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:

The megagametophyte of mature seeds of Araucaria angustifolia consists of cells with thin walls, one or more nuclei, a central vacuole storing proteins, and a cytoplasm rich in amyloplasts, mitochondria and lipid bodies. In this study, we describe the process of mobilization of reserves and analyzed the dismantling of the tissue during germination, using a range of well-established markers of programmed cell death (PCD), including: morphological changes in nuclei and amyloplasts, DNA degradation, and changes in nuclease profiles. TUNEL reaction and DNA electrophoresis demonstrate that DNA fragmentation in nuclei occurs at early stages of germination, which correlates with induction of specific nucleases. The results of the present study add knowledge on the dismantling of the megagametophyte of genus Araucaria, a storage tissue that stores starch as the main reserve substance, as well as on the PCD pathway, by revealing new insights into the role of nucleases and the expression patterns of putative nuclease genes during germination. © 2018 Moyano, Correa, Favre, Rodríguez, Maldonado and López-Fernández.

Registro:

Documento: Artículo
Título:Activation of nucleases, pcd, and mobilization of reserves in the araucaria angustifolia megagametophyte during germination
Autor:Moyano, L.; Correa, M.D.; Favre, L.C.; Rodríguez, F.S.; Maldonado, S.; López-Fernández, M.P.
Filiación:Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas Técnicas, Instituto de Biodiversidad y Biología Experimental y Aplicada, Buenos Aires, Argentina
Departamentos de Industrias y Departamento de Química Orgánica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Palabras clave:Araucaria angustifolia; Cys-EP; Germination; Megagametophyte; Nucleases; PCD; Starch
Año:2018
Volumen:9
DOI: http://dx.doi.org/10.3389/fpls.2018.01275
Título revista:Frontiers in Plant Science
Título revista abreviado:Front. Plant Sci.
ISSN:1664462X
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_1664462X_v9_n_p_Moyano

Referencias:

