Mechanisms of protein degradation and their role in plant resistance to frost and drought
Barbara Zagdańska
b.zagdanska@ihar.edu.plZakład Fizjologii i Biochemii Roślin, Instytut Hodowli i Aklimatyzacji Roślin w Radzikowie (Poland)
Abstract
The intracellular protein level depends both on the rate of synthesis and degradation. Protein degradation may proceed by two main pathways: the less selective vacuolar pathway and the selective non-vacuolar pathway. The vacuolar proteolysis is energy-independent, although energy is required for the transport of substrates to vacuoles. The non-vacuolar proteolysis may be either energy-dependent or energy-independent. The remodelling of cellular proteins in dehydrated wheat leaves is associated with an extensive proteolysis mediated by both vacuolar and non-vacuolar, ATP-dependent pathways. Experiments with ten genotypes of spring wheat differing in dehydration tolerance and acclimation ability indicate that dehydration tolerance is associated with a lower induction of the vacuolar proteolysis, including cysteine endoproteinases and derepression of the ATP-dependent proteolysis as compared with drought sensitive genotypes. At the heading phase similar compensation did not occur in the drought tolerant genotypes as well as genotype-dependent dehydration tolerance was not related to the derepression of ATP-dependent proteolysis in acclimated leaves. Among the winter wheat genotypes, induction of cysteine endoproteinases was significantly negatively correlated with the level of both frost resistance and dehydration tolerance. One can suppose that genetically-dependent response of wheat to abiotic stresses is generally reflected by the rate of removal of non-required or damaged proteins by the vacuolar proteolysis.
Keywords:
ATP-dependent proteolysis, cysteine endoproteinases, dehydration tolerance, frost resistance, vacuolar proteolysisReferences
Andersson B., Aro E. M. 1997. Proteolytic activities and proteases of plant chloroplasts. Physiol. Plant. 100: 794 — 805.
Google Scholar
Aubert S., Gout E., Bligny R., Marty-Mazars F., Alabouvette J., Marty F., Douce R. 1996. Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: Control by the supply of mitochondria with respiratory substrates. J. Cell Biol. 133, 1251 — 1263.
Google Scholar
Bachmair A., Finley D., Varschavsky A. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179 — 186.
Google Scholar
Barakat S., Pearce D. A., Sherman F., Rapp W. D. 1998. Maize contains a Lon protease gene that partially complements a yeast pim-1 deletion mutant. Plant Mol. Biol. 37: 141-154.
Google Scholar
Baumeister W., Walz J., Zühl F., Seemüller E. 1998. The proteasome: paradigm of a self-compartmentalizing protease. Cell 92: 367 — 380.
Google Scholar
Belozersky M. A., Sarbakanova S. T., Dunaevsky Y. E. 1989. Aspartic proteinase from wheat seeds: location, properties and action on gliadin. Planta 177: 321 — 326.
Google Scholar
Bethke P. C., Hillmer S., Jones R. L. 1996. Isolation of intact protein storage vacuoles from barley aleurone. Identification of aspartic and cysteine proteases. Plant Physiol. 110: 521 — 529.
Google Scholar
Bethke P. C., Swanson S. J., Hillmer S., Jones R. L. 1998. From storage compartment to lytic organelle: the metamorphosis of the aleurone protein storage vacuole. Ann. Bot. 82: 399 — 412.
Google Scholar
Callis J. 1995. Regulation of protein degradation. The Plant Cell 7: 845 — 857.
Google Scholar
Cordeiro M. C., Pais M. S., Brodelius P. E. 1994 a. Tissue-specific expression of multiple forms of cyprosin (aspartic proteinase) in flowers of Cynara cardunculus. Physiol. Plant. 92: 645 — 653.
Google Scholar
Cordeiro M. C., Xue Z. T., Pietrzak M., Pais M .S., Brodelius P. E. 1994 b. Isolation and characterization of a cDNA from flowers of Cynara cardunculus encoding cyprosin (an aspartic proteinase) and its use to study the organ-specific expression of cyprosin. Plant Mol. Biol. 24: 733 — 741.
Google Scholar
D’Andrea A., Pellman D. 1998. Deubiquitinting enzymes: a new class of biological regulators. CR Biochem. Mol. Biol. 33: 337 — 352.
