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Abstract:

Lotus species are important forage legumes due to their high nutritional value and adaptability to marginal conditions. However, the dry matter production and regrowth rate of cultivable Lotus spp. is drastically reduced during colder seasons. In this work, we evaluated the chilling response of Lotus japonicus ecotypes MG-1 and MG-20. No significant increases were observed in reactive oxygen species and nitric oxide production or in lipid peroxidation, although a chilling-induced redox imbalance was suggested through NADPH/NADP+ ratio alterations. Antioxidant enzyme catalase, ascorbate peroxidase, and superoxide dismutase activities were also measured. Superoxide dismutase, in particular the chloroplastic isoform, showed different activity for different ecotypes and treatments. Stress-induced photoinhibition also differentially influenced both ecotypes, with MG-1 more affected than MG-20. Data showed that the D2 PSII subunit was more affected than D1 after 1 d of low temperature exposure, although its protein levels recovered over the course of the experiment. Interestingly, D2 recovery was accompanied by improvements in photosynthetic parameters (Asat and Fv/Fm) and the NADPH/NADP+ ratio. Our results suggest that the D2 protein is involved in the acclimation response of L. japonicus to low temperature. This may provide a deeper insight into the chilling tolerance mechanisms of the Lotus genus. © 2016 Elsevier Ireland Ltd.

Registro:

Documento: Artículo
Título:Photosynthetic responses mediate the adaptation of two Lotus japonicus ecotypes to low temperature
Autor:Calzadilla, P.I.; Signorelli, S.; Escaray, F.J.; Menéndez, A.B.; Monza, J.; Ruiz, O.A.; Maiale, S.J.
Filiación:UB1, Instituto de Investigaciones Biotecnológicas, Instituto Tecnológico de Chascomús, UNSAM-CONICET, Chascomús, Argentina
Departamento de Biología Vegetal, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay
School of Plant Biology and the UWA Institute of Agriculture, University of Western Australia, Perth, Australia
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, PROPLAME-PRHIDEB (CONICET), Buenos Aires, Argentina
Palabras clave:Chilling; D2 protein; Legumes; Photoinhibition; PSII; ROS; antioxidant; reactive oxygen metabolite; adaptation; cold; ecotype; enzymology; genetics; Lotus (genus); metabolism; oxidative stress; photosynthesis; Adaptation, Biological; Antioxidants; Cold Temperature; Ecotype; Loteae; Oxidative Stress; Photosynthesis; Reactive Oxygen Species
Año:2016
Volumen:250
Página de inicio:59
Página de fin:68
DOI: http://dx.doi.org/10.1016/j.plantsci.2016.06.003
Título revista:Plant Science
Título revista abreviado:Plant Sci.
ISSN:01689452
CODEN:PLSCE
CAS:Antioxidants; Reactive Oxygen Species
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_01689452_v250_n_p59_Calzadilla

Referencias:

  • Escaray, F.J., Menendez, A.B., Gárriz, A., Pieckenstain, F.L., Estrella, M.J., Castagno, L.N., Ecological and agronomic importance of the plant genus Lotus. Its application in grassland sustainability and the amelioration of constrained and contaminated soils (2012) Plant Sci., 182, pp. 121-133
  • Cyranoski, D., Japanese legume project may help to fix nitrogen problem (2001) Nature, 409, p. 272
  • Fukai, E., Soyano, T., Umehara, Y., Nakayama, S., Hirakawa, H., Tabata, S., Establishment of a Lotus japonicus gene tagging population using the exon targeting endogenous retrotransposon LORE1 (2012) Plant J., 69, pp. 720-730
  • Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., Kato, T., Nakao, M., Genome structure of the legume, Lotus japonicus (2008) DNA Res., 15, pp. 227-239