  • Bethke, P., Lonsdale, J., Fath, A., Jones, R., Hormonally regulated programmed cell death in barley aleurone cells (1999) Plant Cell, 11, pp. 1033-1046
  • Bewley, J.D., Bradford, K.J., Hilhorst, H.W.M., Nonogaki, H., (2013) Seeds: Physiology of Development, Germination and Dormancy, , 3rd Edn, Berlin, Springer Science & Business Media
  • Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal. Biochem, 72, pp. 248-254
  • Burrieza, H.P., López-Fernández, M.P., Maldonado, S., Analogous reserve distribution and tissue characteristics in quinoa and grass seeds suggest convergent evolution (2014) Front. Plant Sci, 5 (546). , 25360139
  • Cardemil, L., Reinero, A., Changes of Araucaria araucana seed reserves during germination and early seedling growth (1982) Can. J. Bot, 60, pp. 1629-1638
  • Cardemil, L., Varner, J.E., Starch degradation metabolism towards sucrose synthesis in germinating Araucaria araucana seeds (1984) Plant Physiol, 76, pp. 1047-1054. , 16663947
  • Casani, S., Fontanini, D., Capocchi, A., Lombardi, L., Galleschi, L., Investigation on cell death in the megagametophyte of Araucaria bidwillii Hook. post-germinated seeds (2009) Plant Physiol. Biochem, 47, pp. 599-607. , 19321357
  • Chang, S., Puryear, J., Cairney, J., A simple and efficient method for isolating RNA from pine trees (1993) Plant Mol. Biol. Rep, 11, pp. 113-116. , 11725489
  • Coll, N.S., Vercammen, D., Smidler, A., Clover, C., Van Breusegem, F., Dangl, J.L., Arabidopsis type I metacaspases control cell death (2010) Science, 330, pp. 1393-1397. , 21097903
  • Domínguez, F., Cejudo, F.J., Programmed cell death (PCD): an essential process of cereal seed development and germination (2014) Front. Plant Sci, 5 (366). , 25120551
  • Doyle, J., DNA Protocols for Plants,” in (1991) Molecular Techniques in Taxonomy, pp. 283-293. , Godfrey M.H., Johnston A.W.B., Young J.P.W., (eds), Berlin, Springer
  • Fath, A., Bethke, P., Lonsdale, J., Meza-Romero, R., Jones, R., Programmed cell death in cereal aleurone (2000) Plant Mol. Biol, 44, pp. 255-266
  • Gernandt, D.S., Magallón, S., Geada López, G., Zerón Flores, O., Willyard, A., Liston, A., Use of simultaneous analyses to guide fossil-based calibrations of pinaceae phylogeny (2008) Int. J. Plant Sci, 169, pp. 1086-1099
  • Gietl, C., Schmid, M., Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues (2001) Naturwissenschaften, 88, pp. 49-58. , 11320888
  • Harris, K.F., Esbroeck, Z.P., Duffus, J.E., Moderate-temperature polymerization of LR white in a nitrogen atmosphere (1995) Microsc. Res. Tech, 32, pp. 264-265. , 8527860
  • He, X., Kermode, A.R., Proteases associated with programmed cell death of megagametophyte cells after germination of white spruce (Picea glauca) seeds (2003) Plant Mol. Biol, 52, pp. 729-744. , 13677463
  • He, X., Kermode, A.R., Programmed cell death of the megagametophyte during post-germinative growth of white spruce (Picea glauca) seeds species is regulated by reactive oxygen ubiquitin the-mediated proteolytic system (2010) Plant Cell Physiol, 51, pp. 1707-1720. , 20833629
  • Jensen, W.A., (1962) Botanical Histochemistry: Principles and Practice, , San Francisco, CA, W.H. Freeman & Co
  • Jones, W., Hill, K., Allen, J., Wollemia nobilis, a new living Australian genus and species in the Araucariaceae (1995) Telopea, 6, pp. 173-176
  • Ko, C.Y., Lai, Y.L., Liu, W.Y., Lin, C.H., Chen, Y.T., Chen, L.F.O., Arabidopsis ENDO2: its catalytic role and requirement of n-glycosylation for function (2012) J. Agric. Food Chem, 60, pp. 5169-5179. , 22506810
  • Kourtis, N., Tavernarakis, N., Autophagy and cell death in model organisms (2009) Cell Death. Differ, 16, pp. 21-30. , 19079286
  • Kuma, A., Mizushima, N., Physiological role of autophagy as an intracellular recycling system: with an emphasis on nutrient metabolism (2010) Semin. Cell Dev. Biol, 21, pp. 683-690. , 20223289
  • Lambert, R., Quiles, F.A., Cabello-Díaz, J.M., Piedras, P., Purification and identification of a nuclease activity in embryo axes from French bean (2014) Plant Sci, 224, pp. 137-143. , 24908514
  • Leslie, A.B., Beaulieu, J.M., Rai, H.S., Crane, P.R., Donoghue, M.J., Mathews, S., Hemisphere-scale differences in conifer evolutionary dynamics (2012) Proc. Natl. Acad. Sci. U.S.A, 109, pp. 16217-16221. , 22988083
  • Lesniewicz, K., Karlowski, W.M., Pienkowska, J.R., Krzywkowski, P., Poreba, E., The plant S1-Like nuclease family has evolved a highly diverse range of catalytic capabilities (2013) Plant Cell Physiol, 54, pp. 1064-1078. , 23620482
  • Leśniewicz, K., Pieńkowska, J., Poręba, E., Characterization of nucleases involved in seedling development of cauliflower (2010) J. Plant Physiol, 167, pp. 1093-1100. , 20447722
  • Levine, B., Klionsky, D.J., Development by self-digestion: molecular mechanisms and biological functions of autophagy (2004) Dev. Cell, 6, pp. 463-477. , 15068787
  • Liu, S., Jia, J., Gao, Y., Zhang, B., Han, Y., The AtTudor 2, a protein with SN-Tudor domains, is involved in control of seed germination in Arabidopsis (2010) Planta, 232, pp. 197-207. , 20396901
