Artículo

Lorenzo, M.; Pinedo, M.L.; Equiza, M.A.; Fernández, P.V.; Ciancia, M.; Ganem, D.G.; Tognetti, J.A."Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves" (2019) Plant Biology. 21:84-94
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Abstract:

Temperate grasses, such as wheat, become compact plants with small thick leaves after exposure to low temperature. These responses are associated with cold hardiness, but their underlying mechanisms remain largely unknown. Here we analyse the effects of low temperature on leaf morpho-anatomical structure, cell wall composition and activity of extracellular peroxidases, which play key roles in cell elongation and cell wall thickening, in two wheat cultivars with contrasting cold-hardening ability. A combined microscopy and biochemical approach was applied to study actively growing leaves of winter (ProINTA-Pincén) and spring (Buck-Patacón) wheat developed under constant warm (25 °C) or cool (5 °C) temperature. Cold-grown plants had shorter leaves but longer inter-stomatal epidermal cells than warm-grown plants. They had thicker walls in metaxylem vessels and mestome sheath cells, paralleled with accumulation of wall components, predominantly hemicellulose. These effects were more pronounced in the winter cultivar (Pincén). Cold also induced a sharp decrease in apoplastic peroxidase activity within the leaf elongating zone of Pincén, and a three-fold increase in the distal mature zone of the leaf. This was consistent with the enhanced cell length and thicker cell walls in this cultivar at 5 °C. The different response to low temperature of apoplastic peroxidase activity and hemicellulose between leaf zones and cultivar types suggests they might play a central role in the development of cold-induced compact morphology and cold hardening. New insights are presented on the potential temperature-driven role of peroxidases and hemicellulose in cell wall dynamics of grasses. © 2018 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands

Registro:

Documento: Artículo
Título:Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves
Autor:Lorenzo, M.; Pinedo, M.L.; Equiza, M.A.; Fernández, P.V.; Ciancia, M.; Ganem, D.G.; Tognetti, J.A.
Filiación:INTA, Unidad Integrada Balcarce, Balcarce, Buenos Aires, Argentina
Instituto de Investigaciones Biológicas, Universidad Nacional de Mar del Plata-CONICET, Mar del Plata, Argentina
Department of Renewable Resources, University of Alberta, Edmonton, Canada
Cátedra de Química de Biomoléculas, Departamento de Biología Aplicada y Alimentos, Facultad de Agronomía, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina
CIHIDECAR-CONICET, Departamento de Química Orgánica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina
Research Member of the National Research Council of Argentina (CONICET), Ciudad Autónoma de Buenos Aires, Argentina
Laboratorio de Fisiología Vegetal, Facultad de Ciencias Agrarias, Universidad Nacional de Mar del Plata, Balcarce, Buenos Aires, Argentina
Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC), La Plata, Buenos Aires, Argentina
Palabras clave:Cell elongation; cell wall; cold hardiness; hemicellulose; peroxidase; wheat; anatomy; cell component; cellulose; cold tolerance; cultivar; enzyme activity; grass; leaf morphology; low temperature; wheat; Poaceae; Triticum aestivum; hemicellulose; peroxidase; plant protein; polysaccharide; anatomy and histology; cell wall; cold; metabolism; physiology; plant leaf; season; wheat; Cell Wall; Cold Temperature; Peroxidase; Plant Leaves; Plant Proteins; Polysaccharides; Seasons; Triticum
Año:2019
Volumen:21
Página de inicio:84
Página de fin:94
DOI: http://dx.doi.org/10.1111/plb.12709
Handle:http://hdl.handle.net/20.500.12110/paper_14358603_v21_n_p84_Lorenzo
Título revista:Plant Biology
Título revista abreviado:Plant Biol.
