Plant cysteine endoproteinases and their multiple physiological roles

Małgorzata Grudkowska

m.grudkowska@ihar.edu.pl
Instytut Hodowli i Aklimatyzacji Roślin w Radzikowie (Poland)

Barbara Zagdańska


Zakład Biochemii, Szkoła Główna Gospodarstwa Wiejskiego w Warszawie (Poland)

Abstract

Cysteine endoproteinases are recognised as the major enzymes responsible for the initiation and subsequent massive hydrolysis of seed storage proteins during germination and early seedling growth and development. These enzymes are also involved in such important processes as organ senescence and xylogenesis. In response to unfavourable environmental conditions like low and high temperature, water deficit and salinity as well as to biotic stresses, the up-regulation of expression of genes encoding cysteine endoproteinases has been shown. Their supposed physiological function is not restricted to removal of denatured proteins, toxic in cases of pathogen infection or insect attack, abnormal proteins resulting from the stress-induced changes and to degradation of proteins no longer required by a cell in a new metabolic state. Another important function of these enzymes may be linked to activation of stress-induced non-specific proteins. On the basis of experiments carried out on 55 cultivars and strains of winter wheat and on ten cultivars of spring wheat it has been shown that the induction of cysteine endoproteinases was significantly correlated with the level of drought tolerance of spring and winter wheat as well as with the level of frost tolerance of winter wheat.


Keywords:

cysteine endoproteinases, protein hydrolysis, frost resistance, drought resistance, biotic stress resistance

Beers E. P., Freeman T. B. 1997. Proteinase activity during tracheary element differentiation in Zinnia mesophyll cultures. Plant Physiol. 113:873 — 880. DOI: https://doi.org/10.1104/pp.113.3.873
Google Scholar

Beers E. P., Woffenden B. J., Zhao Ch. 2000. Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44: 399 — 415. DOI: https://doi.org/10.1023/A:1026556928624
Google Scholar

Bethke P. C., Swanson S. J., Hillmer S., Jones R. 1998. From storage compartment to lytic organelle: the metamorphosis of the aleurone protein storage vacuole. Ann. Bot. 82: 399 — 412. DOI: https://doi.org/10.1006/anbo.1998.0702
Google Scholar

Bewley J. D., Black M. 1994. Seeds. Physiology of Development and Germination, 2nd ed. Plenum, New York. DOI: https://doi.org/10.1007/978-1-4899-1002-8
Google Scholar

Bottari A., Cappocchi A., Fontanini D., Galeschi L. 1996. Major proteinase hydrolysing gliadin during wheat germination. Phytochem. 43: 39 — 44. DOI: https://doi.org/10.1016/0031-9422(96)00193-8
Google Scholar

Callis J. 1995. Regulation of protein degradation. Plant Cell 7: 845 – 857. DOI: https://doi.org/10.1105/tpc.7.7.845
Google Scholar

Cercós M., Harris N., Carbonell J. 1993. Immunolocalization of a thiol-protease induced during the senescence of unpollinated pea ovaries. Physiol. Plant. 88: 275 — 280. DOI: https://doi.org/10.1111/j.1399-3054.1993.tb05499.x
Google Scholar

deBarros E.G., Larkins B.A. 1994. Cloning of a cDNA encoding a putative cysteine protease gliadin during wheat germination. Phytochem. 43: 39 — 44.
Google Scholar

del Pozo O., Lam E. 1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8: 1129 — 1132. DOI: https://doi.org/10.1016/S0960-9822(98)70469-5
Google Scholar

Diaz P., Wilson K. A., Tan-Wilson A. L. 1993. Immunocytochemical analysis of proteolysis in germinating soybean. Phytochem. 33 (5): 961 — 968. DOI: https://doi.org/10.1016/0031-9422(93)85005-C
Google Scholar