  • López-Fernández, M.P., Maldonado, S., Programmed cell death during quinoa perisperm development (2013) J. Exp. Bot, 64, pp. 3313-3325. , a, 23833197
  • López-Fernández, M.P., Maldonado, S., Ricinosomes provide an early indicator of suspensor and endosperm cells destined to die during late seed development in quinoa (Chenopodium quinoa) (2013) Ann. Bot, 112, pp. 1253-1262. , b, 24061488
  • Mella, R.A., Sànchez, R.A., Maldonado, S., Phytochrome-induced structural changes and protein degradation prior to radicle protrusion in Datura ferox seeds (1995) Can. J. Bot, 73, pp. 1371-1378
  • Mizushima, N., Autophagy: process and function (2007) Genes Dev, 21, pp. 2861-2873. , 18006683
  • Owens, J.N., Morris, S.J., Misra, S., The ultrastructural, histochemical, and biochemical development of the post-fertilization megagametophyte and the zygotic embryo of Pseudotsuga menziesii (1993) Can. J. For. Res, 23, pp. 816-827
  • Panza, V., Lainez, V., Maroder, H., Prego, I., Maldonado, S., Storage reserves and cellular water in mature seeds of Araucaria angustifolia (2002) Bot. J. Linn. Soc, 140, pp. 273-281
  • Pérez-Amador, M., Abler, M.L., De Rocher, E.J., Thompson, D.M., van Hoof, A., LeBrasseur, N.D., Identification of BFN 1, a bifunctional nuclease induced during leaf and stem senescence in Arabidopsis (2000) Plant Physiol, 122, pp. 169-180
  • Ralph, S.G., Chun, H.J.E., Kolosova, N., Cooper, D., Oddy, C., Ritland, C.E., A conifer genomics resource of 200,000 spruce (Picea spp.) ESTs and 6,464 high-quality, sequence-finished full-length cDNAs for Sitka spruce (Picea sitchensis) (2008) BMC Genomics, 9 (484). , 18854048
  • Reape, T.J., McCabe, P.F., Apoptotic-like regulation of programmed cell death in plants (2010) Apoptosis, 15, pp. 249-256. , 20094801
  • Rodriguez-Navarro, J.A., Cuervo, A.M., Autophagy and lipids: tightening the knot (2010) Semin. Immunopathol, 32, pp. 343-353. , 20730586
  • Sabelli, P.A., Replicate and die for your own good: endoreduplication and cell death in the cereal endosperm (2012) J. Cereal Sci, 56, pp. 9-20
  • 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. , 24634485
  • Schlögl, P.S., dos Santos, A.L.W., do Nascimento Vieira, L., Floh, E.I.S., Guerra, M.P., Gene expression during early somatic embryogenesis in Brazilian pine (Araucaria angustifolia (Bert) O. Ktze) (2012) Plant Cell. Tissue Organ Cult, 108, pp. 173-180
  • Schmid, M., Simpson, D., Gietl, C., Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes (1999) Proc. Natl. Acad. Sci. U.S.A, 96, pp. 14159-14164. , 10570215
  • Schmid, M., Simpson, D., Kalousek, F., Gietl, C., A cysteine endopeptidase with a C-terminal KDEL motif isolated from castor bean endosperm is a marker enzyme for the ricinosome, a putative lytic compartment (1998) Planta, 206, pp. 466-475. , 9763713
  • Schmid, M., Simpson, D.J., Sarioglu, H., Lottspeich, F., Gietl, C., The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum (2001) Proc. Natl. Acad. Sci. U.S.A, 98, pp. 5353-5358. , 11296243
  • Setoguchi, H., Asakawa Osawa, T., Pintaud, J.C., Jaffré, T., Veillon, J.M., Phylogenetic relationships within Araucariaceae based on rbcL gene sequences (1998) Am. J. Bot, 85, pp. 1507-1516. , 21680310
  • Sugiyama, M., Ito, J., Aoyagi, S., Fukuda, H., Endonucleases (2000) Plant Mol. Biol, 44, pp. 387-397
  • Sundström, J.F., Vaculova, A., Smertenko, A.P., Savenkov, E.I., Golovko, A., Minina, E., Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome (2009) Nat. Cell Biol, 11, pp. 1347-1354. , 19820703
  • Tompsett, P.B., Desiccation studies in relation to the storage of Araucaria seed (1984) Ann. Appl. Biol, 105, pp. 581-586
  • Toyooka, K., Okamoto, T., Minamikawa, T., Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components (2001) J. Cell Biol, 154, pp. 973-982. , 11524437
  • Tsiatsiani, L., Van Breusegem, F., Gallois, P., Zavialov, A., Lam, E., Bozhkov, P.V., Metacaspases (2011) Cell Death Differ, 18, pp. 1279-1288. , 21597462
  • Untergasser, A., Nijveen, H., Rao, X., Bisseling, T., Geurts, R., Leunissen, J.A.M., Primer3Plus, an enhanced web interface to Primer3 (2007) Nucleic Acids Res, 35, pp. W71-W74. , 17485472
  • Wada, S., Ishida, H., Izumi, M., Yoshimoto, K., Ohsumi, Y., Mae, T., Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves (2008) Plant Physiol, 149, pp. 885-893. , 19816145
  • Young, T.E., Gallie, D.R., Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals (1999) Plant Mol. Biol, 39, pp. 915-926. , 10344197
  • Young, T.E., Gallie, D.R., Programmed cell death during endosperm development (2000) Plant Mol. Biol, 44, pp. 283-301. , a
  • Young, T.E., Gallie, D.R., Regulation of programmed cell death in maize endosperm by abscisic acid (2000) Plant Mol. Biol, 42, pp. 397-414. , b
  • Zheng, Y., Zhang, H., Deng, X., Liu, J., Chen, H., The relationship between vacuolation and initiation of PCD in rice (Oryza sativa) aleurone cells (2017) Sci. Rep, 7 (41245). , 28117452

