Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In the 1970s, during excavations at Los Morrillos, San Juan, Argentina, quinoa seeds were found within ancient pumpkin crocks protected from the light and high temperatures, and preserved in the very dry conditions of the region. The radiocarbon dates confirmed the age of these seeds at around 2300 years. Sectioning of some of these seeds showed reddish-brown embryos, different from the white embryos of recently harvested quinoa seeds. The ancient seeds did not germinate. The structure of the embryo cells was examined using light and transmission electron microscopy; proteins were analyzed by electrophoresis followed by Coomassie blue and periodic acid Schiff staining and fatty acids by gas chromatography. The state of nuclear DNA was investigated by TUNEL assay, DAPI staining, ladder agarose electrophoresis and flow cytometry. Results suggest that, although the embryo tissues contained very low water content, death occurred by a cell death program in which heterochromatin density was dramatically reduced, total DNA was degraded into small fragments of less than 500 bp, and some proteins were modified by non-enzymatic glycation, generating Maillard products. Polyunsaturated fatty acids decreased and became fragmented, which could be attributable to the extensive oxidation of the most sensitive species (linolenic and linoleic acids) and associated with a collapse of lipid bodies. © 2016 Elsevier Ireland Ltd

Registro:

Documento: Artículo
Título:Death of embryos from 2300-year-old quinoa seeds found in an archaeological site
Autor:Burrieza, H.P.; Sanguinetti, A.; Michieli, C.T.; Bertero, H.D.; Maldonado, S.
Filiación:Instituto de Biodiversidad y Biología Experimental y Aplicada, Consejo Nacional de Investigaciones Científicas y Tecnológicos (IBBEA-CONICET), Argentina
Instituto de Investigaciones Arqueológicas y Museo Prof. Mariano Gambier, Facultad de Filosofía, Humanidades y Artes, Universidad Nacional de San Juan, Argentina
Cátedra de Producción Vegetal, Facultad de Agronomía, Universidad de Buenos Aires, Argentina
Palabras clave:Archaeological seed; Chenopodium quinoa Willd.; Fatty acid oxidation; Necrosis; Programmed cell death; Protein glcation; plant protein; unsaturated fatty acid; archeology; chemistry; Chenopodium quinoa; DNA damage; embryology; germination; plant seed; transmission electron microscopy; ultrastructure; Archaeology; Chenopodium quinoa; DNA Damage; Fatty Acids, Unsaturated; Germination; Microscopy, Electron, Transmission; Plant Proteins; Seeds
Año:2016
Volumen:253
Página de inicio:107
Página de fin:117
DOI: http://dx.doi.org/10.1016/j.plantsci.2016.10.001
Título revista:Plant Science
Título revista abreviado:Plant Sci.
ISSN:01689452
CODEN:PLSCE
CAS:Fatty Acids, Unsaturated; Plant Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01689452_v253_n_p107_Burrieza

Referencias:

  • Tapia, M.E., Agrobiodiversidad En Los Andes (1999), Fundación Friederich Ebert Lima; Bertero, H.D., de la Vega, A.J., Correa, G., Jacobsen, S.E., Mujica, A., Genotype and genotype-by-environment interaction effects for grain yield and grain size in quinoa (Chenopodium quinoa Willd.) as revealed by pattern analysis of international multi-environment trials (2004) Field Crop. Res., 89, pp. 299-318
  • Prego, I., Maldonado, S., Otegui, M., Seed structure and localization of reserves in Chenopodium quinoa (1998) Ann. Bot.-London, 82, pp. 481-488
