Skip to main content
SpringerLink
Log in

Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Reduction of turgor in pea shoots caused the accumulation of several poly(A) RNAs. cDNA clones derived from three different poly(A) RNAs which accumulate in wilted pea shoots were isolated, sequenced and expression of the corresponding genes examined. Clone 7a encoded a 289 amino acid protein. The C-terminal 180 amino acids of this protein were homologous to soybean nodulin-26. RNA hybridizing to cDNA 7a was abundant in roots, and induced in shoots by dehydration, heat shock and to a small extent by ABA. Hydropathic plots indicate that the protein encoded by cDNA 7a contains six potential membrane spanning domains similar to proteins which form ion channels. Clone 15a encoded a 363 amino acid protein with high homology to cysteine proteases. RNA hybridizing to cDNA 15a was more abundant in roots than shoots of control plants. Dehydration of pea shoots induced cDNA 15a mRNA levels whereas heat shock or ABA treatment did not. Clone 26g encoded a 508 amino acid protein with 30% residue identity to several aldehyde dehydrogenases. RNA hybridizing to cDNA 26g was induced by dehydration of shoots but not roots and heat shock and ABA did not modulate RNA levels. Levels of the three poly(A) RNAs increased 4–6-fold by 4 h after wilting and this increase was not altered by pretreatment of shoots with cycloheximide. When wilted shoots were rehydrated, RNA hybridizing to cDNA 26g declined to pre-stress levels within 2 h. Run-on transcription experiments using nuclei from pea shoots showed that transcription of the genes which encode the three poly(A) RNAs was induced within 30 min following reduction of shoot turgor. One of the genes showed a further increase in transcription by 4 h after dehydration whereas transcription of the other 2 genes declined. These results indicate that plant cells respond to changes in cell turgor by rapidly increasing transcription of several genes. Furthermore, the expression of the turgor-responsive genes varies with respect to the time course of induction and reversibility of the wilting-induced changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bewley JD, Larsen KM: Differences in the responses to water stress of growing and non-growing regions of maize mesocotyls: Protein synthesis on total, free and membrane-bound polyribosome fractions. J Expt Bot 33: 406–415 (1982).

    Google Scholar 

  2. Bewley JD, Larson KM, Papp JET: Water-stress-induced changes in the pattern of protein synthesis in maize seedling mesocotyls: A comparsion with the effects of heat shock. J Expt Bot 34: 1126–1133 (1983).

    Google Scholar 

  3. Boyer JS: Relationship of water potential to growth of leaves. Plant Physiol 43: 1056–1062 (1968).

    Google Scholar 

  4. Bray EA: Drought- and ABA-induced changes in polypeptide and mRNA accumulation in tomato leaves. Plant Physiol 88: 1210–1214 (1988).

    Google Scholar 

  5. Brown AW: H+ excretion in mechanically isolated mesophyll cell from Asparagus cladophylls. Plant Sci Lett 22: 155–160 (1981).

    Google Scholar 

  6. Chiang RG, Davey KG: A novel receptor capable of monitoring applied pressure in the abdomen of an insect. Science 241: 1665–1667 (1988).

    Google Scholar 

  7. Choi JH, Liu L, Borkird C, Sung ZR: Cloning of genes developmentally regulated during plant embryogenesis. Proc Natl Acad Sci USA 84: 1906–1910 (1987).

    Google Scholar 

  8. Close TH, Kortt AA, Chandler PM: A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13: 95–108 (1989).

    PubMed  Google Scholar 

  9. Cosgrove D: Biophysical control of plant cell growth. Ann Rev Plant Physiol 37: 377–405 (1986).

    Google Scholar 

  10. Creelman RA, Mason HS, Bensen RJ, Boyer JS, Mullet JE: Water deficit and ABA cause differential inhibition of shoot vs root growth in soybean seedlings. Analysis of growth, sugar accumulation and gene expression. Plant Physiol (in press).

  11. Creelman RA, Zeevaart JAD: Incorporation of oxygen into abscisic acid and phaseic acid from molecular oxygen. Plant Physiol 75: 166–169 (1984).

    Google Scholar 

  12. Creelman RA, Zeevaart JAD: Abscisic acid accumulation in spinach leaf slices in the presence of penetrating and nonpenetrating solutes. Plant Physiol 77: 25–28 (1985).

