The wheat LEA protein Em functions as an osmoprotective molecule in Saccharomyces cerevisiae

Plant Molecular Biology

Volumn 39, Issue 1, 1999, Pages 117-128

  Swire Clark, Ginger A ^a   Marcotte Jr , William R ^a  

^a CLEMSON UNIVERSITY   (United States)

Author keywords

Drought; LEA protein; Osmotic stress; Saccharomyces cerevisiae; Salt

Indexed keywords

GROWTH INHIBITION; LATE EMBRYOGENESIS ABUNDANT PROTEIN; OSMOLARITY; OSMOTIC STRESS; WHEAT;

FREEZING; HEAT-SHOCK PROTEINS; OSMOSIS; PLANT PROTEINS; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSFECTION; TRITICUM; WATER;

EID: 0033059242     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006106906345     Document Type: Article

References (67)

1. Albertyn J, Hohmann S, Thevelein JM, Prior BA: GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14: 4135-4144 (1994).
2. Almoguera C, Jordano J: Developmental and environmental concurrent expression of sunflower dry-seed stored molecular weight heat shock protein and Lea mRNA. Plant Mol Biol 19: 781-792 (1992).
3. Baker JC, Steele C, Dure III L: Sequence and characterization of 6 Lea proteins and their genes in cotton. Plant Mol Biol 11: 277-291 (1988).
4. Baler R, Welch WJ, Voellmy R: Heat shock gene regulation by nascent polypeptides and denatured proteins: hsp70 as a potential autoregulatory factor. J Cell Biol 117: 1151-1159 (1992).
5. Bartels D, Singh M, Salamini F: Onset of desiccation tolerance during development of the barley embryo. Planta 175: 485-492 (1988).
6. Becker DM, Guarente L: High-efficiency transformation of yeast by electroporation. Meth Enzymol 194: 182-187 (1991).
7. Berge SK, Bartholomew DM, Quatrano RS: Control of the expression of wheat embryo genes by abscisic acid. In: Goldberg RL (ed) Molecular Basis of Plant Development, pp. 193-201. Alan R. Liss, New York (1989).
8. Blomberg A, Adler L: Physiology of osmotolerance in yeast. Adv Microbiol Physiol 33: 145-212 (1992).
9. Bostock RM, Quatrano RS: Regulation of Em gene expression in rice. Plant Physiol 98: 1356-1363 (1992).
10. Bradford M: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254 (1976).
11. Bray EA: Molecular responses to water deficit. Plant Physiol 103: 1035-1040 (1993).
12. Cherry JM, Adler C, Ball C, Dwight S, Chervitz S, Jia Y, Juvik G, Weng S, Botstein D: Saccharomyces Genome Database, http://genome-www.stanford.edu/Saccharomyces/, Non-Redundant S. cerevisiae Protein Data Set, May 13, 1997 (1997).
13. Cherry JM: Codon tables from http://128.252.119.253/ docs/bio/cod.html (1994).
14. Close TJ, Kortt AA, Chandler PM: A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13: 95-108 (1989).
15. Compagno C, Coraggio I, Ranzi BM, Alberghian L, Viotti A, Martegani E: Translational regulation of the expression of zein cloned in yeast under an inducible GAL promoter. Biochem Biophys Res Comm 146: 809-814 (1987).
16. Dure III L, Greenway S, Galau GA: Developmental biochemistry of cottonseed embryogenesis and germination XIV. Changing mRNA populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20: 4162-4168 (1981).
17. Dure III L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano RS, Thomas T, Sung ZR: Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12: 475-486 (1989).
18. Dure III L: Structural motifs in LEA proteins. In: Close TJ (ed) Plant Responses to Cellular Dehydration during Environmental Stress, pp. 91-103. American Society of Plant Physiologists, Rockville, MN (1993).
19. Espelund M, Saebøe-Larssen S, Hughes DW, Galau GA, Larsen F, Jakobsen KS: Late embryogenesis-abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. Plant J 2: 241-252 (1992).
