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Water deficit modulates gene expression in growing zones of soybean seedlings. Analysis of differentially expressed cDNAs, a new β-tubulin gene, and expression of genes encoding cell wall proteins

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Abstract

Transfer of soybean seedlings to low-water-potential vermiculite (ψw = −0.3 MPa) results in a reversible decrease in hypocotyl growth and modulation of several polysomal mRNAs (Plant Physiol 92: 205–214). We report here the isolation of two cDNA clones (pGE16 and pGE95) which correspond to genes whose mRNA levels are increased, and one cDNA clone (pGE23) which corresponds to a gene whose mRNA level is decreased in the hypocotyl zone of cell elongation by water deficit. In well-watered seedlings mRNAs hybridizing to pGE16 and pGE95 are most abundant in mature regions of the seedling, but in water-deficient seedlings mRNA levels are reduced in mature regions and enhanced in elongating regions. RNA corresponding to soybean proline-rich protein 1 (sbPRP1) shows a similar tissue distribution and response to water deficit. In contrast, in well-watered seedlings, the gene corresponding to pGE23 was highly expressed in the hypocotyl and root growing zones. Transfer of seedlings to low-water-potential vermiculite caused a rapid decrease in mRNA hybridizing to pGE23. Sequence analysis revealted that pGE23 has high homology with β-tubulin. Water deficit also reduced the level of mRNA hybridizing to JCW1, an auxin-modulated gene, although with different kinetics. Furthermore, mRNA encoding actin, glycine-rich proteins (GRPs), and hydroxyproline-rich glycoproteins (HRGPs) were down-regulated in the hypocotyl zone of elongation of seedlings exposed to water deficit. No effect of water deficit was observed on the expression of chalcone synthase. Decreased expression of β-tubulin, actin, JCW1, HRGP and GRP and increased expression of sbPRP1, pGE95 and pGE16 in the hypocotyl zone of cell elongation could participate in the reversible growth inhibition observed in water-deficient soybean seedlings.

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References

  1. Ainley, WM, Walker, JC, Nagao, RT, Key, JL: Sequence and characterization of two auxin-regulated genes from soybean. J Biol Chem 263: 10658–10666 (1988).

    Google Scholar 

  2. Ausubel, FM, Brent, R, Kingston, RE, Moore, DD, Seidman, JG, Smith, JA, Struhl, K: Current Protocols in Molecular Biology. John Wiley, New York (1987).

    Google Scholar 

  3. Baker, EJ, Schloss, JA, Rosenbaum, JL: Rapid changes in tubulin RNA synthesis and stability induced by deflagellation in Chlamydomonas. J Cell Biol 99: 2074–2081 (1984).

    Google Scholar 

  4. Bensen, RJ, Boyer, JS, Mullet, JE: Water-deficit-induced changes in abscisic acid, growth, polysomes, and translatable RNA in soybean hypocotyls. Plant Physiol 88: 289–294 (1988).

    Google Scholar 

  5. Bensen, RJ, Beall, FD, Mullet, JE, Morgan, PW: Identification of endogenous gibberellins and their relationship to hypocotyl elongation in soybean seedlings. Plant Physiol 94: 77–84 (1990).

    Google Scholar 

  6. Boyer, JS, Wu, G: Auxin increases the hydraulic conductivity of auxin-sensitive hypocotyl tissue. Planta 139: 22–237 (1978).

    Google Scholar 

  7. Bozarth, CS, Mullet, JE, Boyer, JS: Cell wall proteins at low water potentials. Plant Physiol 85: 261–267 (1987).

    Google Scholar 

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

    Google Scholar 

  9. Bustos, MM, Guiltinan, MJ, Cyr, RJ, Ahdoot, D, Fosket, DE: Light regulation of β-tubulin gene expression during internode development in soybean (Glycine max [L.] Merr.). Plant Physiol 91: 1157–1161 (1989).

    Google Scholar 

  10. Cassab, Gi, Varner, JE: Cell wall proteins. Ann Rev Plant Physiol Plant Mol Biol 39: 321–353 (1988).

    Google Scholar 

  11. 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).

