Abstract
Dehydrins is a complex family of hydrophilic heat-stable proteins. Their properties and functions are inadequately studied. They are accumulated in plant tissues in response to any external stimulus causing dehydration of the cells. These stimuli may result from drought, salt stress, cooling, treatments with hormones, and seed maturation. Dehydrins are identified in cyanobacteria, tissues of gymnospermous and angiospermous plants, herbaceous and woody species, vegetative organs, and various embryonic tissues of seeds. They are thought to be essential elements in plants' resistance or tolerance to dehydration. Plant seeds are of special interest for investigating this group of proteins. In the resistant to dehydration orthodox seeds, dehydrins are synthesized and accumulated at the final stages of maturation associated with seed desiccation. Recalcitrant seeds that are sensitive to dehydration do not dry out upon maturation and retain high moisture content and active metabolism. These seeds are capable of dehydrin production but remain sensitive to water loss and cannot cope with a profound desiccation, unlike orthodox-type seeds. The review considers main properties and functions of dehydrins, their structure, classification, spread, and intracellular localization. Roles of dehydrins in recalcitrant seeds are discussed.
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REFERENCES
Palta, J.P., Stress interactions at the cellular and membrane levels, Hort. Sci., 1990, vol. 25, no. 11, p. 1377.
Levitt, J., Responses of Plants to Environmental Stresses, Vol. 1: Chilling, Freezing and High Temperature Stresses, New York: Academic, 1980.
Bewley, D.J., Bradford, K.J., Hilhorst, H.W.M., and Nonogaki, H., Seeds: Physiology of Development, Germination and Dormancy, New York: Springer, 2013.
Bray, E.A., Molecular responses to water deficit, Plant Physiol., 1993, vol. 103, p. 1035.
Beck, E.H., Fettig, S., Knake, C., Hartig, K., and Bhattarai, T., Specific and unspecific responses of plants to cold and drought stress, J. Biosci., 2007, vol. 32, p. 501.
Close, T.J., Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins, Physiol. Plant., 1996, vol. 97, p. 795.
Dure, L., III., Greenway, S.C., and Galau, G.A., Developmental biochemistry of cotton seed embryogenesis and germination—changing messenger ribonucleic acid population as shown by in vitro and in vivo protein synthesis, Biochemistry, 1981, vol. 20, p. 4162.
Allagulova, Ch.R., Gimalov, F.R., Shakirova, F.M., and Vakhitov, V.A., The plant dehydrins: structure and putative functions, Biochemistry (Moscow), 2003, vol. 68, p. 945.
Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., and Covarrubias, A.A., The enigmatic LEA proteins and other hydrophillins, Plant Physiol., 2008, vol. 148, p. 6. https://doi.org/10.1104/pp.108.120725
Amara, I., Zaidi, I., Masmoudi, K., Ludevid, M.D., Pagès, M., Goday, A., and Brini, F., Insights into late embryogenesis abundant (LEA) proteins in plants: from structure to the functions, Am. J. Plant Sci., 2014, vol. 5, p. 3440. https://doi.org/10.4236/ajps.2014.522360 https://doi.org/10.4236/ajps.2014.522360
Rorat, T., Plant dehydrins—tissue location, structure and function, Cell Mol. Biol. Lett., 2006, vol. 11, p. 536. https://doi.org/10.2478/s11658-006-0044-0
Tunnacliffe, A. and Wise, M.J., The continuing conundrum of the LEA proteins, Naturwissenschaften, 2007, vol. 94, p. 791.
Close, T.J., Kortt, A.A., and Chandler, P.M., A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn, Plant Mol. Biol., 1989, vol. 13, p. 95.
Galau, G.H., Huges, D.W., and Dure, L., III., Abscisic acid induction of cloned cotton late embryogenesis-abundant (LEA) mRNAs, Plant Mol. Biol., 1986, vol. 7, p. 150.
Mundy, J. and Chua, N.H., Abscisic acid and water-stress induce the expression of a novel rice gene, EMBO J., 1988, vol. 7, p. 2279.
Close, T.J., Dehydrins: a commonality in the response of plants to dehydration and low temperature, Physiol. Plant., 1997, vol. 100, p. 291. https://doi.org/10.1111/j.1399-3054.1997.tb.04785.x
Shakirova, F.M., Allagulova, Ch.R., Bezrukova, M.V., Aval’baev, A.M., and Gimalov, F.R., The role of endogenous ABA in cold-induced expression of the TADHN dehydrin gene in wheat seedlings, Russ. J. Plant Physiol., 2009, vol. 56, p. 720.
