Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T11:50:02.220Z Has data issue: false hasContentIssue false
  • English
  • Français

The reduction of seed-specific dehydrins reduces seed longevity in Arabidopsis thaliana

Published online by Cambridge University Press:  08 April 2011

Michaela Hundertmark ,
Julia Buitink ,
Olivier Leprince  and
Dirk K. Hincha
Michaela Hundertmark*
Affiliation:
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, D-14476Potsdam, Germany
Julia Buitink
Affiliation:
INRA, UMR 1191, Physiologie Moléculaire des Semences, IFR 149 Quasav, 16 Bd Lavoisier, F-49045Angers, France
Olivier Leprince
Affiliation:
Agrocampus-Ouest, UMR 1191, Physiologie Moléculaire des Semences, IFR 149 Quasav, 16 Bd Lavoisier, F-49045Angers, France
Dirk K. Hincha
Affiliation:
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, D-14476Potsdam, Germany
*
*Correspondence Email: michaela.hundertmark@univ-angers.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Dehydrins are late embryogenesis abundant (LEA) proteins that accumulate during seed maturation and in response to abiotic stresses in vegetative tissues. They are thought to protect cellular components from dehydration stress. However, whether they play a role in survival in the dry state is not clear. In this study, an RNA interference (RNAi)-construct against the seed-expressed dehydrin of Arabidopsis thaliana, LEA14 (At2g21490), was introduced to wild-type plants, which led to a strong reduction in transcript abundance of the target gene as well as that of two other seed-expressed dehydrin homologues, XERO1 (At3g50980) and RAB18 (responsive to abscisic acid 18, At5g66400) in the transformants. Mature, dry seeds from the RNAi plants germinated to at least 95% after rehydration, indicating that seed desiccation tolerance was not affected, while they exhibited a twofold reduction in longevity. When stored at 75% relative humidity and 35°C, the seeds of two independent RNAi lines lost 50% of their viability in 10 d and 5 d, respectively, while it took 17 d for wild-type seeds to lose 50% viability. In addition, when seeds were imbibed in the presence of 100 mM NaCl, the seeds of RNAi plants exhibited reduced germination compared to wild-type seeds, suggesting that at least one of the three seed-specific dehydrins plays a role both against deterioration during storage at low moisture content and when imbibed tissues are submitted to salt stress at high moisture.

Keywords

Arabidopsis thalianadehydrindesiccation tolerancelate embryogenesis abundant (LEA) proteinRNAiseed storage
Type
Research Article
Information
Seed Science Research , Volume 21 , Issue 3 , September 2011 , pp. 165 - 173
Copyright
Copyright © Cambridge University Press 2011