ISSN:14358603
CODEN:PBIOF
CAS:hemicellulose, 63100-39-0, 63100-40-3, 9034-32-6; peroxidase, 9003-99-0; hemicellulose; Peroxidase; Plant Proteins; Polysaccharides
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_14358603_v21_n_p84_Lorenzo

Referencias:

  • Abedon, B.G., Hatfield, R.D., Tracy, W.F., Cell wall composition in juvenile and adult leaves of maize (Zea mays L.) (2006) Journal of Agricultural and Food Chemistry, 54, pp. 3896-3900
  • Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P., The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism (2008) The Plant Cell, 20, pp. 2117-2129
  • Ahmed, A.E.R., Labavitch, J.M., A simplified method for accurate determination of cell wall uronide content (1977) Journal of Food Biochemistry, 1, pp. 361-365
  • Atkin, O.K., Loveys, B.R., Atkinson, L.J., Pons, T.L., Phenotypic plasticity and growth temperature: understanding interspecific variability (2006) Journal of Experimental Botany, 57, pp. 267-281
  • Boese, S.R., Hüner, N.P.A., Effect of growth temperature and temperature shifts on spinach leaf morphology and photosynthesis (1990) Plant Physiology, 94, pp. 1830-1836
  • Buckeridge, M.S., Rayon, C., Urbanowicz, B., Tiné, M.A.S., Carpita, N.C., Mixed linkage (1→ 3), (1→ 4)-β-D-glucans of grasses (2004) Cereal Chemistry, 81, pp. 115-127
  • Cavender-Bares, J., Impacts of freezing on long-distance transport in woody plants (2005) Vascular Transport in Plants, pp. 401-424. , Holbrook N. M., Zwieniecki M., Melcher P., (Eds),, Elsevier, Oxford, UK, pp
  • Ceulemans, R., Van Praet, L., Jiang, X.N., Effects of CO2 enrichment, leaf position and clone on stomatal index and epidermal cell density in poplar (Populus) (1995) New Phytologist, 131, pp. 99-107
  • Chen, P.M., Li, P.H., Cunningham, W.P., Ultrastructure difference in leaf cells of Solanum species in relation to their frost resistance (1977) Botanical Gazette, 138, pp. 267-285
  • Chinnusamy, V., Zhu, J., Zhu, J.K., Cold stress regulation of gene expression in plants (2007) Trends in Plant Science, 12, pp. 444-451
  • Coelho, E., Rocha, M.A.M., Moreira, A.S.P., Domingues, M.R.M., Coimbra, M.A., Revisiting the structural features of arabinoxylans from brewers’ spent grain (2016) Carbohydrate Polymers, 139, pp. 167-176
  • Córdoba-Pedregosa, M.C., González-Reyes, J.A., Cañadillas, M.S., Navas, P., Córdoba, F., Role of apoplastic and celi-wall peroxidases on the stimulation of root elongation by ascorbate (1996) Plant Physiology, 112, pp. 1119-1125
  • Córdoba-Pedregosa, M.C., Villalba, J.M., Córdoba, F., Gonzalez-Reyes, J.A., Changes in intracellular and apoplastic peroxidase activity, ascorbate redox status, and root elongation induced by enhanced ascorbate content in Allium cepa L (2005) Journal of Experimental Botany, 56, pp. 685-694
  • Cosgrove, D.J., Growth of the plant cell wall (2005) Nature, 6, pp. 850-861
  • Cosio, C., Dunand, C., Specific functions of individual class III peroxidase genes (2009) Journal of Experimental Botany, 60, pp. 391-408
  • De Souza, I.R.P., MacAdam, J.W., A transient increase in apoplastic peroxidase activity precedes decrease in elongation rate of B73 maize (Zea mays) leaf blades (1998) Physiologia Plantarum, 104, pp. 556-562
  • Derbyshire, P., Findlay, K., McCann, M.C., Roberts, K., Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness (2007) Journal of Experimetal Botany, 58, pp. 2079-2089
  • Dubois, M., Gilles, K.A., Hamilton, P., Rebers, P.A., Smith, F., Colorimetric method of determination of sugars and related substances (1956) Analytical Chemistry, 28, pp. 350-356
  • Dumlao, M.R., Darehshouri, A., Cohu, C.M., Muller, O., Mathias, J., Adams, W.W., Demmig-Adams, B., Low temperature acclimation of photosynthetic capacity and leaf morphology in the context of phloem loading type (2012) Photosynthesis Research, 113, pp. 181-189
  • Equiza, M.A., Tognetti, J.A., Morphological plasticity of spring and winter wheats under changing temperatures (2002) Functional Plant Biology, 29, pp. 1427-1436
  • Equiza, M.A., Mirave, J.P., Tognetti, J.A., Morphological, anatomical and physiological responses related to differential shoot vs. root growth inhibition at low temperature in spring and winter wheat (2001) Annals of Botany, 87, pp. 67-76