    Google Scholar 

  13. Damerval C, Vartanian N, de Vinne D: Differential two-dimensional protein patterns as related to tissue specificity and water conditions in Brassica napus var oleifera root system. Plant Physiol 86: 1304–1309 (1988).

    Google Scholar 

  14. Dasgputa J, Bewley JD: Desiccation of axes of Phaseolus vulgaris during development of a switch from a development pattern of protein synthesis to a germination pattern. Plant Physiol 70: 1224–1227 (1982).

    Google Scholar 

  15. Dhindsa RS, Cleland RE: Water stress and protein synthesis. I. Differential inhibition of protein synthesis. Plant Physiol 55: 778–781 (1975).

    Google Scholar 

  16. Dure L, Crouch M, Harada J, Ho THD, Mundy J, Quatrano R, Thomas T, Sung ZR: Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12: 475–486 (1989).

    Google Scholar 

  17. Fortin MG, Morrison NA, Verma DPS: Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15: 813–824 (1987).

    PubMed  Google Scholar 

  18. Galau GA, Bijaisoradat N, Hughes DW: Accumulation kinetics of cotton late embryogenesis-abundant mRNAs and storage protein mRNAs: Coordinate regulation during embryogenesis of the role of abscisic acid. Devel Biol 123: 198–212 (1987).

    Google Scholar 

  19. Gamble PE, Mullet JE: Inhibition of carotenoid accumulation and abscisic acid biosynthesis in fluridone-treated dark-grown barley. Eur J Biochem 160: 117–121 (1986).

    PubMed  Google Scholar 

  20. Goday A, Sánchez-Martínez D, Gómez J, Puigdoménech P, Pagès M: Gene expression in developing Zea mays embryos: Regulation by abscisic acid of a highly phosphorylated 23- to 25-kD group of proteins. Plant Physiol 88: 564–569 (1988).

    Google Scholar 

  21. Gómez J, Sánchez-Martínez D, Stiefel V, Rigau J, Puigdoménech P, Pagès 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).

    PubMed  Google Scholar 

  22. Grumet R, Hanson AD: Genetic evidence for an osmoregulatory function of glycinebetaine accumulation in barley. Aust J Plant Physiol 13: 353–364 (1986).

    Google Scholar 

  23. Guerrero F, Mullet JE: Increased abscisic acid biosynthesis during plant dehydration requires transcription. Plant Physiol 80: 588–591 (1986).

    Google Scholar 

  24. Guerrero FD, Mullet JE: Reduction of turgor induces rapid changes in leaf translatable RNA. Plant Physiol 88: 401–408 (1988).

    Google Scholar 

  25. Hagen G, Guilfoyle TJ: Rapid induction of selective transcription by auxins. Mol Cell Biol 5: 1197–1203 (1985).

    PubMed  Google Scholar 

  26. Hanson AD, Scott NA: Betaine synthesis from radio-active precursors in attached, water-stressed barley leaves. Plant Physiol 66: 342–348 (1980).

    Google Scholar 

  27. Harada J, DeLisle A, Baden C, Crouch M: Unusual sequence of an abscisic acid-inducible mRNA which accumulates late Brassica napus development. Plant Mol Biol 12: 395–401 (1989).

    Google Scholar 

  28. Heikkila JJ, Papp JET, Schultz GA, Bewley JD: Induction of heat shock protein messenger RNA in maize mesocotyls by water stress, abscisic acid, and wounding. Plant Physiol 76: 270–274 (1984).

    Google Scholar 

  29. Heijne GV: A new method for predicting signal sequence cleavage sites. Nucl Acids Res 14: 4683–4690 (1986).

    PubMed  Google Scholar 

  30. Higgins CF, Cairney J, Stirling DA, Sutherland L, Booth IR: Osmotic regulation of gene expression: Ionic strength as an intracellular signal? Trends Biochem Sci 12: 239–244 (1987).

    Article  Google Scholar 

  31. Hong B, Uknes SJ, Ho THD: Cloning and characterization of a cDNA encoding a mRNA rapidly-induced by ABA in barley aleurone layers. Plant Mol Biol 11: 495–506 (1988).

    Google Scholar 

  32. Hsaio TC: Rapid changes in levels of polyribosomes in Zea mays in response to water stress. Plant Physiol 46: 281–285 (1970).