Google Scholar
Davies D.R. 1990. The structure and function of the aspartic proteinases. Annu Rev. Biophys. Biophys. Chem. 19: 189 — 215.
Google Scholar
Ehlers K., Schulz M., Kollmann R. 1996. Subcellular localization of ubiquitin in plant protoplasts and the function of ubiquitin in selective degradation of outer-wall plasmodesmata in regenerating protoplasts. Planta 199: 139 — 151.
Google Scholar
Fenteany G., Standaert R. F., Lane W. S., Choi S., Corey E. J., Schreiber S. L. 1995. Inhibition of proteasome activities and subunit-specific amino-acid terminal threonine modification by lactacystin. Science, 268: 726 — 731.
Google Scholar
Guerrero F. D., Jones J. T., Mullet J. E. 1990. Turgor-responsive gene transcription and RNA levels increase rapidly when pea shoots are wilted and expression of three inducible genes. Plant Mol. Biol. 15:
Google Scholar
— 26.
Google Scholar
Heimgartner U., Pietrzak M., Geertsen R., Brodelius P., da Silva Figueiredo A.C., Pais M.S.S. 1990. Purification and partial characterization of milk clotting proteases from flowers of Cynara cardunculus. Phytochem. 29: 1405 — 1410.
Google Scholar
Herman E.M., Larkins B. 1999. Protein storage bodies and vacuoles. Plant Cell 11: 601 — 613.
Google Scholar
Hershko A., Ciechanover A. 1982. Mechanisms of intracellular protein breakdown. Ann. Rev. Biochem. 51: 335 — 364.
Google Scholar
Hershko A., Ciechanover A. 1992. The ubiquitin system for protein degradation. Annu. Rev. Biochem. 61: 761 — 807.
Google Scholar
Hicke L., Riezman H. 1996. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84: 277 — 287.
Google Scholar
Hicke, L. 2001. Protein regulation by monoubiquitin. Nature Reviews 2 (3): 195 — 201.
Google Scholar
Higgins T.J.V. 1984. Synthesis and regulation of major proteins in seeds. Annu. Rev. Plant Physiol. 35: 191 — 221.
Google Scholar
Hilt W., Wolf D. H. 1996. Protesomes: destruction as a programme. Trends Plant Sci. 21: 96 — 101.
Google Scholar
Holverda B. C., Padgett H. S., Rogers J. C. 1992. Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions. Plant Cell 4: 307 — 318.
Google Scholar
Holverda B.C., Rogers J.C. 1992. Purification and characterization of aleurain. A plant thiol protease functionally homologous to mammalian cathepsin H. Plant Physiol. 99: 848 — 855.
Google Scholar
Guerrero F.D., Jones J.T., Mullet J.E., 1990. 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.
Google Scholar
Ingram J., Bartels D. 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 377 — 403.
Google Scholar
Jones J.T., Mullet J.E. 1995. A salt- and dehydration-inducible pea gene, Cyp15a, encodes a cell-wall protein with sequence similarity to cysteine proteases. Plant Mol. Biol. 28: 1055 — 1065.
Google Scholar
Kervinen J., Kontturi M., Mikola J. 1990. Changes in the proteinase composition of barley leaves during senescence in field conditions. Cereal Res. Commun. 18: 191 — 197.
Google Scholar
Kjellbom P., Larsson C., Johansson I., Karlsson M., Johanson U. 1994. Aquaporins and water homeostasis in plants. Trends Plant Sci 4: 308 — 314.
Google Scholar
Kuwabara T., Suzuki K. 1995. Reversible changes in conformation of the 25-kDa protein of photosystem II and their relationship to the susceptibility of the protein to a proteinase from photosystem II membranes. Plant Cell Physiol. 36: 495 — 504.
Google Scholar
Lupas A., Flanagan J. M., Tamura T., Baumeister W. 1997. Self-compartmentalizing proteases. 22: 399 — 404.
Google Scholar
Martilla S., Jones B. L., Mikkonen A. 1995. Differential localization of two acid proteinases in germinating barley (Hordeum vulgare) seed. Physiol. Plant. 93: 317 — 327.
Google Scholar
Marty F. 1999. Plant vacuoles. The Plant Cell 11: 587 — 599.
