Abstract
We have examined growth, water status and gene expression in dark-grown soybean (Glycine max L. Merr.) seedlings in response to water deficit (low water potentials) during the first days following germination. The genes encoded the plasma membrane proton ATPase and two proteins of 28 kDa and 31 kDa putatively involved in vegetative storage. Water potentials of stems and roots decreased when 2-day-old seedlings were transferred to water-saturated air. Stem growth was inhibited immediately. Root growth continued at control rates for one day and then was totally inhibited when the normal root-stem water potential gradient was reversed.
Expression of mRNA for the 28 kDa and 31 kDa proteins, measured independently using specific 3′-end probes, occurred about equally in stems. However, only the mRNA for the 31 kDa protein was detected in roots and at a lower abundance than in stems. Low water potentials increased the mRNA only for the 28 kDa protein in stems and the 31 kDa protein in roots. This differential expression followed the inhibition of stem growth but preceded the inhibition of root growth.
The expression of the message for the ATPase, measured using a probe synthesized from a partial oat ATPase clone, was low in stems and roots but there was a 6-fold increase at low water potentials in roots. The increase followed the inhibition of root growth. This appears to be the first instance of regulation of ATPase gene expression in plants and the first demonstration of differential expression of the 28 kDa, 31 kDa, and ATPase messages. The correlation with the differential growth responses of the stems and roots raises the possibility that the differential gene expression could be involved in the growth response to low water potentials.
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References
Andrews DL, Beames B, Summers MD, Park WD: Characterization of the lipid acyl hydrolase activity of the major potato (Solanum tuberosum) tuber protein, patatin by cloning and abundant expression in a baculovirus vector. Biochem J 252: 199–206 (1988).
Bennet AB, Ewing NN, Wimmers LE: Molecular analysis of cation-sensitive ion-translocating ATPases in tomato. Proceedings of the 8th International Workshop on Plant Membrane Transport, Venice, Italy, June 25–30, 1989. Elsevier Science Publishing Co., New York. In Press.
Bensen RJ, Boyer JS, Mullet JE: Water deficit-induced changes in abscisic acid content, growth, polysomes, and translatable RNA in soybean hypocotyls. Plant Physiol 88: 289–294 (1988).
Boutry M, Michelet B, Goffeau a: Molecular cloning of a family of plant genes encoding a protein homologous to plasma membrane H+-translocating ATPases. Biochem Biophys Res Commun 162: 567–574 (1989).
Boyer JS: Isopiestic technique: measurement of accurate leaf water potentials. Science 154: 1459–1460 (1966).
Boyer JS: Water transport. Ann Rev Plant Physiol 36: 473–516 (1985).
Boyer JS: Hydraulics, wall extensibility and wall proteins. In: Cosgrove DJ, Knievel DP (eds) Physiology of Cell Expansion During Plant Growth, pp. 109–121. The American Society of Plant Physiology, Rockville, MD (1987).
Boyer JS, Knipling EB: Isopiestic technique for measuring leaf water potentials with a thermocouple psychrometer. Proc Natl Acad Sci USA 54: 1044–1051 (1965).
Bozarth CS, Mullet JE, Boyer JS: Cell wall proteins at low water potentials. Plant Physiol 85: 261–267 (1987).
Cassab GI, Varner JE: Cell wall proteins. Ann Rev Plant Physiol Plant Mol Biol 39: 321–353 (1988).
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. Plant Physiol 92: 205–214 (1990).
Dunham RJ, Nye PH: The influence of soil water content on the uptake of ions by roots. III. Phosphate, potassium, calcium and magnesium uptake and concentration gradients in soil. J Appl Ecol 13: 967–984 (1974).
Dure LIII, Crouch M, Harada J, Ho T-HD, 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).
Gomez K, 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).
Harper J, Surowy TK, Sussman MR: Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc Natl Acad Sci USA 86: 1234–1238 (1989).
Labrador E, Nicolas G: Autolysis of cell walls in pea hypocotyls during growth. Enzymatic activities involved. Physiol Plant 64: 541–546 (1984).
Lüttge U, Higinbotham N: Transport in Plants. Springer-Verlag, Berlin (1979).