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

Bechtold, N., Ellis, J. and Pelletier, G. (1993) In-planta agrobacterium-mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. Comptes Rendus de l'Academie des Sciences. Series III, Sciences de la Vie/Life Sciences 316, 1194–1199.Google Scholar
Boswell, V.R., Toole, E.H., Toole, V.K. and Fisher, D.F. (1940) A study of rapid deterioration of vegetable seeds and methods for its prevention. US Department of Agriculture Technical Bulletin 708, 1–48.Google Scholar
Boucher, V., Buitink, J., Lin, X., Boudet, J., Hoekstra, F.A., Hundertmark, M., Renard, D. and Leprince, O. (2009) MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins. Plant, Cell and Environment 33, 418–430.CrossRefGoogle ScholarPubMed
Boudet, J., Buitink, J., Hoekstra, F.A., Rogniaux, H., Larre, C., Satour, P. and Leprince, O. (2006) 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 Physiology 140, 1418–1436.CrossRefGoogle ScholarPubMed
Brini, F., Hanin, M., Lumbreras, V., Amara, I., Khoudi, H., Hassairi, A., Pagès, M. and Masmoudi, K. (2007) Overexpression of wheat dehydrin dhn-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Reports 26, 2017–2026.CrossRefGoogle ScholarPubMed
Buitink, J. and Leprince, O. (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48, 215–228.CrossRefGoogle ScholarPubMed
Buitink, J., Leprince, O., Hemminga, M.A. and Hoekstra, F.A. (2000) Molecular mobility in the cytoplasm: An approach to describe and predict lifespan of dry germplasm. Proceedings of the National Academy of Sciences USA 97, 2385–2390.CrossRefGoogle ScholarPubMed
Chakrabortee, S., Boschetti, C., Walton, L.J., Sarkar, S., Rubinsztein, D.C. and Tunnacliffe, A. (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proceedings of the National Academy of Sciences USA 104, 18073–18078.CrossRefGoogle ScholarPubMed
Clerkx, E.J.M., El-Lithy, M.E., Vierling, E., Ruys, G.J., Blankestijn-De Vries, H., Groot, S.P.C., Vreugdenhil, D. and Koornneef, M. (2004) Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiology 135, 432–443.CrossRefGoogle ScholarPubMed
Clough, S.J. and Bent, A.F. (1998) Floral dip: A simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.CrossRefGoogle Scholar
El-Shishiny, E.D.H. (1953) Effect of temperature and desiccation during storage on germination and keeping quality of Kochia indica seeds. Journal of Experimental Botany 4, 403–406.CrossRefGoogle Scholar
Figueras, M., Pujal, J., Saleh, A., Save, R., Pages, M. and Goday, A. (2004) Maize rab17 overexpression in Arabidopsis plants promotes osmotic stress tolerance. Annals of Applied Biology 144, 251–257.CrossRefGoogle Scholar
Finch-Savage, W.E., Pramanik, S.K. and Bewley, J.D. (1994) The expression of dehydrin proteins in desiccation-sensitive (recalcitrant) seeds of temperate trees. Planta (Heidelberg) 193, 478–485.CrossRefGoogle Scholar
Gee, O.H., Probert, R.J. and Coomber, S.A. (1994) ‘Dehydrin-like’ proteins and desiccation tolerance in seeds. Seed Science Research 4, 135–141.CrossRefGoogle Scholar
Greggains, V., Finch-Savage, W.E., Quick, W.P. and Atherton, N.M. (2000) Putative desiccation tolerance mechanisms in orthodox and recalcitrant seeds of the genus Acer. Seed Science Research 10, 317–327.CrossRefGoogle Scholar
Hay, F.R., Mead, A., Manger, K. and Wilson, F.J. (2003) One-step analysis of seed storage data and the longevity of Arabidopsis thaliana seeds. Journal of Experimental Botany 54, 993–1011.CrossRefGoogle ScholarPubMed
Hendry, G.A.F. (1993) Oxygen, free radical processes and seed longevity. Seed Science Research 3, 141–153.CrossRefGoogle Scholar
Hundertmark, M. and Hincha, D.K. (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9, 118.CrossRefGoogle ScholarPubMed