Google Scholar
Miao G. H., Verma D. P. S. 1993. Soybean nodulin-26 gene encoding a channel protein is expressed only in the infected cells of nodules and is regulated differently in roots of homologous and heterologous plants. Plant Cell 5: 781 — 794.
Google Scholar
Miller B. L., Huffaker R. C. 1981. Partial purification and characterization of endoproteinases from senescing barley leaves. Plant Physiol. 68: 930 — 936.
Google Scholar
Moriyasu Y., Ohsumi Y. 1996. Autophagy in tobacco suspension — cultured cells in response to sucrose starvation. Plant Physiol. 111: 1233 — 1241.
Google Scholar
Mutlu A., Gal S. 1999. Plant aspartic proteinases: enzymes on the way to a function. Physiol. Plant. 105: 569 — 576.
Google Scholar
Neuhaus J. .M., Rogers J. C. 1998. Sorting of proteins to vacuoles in plant cells. Plant Mol. Biol. 38: 127 — 144.
Google Scholar
Paris N., Stanley C. M., Jones R. L., Rogers J. C. 1996. Plant cells contain two functionally distinct vacuolar compartments. Cell 85: 563 — 572.
Google Scholar
Radłowski M., Kalinowski A., Adamczyk J., Królikowski Z., Bartkowiak S. 1996. Proteolytic activity in the maize pollen wall. Physiol. Plant. 98: 172 — 178.
Google Scholar
Ramalho-Santos M., Pissarra J., Verissimo P., Pereira S., Salema R., Pires E., Faro C. 1997. Cardosin A, an abundant aspartic proteinase accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 203: 204 — 212.
Google Scholar
Rawlings N. D., Barret A. J. 1995. Families of aspartic peptidases, and those of unknown catalytic mecha¬nism. Meth. Enzymol. 248: 105 — 120.
Google Scholar
Rechsteiner M., Hoffman L., Dubiel W. 1993. The multicatalytic and 26S proteases. J. Biol. Chem. 268: 6065 — 6068.
Google Scholar
Rodrigo I., Vera P., Conejero V. 1989. Degradation of tomato pathogenesis — related protein by an endogenous 37 kDa aspartyl endoproteinase. Eur. J. Biochem. 184: 663 — 669.
Google Scholar
Rogers J. C., Dean D., Heck G. R. 1985. Aleurain: a barley thiol protease closely related to mammalian cathepsin H. Proc. Natl. Acad. Sci USA 82: 6512 — 6516.
Google Scholar
Runenberg-Roos P., Saarma M. 1998. Phytepsin, a barley vacuolar aspartic proteinase is highly expressed during autolysis of developing tracheary elements and sieve cells. Plant J. 15: 139 — 145.
Google Scholar
Schaffer M. A A., Fisher R. L.1990. Transcriptional activation by heat and cold of a thiol protease gene in tomato. Plant Physiol. 93: 1486 — 1492.
Google Scholar
Shuthov A. D., Vaintraub I. A. 1987. Degradation of storage proteins in germinating seeds. Phytochemistry 26: 1557 — 1566.
Google Scholar
Staszczak M., Zdunek E. 1999. Proteoliza wewnątrzkomórkowa. Postępy Biochemii 45: 32 — 41.
Google Scholar
Swanson S. J., Bethke P. C., Jones R. L. 1998. Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes. Plant Cell 10: 685 — 698.
Google Scholar
Tanaka K. 1998. Proteasomes: structure and biology. J. Biochem. 123: 195 — 204.
Google Scholar
von Kampen J., Wettern M., Schulz M. 1996. The ubiquitin system in plants. Physiol. Plant. 97: 618 — 624.
Google Scholar
Varshavsky A. 1997 a. The N-end rule pathway of protein degradation. Genes and Cells 2: 13 — 28.
Google Scholar
Varshavsky A. 1997 b. The ubiquitin system. Trends Biochem. Sci 22: 383 — 387.
Google Scholar
Verissimo P., Faro C., Moir A.J.G., Lin Y., Tang J., Pires E. 1996. Purification, characterization and partial amino acid sequencing of two new aspartic proteinases from fresh flowers of Cynara cardunculus L. Eur. J. Biochem. 235: 762 — 768.
Google Scholar
Vierstra R. D. 1993. Protein degradation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 385 — 410.