  • Farrell, A.D., Ougham, H.J., Tomos, A.D., The effect of gibberellic acid on the response of leaf extension to low temperature (2006) Plant, Cell and Environment, 29, pp. 1329-1337
  • Filisetti-Cozzi, T.M.C.C., Carpita, M., Measurement of uronic acids without interference from neutral sugars (1991) Analytical Biochemistry, 197, pp. 157-162
  • Friend, D.J.C., Helson, V.A., Fisher, J.E., Leaf growth in Marquis wheat, as regulated by temperature, light intensity, and daylength (1962) Canadian Journal of Botany, 40, pp. 1299-1311
  • Ganem, D.G., Equiza, M.A., Lorenzo, M., Tognetti, J.A., Cambios en la anatomía epidérmica foliar de cereales de clima templado en respuesta al frío (2014) Revista de la Facultad de Agronomía, La Plata, 113, pp. 157-164
  • Goering, H.K., Van Soest, P.J., Forage fibre analyses (apparatus, reagents, procedures, and some applications) (1970) Agriculture Handbook N° 379. Agricultural Research Services, pp. 1-20. , In U.S. Government Printing Office (Ed),, USDA, Washington, DC, USA
  • González, M.V., Sadras, V.O., Equiza, M.A., Tognetti, J.A., Suboptimal temperature favors reserve formation in biennial carrot (Daucus carota) plants (2009) Physiologia Plantarum, 137, pp. 10-21
  • Gorsuch, P.A., Pandey, S., Atkin, O.K., Thermal de-acclimation: how permanent are leaf phenotypes when cold-acclimated plants experience warming? (2010) Plant, Cell and Environment, 33, pp. 1124-1137
  • Hiraga, S., Sasaki, K., Ito, H., Ohashi, Y., Matsui, H., A large family of class III plant peroxidases (2001) Plant and Cell Physiology, 42, pp. 462-468
  • Hoagland, D.R., Arnon, D.I., The water-culture method for growing plants without soil (1950) California Agricultural Experiment Station Circular, 347, pp. 1-32
  • Hoson, T., Nishitani, K., Miyamoto, K., Ueda, J., Kamisaka, S., Yamamoto, R., Masuda, Y., Effects of hypergravity on growth and cell wall properties of cress hypocotyls (1996) Journal of Experimental Botany, 47, pp. 513-518
  • Hromádková, Z., Paulsen, B.S., Polovka, M., Košt’álová, Z., Ebringerová, A., Structural features of two heteroxylan polysaccharide fractions from wheat bran with anti-complementary and antioxidant activities (2013) Carbohydrate Polymers, 93, pp. 22-30
  • Hüner, N.P.A., Palta, J.P., Li, P.H., Carter, J.V., Anatomical changes in leaves of puma rye in response to growth at cold hardening temperatures (1981) Botanical Gazette, 142, pp. 55-62
  • Hüner, N.P.A., Öquist, G., Sarhan, F., Energy balance and acclimation to light and cold (1998) Trends in Plant Science, 3, pp. 224-230
  • Hüner, N.P.A., Bode, R., Dahal, K., Hollis, L., Rosso, D., Krol, M., Ivanov, A.G., Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited (2012) Frontiers in Plant Science, 3, p. 255
  • Hüner, N.P.A., Dahal, K., Kurepin, L.V., Savitch, L., Singh, J., Ivanov, A.G., Kane, K., Sarhan, F., Potential for increased photosynthetic performance and crop productivity in response to climate change: role of CBFs and gibberellic acid (2014) Frontiers in Chemistry, 2, p. 18
  • Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y., Guy, C.L., Exploring the temperature stress metabolome of Arabidopsis (2004) Plant Physiology, 136, pp. 4159-4168
  • Kruger, N., The Bradford Method for Protein Quantitation (2002) The Protein Protocols Handbook, , Walker J. M., (Ed),, 2nd edn, Humana Press, Totowa, NJ, USA
  • Kurepin, L., Dahal, K., Savitch, L., Singh, J., Bode, R., Ivanov, A., Hurry, V., Hüner, N.P.A., Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation (2013) International Journal of Molecular Science, 14, pp. 12729-12763
  • Kutschera, U., Cell-wall synthesis and elongation growth in hypocotyls of Heliantus annuus L (1990) Planta, 181, pp. 316-323
  • Le Gall, H., Philippe, F., Domon, J.M., Gillet, F., Pelloux, J., Rayon, C., Cell wall metabolism in response to abiotic stress (2015) Plants, 4, pp. 112-166
  • Lee, S.H., Singh, A.P., Chung, G.C., Ahn, S.J., Noh, E.K., Steudle, E., Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients (2004) Physiologia Plantarum, 120, pp. 413-420