Citas:

---------- APA ----------
Moyano, L., Correa, M.D., Favre, L.C., Rodríguez, F.S., Maldonado, S. & López-Fernández, M.P. (2018) . Activation of nucleases, pcd, and mobilization of reserves in the araucaria angustifolia megagametophyte during germination. Frontiers in Plant Science, 9.
http://dx.doi.org/10.3389/fpls.2018.01275
---------- CHICAGO ----------
Moyano, L., Correa, M.D., Favre, L.C., Rodríguez, F.S., Maldonado, S., López-Fernández, M.P. "Activation of nucleases, pcd, and mobilization of reserves in the araucaria angustifolia megagametophyte during germination" . Frontiers in Plant Science 9 (2018).
http://dx.doi.org/10.3389/fpls.2018.01275
---------- MLA ----------
Moyano, L., Correa, M.D., Favre, L.C., Rodríguez, F.S., Maldonado, S., López-Fernández, M.P. "Activation of nucleases, pcd, and mobilization of reserves in the araucaria angustifolia megagametophyte during germination" . Frontiers in Plant Science, vol. 9, 2018.
http://dx.doi.org/10.3389/fpls.2018.01275
---------- VANCOUVER ----------
Moyano, L., Correa, M.D., Favre, L.C., Rodríguez, F.S., Maldonado, S., López-Fernández, M.P. Activation of nucleases, pcd, and mobilization of reserves in the araucaria angustifolia megagametophyte during germination. Front. Plant Sci. 2018;9.
http://dx.doi.org/10.3389/fpls.2018.01275