  • Gambier, M., La Cultura De Ansilta (1977), pp. 1-276. , Instituto De Investigaciones Arqueológicas Y Museo, universidad Nacional de San Juan San Juan; Gambier, M., La Cultura De Los Morrillos (1985), pp. 1-232. , Instituto De Investigaciones Arqueológicas Y Museo, Universidad Nacional de San Juan San Juan; Roig, F.A., Frutos y semillas arqueológicos de Calingasta, San Juan (1977) La Cultura De Ansilta, pp. 215-250. , M. Gambier Instituto de Investigaciones Arqueológicas y Museo, Universidad Nacional de San Juan San Juan
  • Roberts, E.H., Predicting the storage life of seeds (1973) Seed Sci. Technol., 1, pp. 499-514
  • Daws, M.I., Davies, J., Vaes, E., van Gelder, R., Pritchard, H.W., Two-hundred year seed survival of Leucospermum and two other woody species from the Cape floristic region, South Africa (2007) Seed Sci. Res., 17, pp. 73-79
  • Sallon, S., Solowey, E., Cohen, Y., Korchinsky, R., Egli, M., Woodhatch, I., Simchoni, O., Kislev, M., Germination, genetics, and growth of an ancient date seed (2008) Science, 320, p. 1464
  • Shen-Miller, J.M.B., Mudgett, J.W., Schopf, S., Berger, C.R., Exceptional seed longevity and robust growth: ancient Sacred Lotus from China (1995) Am. J. Bot., 82, pp. 1367-1380
  • Shen-Miller, J., Schopf, J.W., Harbottle, G., Cao, R.J., Ouyang, S., Zhou, K.S., Southon, J.R., Liu, G.H., Long-living lotus: germination and soil γ-irradiation of centuries-old fruits, and cultivation, growth and phenotypic abnormalities of offspring (2002) Am. J. Bot., 89, pp. 236-247
  • Farrant, J.M., Pammenter, N.W., Berjak, P., Walters, C., Subcellular organization and metabolic activity during the development of seeds that attain different levels of desiccation tolerance (1997) Seed Sci. Res., 7, pp. 135-144
  • Pammenter, N.W., Berjak, P., A review of recalcitrant seed physiology in relation to desiccation-tolerance mechanisms (1999) Seed Sci. Res., 9, pp. 13-37
  • Kranner, I., Chen, H., Pritchard, H.W., Pearce, S.R., Birtić, S., Inter-nucleosomal DNA fragmentation and loss of RNA integrity during seed ageing (2011) Plant Growth Regul., 63, pp. 63-72
  • Van Doorn, W.G., Beers, E.P., Dangl, J.L., Franklin-Tong, V.E., Gallois, P., Hara-Nishimura, I., Jones, A.M., Bozhkov, P.V., Morphological classification of plant cell deaths (2011) Cell Death Differ., 18, pp. 1241-1246
  • Bozhkov, P.V., Filonova, L.H., Suárez, M.F., Programmed cell death in plant embryogenesis (2005) Curr. Top. Dev. Biol., 67, pp. 135-179
  • Bozhkov, P.V., Suarez, M.F., Filonova, L.H., Daniel, G., Zamyatnin, A.A., Rodriguez-Nieto, S., Zhivotovsky, B., Smertenko, A., (2005) Cysteine Protease McII-Pa Executes Programmed Cell Death During Plant Embryogenesis, 102, pp. 14463-14468. , PNAS USA
  • Domínguez, F.J., Cejudo, F.J., Identification of a nuclear-localized nuclease from wheat cells undergoing programmed cell death that is able to trigger DNA fragmentation and apoptotic morphology on nuclei from human cells (2006) Biochem. J., 397, pp. 529-536
  • Domínguez, F.J., Cejudo, F.J., A comparison between nuclear dismantling during plant and animal programmed cell death (2012) Plant Sci., 197, pp. 114-121
  • Sakamoto, W., Takami, T., Nucleases in higher plants and their possible involvement in DNA degradation during leaf senescence (2014) J. Exp. Bot., 65, pp. 3835-3843
