1993) Regreening of the desiccated leaves of the poikilochlorophyllous Xerophyta scabrida upon rehydration. J Plant Physiol 142: 103-108.
92. 2 assimilation upon rehydration in the desiccated poikilochlorophyllous plant Xerophyta scabrida. Planta 192: 414-420.
93. Vicre M, Farrant JM, Driouich A (2004) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant Cell Environ 27(11): 1329-1340.
94. Vierling E (1991) The role of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42: 579-620.
95. Walford SA, Denby K, Shen A, Farrant JM, Illing N (2007) Comparison of desiccation-induced gene expression in vegetative tissue and seed of the resurrection plant, Xerophyta humilis. S Afri J Bot 73(3): 495-500.
96. Walker JE, Saraste M, Gay NJ (1984) The unc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim Biophys Acta 768(2): 164-200.
97. Walters C, Farrant JM, Pammenter NW, Berjak P (2002) Desiccation and damage. In: Black M, Pritchard H (eds) Desiccation and survival in plants: drying without dying. CAB International, London, pp 263-291.
98. Whitcomb J, Hughes S (1992) Retroviral reverse transcription and integration: progress and problems. Annu Rev Cell Biol 8: 275-306.
99. Willsie JK, Clegg JS (2002) Small heat shock protein p26 associates with nuclear lamins and HSP70 in nuclei and nuclear matrix fractions from stressed cells. J Cell Biochem 84(3): 601-614.
100. Woolford J, Warner J (1991) The ribosome and its synthesis. Cold Spring Harbor Laboratory Press, New York.
101. Worringer K, Anning B (2007) Zinc finger protein Zn72D promotes productive splicing of the maleless transcript. Mol Cell Biol 27(24): 8760-8769.
102. Yu J, Hu S, Wang J, Wong G, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 9-92.
103. Zhang X, Liu S, Takano T (2008) Overexpression of a mitochondrial ATP synthase small subunit gene (AtMtATP6) confers tolerance to several abiotic stresses in Saccharomyces cerevisiae and Arabidopsis thaliana. Biotechnol Lett 30(7): 1289-1294.