Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T04:49:11.708Z Has data issue: false hasContentIssue false
  • English
  • Français

The heat-shock response of developing barley aleurone layers

Published online by Cambridge University Press:  22 February 2007

Melissa A. Harju ,
Sunita deSouza  and
Mark R. Brodl
Melissa A. Harju
Affiliation:
Department of Biology, Knox College, Galesburg, IL 61401, USA
Sunita deSouza
Affiliation:
Department of Biology, Knox College, Galesburg, IL 61401, USA
Mark R. Brodl*
Affiliation:
Current addresses: Division of Biochemistry, New York University School of Medicine, New York, NY 10016, USA
*
*Correspondence Fax: +1 210999 7229, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Aleurone layers of mature germinating barley (Hordeum vulgare, cv. Himalaya) grains respond to heat shock by synthesizing heat-shock proteins (HSPs) and by selectively suppressing the synthesis of proteins normally translated by endoplasmic reticulum (ER)-bound ribosomes. To determine if this also was the case during seed development, we investigated the synthesis of proteins translated by ER-bound ribosomes in heat-shocked aleurone layers isolated from developing barley grains. The optimal induction temperature for the heat shock response in developing aleurone layers was 37.5°C, and temperatures above 42°C inhibited translation. HSPs with apparent molecular masses of 71.1, 66.2, 57.8, 19.1 and 18.8 kDa were induced. Other studies have shown that, in gibberellic acid (GA)-induced aleurone layers from mature barley grains, these temperatures were 40°C and 45°C, respectively. Furthermore, in developing aleurone layers, mRNAs encoding proteins translated by ER-bound ribosomes (mRNAs for a lipid transfer protein and a putative amylase/protease inhibitor) remained stable during heat shock. The ER membranes themselves remained in stacks, but the lumen became distended with electron-dense material. Heat shock prevented the movement of proteins from the ER into the rest of the endomembrane pathway. In contrast, other studies show that in mature, GA-induced aleurone layers, heat shock dissociates ER stacks and blocks translation, but the processing of secretory proteins in the endomembrane pathway is not inhibited. The observation that the same tissue at different developmental stages may respond differently to heat shock indicates that components of the heat-shock response are developmentally regulated. This system provides an opportunity to better understand the nuances of the heat-shock response, especially the post-transcriptional gene regulatory mechanisms that occur.

Keywords

aleuroneendoplasmic reticulumheat shockHimalaya barleyHordeum vulgaremRNA stability
Type
Research Article
Information
Seed Science Research , Volume 13 , Issue 3 , September 2003 , pp. 229 - 238
Copyright
Copyright © Cambridge University Press 2003