  • Babuin, M.F., Campestre, M.P., Rocco, R., Bordenave, C.D., Escaray, F.J., Antonelli, C., Response to long-term NaHCO 3-derived alkalinity in model Lotus japonicus ecotypes Gifu B-129 and Miyakojima MG-20: transcriptomic profiling and physiological characterization (2014) PLoS One, 9
  • Díaz, P., Betti, M., Sánchez, D.H., Udvardi, M.K., Monza, J., Márquez, A.J., Deficiency in plastidic glutamine synthetase alters proline metabolism and transcriptomic response in Lotus japonicus under drought stress (2010) New Phytol., 188, pp. 1001-1013
  • Calzadilla, P.I., Maiale, S.J., Ruiz, O.A., Escaray, F.J., Transcriptome response mediated by cold stress in Lotus japonicus (2016) Front. Plant Sci., 7, p. 374
  • Thakur, P., Kumar, S., Malik, J.A., Berger, J.D., Nayyar, H., Cold stress effects on reproductive development in grain crops: an overview (2010) Environ. Exp. Bot., 67, pp. 429-443
  • Ruelland, E., Vaultier, M.-N., Zachowski, A., Hurry, V., Cold signalling and cold acclimation in plants (2009) Adv. Bot. Res., 49, pp. 35-150
  • Long, S.P., Humphries, S., Falkowski, P.G., Photoinhibition of photosynthesis in nature (1994) Annu. Rev. Plant Biol., 45, pp. 633-662
  • Huner, N.P.A., Öquist, G., Hurry, V.M., Krol, M., Falk, S., Griffith, M., Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants (1993) Photosynth. Res., 37, pp. 19-39
  • Murata, N., Takahashi, S., Nishiyama, Y., Allakhverdiev, S.I., Photoinhibition of photosystem II under environmental stress (2007) Biochim. Biophys. Acta Bioenerg., 1767, pp. 414-421
  • Pagter, M., Liu, F., Jensen, C.R., Petersen, K.K., Effects of chilling temperatures and short photoperiod on PSII function, sugar concentrations and xylem sap ABA concentrations in two Hydrangea species (2008) Plant Sci., 175, pp. 547-555
  • Takahashi, S., Murata, N., How do environmental stresses accelerate photoinhibition? (2008) Trends Plant Sci., 13, pp. 178-182
  • Signorelli, S., Casaretto, E., Sainz, M., Díaz, P., Monza, J., Borsani, O., Antioxidant and photosystem II responses contribute to explain the drought-heat contrasting tolerance of two forage legumes (2013) Plant Physiol. Biochem., 70, pp. 195-203
  • Sainz, M., Díaz, P., Monza, J., Borsani, O., Heat stress results in loss of chloroplast Cu/Zn superoxide dismutase and increased damage to Photosystem II in combined drought-heat stressed Lotus japonicus (2010) Physiol. Plant., 140, pp. 46-56
  • Hashiguchi, M., Tsuruta, S., Akashi, R., Morphological traits of Lotus japonicus (Regal) ecotypes collected in Japan (2011) Interdiscip. Bio Central, 3, pp. 1-4
  • Hoagland, D.R., Arnon, D.I., (1950) The Water-culture Method for Growing Plants without Soil., Circular, 347. , California Agricultural Experiment Station
  • Inskeep, W.P., Bloom, P.R., Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone (1985) Plant Physiol., 77, pp. 483-485
  • Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K., Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds (1999) Planta, 207, pp. 604-611
  • Thordal-Christensen, H., Zhang, Z., Wei, Y., Collinge, D.B., Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction (1997) Plant J., 11, pp. 1187-1194
  • Jabs, T., Dietrich, R.A., Dangl, J.L., Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide (1996) Science, 273, pp. 1853-1856
  • Aebi, H., Catalase in vitro (1984) Methods Enzymol., 105, pp. 121-126
  • Hossain, M., Asada, K., Ascorbate-regenerating enzymes in chloroplasts (1987) Indian J. Biochem. Biophys., 24, p. 52
  • Beauchamp, C., Fridovich, I., Superoxide dismutase: improved assays and an assay applicable to acrylamide gels (1971) Anal. Biochem., 44, pp. 276-287