  • Liem, H.H., Cardenas, F., Tavassoli, M., Poh-Fitzpatrick, M.B., Muller-Eberhard, U., Quantitative determination of hemoglobin and cytochemical staining for peroxidase using 3, 3’, 5, 5’-tetramethylbenzidine dihydrochloride, a safe substitute for benzidene (1979) Analytical Biochemistry, 98, pp. 388-393
  • Lorenzo, M., Assuero, S.G., Tognetti, J.A., Low temperature differentially affects tillering in spring and winter wheat in association with changes in plant carbon status (2015) Annals of Applied Biology, 166, pp. 236-248
  • MacAdam, J.W., Grabber, J.H., Relationship of growth cessation with the formation of diferulate cross-links and p-coumaroylated lignins in tall fescue leaf blades (2002) Planta, 215, pp. 785-793
  • Maksimović, J.D., Maksimović, V., Živanović, B., Šukalović, V.H.T., Vuletić, M., Peroxidase activity and phenolic compound content in maize root and leaf apoplast, and their association with growth (2008) Plant Science, 175, pp. 656-662
  • Mendis, M., Simsek, S., Production of structurally diverse wheat arabinoxylan hydrolyzates using combinations of xylanase and arabinofuranosidase (2015) Carbohydrate Polymers, 132, pp. 452-459
  • Morrison, I.M., Hydrolysis of plant cell walls with trifluoroacetic acid (1988) Phytochemistry, 27, pp. 1097-1100
  • Murai-Hatano, M., Kuwagata, T., Sakurai, J., Nonami, H., Ahamed, A., Nagasuga, K., Matsunami, T., Okada, M., Effect of low root temperature on hydraulic conductivity of rice plants and the possible role of aquaporins (2008) Plant and Cell Physiology, 49, pp. 1294-1305
  • Park, Y.B., Cosgrove, D.J., Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of arabidopsis (2012) Plant Physiology, 158, pp. 465-475
  • Passardi, F., Penel, C., Dunand, C., Performing the paradoxical: how plant peroxidase modify the cell wall (2004) Trends in Plant Science, 9, pp. 534-540
  • Patel, D., Franklin, K.A., Temperature-regulation of plant architecture (2009) Plant Signaling and Behavior, 4, pp. 577-579
  • Pearce, R.S., Plant freezing and damage (2001) Annals of Botany, 87, pp. 417-424
  • Penfield, S., Temperature perception and signal transduction in plants (2008) New Phytologist, 179, pp. 615-628
  • Pinedo, M., Segarra, C., Conde, R., Occurrence of two endoproteinases in wheat leaf intercellular washing fluid (1993) Physiologia Plantarum, 88, pp. 287-293
  • Pinedo, M., Hernandez, G., Conde, R., Tognetti, J., Effect of low temperature on the protein metabolism of wheat leaves (2000) Biologia Plantarum, 43, pp. 363-367
  • Pinedo, M., Lechner, L., Creus, C., Simontacchi, M., Aguirrezabal, L., Ascorbate modulates apoplastic peroxidase activity during sunflower leaf development (2013) Plant Biology, 15, pp. 60-66
  • Polle, A., Otter, T., Seifert, F., Apoplastic peroxidases and lignification in needles of Norway Spruce (Picea abies L.) (1994) Plant Physiology, 106, pp. 53-60
  • Preston, J.C., Sandve, S.R., Adaptation to seasonality and the winter freeze (2013) Frontiers in Plant Science, 4, p. 167
  • Rajashekar, C.B., Lafta, A., Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and ceii cuitures (1996) Plant Physiology, 111, pp. 605-612
  • Rakszegi, M., Lovegrove, A., Balla, K., Láng, L., Bedö, Z., Veisz, O., Shewry, P.R., Effect of heat and drought stress on the structure and composition of arabinoxylan and □-glucan in wheat grain (2014) Carbohydrate Polymers, 102, pp. 557-565
  • Ralph, J., Bunzel, M., Marita, M.J., Hatfield, R., Lu, F., Kim, H., Schatz, P., Steinhart, H., Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls (2004) Phytochemistry Reviews, 3, pp. 79-96
  • Rancour, D.M., Marita, J.M., Hatfield, R.D., Cell wall composition throughout development for the model grass Brachypodium distachyon (2012) Frontiers in Plant Science, 3, p. 266
  • Reich, P.B., Luo, Y., Bradford, J.B., Poorter, H., Perry, C.H., Oleksyn, J., Temperature drives global patterns in forest biomass distribution in leaves, stems, and roots (2014) Proceedings of the National Academy of Sciences USA, 111, pp. 13721-13726
  • Ritchie, G.A., Shula, R.G., Seasonal changes of tissue-water relations in shoots and root systems of Douglas-fir seedlings (1984) Forest Science, 30, pp. 538-548
  • Roberts, D.W.A., The effect of light on development of the rosette growth habit of winter wheat (1984) Canadian Journal of Botany, 62, pp. 818-822