  • Battelli, R., Lombardi, L., Roger, H.J., Picciarelli, P., Lorenzi, R., Ceccarelli, N., Changes in ultrastructure, protease and caspase-like activities during flower senescence in Lilium longiflorum (2011) Plant Sci., 180, pp. 716-725
  • López-Fernández, M.P., Burrieza, H.P., Rizzo, A.J., Martínez-Tosar, L.J., Maldonado, S., Cellular and molecular aspects of quinoa leaf senescence (2015) Plant Sci., 238, pp. 178-187
  • Rantong, G., Gunawardena, A.H., Programmed cell death: genes involved in signaling, regulation, and execution in plants and animals (2015) Botany, 93, pp. 193-210
  • Tang, D.G., La, E., Kern, J., Kehrer, J.P., Fatty acid oxidation and signaling in apoptosis (2002) Biol. Chem., 383, pp. 425-442
  • Tsanko, S., Gechev-Van Breusegem, F., Stone, J.M., Denev, I., Laloi, C., Reactive oxygen species as signals that modulate plant stress responses and programmed cell death (2006) Bioessays, 28, pp. 1091-1101
  • Lichtenstein, R.G., Rabinovich, G.A., Glycobiology of cell death: when glycans and lectins govern cell fate (2013) Cell Death Differ., 20, pp. 976-986
  • Van Breusegem, F., Dat, J.F., Reactive oxygen species in plant cell death (2006) Plant Physiol., 141, pp. 384-390
  • VanDoorn, W.G., Woltering, E.J., Many ways to exit? Cell death categories in plants (2005) Trends Plant Sci., 10, pp. 117-122
  • Walters, C., Reilley, A.A., Reeves, P.A., Baszczak, J., Richards, C.M., The utility of aged seeds in DNA banks (2006) Seed Sc. Res., 16, pp. 169-178
  • Goloubinoff, P., Páábo, S., Wilson, A.C., (1993) Evolution of Maize Inferred from Sequence Diversity of an Adh2 Gene Segment from Archaeological Specimens, 90, pp. 1997-2001. , PNAS USA
  • Threadgold, J., Brown, T.A., Degradation of DNA in artificially charred wheat seeds (2003) J. Arch. Sci., 30, pp. 1067-1076
  • Ellis, R.H., Hong, T.D., Roberts, E.H., A low moisture-content limit to logarithmic relation between seed moisture content and longevity (1988) Ann. Bot.-London, 61, pp. 405-408
  • Castellión, M., Matiacevich, S., Buera, M.P., Maldonado, S., Protein deterioration and longevity of quinoa seeds during long-term storage (2010) Food Chem., 121, pp. 952-958
  • Castellión, M., Maldonado, S., Buera, M.P., Molecular mobility and seed longevity in Chenopodium quinoa (2010) Water Properties in Food, Health, Pharmaceutical and Biological Systems: ISOPOW 10, pp. 647-656. , D.S. Reid T. Sajjaanantakul P.J. Lillford S. Charoenrein Wiley-Blackwell Oxford
  • Harris, K.F., Pesic-Van Esbroeck, Z., Duffus, J.E., Moderate-temperature polymerization of LR White in a nitrogen atmosphere (1995) Microsc. Res.Tech., 32, pp. 264-265
  • Otto, F., DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA (1990) Methods Cell Biol., 33, pp. 105-110
  • Riccardi, C., Nicoletti, I., Analysis of apoptosis by propidium iodide staining and flow cytometry (2006) Nat. Protoc., 1, pp. 1458-1461
  • Thornton, D.J., Carlsteldt, I., Sheehan, J.K., Identification of glycoproteins on nitrocellulose membranes and gels (1996) Mol. Biotechnol., pp. 171-176
  • Bligh, E.G., Dyer, W.J., A rapid method of total lipid extraction and purification (1959) Can. J. Biochem. Physiol., 37, pp. 911-917
  • Nicoletti, G., Migliorati, M.C., Pagliacci, F., Grignani, C., Riccardi, A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry (1991) J. Immunol. Methods, 139, pp. 271-279
  • Wright, D.J., The seed globulins (1987) Development in Food Proteins, pp. 81-157. , B.J.F. Hudson Elsevier Applied Science London