  • Signorelli, S., Corpas, F.J., Borsani, O., Barroso, J.B., Monza, J., Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus (2013) Plant Sci., 201, pp. 137-146
  • Matsumura, H., Miyachi, H.S., Cycling assay for nicotinamide adenine (1980) Methods Enzymol., 69, pp. 465-470
  • Strasser, R.J., Srivastava, A., Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria (1995) Photochem. Photobiol., 61, pp. 32-42
  • Strasser, R.J., Stirbet, A.D., Estimation of the energetic connectivity of PS II centres in plants using the fluorescence rise O-J-I-P: fitting of experimental data to three different PS II models (2001) Math. Comput. Simul, 56, pp. 451-462
  • Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular Cloning, , Cold spring harbor laboratory press, New York
  • Escaray, F.J., Passeri, V., Babuin, F.M., Marco, F., Carrasco, P., Damiani, F., Lotus tenuis x L. corniculatus interspecific hybridization as a means to breed bloat-safe pastures and gain insight into the genetic control of proanthocyanidin biosynthesis in legumes (2014) BMC Plant Biol., 14, p. 1
  • Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., (2008) InfoStat, Versión, , Grupo InfoStat, FCA, Universidad Nacional De Córdoba, Argentina
  • Airaki, M., Leterrier, M., Mateos, R.M., Valderrama, R., Chaki, M., Barroso, J.B., Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress (2012) Plant Cell Environ., 35, pp. 281-295
  • Melchiorre, M., Quero, G.E., Parola, R., Racca, R., Trippi, V.S., Lascano, R., Physiological characterization of four model Lotus diploid genotypes: l. japonicus (MG20 and Gifu), L. filicaulis, and L. burttii under salt stress (2009) Plant Sci., 177, pp. 618-628
  • Kim, H.-S., Oh, J.-M., Luan, S., Carlson, J.E., Ahn, S.-J., Cold stress causes rapid but differential changes in properties of plasma membrane H+-ATPase of camelina and rapeseed (2013) J. Plant Physiol., 170, pp. 828-837
  • Balestrasse, K.B., Tomaro, M.L., Batlle, A., Noriega, G.O., The role of 5-aminolevulinic acid in the response to cold stress in soybean plants (2010) Phytochemistry, 71, pp. 2038-2045
  • Krüger, G.H.J., De Villiers, M.F., Strauss, A.J., de Beer, M., van Heerden, P.D.R., Maldonado, R., Inhibition of photosystem II activities in soybean (Glycine max) genotypes differing in chilling sensitivity (2014) S. Afr. J. Bot., 95, pp. 85-96
  • Bonnecarrère, V., Borsani, O., Díaz, P., Capdevielle, F., Blanco, P., Monza, J., Response to photoxidative stress induced by cold in japonica rice is genotype dependent (2011) Plant Sci., 180, pp. 726-732
  • Strauss, A.J., Krüger, G.H.J., Strasser, R.J., Van Heerden, P.D.R., Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient OJIP (2006) Environ. Exp. Bot., 56, pp. 147-157
  • Hogewoning, S.W., Harbinson, J., Insights on the development, kinetics, and variation of photoinhibition using chlorophyll fluorescence imaging of a chilled variegated leaf (2007) J. Exp. Bot., 58, pp. 453-463
  • Stirbet, A., Excitonic connectivity between photosystem II units: what is it, and how to measure it? (2013) Photosynth. Res., 116, pp. 189-214
  • Kettunen, R., Tyystjarvi, E., Aro, E.-M., Degradation pattern of photosystem II reaction center protein D1 in lntact leaves (1996) Plant Physiol., pp. 1183-1190
  • Frascaroli, E., Landi, P., Divergent selection in a maize population for germination at low temperature in controlled environment: study of the direct response, of the trait inheritance and of correlated responses in the field (2013) Theor. Appl. Genet., 126, pp. 733-746
  • Kollipara, K.P., Saab, I.N., Wych, R.D., Lauer, M.J., Singletary, G.W., Expression profiling of reciprocal maize hybrids divergent for cold germination and desiccation tolerance (2002) Plant Physiol., 129, pp. 974-992