Baker, J., Steele, C., and Dure, L., III, Sequence and characterization of 6 LEA proteins and their genes from cotton, Seed Sci. Res., 1988, vol. 5, p. 185.
Borovskii, G.B., Stupnikova, I.V., Antipina, A.I., Vladimirova, S.V., and Voinikov, V.K., Accumulation of dehydrin-like proteins in the mitochondria of cereals in response to cold, freezing, drought and ABA treatment, BMC Plant Biol., 2002, vol. 2, p. 5.
Close, T.J. and Lammers, P.J., An osmotic stress protein of cyanobacteria is immunologically related to plant dehydrins, Plant Physiol., 1993, vol. 101, p. 773.
Takahashi, R., Joshee, N., and Kitagawa, Y., Induction of chilling resistance by water stress, and cDNA sequence analysis and expression of water stress-regulated genes in rice, Plant Mol. Biol., 1994, vol. 26, p. 339.
Ouelett, F., Houde, M., and Sarhan, F., Purification, characterization and cDNA cloning of the 200 kDa protein induced by cold acclimation in wheat, Plant Cell Physiol., 1993, vol. 34, p. 59.
Graether, S.P. and Boddington, K.F., Disorder and function: a review of the dehydrin protein family, Front. Plant Sci., 2014, vol. 5: 1. https://doi.org/10.3389/fpls.2014.00576
Clarke, M.W., Boddington, K.F., Warnica, J.M., Atkinson, J., McKenna, S., Madge, J., Barker, C.H., and Graether, S.P., Structural and functional insights into the cryoprotection of membranes by the intrinsically disordered dehydrins, J. Biol. Chem., 2015, vol. 290, no. 45, p. 26900.
Close, T.J., Fenton, R.D., and Moonan, F., A view of plant dehydrins using antibodies specific to the carboxy terminal peptide, Plant Mol. Biol., 1993, vol. 23, p. 279.
Hanin, M., Brini, F., Ebel, C., Toda, Y., Takeda, S., and Masmoudi, K., Plant dehydrins and stress tolerance, Plant Signal. Behav., 2011, vol. 6, p. 1503. https://doi.org/10.4161/psb.6.10.17088
Riley, A.C., Ashlock, D.A., and Graether, S.P., Evolution of the modular, disordered stress proteins known as dehydrins, PLoS One, 2019, vol. 14: e0211813. https://doi.org/10.1371/journal.pone.0211813
Hernandez-Sanchez, I.E., Martynowicz, D.M., Rodriguez-Hernandez, A.A., Perez-Morales, M.B., Graether, S.P., and Jimenez-Bremont, J.F., A dehydrin–dehydrin interaction: the case of SK3 from Opuntia streptacantha,Front. Plant Sci., 2014, vol. 5: 520.
Eriksson, S., Eremina, N., Barth, A., Danielsson, J., and Harryson, P., Membrane-induced folding of the plant stress dehydrin Lti30, Plant Physiol., 2016, vol. 171, p. 932.
Rosales, R., Romero, I., Escribano, M.I., Merodio, C., and Sanchez-Ballesta, M.T., The crucial role of F- and K-segments in the in vitro functionality of Vitis vinifera dehydrin DHN1a, Phytochemistry, 2014, vol. 108, p. 17.
Hernandez-Sanchez, I.E., Maruri-Lopez, I., Ferrando, A., Carbonelly, J., Graether, S.P., and Jimenez-Bremont, J.F., Nuclear localization of the dehydrin OpsDHN1 is determined by histidine-rich motif, Front. Plant Sci., 2015, vol. 6: 702.
Strimbeck, G.R., Hiding in plain sight: the F-segment and other conserved features of seed plant SKn dehydrins, Planta, 2017, vol. 245, p. 1061. https://doi.org/10.1007/s00425-017-2679-7
Yang, W., Zhang, L., Lv, H., Li, H., Zhang, Y., Xu, Y., and Yu, J., The K-segments of wheat dehydrin WZY2 are essential for its protective functions under temperature stress, Front. Plant Sci., 2015, vol. 6: 406.
Kalemba, E.M. and Litkowiec, M., Functional characterization of a dehydrin protein from Fagus silvatica seeds using experimental and in silico approaches, Plant Physiol. Biochem., 2015, vol. 97, p. 246.