    Google Scholar 

  33. Hsiao TC: Plant responses to water stress. Ann Rev Plant Physiol 24: 519–570 (1973).

    Article  Google Scholar 

  34. Jendriask JJ, Guilfoyle TJ: Eukaryotic RNA polymerases: Comparative subunit structures, immunological properties and α-amanitin sensitivities of the class II enzymes from higher plants. Biochemistry 17: 1322–1327 (1978).

    PubMed  Google Scholar 

  35. Kyte J, Doolittle RF: A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132 (1982).

    PubMed  Google Scholar 

  36. Lin L-S, Ho T-HD: Mode of action of abscisic acid in barley aleurone layers. Induction of new proteins by abscisic acid. Plant Physiol 82: 289–297 (1986).

    Google Scholar 

  37. Love JD, Minton KW: Screening of λ library for differentially expressed genes using in vitro transcripts. Anal Biochem 150: 429–441 (1985).

    PubMed  Google Scholar 

  38. Maelicke A: Structural similarities between ion channel proteins. Trends Biochem Sci 13: 199–202 (1988).

    Article  PubMed  Google Scholar 

  39. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York (1982).

    Google Scholar 

  40. Marcotte WR, Bayley CC, Quatrano RS: Regulation of a wheat promoter by abscisic acid in rice protoplasts. Nature 335: 454–457 (1988).

    Article  Google Scholar 

  41. Mason HS, Matsuda K: Polyribosome metabolism, growth and water status in the growing tissues of osmotically stressed plant seedlings. Physiol Plant 64: 95–104 (1985).

    Google Scholar 

  42. Mason HS, Mullet JE, Boyer JS: Polysomes, messenger RNA, and growth in soybean stems during development and water deficit. Plant Physiol 86: 725–733 (1988).

    Google Scholar 

  43. Meyer RF, Boyer JS: Osmoregulation, solute distribution, and growth in soybean seedlings having low water potentials. Planta 151: 482–489 (1981).

    Google Scholar 

  44. Mahapatra SS, Poole RJ, Dhindsa RS: Abscisic acid-regulated gene expression in relation to freezing tolerance in alfalfa. Plant Physiol 87: 468–473 (1988).

    Google Scholar 

  45. Morilla CA, Boyer JS, Hageman RH: Nitrate reductase activity and polyribosomal content of corn (Zea mays L.) having low leaf water potentials. Plant Physiol 51: 817–824 (1973).

    Google Scholar 

  46. Morris CE, Sigurdson WJ: Stretch-inactivated ion channels coexist with stretch-activated ion channels. Science 243: 807–809 (1989).

    PubMed  Google Scholar 

  47. Mundy J, Chua N-H: Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279–2286 (1988).

    PubMed  Google Scholar 

  48. Mullet JE, Klein RR, Grossman AR: Optimization of protein synthesis in isolated higher plant chloroplasts. Identification of paused translation intermediates. Eur J Biochem 155: 331–338 (1986).

    PubMed  Google Scholar 

  49. Nonami H, Boyer JS: Turgor and growth at low water potentials. Plant Physiol 89: 798–804 (1989).

    Google Scholar 

  50. Oliver MJ, Bewley JD: 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 Physiol 74: 923–927 (1984).

    Google Scholar 

  51. Picket M, Gwynne DI, Buxton FP, Elliott R, Davies RW, Lockington RA, Scazzocchio C, Sealy-Lewis HM: Cloning and characterization of the aldA gene of Aspergllus nidulans. Gene 51: 217–226 (1987).

    Article  PubMed  Google Scholar 

  52. Pierce M, Raschke K: Synthesis and metabolism of abscisic acid in detached leaves of Phaseolus vulgaris L. after loss and recovery of turgor. Planta 153: 156–165 (1981).

    Google Scholar 

  53. Pietruszko R: Biochemistry and Physiology of Substance Abuse 1: 89–127 (1989).

    Google Scholar 

  54. Quarrie SA, Lister PG: Effects of inhibitors of protein synthesis on abscisic acid accumulation in wheat. Z Pflanzenphysiol 114: 309–314 (1984).

    Google Scholar 

  55. Reed NR, Bonner BA: The effect of abscisic acid on the uptake of potassium and chloride into Avena coleptile sections. Planta (Berl) 116: 173–185 (1974).