    Google Scholar 

  12. Chen, JA, Varner, JE: Isolation and characterization of cDNA clones for carrot extensin and a proline-rich 33-kDa protein. Proc Natl Acad Sci USA 82: 4399–4403 (1985).

    Google Scholar 

  13. 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 

  14. Cleveland, DW: Autoregulated instability of tubulin mRNAs: a novel eukaryotic regulatory mechanism. Trends Biochem Sci 13: 339–343 (1988).

    Google Scholar 

  15. 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).

    Google Scholar 

  16. Colbert, JT, Hershey, HP, Quail, PH: Phytochrome regulation of phytochrome mRNA abundance. Plant Mol Biol 5: 91–101 (1985).

    Google Scholar 

  17. Condit, CM, Meagher, RB: A gene encoding a novel glycine-rich structural protein of petunia. Nature 323: 178–181 (1986).

    Google Scholar 

  18. Creelman, RA, Mason, HS, Bensen, RJ, Boyer, JS, Mullet, JE: Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings. Analysis of growth, sugar accumulation, and gene expression. Plant Physiol 92: 205–214 (1990).

    Google Scholar 

  19. Darbyshire, B: Changes in indoleacetic acid oxidase activity associated with plant water potential. Physiol Plant 25: 80–84 (1971).

    Google Scholar 

  20. Datta, K, Schmidt, A, Marcus, A: Characterization of two soybean repetitive proline-rich proteins and a cognate cDNA from germinated axes. Plant Cell 1: 945–952 (1989).

    Google Scholar 

  21. Dure, III, L, Crouch, M, Harada, J, Ho, T-H, 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 

  22. 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 

  23. Gatehouse, LN, Evans, IM, Gatehouse, JA, Croy, RRD: Characterization of a rape (Brassica napus L.) extensin gene encoding a polypeptide relatively rich in tyrosine. Plant Sci 71: 223–231 (1990).

    Google Scholar 

  24. Gay, DA, Yen, TJ, Lau, JTY, Cleveland, DW: Sequences that confer β-tubulin autoregulation stability reside within exon 1 of β-tubulin mRNA. Cell 50: 671–679 (1987).

    Google Scholar 

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

    Google Scholar 

  26. Gómez, J, Sanchez-Martinez, 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).

    Google Scholar 

  27. Guerrero, F, Mullet, JE: Reduction of turgor induces rapid changes in leaf translatable RNA. Plant Physiol 80: 588–591 (1986).

    Google Scholar 

  28. Guiltinan, MJ, Ma, D-P, Barker, RF, Bustos, MM, Cyr, RJ, Yadegari, R, Fosket, DE: The isolation, characterization and sequence of two divergent β-tubulin genes from soybean (Glycine max L.). Plant Mol Biol 10: 171–184 (1987).

    Google Scholar 

  29. Gunning, BES, Hardham, AR: Microtubules. Ann Rev Plant Physiol 33: 651–698 (1982).

    Google Scholar 

  30. Hanson, AD, Hitz, WD: Metabolic responses of mesophytes to plant water deficits. Ann Rev Plant Physiol 33: 163–203 (1982).

    Google Scholar 

  31. 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 

  32. 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 

  33. Hightower, RC, Meagher, RB: Divergence and differential expression of soybean actin genes. EMBO 4: 1–8 (1985).

    Google Scholar 

  34. 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 

  35. Hong, JC, Nagao, RT, Key, JL: Developmentally regulated expression of soybean proline-rich cell wall protein genes. Plant Cell 1: 937–943 (1989).

    Google Scholar 

  36. Keller, B, Sauer, N, Lamb, CJ: Glycine-rich cell wall proteins in bean: gene structure and association of the protein with the vascular system. EMBO 7: 3625–3633 (1988).

    Google Scholar 

  37. Keller, LR, Schloss, JA, Siflow, CD, Rosenbaum, JL: Transcription of α- and β-tubulin genes in vitro in isolated Chlamydomonas reinhardtii nuclei. J Cell Biol 98: 1138–1143 (1984).