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschuler, M. and Mascarenhas, J.P. (1985) Transcription and translation of heat shock and normal proteins in seedlings and developing seeds of soybean exposed to a gradual temperature increase. Plant Molecular Biology 5, 291–297.CrossRefGoogle ScholarPubMed
Belanger, F.C., Brodl, M.R. and Ho, T.-h.D. (1986) Heat shock causes destabilization of specific mRNAs and destruction of endoplasmic reticulum in barley aleurone cells. Proceedings of the National Academy of Sciences, USA 83, 1354–1358.CrossRefGoogle ScholarPubMed
Bewley, J.D. and Black, M. (1982) Physiology and biochemistry of seeds, Vol. II. New York, Springer Verlag.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Brodl, M.R. and Ho, T.-h.D. (1991) Heat shock causes selective destabilization of secretory protein mRNAs in barley aleurone cells. Plant Physiology 96, 1048–1052.CrossRefGoogle ScholarPubMed
Brodl, M.R. and Ho, T.-h.D. (1992) Heat shock in mechanically wounded carrot root disks causes destabilization of stable secretory protein mRNA and dissociation of endoplasmic reticulum lamellae. Physiologia Plantarum 86, 253–262.CrossRefGoogle Scholar
Campbell, J.D., Fielding, L.A. and Brodl, M.R. (1997) Heat shock temperature acclimation of normal secretory protein synthesis in barley aleurone cells. Plant, Cell and Environment 20, 1349–1360.CrossRefGoogle Scholar
Chirgwin, J.M., Pryzbyla, A.E., MacDonald, R.J. and Rutter, W.J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294–5299.CrossRefGoogle ScholarPubMed
Chrispeels, M.J. and Greenwood, J.S. (1987) Heat stress enhances phytohemagglutinin synthesis but inhibits its transport out of the endoplasmic reticulum. Plant Physiology 83, 778–784.CrossRefGoogle ScholarPubMed
Chu, B., Brodl, M.R. and Belanger, F.C. (1997) Heat shock inhibits release of the signal recognition particle from the endoplasmic reticulum in barley aleurone layers. Journal of Biological Chemistry 272, 7306–7313.CrossRefGoogle ScholarPubMed
Cooper, P. and Ho, T.-h., D. (1983) Heat shock proteins in maize. Plant Physiology 71, 215–222.CrossRefGoogle ScholarPubMed
Cooper, P. and Ho, T.-h.D. (1987) Intracellular localization of heat shock proteins in maize. Plant Physiology 84, 1197–1203.CrossRefGoogle ScholarPubMed
Fernandez, D.E. and Staehelin, L.A. (1987) Does gibberellic acid induce the transfer of lipase from protein bodies to lipid bodies in barley aleurone cells? Plant Physiology 85, 487–496.CrossRefGoogle ScholarPubMed
Glover, C.V.C. (1982) Heat shock induces rapid dephosphorylation of a ribosomal protein in Drosophila. Proceedings of the National Academy of Sciences, USA, 79, 1781–1785.CrossRefGoogle ScholarPubMed
Gram, N.H. (1982) The ultrastructure of germinating barley seeds. I. Changes in the scutellum and the aleurone layer in nordal barley. Carlsberg Research Communications 47, 143–162.CrossRefGoogle Scholar
Grindstaff, K.K., Fielding, L.A. and Brodl, M.R. (1996) Effect of gibberellins and heat shock on the lipid composition of endoplasmic reticulum in barley aleurone layers. Plant Physiology 110, 571–581.CrossRefGoogle ScholarPubMed
Hayat, M.A. (1989) Principles and techniques of electron microscopy: Biological applications. (3rd edition). Boca Raton, FL, CRC Press.CrossRefGoogle Scholar
Jakobsen, K., Klemsdal, S.S., Aalen, R.B., Bosnes, M., Alexander, D. and Olsen, O.-A. (1989) Barley aleurone cell development: Molecular cloning of aleurone-specific cDNAs from immature grains. Plant Molecular Biology 12, 285–293.CrossRefGoogle ScholarPubMed
Johnston, M.K., Benson, P.A.S., Rogers, T.M. and Brodl, M.R. (2002) Slow heating of barley aleurone layers to heat shock temperature preserves heat shock-sensitive cellular properties. American Journal of Botany 89, 401–409.CrossRefGoogle ScholarPubMed
Jones, R.L. (1969a) Gibberellic acid and the fine structure of barley aleurone cells: I. Changes during the lag phase of α-amylase synthesis. Planta 87, 119–133.CrossRefGoogle ScholarPubMed
Jones, R.L. (1969b) Gibberellic acid and the fine structure of barley aleurone cells: II. Changes during the synthesis and secretion of α-amylase. Planta 88, 73–86.CrossRefGoogle ScholarPubMed
Jones, R.L. (1980) The isolation of endoplasmic reticulum from barley aleurone layers. Planta 150, 58–69.CrossRefGoogle ScholarPubMed