Yu, Zh., Wang, X., and Zhang, L., Structural and functional dynamics of dehydrins: a plant protector protein under abiotic stress, Int. J. Mol. Sci., 2018, vol. 19, p. 1. https://doi.org/10.3390/ijms19113420
Hara, M., Shinoda, Y., Tanaka, Y., and Kuboi, T., DNA binding of citrus dehydrin promoted by zinc ion, Plant Cell Environ., 2009, vol. 32, p. 532. https://doi.org/10.1111/j.1365-3040.2009.01947.x
Alsheikh, M.K., Heyen, B.J., and Randal, S.K., Ion binding properties of the dehydrin ERD14 are dependent upon phosphorilation, J. Biol. Chem., 2003, vol. 278, p. 40882.
Farias-Soares, F.L., Burrieza, H.P., Steiner, N., Maldonado, S., and Guerra, M.P., Immunoanalysis of dehydrins in Araucaria angustifolia embryos, Protoplasma, 2013, vol. 250, p. 911. https://doi.org/10.1007/s00709-012-0474-7
Kalemba, E.M. and Pukacka, S., Possible role of LEA proteins and sHSPs in seed protection: a short review, Biol. Lett., 2007, vol. 44, p. 3.
Hara, M., The multifunctionality of dehydrins, Plant Signal. Behav., 2010, vol. 5, p. 503.
Abedini, R., GhaneGolmohammadi, F., PishkamRad, R., Pourabed, E., Jafarnezhad, A., Shobbar, Z.-S., and Shahbazi, M., Plant dehydrins: shedding light on structure and expression patterns of dehydrin gene family in barley, J. Plant Res., 2017, vol. 130, p. 747. https://doi.org/10.1007/s10265-017-0941-5
Ferreira, L.A., Walezyk Mooradally, A., Zaslavsky, B., Uversky, V.N., and Graether, S.P., Effect of an intrinsically disordered plant stress protein on the properties of water, Biophys. J., 2018, vol. 115, no. 6, p. 1696. https://doi.org/10.1016/j.bpj.2018.09.014
Chakrabortee, S., Boschetti, C., Walton, L.J., Sarkar, S., Rubinsztein, D.C., and Tunnacliffe, A., Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, p. 18073. https://doi.org/10.1073/pnas.0706964104
Kosová, K., Prášil, I.T., and Vitámvás, P., Role of dehydrins in plant stress response, in Handbook of Plant and Crop Stress, Pessaracli, M., Ed., Boca Raton: CRC, 2010, p. 239.
Liu, Y., Song, Q., Li, D., Yang, X., and Li, D., Multifunctional roles of plant dehydrins in response to environmental stress, Front. Plant Sci., 2017, vol. 8: 1018. https://doi.org/10.3389/flps.2017.01018
Kovacs, D., Kalmar, E., Torok, Z., and Tompa, P., Chaperon activity of ERD10 and ERD14, two disordered stress-related plant proteins, Plant Physiol., 2008, vol. 147, p. 381. https://doi.org/10.1104/pp.108.118208
Koag, M.Ch., Wilkens, S., Fenton, R.D., Resnik, J., Vo, E., and Close, T.J., The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes, Plant Physiol., 2009, vol. 150, p. 1503.
Eriksson, S.K., Kutzer, M., Procek, J., Gröbner, G., and Harryson, P., Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein, Plant Cell, 2011, vol. 23, p. 2391.
Rahman, L.N., Bamm, V.V., Voyer, J.A.M., Smith, G.S.T., Chen, L., Yaish, M.W., Moffatt, B.A., Dutcher, J.R., and Harauz, G., Zinc induces disorder-to-order transitions in free and membrane-associated Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2: a solution CD and solid-state ATR-FTIR study, Amino Acids, 2011, vol. 40, p. 1485. https://doi.org/10.1007/s00726-010-0759-0
Wisniewski, M., Webb, R., Balsamo, R., Close, T.J., Yu, X.M., and Griffith, M., Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica), Physiol. Plant., 1999, vol. 105, p. 600. https://doi.org/10.1034/j.1399-3054.105402.x
Amara, I., Odena, A., Oliveira, E., Moreno, A., Masmoudi, Kh., Pagés, M., and Goday, A., Insights into maize LEA proteins: from proteomics to functional approaches, Plant Cell Physiol., 2012, vol. 53, p. 312. https://doi.org/10.1093/pcp/pcr183
Kosová, K., Vitámvás, P., Prášilová, P., and Prášil, I.T., Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale, Biol. Plant., 2013, vol. 57, p. 105.
Kosová, K., Vitámvás, P., and Prášil, I.T., Wheat and barley dehydrins under cold, drought and salinity—what can LEA-II proteins tell us about plant stress response? Front. Plant Sci., 2014, vol. 5: 343. https://doi.org/10.3389/fpls.2014.00343
Hara, M., Kondo, M., and Kato, T., A KS-type dehydrin and its related domains reduce Cu-promoted radical generation and the histidine residues contribute to the radical-reducing activities, J. Exp. Bot., 2013, vol. 64, p. 1615.
