Biologia plantarum 57:495-506, 2013 | DOI: 10.1007/s10535-013-0329-x
Cold-induced changes in mineral content in leaves of Coffea spp. Identification of descriptors for tolerance assessment
- 1 Centro de Ambiente, Agricultura e Desenvolvimento, Instituto de Investigação Científica Tropical, Quinta do Marquês, Oeiras, Portugal
- 2 Dept. de Ciências e Tecnologia da Biomassa, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Monte de Caparica, Portugal
Temperature and mineral nutrition are major environmental factors regulating plant growth and development. Yet, cold impact on mineral contents and the ability of the plants to perform changes in specific elements as a part of the acclimation process received little attention. Using five Coffea genotypes previously characterized concerning their cold sensitivity, a mineral analysis was performed considering macro (N, P, K, Ca, Mg, and S) and micro (Na, Fe, Mn, Zn, Cu, and B) nutrients in order to predict their importance in cold tolerance. The results showed a cold-induced dynamics of mineral nutrients in recently mature leaves. The less cold sensitive Icatu, and partially Catuaí, accumulated N, Ca, Mn, Cu, and Zn with potential implications in the maintenance of photosynthetic performance, the reinforcement of the antioxidative defense system, lipid metabolism, and the expression of cold regulated genes, thus constituting interesting traits to evaluate the cold acclimation ability. After a principal component analysis (PCA), N, Fe, Mn, and Cu were further confirmed as strong candidates for an early cold tolerance evaluation due to their dynamics and to specific roles in the activities of Cu/Zn-SOD (Cu), APX (Fe), and PSII (Mn).
Keywords: cold sensitivity; coffee genotypes; mineral dynamics; principal component analysis; tolerance markers
Subjects: cold tolerance; temperature - low; principal component analysis; tolerance markers; nitrogen; phosphorus; potassium; calcium; magnesium; sulfur; natrium; iron; manganese; zinc; copper; boron; superoxide dismutase; ascorbate peroxidase; oxygen evolving complex
Received: October 9, 2012; Accepted: January 10, 2013; Published: September 1, 2013 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Adams, W.W., III, Demmig-Adams, B., Rosenstiel, T.N., Brightwell, A.K., Ebbert, V.: Photosynthesis and photoprotection in overwintering plants. - Plant Biol. 4: 545-557, 2002.
Go to original source... - Aphalo, P.J., Lahti, M., Lehto, T., Repo, T., Rummukainen, A., Mannerkoski, H., Finér, L.: Responses of silver birch saplings to low soil temperature. - Silva fennica 40: 429-442, 2006.
Go to original source... - Asada, K.: Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. - In: Baker, N.R., Bowyer, J.R. (ed.): Photoinhibition of Photosynthesis - From Molecular Mechanisms to the Field. Pp. 129-142, BIOS Scientific Publishers, Oxford 1994.
- Barros, R.S., Maestri, M., Rena, A.B.: Physiology of growth and production of the coffee tree - a review. - J. Coffee Res. 27: 1-54, 1999.
- Batista-Santos, P., Lidon, F.C., Fortunato, A., Leitão, A.E., Lopes, E., Partelli, F., Ribeiro, A.I., Ramalho, J.C.: Cold impact on photosynthesis in genotypes of Coffea spp. - Photosystems sensitivity, photoprotective mechanisms and gene expression. - J. Plant Physiol. 168: 792-806, 2011.
Go to original source... - Bauer, H., Wierer, R., Hatheway, W.H., Larcher, W.: Photosynthesis of Coffea arabica after chilling. - Physiol. Plant. 64: 449-454, 1985.
Go to original source... - Belintani, N.G., Guerzoni, J.T.S., Moreira, R.M.P., Vieira L.G.E.: Improving low-temperature tolerance in sugarcane by expressing the ipt gene under a cold inducible promoter. - Biol Plant 56: 71-77, 2012.
Go to original source... - Bohnert, H.J., Sheveleva, E.: Plant stress adaptations-making metabolism move. - Curr. Opin. Plant Biol. 1: 267-274, 1998.
Go to original source... - Bragança, S.M., Prezotti, L.C., Lani, J.Á.: [Nutrition of Conilon coffee.] - In: Ferrão, R.G., Fonseca, A.F., Bragança, S.M., Ferrão, M.A., Muner, L.H. (ed.): Café Conilon. Pp. 297-327, DCM/Incaper, Vitória, Espírito Santo 2007. [In Port.]
- Cakmak, I.: Role of Mineral Nutrients in Tolerance of Crop Plants to Environmental Stress Factors. - In: Proceedings from the International Symposium on Fertigation - Optimizing the Uilization of Water and Nutrients. Pp. 35-48. Intemational Potash lnstitute, Horgen 2005a.