Downing W. L., Mauxion F., Fauvarque M. O., de Vienne D., Vartanian N., Giraudat J. 1992. A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water stress in leaves, not in seeds. Plant J. 5: 685 — 693. DOI: https://doi.org/10.1046/j.1365-313X.1992.t01-11-00999.x
Google Scholar

Enari T. M., Sopanen T. 1986. Mobilization of endosperm reserves during germination of barley. J. Inst. Brew. 92: 25 — 31. DOI: https://doi.org/10.1002/j.2050-0416.1986.tb04371.x
Google Scholar

Fischer J., Becker C., Hillmer S., Horstmann C., Neubohn B., Schlereth A., Senyuk V., Shutov A., Muntz K. 2000. The families of papain- and legumain like cysteine proteinases from embryonic axes and cotyledons of Vicia seeds: developmental patterns, intercellular localization and functions in globulin proteolysis. Plant Mol. Biol. 48:83 — 101. DOI: https://doi.org/10.1023/A:1006456615373
Google Scholar

Fukuda H. 1996. Xylogenesis: initiation, progression and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 299 — 325. DOI: https://doi.org/10.1146/annurev.arplant.47.1.299
Google Scholar

Funk V., Kositsup B., Zhao Ch., Beers E. P. 2002. The arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog. Plant Physiol. 128: 89 — 94. DOI: https://doi.org/10.1104/pp.010514
Google Scholar

Greenberg J. T. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA. 93: 12094 — 12097. DOI: https://doi.org/10.1073/pnas.93.22.12094
Google Scholar

Grudkowska M., Wiśniewski K., Zagdańska B. 2001. Endoproteinazy cysteinowe w siewkach pszenicy zaaklimatyzowanych do niskiej temperatury i suszy. Streszczenia str. 300. XXXVII Zjazd P T Bioch. Toruń.
Google Scholar

Grudkowska M., Wiśniewski K., Zagdańska B. 2002 Aktywność endoproteinaz cysteinowych wskaźnikiem odporności siewek pszenicy ozimej na mróz i suszę. Biul. IHAR 223/224: 45 — 55.
Google Scholar

Guerrero C., Calle M., Reid M. S., Valpuesta V. 1998. Analysis of the expression of two thiolprotease genes from daylily (Hemerocallis spp.) during flower senescence. Plant Mol. Biol. 36:565 — 571. DOI: https://doi.org/10.1023/A:1005952005739
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. DOI: https://doi.org/10.1007/BF00017720
Google Scholar

Ho S. L., Tong W. F., Yu S. M. 2000. Multiple mode of regulation of cysteine proteinase gene expression in rice. Plant Physiol. 122: 57 — 66. DOI: https://doi.org/10.1104/pp.122.1.57
Google Scholar

Holwerda B. C., Rogers J. C. 1992. Purification and characterization of aleurain Plant Physiol. 99: 848 — 855. DOI: https://doi.org/10.1104/pp.99.3.848
Google Scholar

Huang Y-J., To K-Y., Yap M-N., Chiang W-J., Suen D-F., Chen S-C.G. 2001. Cloning and characterization of leaf senescence up-regulated genes in sweet potato. Physiol. Plant. 113: 384 — 391. DOI: https://doi.org/10.1034/j.1399-3054.2001.1130312.x
Google Scholar

Ingram J., Bartels D. 1996. The molecular basis of dehydration tolerance in plant. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 377 — 403. DOI: https://doi.org/10.1146/annurev.arplant.47.1.377
Google Scholar

Ishii S. I. 1994. Legumain: asparaginyl endopeptidase. Methods Enzymol. 224: 604 — 615. DOI: https://doi.org/10.1016/0076-6879(94)44044-1
Google Scholar

Jabs T., Dietrich R. A., Dangl J. L. 1996. Initiation of runway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273: 1853 — 1856. DOI: https://doi.org/10.1126/science.273.5283.1853
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. DOI: https://doi.org/10.1007/BF00032666
Google Scholar