  • Scheller, H.V., Ulvskov, P., Hemicelluloses (2010) Annual Review of Plant Biology, 61, pp. 263-289
  • Smallwood, M., Bowles, D.J., Plants in a cold climate (2002) Philosophical Transactions of the Royal Society of London, series B: Biological Sciences, 357, pp. 831-847
  • Solecka, D., Boudet, A.M., Kacperska, A., Phenylpropanoid and anthocyanin changes in low-temperature treated winter oilseed rape leaves (1999) Plant Physiology and Biochemistry, 37, pp. 491-496
  • Solecka, D., Zebrowski, J., Kacperska, A., Are Pectins Involved in Cold Acclimation and De-acclimation of Winter Oil-seed Rape Plants? (2008) Annals of Botany, 101, pp. 521-530
  • Stefanowska, M., Kuras, M., Balska, M.K.-Z., Kacperska, A., Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.) (1999) Annals of Botany, 84, pp. 313-319
  • Takahashi, D., Li, B., Nakayama, T., Kawamura, Y., Uemura, M., Plant plasma membrane proteomics for improving cold tolerance (2013) Frontiers in Plant Science, 4, p. 90
  • Thomashow, M.F., Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway (2010) Plant Physiology, 154, pp. 571-577
  • Udén, P., Robinson, P.H., Wiseman, J., Use of detergent system terminology and criteria for submission of manuscripts on new or revised, analytical methods as well as descriptive information on feed analysis and/or variability (2005) Animal Feed Science and Technology, 118, pp. 181-186
  • Valentini, R., Scarascia Mugnozza, G., Giordano, E., Kuzminsky, E., Influence of cold hardening on water relations of three Eucalyptus species (1990) Tree Physiology, 6, pp. 1-10
  • Van Soest, P.J., Robertson, J.B., Lewis, B.A., Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition (1991) Journal of Dairy Science, 74, pp. 3583-3597
  • Vogel, J., Unique aspects of the grass cell wall (2008) Current Opinion in Plant Biology, 11, pp. 301-307
  • Wang, X., Arora, R., Horner, H.T., Krebs, S.L., Structural adaptations in overwintering leaves of thermonastic and nonthermonastic Rhododendron species (2008) Journal of the American Society for Horticultural Science, 133, pp. 768-776
  • Wang, M., Zhang, X., Liu, J.-H., Deep sequencing-based characterization of transcriptome of trifoliate orange (Poncirus trifoliata (L.) Raf.) in response to cold stress (2015) BMC Genomics, 16, p. 555
  • Wei, H., Dhanaraj, A.L., Arora, R., Rowland, L.J., Fu, Y., Sun, L., Identification of cold acclimation-responsive Rhododendron genes for lipid metabolism, membrane transport and lignin biosynthesis: importance of moderately abundant ESTs in genomic studies (2006) Plant, Cell and Environment, 29, pp. 558-570
  • Xue, Y.J., Tao, L., Yang, Z.M., Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide (2008) Journal of Agricultural and Food Chemistry, 56, pp. 9676-9684
  • Yamazaki, T., Kawamura, Y., Uemura, M., Extracellular freezing-induced mechanical stress and surface area regulation on the plasma membrane in cold-acclimated plant cells (2009) Plant Signaling and Behavior, 4, pp. 231-233
  • Zhou, M., Chen, H., Wei, D., Ma, H., Lin, J., Arabidopsis CBF3 and DELLAs positively regulate each other in response to low temperature (2017) Scientific Reports, 7, p. 39819

Citas:

---------- APA ----------
Lorenzo, M., Pinedo, M.L., Equiza, M.A., Fernández, P.V., Ciancia, M., Ganem, D.G. & Tognetti, J.A. (2019) . Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves. Plant Biology, 21, 84-94.
http://dx.doi.org/10.1111/plb.12709
---------- CHICAGO ----------
Lorenzo, M., Pinedo, M.L., Equiza, M.A., Fernández, P.V., Ciancia, M., Ganem, D.G., et al. "Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves" . Plant Biology 21 (2019) : 84-94.
http://dx.doi.org/10.1111/plb.12709
---------- MLA ----------
Lorenzo, M., Pinedo, M.L., Equiza, M.A., Fernández, P.V., Ciancia, M., Ganem, D.G., et al. "Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves" . Plant Biology, vol. 21, 2019, pp. 84-94.
http://dx.doi.org/10.1111/plb.12709
---------- VANCOUVER ----------
Lorenzo, M., Pinedo, M.L., Equiza, M.A., Fernández, P.V., Ciancia, M., Ganem, D.G., et al. Changes in apoplastic peroxidase activity and cell wall composition are associated with cold-induced morpho-anatomical plasticity of wheat leaves. Plant Biol. 2019;21:84-94.
http://dx.doi.org/10.1111/plb.12709