    Google Scholar 

  38. Lei, M, Wu, R: A novel glycine-rich cell wall protein gene in rice. Plant Mol Biol 16: 187–198 (1991).

    Google Scholar 

  39. 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 

  40. 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 

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

    Google Scholar 

  42. Mason, HS, Mullet, JE: Expression of two soybean vegetative storage protein genes during development and in response to water deficit, wounding, and jasmonic acid. Plant Cell 2: 569–579 (1990).

    Google Scholar 

  43. 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 

  44. Meyer, RF, Boyer, JS: Sensitivity of cell division and cell elongation to low water potentials in soybean hypocotyls. Planta 108: 77–87 (1972).

    Google Scholar 

  45. Monroy, AF: Staining immobilized RNA ladder. Focus 10: 14 (1988).

    Google Scholar 

  46. Mullet, JE: Reversible inhibition of hypocotyl growth in soybean seedlings exposed to water deficit. In: Goldberg, R (ed) Plant Gene Transfer, pp. 249–256 Alan R. Liss, New York (1990).

    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).

    Google Scholar 

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

    Google Scholar 

  49. Nonami, H, Boyer, JS: Primary events regulating stem growth at low water potentials. Plant Physiol 94: 1601–1609 (1990).

    Google Scholar 

  50. Nonami, H, Boyer, JS: Wall extensibility and cell hydraulic conductivity decrease in enlarging stem tissues at low water potentials. Plant Physiol 93: 1610–1619 (1990).

    Google Scholar 

  51. Reimold, U, Kroeger, M, Kruzaler, F, Hahlbrock, K: Coding and 3′ non-coding nucleotide sequence of chalcone synthase mRNA and assignment of amino acid sequence of the enzyme. EMBO 2: 1801–1805 (1983).

    Google Scholar 

  52. 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 

  53. Rodriguez, D, Nicholás, G, Aldasoro, JJ, Hernández-Nistal, J, Babiano, MJ, Matilla, A: Altereddevelopment 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 

  54. Ryder, TB, Cramer, CL, Bell, JN, Robbins, MP, Dixon, RA, Lamb, CJ: Elicitor rapidly induces chalcone synthase mRNA in Phaseolus vulgaris cells at the onset of the phytoalexin defense response. Proc Natl Acad Sci USA 81: 5724–5728 (1984).

    Google Scholar 

  55. Saab, IN, Sharp, RE, Pritchard, J, Voetberg, GS: Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93: 1329–1336 (1990).

    Google Scholar 

  56. Sadava, D, Walker, F, Chrispeels, MJ: Hydroxyproline-rich cell wall protein (extensin): biosynthesis and accumulation in growing pea epicotyls. Devel Biol 30: 42–48 (1973).

    Google Scholar 

  57. Shah, DM, Hightower, RC, Meagher, RC: Complete nucleotide sequence of a soybean actin gene. Proc Natl Acad Sci USA 79: 1022–1026 (1982).

    Google Scholar 

  58. Showalter, AM, Varner, JE: Molecular details of plant cell wall hydroxyproline-rich glycoprotein expression during wounding and infection. In: CJ, Arntzen, CA, Ryan (eds) UCLA Symposium on Molecular Strategies for Crop Protection, pp. 375–392. Alan R. Liss, New York (1986).

    Google Scholar 

  59. Staiger, CJ, Schliwa, M: Actin localization and function in higher plants. Protoplasma 141: 1–12 (1987).

    Google Scholar 

  60. Tierney, ML, Weichert, J, Pluymers, D: Analysis of the expression of extensin and p33-related cell wall proteins in carrot and soybean. Mol Gen Genet 211: 393–399 (1988).

    Google Scholar 

  61. Walker, JC, Key, JL: Isolation of cloned cDNAs to auxin-responsive poly(A)+ RNAs of elongating soybean hypocotyl. Proc Natl Acad Sci USA 79: 7185–7189 (1982).

    Google Scholar 

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

    Google Scholar 

  63. Zeevaart, JAD, Creelman, RA: Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39: 439–473 (1988).

    Google Scholar 

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Creelman, R.A., Mullet, J.E. Water deficit modulates gene expression in growing zones of soybean seedlings. Analysis of differentially expressed cDNAs, a new β-tubulin gene, and expression of genes encoding cell wall proteins. Plant Mol Biol 17, 591–608 (1991). https://doi.org/10.1007/BF00037046

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