Koehler S. M., Ho T. D. 1990. A major gibberellic acid-induced barley aleurone cysteine proteinase which digest hordein. Plant Physiol. 94: 251 — 258. DOI: https://doi.org/10.1104/pp.94.1.251
Google Scholar

Koizumi M., Yamaguchi- Shinozaki K., Tsuji H., Shinozaki K. 1993. Structure and expression of two genes that encode distinct drought- inducible cysteine proteinases in Arabidopsis thaliana. Gene 129: 175 — 182. DOI: https://doi.org/10.1016/0378-1119(93)90266-6
Google Scholar

Lam E., del Pozo O. 2000. Caspase-like protease involvement in the control of plant cell death. Plant Mol. Biol. 44: 417 — 428. DOI: https://doi.org/10.1023/A:1026509012695
Google Scholar

Mittler R., Simon L., Lam E. 1997. Pathogen-induced programmed cell death in tobacco. J. Cell Sci. 110: 1333 — 1344. DOI: https://doi.org/10.1242/jcs.110.11.1333
Google Scholar

Mlejnek P., Prochazka S. 2002. Activation of caspase-like proteases and induction of apoptosis by isopeptydyloadenosine in tobacco BY-2 cells. Planta 215: 158 — 166. DOI: https://doi.org/10.1007/s00425-002-0733-5
Google Scholar

Müntz K. 1996. Proteases and proteolytic cleavage of storage proteins in developing and germinating dicotyledonous seeds. J. Exp. Bot. 47: 605 — 622. DOI: https://doi.org/10.1093/jxb/47.5.605
Google Scholar

Nishio N., Satoh H. 1997. A water soluble chlorophyll protein in cauliflower may be identical to BnD22, a drought- induced 22- kilodalton protein in rapeseed. Plant Physiol. 115: 841 — 846. DOI: https://doi.org/10.1104/pp.115.2.841
Google Scholar

Pechan T., Ye L., Chang Y., Mitra A., Lin L., Davies F., Williams W., Luthe D. 2000. A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12: 1031 — 1040. DOI: https://doi.org/10.1105/tpc.12.7.1031
Google Scholar

Phillips H. A., Wallace W. 1989. A cysteine endopeptidase from barley malt which degrades hordein. Phytochem. 28 (12): 3285 — 3290. DOI: https://doi.org/10.1016/0031-9422(89)80332-2
Google Scholar

Rawlings N. D., Barret A. J. 1993. Evolutionary families of peptidases. Biochem. 299: 205 — 218. DOI: https://doi.org/10.1042/bj2900205
Google Scholar

Schaffer M. A., Fischer R. L. 1988. Analysis of mRNAs that accumulate in response to low temperature identifies a thiol protease gene in tomato. Plant Physiol. 87: 431 — 436. DOI: https://doi.org/10.1104/pp.87.2.431
Google Scholar

Schaffer M. A., Fischer R. L. 1990 Transcriptional activation by heat an cold of a thiol protease gene in tomato. Plant Physiol. 93: 1486 — 1491. DOI: https://doi.org/10.1104/pp.93.4.1486
Google Scholar

Schlereth A., Becker C., Horstmann C., Tiedemann J., Müntz K. 2000. Comparison of globulin mobilization and cysteine proteinases in embryonic axes and cotyledons during germination and seedling growth of vetch (Vicia sativa L.). J. Exp. Bot. 51: 1423 — 1433. DOI: https://doi.org/10.1093/jexbot/51.349.1423
Google Scholar

Schlereth A., Standhardt D., Mock H.P., Müntz K. 2001. Stored cysteine proteinases start globulin mobilization in protein bodies of embryonic axes and cotyledons during vetch (Vicia sativa L.) seed germination. Planta 212: 718 — 727. DOI: https://doi.org/10.1007/s004250000436
Google Scholar