    Google Scholar 

  56. Robertson AJ, Gusta LV, Reaney MJT, Ishikawa M: Identification of proteins correlated with increased freezing tolerance in bromegrass (Bromus inermis Leyss. cv Manchar) cell cultures. Plant Physiol 86: 344–347 (1988).

    Google Scholar 

  57. Rodriguez D, Nicholás G, Aldasoro JJ, Hernández-Nistal J, Babiano MJ, Matilla A: Altered development of polysomal RNA activity in chick-pea (Cicer arietinum L.) embryonic axes. Effects of abscisic acid and temperature. Planta 164: 517–523 (1985).

    Google Scholar 

  58. Rogers JC, Dean D, Heck GR: Aleurain: A barley thiol protease closely related to mammalian cathepsin H. Proc Natl Acad Sci USA 82: 6512–6516 (1985).

    PubMed  Google Scholar 

  59. Ryan CA, An G: Molecular biology of wound-inducible proteinase inhibitors in plants. Plant Cell Envir 11: 345–349 (1988).

    Google Scholar 

  60. Schaffer MA, Fischer RL: Analysis of mRNAs that accumulate in response to low temperature identifies a thiol protease gene in tomato. Plant Physiol 87: 431–436 (1988).

    Google Scholar 

  61. Schmitt JM, Michalowski C, Bohnert HJ: Gene expression during CAM induction under salt stress in Mesembryanthemum: cDNA library and increased levels of mRNA for phosphoenolpyruvate carboxylase and pyruvate orthophosphate dikinase. Photosyn Res 17: 159–171 (1988).

    Google Scholar 

  62. Schuster AM, Davies E: Ribonucleic acid and protein metabolism in pea epicotyls. II Response to wounding in aged tissue. Plant Physiol 73: 817–821 (1983).

    Google Scholar 

  63. Scott NS, Munns R, Barlow EWR: Polyribosome content in young and aged wheat leaves subjected to drought. J Expt Bot 30: 905–911 (1979).

    Google Scholar 

  64. Sharp RE, Davies WJ: Solute regulation and growth by roots and shoots of water-stressed maize plants. Planta 147: 43–49 (1979).

    Google Scholar 

  65. Stewart CR, Voetberg G, Rayapati PJ: The effects of benzyladenine, cycloheximide, and cordycepin on wilting-induced abscicic acid and proline accumulations and abscisic acid- and salt-induced proline accumulation in barley leaves. Plant Physiol 82: 703–707 (1986).

    Google Scholar 

  66. Takio K, Towatari T, Katunuma N, Teller DC, Titani K: Homology of amino acid sequences of rat liver cathepsins B and H with that of papain. Proc Natl Acad Sci USA 80: 3666–3670 (1983).

    PubMed  Google Scholar 

  67. Turner NC: Adaptation to water deficits: A changing perspective. Aust J Plant Physiol 13: 175–190 (1986).

    Google Scholar 

  68. Williams JG, North MJ, Mahbubani H: A developmentally regulated cysteine proteinase in Distyostelium discoideum. EMBO J 4: 999–1006 (1985).

    PubMed  Google Scholar 

  69. Williamson JD, Quatrana RS: ABA-regulation of two classes of embryo-specific sequences in mature wheat embryos. Plant Physiol 86: 208–215 (1988).

    Google Scholar 

  70. Wyn Jones RG, Storey R: Betaines. In: Physiology and Biochemistry of Drought Resistance in Plants, pp. 171–204. Academic Press, Australia (1981).

    Google Scholar 

Download references

Author information

Author notes

  1. Felix D. Guerrero

    Present address: CIBA-GEIGY Biotechnology Research, Box 12257, 27709-2257, Research Triangle Park, NC, USA

Authors and Affiliations

  1. Department of Biochemistry and Biophysics, Texas A&M University, 77843-2128, College Station, TX, USA

    Felix D. Guerrero, Jennifer T. Jones & John E. Mullet

Authors
  1. Felix D. Guerrero
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jennifer T. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John E. Mullet
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guerrero, F.D., Jones, J.T. & Mullet, J.E. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted. Sequence and expression of three inducible genes. Plant Mol Biol 15, 11–26 (1990). https://doi.org/10.1007/BF00017720

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00017720

Key words

Search

Navigation