20. Galau GA, Hughes DW, Dure III L: Abscisic acid induction of cloned cotton late embryogenesis-abundant (lea) mRNAs. Plant Mol Biol 7: 155-170 (1986).
21. Galau GA, Wang HYC, Hughes DW: Cotton Lea4 (D19) and LeaA2 (D132) group 1 Lea genes encoding water stress-related proteins containing a 20-amino acid motif. Plant Physiol 99: 783-788 (1992).
22. Gaubier P, Raynal M, Hull G, Huestis GM, Grellet F, Arenas C, Pages M, Delsney M: Two different Em-like genes are expressed in Arabidopsis thaliana seed during maturation. Mol Gen Genet 238: 409-418 (1993).
23. Gaxiola R, Larrinoa IFD, Villalba MJ, Serrano R: A novel and conserved salt-induced protein is an important determinant of salt tolerance in yeast. EMBO J 11: 3157-3164 (1992).
24. Goff SA, Goldberg AL: Production of abnormal proteins in E. coli stimulates transcription of Ion and other heat shock genes. Cell 41: 587-595 (1985).
25. Gomez J, Sanchez-Martinez D, Stiefel V, Rigau J, Puigdomenech P, Pages M: A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334: 262-264 (1988).
26. Grzelczak ZF, Sattolo MH, Hanley-Bowdoin LK, Kennedy TD, Lane BG: Synthesis and turnover of proteins and mRNA in germinating wheat embryos. Can J Biochem 60: 389-397 (1982).
27. Hanahan D: Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580 (1983).
28. Henson IE: Effects of atmospheric humidity on abscisic acid accumulation and water status in leaves of rice. Ann Bot 54: 569-582 (1984).
29. Hoffman CS, Winston F: A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272 (1987).
30. Hofmann T, Kells DIC, Lane BG: Partial amino acid sequence of the wheat germ Ec protein: Comparison with another protein very rich in half-cystein and glycine, wheat germ agglutinin. Can J Biochem Cell Biol 62: 908-913 (1984).
31. Hogue DL, Ellison MJ, Young JD, Cass CE: Identification of a novel membrane transporter associated with intracellular membranes by phenotypic complementation in the yeast Saccharomyces cerevisiae. J Biol Chem 271: 9801-9808 (1996).
32. Imai R, Chang L, Ohta A, Bray E, Takagi M: A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170: 243-248 (1996).
33. Jessee J, Bloom F: DH5αMCR™: New competent cells for cloning methylated DNA. Focus 10: 69-70 (1988).
34. Johnston M, Davis RW: Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol 4: 1440-1448 (1984).
35. Jones H, Leigh RA, Tomos AD, Jones RGW: The effects of abscisic acid on cell turgor pressures, soluble content and growth of wheat roots. Planta 170: 257-262 (1987).
36. Kelley PM, Schlesinger MJ: The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell 15: 1277-1286 (1978).
37. Kyte J, Doolittle RF: A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132 (1982).
38. Lennox ES: Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1: 190-206 (1955).
39. Lifts JC, Colwell GW, Chakerian RL, Quatrano RS: The nucleotide sequence of a cDNA clone encoding the wheat Em protein. Nucl Acids Res 15: 3607-3618 (1987).
40. Lifts JC, Colwell GW, Chakerian RL, Quatrano RS: Sequence analysis of a functional member of the Em gene family from wheat. DNA Sequencing 1: 263-274 (1991).
41. Lifts JC, Erdman MB, Huang N, Karrer EE, Nouiery A, Quatrano RS, Rodriguez RL: Nucleotide sequence of the rice (Oryza sativa) Em protein gene (EMP1). Plant Mol Biol 19: 335-337 (1992).
42. Manickam A, Van Damme EJM, Kalaiselvi K, Verhaert P, Pumans WJ: Isolation and cDNA cloning of an Em-like protein from mung bean (Vigna radiata) axes. Physiol Plant 97: 524-530 (1996).
43. Marcotte Jr WR, Bayley CC, Quatrano RS: Regulation of a wheat promoter by abscisic acid in rice protoplasts. Nature 335: 454-457 (1988).
44. McCubbin WD, Kay CM, Lane BG: Hydrodynamic and optical properties of the wheat germ Em protein. Can J Biochem Cell Biol 63: 803-811 (1985).