Key, J.L., Lin, C.-Y. and Chen, Y.M. (1981) Heat shock proteins of higher plants. Proceedings of the National Academy of Sciences, USA 78, 3526–3530.CrossRefGoogle ScholarPubMed
Lanciloti, D.F., Cwik, C. and Brodl, M.R. (1996) Heat shock proteins do not provide thermoprotection to normal cellular protein synthesis, α-amylase mRNA and endoplasmic reticulum lamellae in barley aleurone layers. Physiologia Plantarum 97, 513–523.CrossRefGoogle Scholar
Lindquist, S. (1981) Regulation of protein synthesis during heat shock. Nature 293, 311–314.CrossRefGoogle ScholarPubMed
Lis, J. and Wu, C. (1993) Protein traffic on the heat shock promoter: Parking, stalling, and trucking along. Cell 74, 1–4.CrossRefGoogle ScholarPubMed
McGarry, T.J. and Lindquist, S. (1985) The preferential translation of Drosophila hsp70 mRNA requires sequences in the untranslated leader. Cell 42, 903–911.CrossRefGoogle ScholarPubMed
Morimoto, R.I., Jurivich, D.A., Kroeger, P.E., Mathur, S.K., Murphy, S.P., Nakai, A., Sarge, K., Abravaya, K. and Sistonen, L.T. (1994) Regulation of heat shock gene transcription by a family of heat shock factors. pp. 417–455in Morimoto, R.I.;Tissières, A.;Georgopulos, C. (Eds) The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory Press.Google Scholar
Mundy, J. and Rogers, J.C. (1986) Selective expression of a probable amylase/protease inhibitor in barley aleurone cells: Comparison to the barley amylase/subtilisin inhibitor. Planta 169, 51–63.CrossRefGoogle Scholar
Nagao, R.T., Kimple, J.K., Vierling, E. and Key, J.L. (1986) The heat shock response: A comparative analysis. pp. 384–438in Miflin, B.J. (Ed.) Oxford surveys of plant molecular and cell biology. Vol. 3. Oxford, UK, Oxford UniversityPress.Google Scholar
Naumann, R. and Dorffling, K. (1982) Variation of free and conjugated abscisic acid, phaseic acid, and dihydrophaseic acid levels in ripening barley grains. Plant Science Letters 27, 111–117.CrossRefGoogle Scholar
Nover, L. (1994) The heat shock response as part of the plant stress network: An overview with six tables. pp. 3–45in Cherry, J. (Ed.) Biochemical and cellular mechanisms of stress tolerance in plants. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Nover, L., Scharf, K.-D. and Neumann, D. (1989) Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Molecular and Cellular Biology 9, 1298–1308.Google ScholarPubMed
Olsen, A.S., Triemer, D.F. and Sanders, M.M. (1983) Dephosphorylation of S6 and expression of the heat shock response in Drosophila melanogaster. Molecular and Cellular Biology, 3, 2017–2027.Google ScholarPubMed
Picton, S. and Grierson, D. (1988) Inhibition of expression of tomato-ripening genes at high temperature. Plant, Cell and Environment 11, 265–272.CrossRefGoogle Scholar
Rastogi, V. and Oaks, A. (1986) Hydrolysis of storage proteins in barley endosperms – analysis of soluble products. Plant Physiology 81, 901–906.CrossRefGoogle ScholarPubMed
Spiess, C., Beil, A. and Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97, 339–347.CrossRefGoogle Scholar
Staehelin, L.A. (1997) The plant ER: A dynamic organelle composed of a large number of discrete functional domains. Plant Journal 11, 1151–1165.CrossRefGoogle Scholar
Sticher, L., Biswas, A.K., Bush, D.S. and Jones, R.L. (1990) Heat shock inhibits α-amylase synthesis in barley aleurone without inhibiting the activity of endoplasmic reticulum marker enzymes. Plant Physiology 92, 506–513.CrossRefGoogle ScholarPubMed
Storti, R.V., Scott, M.P., Rich, A. and Pardue, M.L. (1980) Translational control of protein synthesis in response to heat shock in Drosophila melanogaster cells. Cell 22, 825–834.CrossRefGoogle Scholar
Taiz, L. and Zeiger, E. (2002) Plant physiology. (3rd edition). Sunderland, MA, Sinauer Associates.Google Scholar
Vierling, E. (1991) The roles of heat shock proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 42, 579–620.CrossRefGoogle Scholar
Wolffe, A.P., Perlman, A.J. and Tata, J.R. (1984) Transient paralysis of hormonal regulation of gene expression. EMBO Journal 3, 2763–2770.CrossRefGoogle ScholarPubMed
Zeevaart, J.D.A. and Creelmann, R.A. (1988) Metabolism and physiology of abscisic acid. Annual Review of Plant Physiology and Plant Molecular Biology 39, 439–473.CrossRefGoogle Scholar