  • Brinegar, C., Goundan, S., Isolation and characterization of chenopodin, the 11S seed storage protein of quinoa (Chenopodium quinoa) (1993) J. Agr. Food Chem., 41, pp. 182-185
  • Fairbanks, D.J., Burgener, K.W., Robison, L.R., Andersen, W.R., Ballon, E., Electrophoretic characterization of quinoa seed proteins (2006) Plant Breeding, 104, pp. 190-195
  • Zazula, G.D., Harington, C.-R., Telka, A.M., Brock, F., Radiocarbon dates reveal that Lupinus arcticus plants were grown from modern not Pleistocene seeds (2009) New Phytol., 182, pp. 788-792
  • Porsild, A.E., Harington, C.R., Mulligan, G.A., Lupinus arcticus Wats. grown from seeds of Pleistocene age (1967) Science, 158, pp. 113-114
  • Yashina, S.G., Gubin, S.V., Shabaeva, E.V., Egorova, E.F., Maksimovich, S.V., Viability of higher plant seeds of Late Pleistocene age from permafrost deposits as determined by in vitro culturing (2002) Dokl. Biol. Sci., 282, pp. 151-154
  • Earnshaw, W.C., Nuclear changes in apoptosis (1995) Curr. Opin. Cell Biol., 7, pp. 337-343
  • Gilbert, M.T.P., Willerslev, E., Hansen, A.J., Barnes, I., Rudbeck, L., Lynnerup, N., Cooper, A., Distribution patterns of post-mortem damage in human mitochondrial DNA (2003) Am. J. Hum. Genet., 72, pp. 32-47
  • Gilbert, M.T.P., Willerslev, E., Hansen, A.J., Barnes, I., Rudbeck, L., Lynnerup, N., Cooper, A., Characterisation of genetic miscoding lesions caused by post-mortem damage (2003) Am. J. Hum. Genet., 72, pp. 48-61
  • Pääbo, S., Higuchi, R.G., Wilson, A.C., Ancient DNA and the polymerase chain reaction. The emerging field of molecular archaeology (1989) Biol. Chem., 264, pp. 9709-9712
  • Lindahl, T., Instability and decay of the primary structure of DNA (1993) Nature, 362, pp. 709-715
  • Handt, O., Höss, M., Krings, M., Pääbo, S., Ancient, D.N.A., (methodological challenges) (1994) Experientia, 50, pp. 524-529
  • Höss, M., Jaruga, P., Zastawny, T.H., Dizdaroglu, M., DNA damage and DNA sequence retrieval from ancient tissues (1996) Nucleic Acids Res., 24, pp. 1304-1307
  • Bastos Lima, N., Gomes Trindade, F., Da Cunha, M., Amancio Oliveira, A.E., Tping, J., Lindsey, K., Fernandes, K.V.S., Programmed cell death during development of cowpea (Vigna unguiculata (L.) Walp.) seed coat (2015) Plant Cell Environ., 38, pp. 716-728
  • Swift, H., The constancy of desoxyribose nucleic acid in plant nuclei (1950) Proc. Natl. Acad. Sci. U. S. A., 36, pp. 643-654
  • Pfosser, M., Magyar, Z., Bögre, L., Cell cycle analysis in plants (2007) Flow Cytometry with Plant Cells. Analysis of Genes, Chormosomes and Genome, pp. 323-348. , J. Doležel J. Greilhuber J. Suda WILEY-VCH Verlag GmbH and Co. KGaA Weinheim
  • Bertho, A., Santiago, M.A., Coutinho, S.G., (2000) Flow Cytometry in the Study of Cell Death, 95, pp. 429-433. , Memórias do Instituto Oswaldo Cruz
  • Wilson, D.O., McDonald, M.B., The lipid peroxidation model of seed ageing (1986) Seed Sci.Technol., 14, pp. 269-300
  • Roqueiro, G., Maldonado, S., Ríos, M.C., Maroder, H., Fluctuation of oxidative stress indicators in Salix nigra seeds during priming (2012) J. Exp. Bot., 63, pp. 3631-3642
  • Colville, L., Bradley, E.L., Lloyd, A.S., Pritchard, H.W., Castle, L., Kranner, I., Volatile fingerprints of seeds of four species indicate the involvement of alcoholic fermentation, lipid peroxidation, and Maillard reactions in seed deterioration during ageing and desiccation stress (2012) J.Exp. Bot., 63, pp. 6519-6530