Mason HS, Guerrero FD, Boyer JS, Mullet JE: Proteins homologous to leaf glycoproteins are abundant in stems of dark-grown soybean seedlings. Analysis of proteins and cDNAs. Plant Mol Biol 11: 845–856 (1989).
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).
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).
Meyer RF, Boyer JS: Sensitivity of cell division and cell elongation to low water potentials in soybean hypocotyls. Planta 108: 77–87 (1972).
Meyer RF, Boyer JS: Osmoregulation, solute distribution and growth in soybean seedlings having low water potentials. Planta 151: 482–489 (1981).
Nonami H, Boyer JS: Turgor and growth at low water potentials. Plant Physiol 89: 798–804 (1989).
Nonami H, Boyer JS: Primary events regulating stem growth at low water potentials. Plant Physiol 93: 1601–1609 (1990).
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).
O'Toole JC, Baldia EP: Water deficits and mineral uptake in rice. Crop Sci 22: 1144–1150 (1982).
Pardo JM, Serrano R: Structure of a plasma membrane H+-ATPase gene from the plant Arabidopsis thaliana. J Biol Chem 264: 8557–8562 (1989).
Poole RJ: Energy coupling for membrane transport. Ann Rev Plant Physiol 29: 437–460 (1978).
Rayle DL, Cleland RE: Control of plant cell enlargement by hydrogen ions. Curr Top Develop Biol 11: 187–214 (1977).
Serrano R: Plasma membrane ATPase of plants and fungi. CRC Press, Boca Raton, FL (1985).
Serrano R: Structure and function of proton translocation ATPase in plasma membranes of plants and fungi. Biochim Biophys Acta 947: 1–28 (1988).
Serrano R: Structure and function of plasma membrane ATPase. Ann Rev Plant Physiol Plant Mol Biol 40: 61–94 (1989).
Skriver K, Mundy J: Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2: 503–512 (1990).
Staswick PE: Soybean vegetative storage protein structure and gene expression. Plant Physiol 87: 250–254 (1988).
Staswick PE: Developmental regulation and the influence of plant sinks on vegetative storage protein gene expression in soybean leaves. Plant Physiol 89: 309–315 (1989).
Staswick PE: Correction. Plant Physiol 89: 717 (1989).
Staswick PE: Preferential loss of an abundant storage protein from soybean pods during seed development. Plant Physiol 90: 1252–1255 (1989).
Staswick PE: Novel regulation of vegetative storage protein genes. Plant Cell 2: 1–6 (1990).
Sussman MR, Surowy TK: Physiology and molecular biology of membrane ATPases. In: Mifflin BJ (ed) Oxford Surveys of Plant Molecular and Cell Biology, Vol 4, pp. 47–70. Oxford University Press, Oxford (1987).
Sze H: H+-translocating ATPases: advances using membrane vesicles. Ann Rev Plant Physiol 36: 175–208 (1985).
Tanimoto E, Igari M: Correlation between β-galactosidase and auxin-induced elongation growth in etiolated pea stems. Plant Cell Physiol 17: 673–682 (1976).
VanVolkenburgh E, Boyer JS: Inhibitory effects of water deficit on maize leaf elongation. Plant Physiol 77: 190–194 (1985).
Verasan V, Phillips RE: Effects of soil water stress on growth and nutrient accumulation in corn. Agron J 70: 613–618 (1978).
Verwoerd TC, Dekker BMM, Hockema A: A small-scale procedure for the rapid isolation of plant RNAs. Nucl Acids Res 17: 2362 (1989).
Westgate M, Boyer JS: Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize. Planta 164: 540–549 (1985).
Wittenbach VA: Purification and characterization of a soybean leaf storage glycoprotein. Plant Physiol 73: 125–129 (1983).
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Surowy, T.K., Boyer, J.S. Low water potentials affect expression of genes encoding vegetative storage proteins and plasma membrane proton ATPase in soybean. Plant Mol Biol 16, 251–262 (1991). https://doi.org/10.1007/BF00020556
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DOI: https://doi.org/10.1007/BF00020556