  • Faria, T., Silvério, D., Breia, E., Cabral, R., Abadia, A., Abadia, J., Differences in the response of carbon assimilation to summer stress (water deficits, high light and temperature) in four Mediterranean tree species (1998) Physiol. Plant., 102, pp. 419-428
  • Corpas, F.J., Leterrier, M., Valderrama, R., Airaki, M., Chaki, M., Palma, J.M., Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress (2011) Plant Sci., 181, pp. 604-611
  • Lee, D.H., Lee, C.B., Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays (2000) Plant Sci., 159, pp. 75-85
  • Cantrel, C., Vazquez, T., Puyaubert, J., Rezé, N., Lesch, M., Kaiser, W.M., Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana (2011) New Phytol., 189, pp. 415-427
  • Gill, S.S., Tuteja, N., Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants (2010) Plant Physiol. Biochem., 48, pp. 909-930
  • Zhao, M.-G., Chen, L., Zhang, L.-L., Zhang, W.-H., Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis (2009) Plant Physiol., 151, pp. 755-767
  • Qiao, W., Li, C., Fan, L.-M., Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses (2014) Environ. Exp. Bot., 100, pp. 84-93
  • Bowler, C., van Montagu, M., Inze, D., Superoxide dismutase and stress tolerance (1992) Annu. Rev. Plant Biol., 43, pp. 83-116
  • Tang, L., Kwon, S.-Y., Kim, S.-H., Kim, J.-S., Choi, J.S., Cho, K.Y., Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature (2006) Plant Cell Rep., 25, pp. 1380-1386
  • Noctor, G., Metabolic signalling in defence and stress: the central roles of soluble redox couples Plant (2006) Cell Environ., 29, pp. 409-425
  • Noctor, G., Foyer, C.H., Homeostasis of adenylate status during photosynthesis in a fluctuating environment (2000) J. Exp. Bot., 51, pp. 347-356
  • Pérez-Ruiz, J.M., Spínola, M.C., Kirchsteiger, K., Moreno, J., Sahrawy, M., Cejudo, F.J., Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage (2006) Plant Cell, 18, pp. 2356-2368
  • Michalska, J., Zauber, H., Buchanan, B.B., Cejudo, F.J., Geigenberger, P., NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 9908-9913
  • Nikkanen, L., Rintamäki, E., Thioredoxin-dependent regulatory networks in chloroplasts under fluctuating light conditions (2014) Philos. Trans. R. Soc. Lond. B: Biol. Sci., 369, p. 20130224
  • Ying, W., NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences (2008) Antioxid. Redox Signal., 10, pp. 179-206
  • Foyer, C.H., Shigeoka, S., Understanding oxidative stress and antioxidant functions to enhance photosynthesis (2011) Plant Physiol., 155, pp. 93-100
  • Kratsch, H.A., Wise, R.R., The ultrastructure of chilling stress (2000) Plant Cell Environ., 23, pp. 337-350
  • Noctor, G., Mhamdi, A., Foyer, C.H., The roles of reactive oxygen metabolism in drought: not so cut and dried (2014) Plant Physiol., 164, pp. 1636-1648
  • Gururani, M.A., Venkatesh, J., Ganesan, M., Strasser, R.J., Han, Y., Kim, J.-I., In vivo assessment of cold tolerance through chlorophyll-a fluorescence in transgenic zoysiagrass expressing mutant phytochrome A (2015) PLoS One, 10
  • Zivcak, M., Brestic, M., Kalaji, H.M., Govindjee Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? (2014) Photosynth. Res., 119, pp. 339-354
  • Aro, E.-M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes (2005) J. Exp. Bot., 56, pp. 347-356
  • Murchie, E.H., Hubbart, S., Peng, S., Horton, P., Acclimation of photosynthesis to high irradiance in rice: gene expression and interactions with leaf development (2005) J. Exp. Bot., 56, pp. 449-460
  • Zinta, G., AbdElgawad, H., Domagalska, M.A., Vergauwen, L., Knapen, D., Nijs, I., Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels (2014) Global Change Biol., 20, pp. 3670-3685