  • Kalpana, R., Rao, K.V.M., Lipid changes during accelerated ageing of seeds of pigeonpea (Cajanus cajan (L) Millsp) cultivars (1996) Seed Sci. Technol., 24, pp. 475-483
  • Aiazzi, M.T., Arguello, J.A., Pérez, A., DiRienzo, J., Guzmán, C.A., Deterioration in Atriplex cordobensis (Gandoger et Stuckert) seeds: natural and accelerated ageing (1997) Seed Sci. Technol., 25, pp. 147-155
  • Bailly, C., Benamar, A., Corbineau, F., Come, D., Free radical scavenging as affected by accelerated ageing and subsequent priming in sunflower seeds (1998) Physiol. Plant., 104, pp. 646-652
  • Goel, A., Sheoran, I.S., Lipid peroxidation and peroxide scavenging enzymes in cotton seeds under natural ageing (2003) Biol. Plant., 46, pp. 429-434
  • Tammela, P., Nygren, M., Laasko, I., Hopia, A., Vuorela, H., Hiltunen, R., Volatile compound analysis of ageing Pinus sylvestris L. (Scots pine) seeds (2003) Flavour Frag. J., 18, pp. 290-295
  • Britt, A.B., DNA damage and repair in plants (1996) Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, pp. 75-100
  • Strelec, I., Ugarcic-Hardi, Z., Hlevnjak, M., Accumulation of Amadori and Maillard products in wheat seeds aged under different storage conditions (2008) Croat. Chem. Acta, 8, pp. 131-137
  • Bernal-Lugo, I., Leopold, A., The dynamics of seed mortality (1998) J. Exp. Bot., pp. 1455-1461
  • Sun, W.Q., Leopold, A.C., The Maillard reaction and oxidative stress during ageing of soybean seeds (1995) Physiol. Plant., 94, pp. 94-104
  • Priestley, D.A., Leopold, A.C., Lipid changes during natural ageing of soybeans (1983) Physiol. Plant., 59, pp. 467-470
  • Priestley, D.A., Warner, B.G., Leopold, A.C., McBride, M.B., Organic free radical levels in seeds and pollen (1985) Physiol. Plant., 64, p. 88
  • Stadtman, E., Protein oxidation and ageing (1992) Science, 257, pp. 1220-1224
  • Mudgett, M.B., Clark, S., Characterization of plant l-isoaspartylmethyltransferases that may be involved in seed survival: purification, cloning and sequence analysis of the wheat germ enzyme (1993) Biochemistry, 32, pp. 11100-11111
  • Taylor, A.G., Min, T.G., Paine, D.H., Maillard reaction causes browning in bean seed coat during ageing: inhibition by aminoguanidine (2000) Seed Biology Advances and Applications, pp. 189-196. , M. Black K.J. Bradford J. Vazquez-Ramos CAB International Wallingford

Citas:

---------- APA ----------
Burrieza, H.P., Sanguinetti, A., Michieli, C.T., Bertero, H.D. & Maldonado, S. (2016) . Death of embryos from 2300-year-old quinoa seeds found in an archaeological site. Plant Science, 253, 107-117.
http://dx.doi.org/10.1016/j.plantsci.2016.10.001
---------- CHICAGO ----------
Burrieza, H.P., Sanguinetti, A., Michieli, C.T., Bertero, H.D., Maldonado, S. "Death of embryos from 2300-year-old quinoa seeds found in an archaeological site" . Plant Science 253 (2016) : 107-117.
http://dx.doi.org/10.1016/j.plantsci.2016.10.001
---------- MLA ----------
Burrieza, H.P., Sanguinetti, A., Michieli, C.T., Bertero, H.D., Maldonado, S. "Death of embryos from 2300-year-old quinoa seeds found in an archaeological site" . Plant Science, vol. 253, 2016, pp. 107-117.
http://dx.doi.org/10.1016/j.plantsci.2016.10.001
---------- VANCOUVER ----------
Burrieza, H.P., Sanguinetti, A., Michieli, C.T., Bertero, H.D., Maldonado, S. Death of embryos from 2300-year-old quinoa seeds found in an archaeological site. Plant Sci. 2016;253:107-117.
http://dx.doi.org/10.1016/j.plantsci.2016.10.001