Svensson, J., Palva, E.T., and Welin, B., Purification of recombinant Arabidopsis thaliana dehydrins by metal ion affinity chromatography, Protein Expr. Purif., 2000, vol. 20, p. 169.
Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K., Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis,Plant Cell, 1998, vol. 10, p. 1391.
Chung, S. and Parish, R.W., Combinatorial interactions of multiple cis-elements regulating the induction of the Arabidopsis XERO2 dehydrin gene by abscisic acid and cold, Plant J., 2008, vol. 54, p. 15.
Yu, Zh., Wang, X., and Zhang, L., Structural and functional dynamics of dehydrins: a plant protector protein under abiotic stress, Int. J. Mol. Sci., 2018, vol. 19, no. 3420, p. 1. https://doi.org/10.3390/ijms19113420
Roberts, E.H., Predicting the storage life of seeds, Seed Sci. Technol., 1973, vol. 1, p. 499.
Delahaie, J., Hundertmark, M., Bove, J., Leprince, O., Rogniaux, H., and Buitink, J., LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance, J. Exp. Bot., 2013, vol. 64, p. 4559. https://doi.org/10.1093/jxb/ert274
Hanana, M., Daldoul, S., Fouquet, R., Deluc, L., Leon, C., Hoefer, M., Barrieu, F., and Ghorbel, A., Identification and characterization of seed-specific grapevine dehydrin involved in abiotic stress response within tolerant varieties, Turk. J. Bot., 2014, vol. 38, p. 1157.
Ismail, A.M., Hall, A.E., and Close, T.J., Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea, Plant Physiol., 1999, vol. 120, p. 237.
Haider, A., Characterization and expression of dehydrins in wild Egyptian pea (Pisum sativum L.), Afr. J. Biotech., 2012, vol. 11, no. 55, p. 11789.
Chen, K., Fessehaieb, A., and Arora, R., Dehydrin metabolism is altered during seed osmopriming and subsequent germination under chilling and desiccation in Spinacia oleracea L. cv. Bloomsdale: possible role in stress tolerance, Plant Sci., 2012, vol. 183, p. 27.
Jiménez, J.A., Alonso-Ramírez, A., and Nicolás, C., Two cDNA clones (FsDhn1 and FsClo1) up-regulated by ABA are involved in drought responses in Fagus s-ilvatica L. seeds, J. Plant Physiol., 2008, vol. 165, no. 17, p. 1798.
Leprince, O., Pellizzaro, A., Berriri, S., and Buitink, J., Late seed maturation: drying without dying, J. Exp. Bot., 2017, vol. 68, p. 827. https://doi.org/10.1093/jxb/erw363
Kermode, A.R. and Finch-Savage, W.E., Desiccation sensitivity in orthodox and recalcitrant seeds in relation to development, in Desiccation and Survival in Plants: Drying without Dying, Black, M. and Pritchard, H.W., Eds., Wallingford: CABI, 2002, p. 149.
Soares, G.C.M., Dias, D.C.F.S., Faria, J.M.R., and Borges, E.E.L., Physiological and biochemical changes during the loss of desiccation tolerance in germinating Adenanthera pavonina L. seeds, Ann. Brazilian Acad. Sci., 2015, vol. 87, p. 2001.
Berjak, P. and Pammenter, N.W., Recalcitrance is not an all-or-nothing situation, Seed Sci. Res., 1994, vol. 4, p. 263.
Pukacka, S. and Ratajczak, E., Antioxidative response of ascorbate glutathione pathway enzymes and metabolites to desiccation of recalcitrant Acer saccharinum seeds, J. Plant Physiol., 2006, vol. 163, p. 1259.
Farrant, J.M., Berjak, P., and Pammenter, N.W., Proteins in development and germination of a desiccation sensitive (recalcitrant seed) species, Plant Growth Regul., 1992, vol. 11, p. 257.
Bradford, K.J. and Chandler, P.M., Expression of “dehydrin-like” proteins in embryos and seedlings of Zizania palustris and Oryza sativa during dehydration, Plant Physiol., 1992, vol. 93, p. 488.
Finch-Savage, W.E., Pramanik, S.K., and Bewly, J.D., The expression of dehydrin proteins in desiccation-sensitive (recalcitrant) seeds of temperate trees, Planta, 1994, vol. 193, p. 478.