45. Morris PC, Kumar A, Bowles DJ, Cuming AC: Osmotic stress and abscisic acid induce expression of the wheat Em genes. Eur J Biochem 190: 625-630 (1990).
46. Mundy J, Chua N-H: Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279-2286 (1988).
47. Piper PW, Talreja K, Panaretou B, Moradas-Ferreira P, Byrne K, Praekelt UM, Meacock PA, Récnacq M, Boucherie H: Induction of major heat-shock proteins of Saccharomyces cerevisiae, including plasma membrane Hsp30, by ethanol levels above a critical threshold. Microbiology 140: 3031-3038 (1994).
48. Praekelt UM, Meacock PA: HSP12, a new small heat shock gene of Saccharomyces cerevisiae: analysis of structure, regulation and function. Mol Gen Genet 223: 97-106 (1990).
49. Pringle JR: Methods for avoiding proteolytic artefacts in studies of enzymes and other proteins from yeasts. Meth Cell Biol 12: 149-184 (1975).
50. Raynal M, Depigny D, Cooke R, Delsney M: Characterization of a radish nuclear gene expressed during late seed maturation. Plant Physiol 91: 829-836 (1989).
51. Roberts JK, Noelle AD, Wilma LL, Dure III L: Cellular concentrations and uniformity of cell-type accumulation of two lea proteins in cotton embryos. Plant Cell 5: 769-780 (1993).
52. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).
53. Schmitt ME, Brown TA, Trumpower BL: A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucl Acids Res 18: 3091-3092 (1990).
54. Schneider JC, Guarente L: Vectors for expression of cloned genes in yeast: regulation, overproduction, and underproduction. Meth Enzymol 194: 373-388 (1991).
55. Selden RF: Analysis of RNA by norhern hybridization. In: Ausubel FA et al. (eds) Current Protocols in Molecular Biology, pp. 4.9.4.-4.9.8. Greene Publishing/Wiley-Interscience, New York (1987).
56. Serrano R, Marquez JA, Ríos G: Crucial factors in salt stress tolerance. In: Hohmann S, Mager W (eds) Yeast Stress Responses, pp. 147-169. RG Landes, Austin, TX (1997).
57. Sherman F: Getting started with yeast. Meth Enzymol 194: 3-21 (1991).
58. Steponkus PL, Webb MS: Freeze-induced dehydration and membrane destabilization in plants. In: Somero GN, Osmond CB, Bolis CL (eds) Water and Life: Comparative Analysis of Water Relationships at the Organismic, Cellular and Molecular Levels, pp. 338-362. Springer-Verlag, Berlin (1992).
59. Stone RL, Matarese V, Magee B, Magee PT, Bernlohr DA: Cloning, sequencing and chromosomal assignment of a gene from Saccharomyces cerevisiae which is regulated negatively by glucose and positively by lipids. Gene 96: 171-176 (1990).
60. Tartof KD, Hobbs CA: Improved media for growing plasmid and cosmid clones. Focus 9: 12 (1987).
61. Ulrich TU, Wurtele ES, Nikolau BL: Sequence of EMB-1, an mRNA accumulating specifically in embryos of carrot. Nucl Acids Res 18: 2826 (1990).
62. Varela JCS, van Beekvelt CA, Planta RJ, Mager WH: Osmostress-induced changes in yeast gene expression. Mol Microbiol 6: 2183-2190 (1992).
63. Varela JCS, Mager WH: Response of Saccharomyces cerevisiae to changes in external osmoticum. Microbiology 142: 721-731 (1996).
64. Villardell J, Goday A, Freire MA, Torrent M, Martinez C, Torne H, Pages M: Gene sequence, developmental expression and protein phosphorylation of RAB17 in maize. Plant Mol Biol 14: 423-432 (1990).
65. Williams B, Tsang A: A maize gene expressed during embryogenesis is abscisic acid-inducible and highly conserved. Plant Mol Biol 16: 916-923 (1991).
66. Xu D, Duan X, Wang B, Hong B, Ho T-HD, Wu R: Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110: 249-257 (1996).
67. Zaret KS, Sherman F: DNA sequence required for efficient transcription termination in yeast. Cell 28: 563-573 (1982).