Schmid M., Simpson D., Gietl Ch. 1999. Programmed cell death in castor beam endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. Proc. Natl. Acad. Sci USA 96: 14159 — 14164. DOI: https://doi.org/10.1073/pnas.96.24.14159
Google Scholar

Shewry P. R., Napier J. A., Tatham A. S. 1995. Seed storage proteins: structures and biosynthesis. Plant Cell 7: 945 — 956. DOI: https://doi.org/10.1105/tpc.7.7.945
Google Scholar

Shutov A. D., Vaintraub I. A. 1987. Degradation of storage proteins in germinating seeds. Phytochem. 26: 1557 — 1566. DOI: https://doi.org/10.1016/S0031-9422(00)82245-1
Google Scholar

Simpson D. J. 2001. Proteolytic degradation of cereal prolamins — the problem with proline. Plant Sci. 161: 825 — 838. DOI: https://doi.org/10.1016/S0168-9452(01)00482-4
Google Scholar

Solomon M., Belenghi B., Delledonne M., Menachem E., Levine A. 1999. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plant. Plant Cell 11: 431 — 443. DOI: https://doi.org/10.1105/tpc.11.3.431
Google Scholar

Tiedemann J., Schlereth A., Müntz K. 2001. Differential tissue- specific expression of cysteine proteinases forms the basis for the fine-tuned mobilization of storage globulin during and after germination in legume seeds. Planta 212: 728 — 738. DOI: https://doi.org/10.1007/s004250000435
Google Scholar

Vincent J. L., Brewin N. J. 2000. Immunolocalization of cysteine protease in vacuoles, vesicles, and symbiosomes of pea nodule cells. Plant Physiol. 123: 521 — 530. DOI: https://doi.org/10.1104/pp.123.2.521
Google Scholar

Wagstaff C., Leverentz M. K., Griffith G., Thomas B., Chanasut U., Stead A. D., Roger H. J. 2002. Cysteine protease gene expression and proteolytic activity during senescence of Alstroemeria petals. J. Exp. Bot. 53: 233 — 240. DOI: https://doi.org/10.1093/jexbot/53.367.233
Google Scholar

Wiśniewski K., Zagdańska B. 2001. Genotype- dependent proteolytic response of spring wheat to water deficiency. J. Exp. Bot. 52: 1455 — 1463. DOI: https://doi.org/10.1093/jexbot/52.360.1455
Google Scholar

Xu Y., Hanson R. 2000. Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol. 122: 1323 — 1333. DOI: https://doi.org/10.1104/pp.122.4.1323
Google Scholar

Zagdańska B., Wiśniewski K. 1996. Endoproteinase activities in wheat leaves upon water deficit. Acta Biochim. Polon. 43: 515 — 520. DOI: https://doi.org/10.18388/abp.1996_4485
Google Scholar

Zhang N., Jones B. L. 1996. Purification and partial characterization of a 31-kDa cysteine endopeptidase from germinated barley. Planta 199: 565 — 572. DOI: https://doi.org/10.1007/BF00195188
Google Scholar

Zhao C., Johnson B. J., Kositsup B., Beers E. P. 2000. Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol. 123: 1185 — 1196. DOI: https://doi.org/10.1104/pp.123.3.1185
Google Scholar


Published
2002-12-31

Cited by

Grudkowska, M. and Zagdańska, B. (2002) “Plant cysteine endoproteinases and their multiple physiological roles”, Bulletin of Plant Breeding and Acclimatization Institute, (223/224), pp. 33–43. doi: 10.37317/biul-2002-0002.

Authors

Małgorzata Grudkowska 
m.grudkowska@ihar.edu.pl
Instytut Hodowli i Aklimatyzacji Roślin w Radzikowie Poland

Authors

Barbara Zagdańska 

Zakład Biochemii, Szkoła Główna Gospodarstwa Wiejskiego w Warszawie Poland

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Copyright (c) 2002 Małgorzata Grutkowska, Barbara Zagdańska

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