Šunderlíková, V., Salaj, J., Kopecky, D., Salaj, T., Wilhem, E., and Marušíková, I., Dehydrin genes and their expression in recalcitrant oak (Quercus robur) embryos, Plant Cell Rep., 2009, vol. 28, p. 1011. https://doi.org/10.1007/s00299-009-0710-6
Gumilevskaya, N.A. and Azarkovich, M.I., Identification and characterization of dehydrins in horse chestnut recalcitrant seeds, Russ. J. Plant Physiol., 2010, vol. 57, p. 859.
Farrant, J.M., Pammenter, N.W., Berjak, P., Farnsworth, E.J., and Vertucci, C.W., Presence of dehydrin-like proteins and level of abscisic acid in recalcitrant (desiccation sensitive) seeds may be related to habitat, Seed Sci. Res., 1996, vol. 6, p. 175.
Talanova, V.V. and Titov, A.F., Endogenous abscisic-acid content in cucumber leaves under the influence of unfavorable temperature and salinity, J. Exp. Bot., 1994, vol. 45, p. 1031. https://doi.org/10.1093/jxb/45.7.1031
Han, B., Berjak, P., Pammenter, N., Farrant, J., and Kermode, A.R., The recalcitrant plant species, Ca-stanospermum australe and Trichilia dregeana, differ in their ability to produce dehydrin-related polypeptides during seed maturation and in response to ABA or water-deficit-related stresses, J. Exp. Bot., 1997, vol. 48, p. 1717.
Mehta, P.A., Rebala, K.C., Venkataraman, G., and Parida, A., A diurnally regulated dehydrin from Avicen-nia marina that shows nucleo-cytoplasmic localization and is phosphorylated by casein kinase II in vitro, Plant Physiol. Biochem., 2009, vol. 47, p. 701.
Gumilevskaya, N.A., Azarkovich, M.I., Komarova, M.E., and Obroucheva, N.V., Proteins of axial organs of dormant and germinating horse chestnut seeds. 1. General characterization, Russ. J. Plant Physiol., 2001, vol. 48, p. 1.
Azarkovich, M.I. and Gumilevskaya, N.A., Proteins of cotyledons of mature horse chestnut seeds, Russ. J. Plant Physiol., 2006, vol. 53, p. 629.
Kleinwächter, M., Radwan, A., Hara, M., and Selmar, D., Dehydrin expression in seeds: an issue of maturation drying, Front. Plant Sci., 2014, vol. 5: 402.
Radwan, A., Hara, M., Kleinwächter, M., and Selmar, D., Dehydrin expression in seeds and maturation drying: a paradigm change, Plant Biol., 2014, vol. 16, p. 853. https://doi.org/10.1111/plb.12228
Ellis, R.H., Hong, T.D., and Roberts, E.H., An intermediate category of seed storage behaviour? I. Coffee, J. Exp. Bot., 1990, vol. 41, p. 1167.
Prokof'ev, A.A., Formirovanie semyan kak organov zapasa. 27-e Timiryazevskoe chtenie (Seed Formation as Storage Organs, the 27th Timiryazev Lecture), Moscow: Nauka, 1968.
Castañeda-Saucedo, M.C., Córdova-Téllez, L., Tapia-Campos, E., Delgado-Alvarado, A., González-Hernández, V.A., Santacruz-Varela, A., Loza-Tavera, H., García-de-los-Santos, G., and Vargas-Suárez, M., Dehydrins patterns in common bean exposed to drought and watered conditions, Rev. Fitotec. Mex., 2014, vol. 37, no. 1, p. 59.
Kalemba, E.M. and Pukacka, S., Association of protective proteins with dehydration and desiccation of orthodox and recalcitrant category seeds of three Acer genus species, J. Plant Growth Regul., 2012, vol. 31, p. 351. https://doi.org/10.1007/s00344-011-9246-4
Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larré, C., Satour, P., and Leprince, O., Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance, Plant Physiol., 2006, vol. 140, p. 1418.
Chatelain, E., Hundertmark, M., Leprince, O., Le Gall, S., Satour, P., Deligny-Penninck, S., Rogniaux, H., and Buitink, J., Temporal profilling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevity, Plant Cell Environ., 2012, vol. 35, p. 1440.
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Translated by A. Aver’yanov
Abbreviations: LEA proteins—late embryogenesis abundant proteins; SDS electrophoresis—electrophoresis under denaturing conditions.
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Azarkovich, M.I. Dehydrins in Orthodox and Recalcitrant Seeds. Russ J Plant Physiol 67, 221–230 (2020). https://doi.org/10.1134/S1021443720020028
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DOI: https://doi.org/10.1134/S1021443720020028