Illing, N., Denby, K.J., Collett, H., Shen, A. and Farrant, J.M. (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integrative and Comparative Biology 45, 771–787.CrossRefGoogle ScholarPubMed
Ismail, A.M., Hall, A.E. and Close, T.J. (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proceedings of the National Academy of Sciences USA 96, 13566–13570.CrossRefGoogle ScholarPubMed
Kranner, I., Birtic, S., Anderson, K.M.andPritchard, H.W. (2006) Glutathione half-cell reduction potential: a universal stress marker and modulator of programmed cell death? Free Radical Biology and Medicine 40, 2155–2165.CrossRefGoogle ScholarPubMed
Lerman, J.C. and Cigliano, E.M. (1971) New carbon-14 evidence for six hundred years old Canna compacta seed. Nature 232, 568–570.CrossRefGoogle ScholarPubMed
Manfre, A.J., Lanni, L.M. and Marcotte, W.R. Jr (2006) The Arabidopsis group 1 late embryogenesis abundant protein ATEM6 is required for normal seed development. Plant Physiology 140, 140–149.CrossRefGoogle ScholarPubMed
Manfre, A.J., LaHatte, G.A., Climer, C.R. and Marcotte, W.R. Jr (2009) Seed dehydration and the establishment of desiccation tolerance during seed maturation is altered in the Arabidopsis thaliana mutant atem6-1. Plant and Cell Physiology 50, 243–253.CrossRefGoogle ScholarPubMed
McDonald, M.B. (1999) Seed deterioration: physiology, repair and assessment. Seed Science and Technology 27, 177–237.Google Scholar
Mouillon, J.-M., Gustafsson, P. and Harryson, P. (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiology 141, 638–650.CrossRefGoogle ScholarPubMed
Niedzielski, M., Walters, C., Luczak, W., Hill, L.M., Wheeler, L.J. and Puchalski, J. (2009) Assessment of variation in seed longevity within rye, wheat and the intergeneric hybrid triticale. Seed Science Research 19, 213–224.CrossRefGoogle Scholar
Oge, L., Bourdais, G., Bove, J., Collet, B., Godin, B., Granier, F., Boutin, J.-P., Job, D., Jullien, M. and Grappin, P. (2008) Protein repair l-isoaspartyl methyltransferase1 is involved in both seed longevity and germination vigor in Arabidopsis. The Plant Cell 20, 3022–3037.CrossRefGoogle Scholar
Perez, M.A. and Argüello, J.A. (1995) Deterioration in peanut (Arachis hypogaea l. Cv. Florman) seeds under natural and accelerated ageing. Seed Science and Technology 23, 439–445.Google Scholar
Pouchkina-Stantcheva, N.N., McGee, B.M., Boschetti, C., Tolleter, D., Chakrabortee, S., Popova, A.V., Meersman, F., Macherel, D., Hincha, D.K. and Tunnacliffe, A. (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318, 268–271.CrossRefGoogle Scholar
Priestley, D.A., Cullinan, V.I. and Wolfe, J. (1985) Differences in seed longevity at the species level. Plant, Cell & Environment 8, 557–562.CrossRefGoogle Scholar
Prieto-Dapena, P., Castano, R., Almoguera, C. and Jordano, J. (2006) Improved resistance to controlled deterioration in transgenic seeds. Plant Physiology 142, 1102–1112.CrossRefGoogle ScholarPubMed
Rajjou, L., Lovigny, Y., Groot, S.P.C., Belghazi, M., Job, C. and Job, D. (2008) Proteome-wide characterization of seed ageing in Arabidopsis: A comparison between artificial and natural ageing protocols. Plant Physiology 148, 620–641.CrossRefGoogle Scholar
Rao, N.K., Roberts, E.H. and Ellis, R.H. (1987) Loss of viability in lettuce seeds and the accumulation of chromosome damage under different storage conditions. Annals of Botany 60, 85–96.CrossRefGoogle Scholar
Roberts, E.H. (1960) The viability of cereal seed in relation to temperature and moisture. Annals of Botany 24, 12–31.CrossRefGoogle Scholar
Rohde, P., Hincha, D.K. and Heyer, A.G. (2004) Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (columbia-0 and c24) that show differences in non-acclimated and acclimated freezing tolerance. The Plant Journal 38, 790–799.CrossRefGoogle ScholarPubMed