Google Scholar
Vincent J. L., Brewin N. J. 2000. Immunolocalization of a cysteine protease in vacuoles, vesicles, and symbiosomes of pea nodule cells. Plant Physiol. 123: 521 — 530.
Google Scholar
Watanabe H., Abe K., Emori K., Hosoyama H., Arai S. 1991. Molecular cloning and gibberellin — induced expression of multiple cysteine proteinases of rice seeds (oryzains). J. Biol. Chem. 266: 16897 — 16902.
Google Scholar
Weissman A. M. 2001. Themes and variations on ubiquitylaton. Nature Reviews 2(3): 169 — 178.
Google Scholar
Williams R. J., Bullman M., Huttly A., Phillips A., Neil S. 1994. Characterization of a cDNA from Arabidopsis thaliana encoding a potential thiol protease whose expression is induced independently by wilting and abscisic acid. Plant Mol. Biol. 25: 259 — 270.
Google Scholar
Wiśniewski K., Zagdańska B. 2001. Genotype — dependent proteolytic response of spring wheat to water deficiency. J. Exp. Bot. 52 (w druku).
Google Scholar
Zagdańska B. 1995. Respiratory energy demand for protein turnover and ion transport in wheat leaves upon water deficit. Physiol. Plant. 95: 428 — 436.
Google Scholar
Zagdańska B., Wiśniewski K. 1996. Endoproteinase activities in wheat leaves upon water deficits. Acta Bioch. Pol. 43: 512 — 520.
Google Scholar
Zagdańska B., Wiśniewski K. 1998. ATP-dependent proteolysis contributes to the acclimation — induced drought resistance in spring wheat. Acta Physiol. Plant. 20: 55 — 58.
Google Scholar
Authors
Barbara Zagdańskab.zagdanska@ihar.edu.pl
Zakład Fizjologii i Biochemii Roślin, Instytut Hodowli i Aklimatyzacji Roślin w Radzikowie Poland
Statistics
Abstract views: 9PDF downloads: 17
License
Copyright (c) 2025 Barbara Zagdańska

This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Upon submitting the article, the Authors grant the Publisher a non-exclusive and free license to use the article for an indefinite period of time throughout the world in the following fields of use:
- Production and reproduction of copies of the article using a specific technique, including printing and digital technology.
- Placing on the market, lending or renting the original or copies of the article.
- Public performance, exhibition, display, reproduction, broadcasting and re-broadcasting, as well as making the article publicly available in such a way that everyone can access it at a place and time of their choice.
- Including the article in a collective work.
- Uploading an article in electronic form to electronic platforms or otherwise introducing an article in electronic form to the Internet or other network.
- Dissemination of the article in electronic form on the Internet or other network, in collective work as well as independently.
- Making the article available in an electronic version in such a way that everyone can access it at a place and time of their choice, in particular via the Internet.
Authors by sending a request for publication:
- They consent to the publication of the article in the journal,
- They agree to give the publication a DOI (Digital Object Identifier),
- They undertake to comply with the publishing house's code of ethics in accordance with the guidelines of the Committee on Publication Ethics (COPE), (http://ihar.edu.pl/biblioteka_i_wydawnictwa.php),
- They consent to the articles being made available in electronic form under the CC BY-SA 4.0 license, in open access,
- They agree to send article metadata to commercial and non-commercial journal indexing databases.
Most read articles by the same author(s)
- Janusz Bogdan, Barbara Zagdańska, Drought resistance of spring wheat during germination and seedling growth , Bulletin of Plant Breeding and Acclimatization Institute: No. 233 (2004): Regular issue
- Małgorzata Grutkowska, Barbara Zagdańska, Zbigniew Rybka, Tolerance of spring wheat to soil drought at a heading phase , Bulletin of Plant Breeding and Acclimatization Institute: No. 228 (2003): Regular issue
- Małgorzata Grudkowska, Krzysztof Wiśniewski, Barbara Zagdańska, Cysteine endoproteinases activity as an indicator of wheat resistance to frost and drought , Bulletin of Plant Breeding and Acclimatization Institute: No. 223/224 (2002): Regular Issue
- Małgorzata Grudkowska, Barbara Zagdańska, Plant cysteine endoproteinases and their multiple physiological roles , Bulletin of Plant Breeding and Acclimatization Institute: No. 223/224 (2002): Regular Issue