  • Foyer, C.H., Neukermans, J., Queval, G., Noctor, G., Harbinson, J., Photosynthetic control of electron transport and the regulation of gene expression (2012) J. Exp. Bot., 63, pp. 1637-1661
  • Huner, N.P.A., Öquist, G., Sarhan, F., Energy balance and acclimation to light and cold (1998) Trends Plant Sci., 3, pp. 224-230
  • Aro, E.-M., Virgin, I., Andersson, B., Photoinhibition of photosystem II. Inactivation, protein damage and turnover (1993) Biochim. Biophys. Acta Bioenerg., 1143, pp. 113-134
  • Bascuñán-Godoy, L., Sanhueza, C., Cuba, M., Zuñiga, G.E., Corcuera, L.J., Bravo, L.A., Cold-acclimation limits low temperature induced photoinhibition by promoting a higher photochemical quantum yield and a more effective PSII restoration in darkness in the Antarctic rather than the Andean ecotype of Colobanthus quitensis Kunt Bartl (Cariophyllaceae) (2012) BMC Plant Biol., 12, p. 1
  • Zhou, B., Deng, Y.-S., Kong, F.-Y., Li, B., Meng, Q.-W., Overexpression of a tomato carotenoid ε-hydroxylase gene alleviates sensitivity to chilling stress in transgenic tobacco (2013) Plant Physiol. Biochem., 70, pp. 235-245
  • Tikkanen, M., Aro, E.-M., Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants (2012) Biochim. Biophys. Acta, pp. 232-238
  • de Vitry, C., Olive, J., Drapier, D., Recouvreur, M., Wollman, F.-A., Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii (1989) J. Cell Biol., 109, pp. 991-1006
  • Komenda, J., Sobotka, R., Nixon, P.J., Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria (2012) Curr. Opin. Plant Biol., 15, pp. 245-251
  • Dobáková, M., Tichý, M., Komenda, J., Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803 (2007) Plant Physiol., 145, pp. 1681-1691
  • Nelson, C.J., Alexova, R., Jacoby, R.P., Millar, A.H., Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling (2014) Plant Physiol., 166, pp. 91-108
  • Schnettger, B., Critchley, C., Santore, U.J., Graf, M., Krause, G.H., Relationship between photoinhibition of photosynthesis, D1 protein turnover and chloroplast structure: effects of protein synthesis inhibitors (1994) Plant Cell Environ., 17, pp. 55-64
  • Schwarz, C., Elles, I., Kortmann, J., Piotrowski, M., Nickelsen, J., Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40 (2007) Plant Cell, 19, pp. 3627-3639
  • Mulo, P., Sakurai, I., Aro, E.-M., Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair (2012) Biochim. Biophys. Acta Bioenerg., 1817, pp. 247-257

Citas:

---------- APA ----------
Calzadilla, P.I., Signorelli, S., Escaray, F.J., Menéndez, A.B., Monza, J., Ruiz, O.A. & Maiale, S.J. (2016) . Photosynthetic responses mediate the adaptation of two Lotus japonicus ecotypes to low temperature. Plant Science, 250, 59-68.
http://dx.doi.org/10.1016/j.plantsci.2016.06.003
---------- CHICAGO ----------
Calzadilla, P.I., Signorelli, S., Escaray, F.J., Menéndez, A.B., Monza, J., Ruiz, O.A., et al. "Photosynthetic responses mediate the adaptation of two Lotus japonicus ecotypes to low temperature" . Plant Science 250 (2016) : 59-68.
http://dx.doi.org/10.1016/j.plantsci.2016.06.003
---------- MLA ----------
Calzadilla, P.I., Signorelli, S., Escaray, F.J., Menéndez, A.B., Monza, J., Ruiz, O.A., et al. "Photosynthetic responses mediate the adaptation of two Lotus japonicus ecotypes to low temperature" . Plant Science, vol. 250, 2016, pp. 59-68.
http://dx.doi.org/10.1016/j.plantsci.2016.06.003
---------- VANCOUVER ----------
Calzadilla, P.I., Signorelli, S., Escaray, F.J., Menéndez, A.B., Monza, J., Ruiz, O.A., et al. Photosynthetic responses mediate the adaptation of two Lotus japonicus ecotypes to low temperature. Plant Sci. 2016;250:59-68.
http://dx.doi.org/10.1016/j.plantsci.2016.06.003