Roqueiro, G., Facorro, G.B., Huarte, M.G., Rubin de Celis, E., Garcia, F., Maldonado, S. and Maroder, H. (2010) Effects of photooxidation on membrane integrity in Salix nigra seeds. Annals of Botany 105, 1027–1034.CrossRefGoogle ScholarPubMed
Rorat, T. (2006) Plant dehydrins – tissue location, structure and function. Cellular & Molecular Biology Letters 11, 536–556.CrossRefGoogle ScholarPubMed
Sallon, S., Solowey, E., Cohen, Y., Korchinsky, R., Egli, M., Woodhatch, I., Simchoni, O. and Kislev, M. (2008) Germination, genetics, and growth of an ancient date seed. Science 320, 1464.CrossRefGoogle ScholarPubMed
Sattler, S.E., Gilliland, L.U., Magallanes-Lundback, M., Pollard, M. and DellaPenna, D. (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. The Plant Cell 16, 1419–1432.CrossRefGoogle ScholarPubMed
Seki, M., Carninci, P., Nishiyama, Y., Hayashizaki, Y. and Shinozaki, K. (1998) High-efficiency cloning of Arabidopsis full-length cDNA by biotinylated cap trapper. The Plant Journal 15, 707–720.CrossRefGoogle ScholarPubMed
Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., Muramatsu, M., Hayashizaki, Y., Kawai, J., Carninci, P., Itoh, M., Ishii, Y., Arakawa, T., Shibata, K., Shinagawa, A. and Shinozaki, K. (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296, 141–145.CrossRefGoogle ScholarPubMed
Shen-Miller, J. (2002) Sacred lotus, the long-living fruits of China Antique. Seed Science Research 12, 131–143.CrossRefGoogle Scholar
Shimizu, T., Kanamori, Y., Furuki, T., Kikawada, T., Okuda, T., Takahashi, T., Mihara, H. and Sakurai, M. (2010) Desiccation-induced structuralization and glass formation of group 3 late embryogenesis abundant protein model peptides. Biochemistry 49, 1093–1104.CrossRefGoogle ScholarPubMed
Thalhammer, A., Hundertmark, M., Popova, A.V., Seckler, R. and Hincha, D.K. (2010) Interaction of two intrinsically disordered plant stress proteins (COR15a and COR15b) with lipid membranes in the dry state. Biochimica et Biophysica Acta (BBA) – Biomembranes 1798, 1812–1820.CrossRefGoogle ScholarPubMed
Tolleter, D., Jaquinod, M., Mangavel, C., Passirani, C., Saulnier, P., Manon, S., Teyssier, E., Payet, N., Avelange-Macherel, M.-H. and Macherel, D. (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. The Plant Cell 19, 1580–1589.CrossRefGoogle ScholarPubMed
Tunnacliffe, A. and Wise, M. (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94, 791–812.CrossRefGoogle ScholarPubMed
Walters, C. (1998) Understanding the mechanisms and kinetics of seed ageing. Seed Science Research 8, 223–244.CrossRefGoogle Scholar
Walters, C., Ried, J.L. and Walker-Simmons, M.K. (1997) Heat-soluble proteins extracted from wheat embryos have tightly bound sugars and unusual hydration properties. Seed Science Research 7, 125–134.CrossRefGoogle Scholar
Walters, C., Wheeler, L.M. and Grotenhuis, J.M. (2005) Longevity of seeds stored in a genebank: species characteristics. Seed Science Research 15, 1–20.CrossRefGoogle Scholar
Wechsberg, G.E., Probert, R.J. and Bray, C.M. (1994) The relationship between ‘dehydrin-like’ proteins and seed longevity in Ranunculus sceleratus L. Journal of Experimental Botany 45, 1027–1030.CrossRefGoogle Scholar
Wehmeyer, N. and Vierling, E. (2000) The expression of small heat shock proteins in seeds responds to discrete developmental signals and suggests a general protective role in desiccation tolerance. Plant Physiology 122, 1099–1108.CrossRefGoogle ScholarPubMed
Wolkers, W.F., Tetteroo, F.A.A., Alberda, M. and Hoekstra, F.A. (1999) Changed properties of the cytoplasmic matrix associated with desiccation tolerance of dried carrot somatic embryos. An in situ Fourier transform infrared spectroscopic study. Plant Physiology 120, 153–163.CrossRefGoogle Scholar
Wolkers, W.F., McCready, S., Brandt, W.F., Lindsey, G.G. and Hoekstra, F.A. (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochimica et Biophysica Acta 1544, 196–206.CrossRefGoogle ScholarPubMed