- Cakmak, I.: The role of potassium in alleviating detrimental effects of abiotic stresses in plants. - J. Plant Nutr. Soil Sci. 168: 521-530, 2005b.
Go to original source... - Campos, P.S., Quartin, V., Ramalho, J.C., Nunes, M.A.: Electrolytic leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. - J. Plant Physiol. 160: 283-292, 2003.
Go to original source... - Carvajal, J.: Cafeto - Cultivo y Fertilization.[[Coffee - Cultivation and Fertilization] - Instituto Intemacional de la Potassa, Bern 1984.[In Span.]
- Chapman, H.D., Pratt P.F.: Methods of Analysis of Soils, Plants, and Waters. - University of California, Berkeley 1961.
- Correia, J.H.D.: [Determination of total nitrogen through the Kjeldahl method.] - Bioq. Aplic. 1: 43-57, 1984. [In Port.]
- DaMatta, F.M., Ramalho, J.C.: Impacts of drought and temperature stress on coffee physiology and production: a review. - Braz. J. Plant Physiol. 18: 55-81, 2006.
Go to original source... - Dunn, S.: Factors affecting cold resistance in plants. - Plant Physiol. 12: 519-526, 1937.
Go to original source... - Ensminger, I., Busch, F., Huner, N.P.A.: Photosynthesis and cold acclimation: sensing low temperature through photosynthesis. - Physiol. Plant. 126: 28-44, 2006.
Go to original source... - Fahl, J.I., Carelli, M.L.C., Vega, J., Magalhães, A.C.: Nitrogen and irradiance levels affecting net photosynthesis and growth of young coffee plants (Coffea arabica L.). - J. hort. Sci. 69: 161-169, 1994.
Go to original source... - Fortunato, A., Lidon, F.C., Batista-Santos, P., Leitão, A.E., Pais, I.P., Ribeiro, A.I., Ramalho, J.C.: Biochemical and molecular characterization of the antioxidative system of Coffea sp. under cold conditions in genotypes with contrasting tolerance. - J. Plant Physiol. 167: 333-342, 2010.
Go to original source... - Foyer, C.H.: The contribution of photosynthetic oxygen metabolism to oxidative stress in plants. - In: Inzé, D., Van Montagu, M. (ed.): Oxidative Stress in Plants. Pp. 33-68. Taylor & Francis, London 2002.
- Gao, J.-J., Li, T., Yu, X.-C.: Gene expression and activities of SOD in cucumber seedlings were related with concentrations of Mn2+, Cu2+, or Zn2+ under low temperature stress. - Agr. Sci. China 8: 678-684, 2009.
Go to original source... - Garmash, E.V.: Temperature controls a dependence of barley plant growth on mineral nutrition level. - Russ. J. Plant Physiol. 52: 338-344, 2005.
Go to original source... - Geiger, D.R., Koch, K.E., Shieh, W.J.: Effect of environmental factors on whole plant assimilate partitioning and associated gene expression. - J. exp. Bot. 47: 1229-1238, 1996.
Go to original source... - Ghanotakis, D.F., Yocum C.F.: Photosystem II and the oxygen evolving complex. - Annu. Rev. Plant Physiol. Plant mol. Biol. 41: 255-276, 1990.
Go to original source... - Groot, C.C., Marcelis, L.F.M., Van den Boogaard, R., Kaiser, W.M., Lambers, H.: Interaction of nitrogen and phosphorus nutrition in determining growth. - Plant Soil 248: 257-268, 2003.
Go to original source... - Halliwell, B., Gutteridge, J.M.C.: Free Radicals in Biology and Medicine. 2nd Ed. - Clarendon Press, Oxford 1989.
- Harwood, J.L.: Involvement of chloroplast lipids in the reaction of plants submitted to stress. - In: Siegenthaler, P.-A., Murata, N. (ed.): Lipids in Photosynthesis: Structure, Function and Genetics. Pp. 287-302. Kluwer Academic Publishers, Dordrecht 1988.
Go to original source... - Hewezi, T., Léger, M., El Kayal, W., Gentzbittel, L.: Transcriptional profiling of sunflower plants growing under low temperatures reveals an extensive down-regulation of gene expression associated with chilling sensitivity. - J. exp. Bot. 57: 3109-3122, 2006.
Go to original source... - Hoagland, D.R., Snyder, W.C.: Nutrition of strawberry under controlled conditions. (a) Effects of deficiencies of boron and certain other elements. (b) Susceptibility to injury from sodium salts. - Proc. amer. Soc. hort. Sci. 30: 288-294, 1933.
- Ishikawa, T., Madhusudhan, R., Shigeoka, S.: Effect of iron on the expression of ascorbate peroxidase in Euglena gracilis. - Plant Sci. 165: 1363-1367, 2003.
Go to original source... - Kayihan, C., Eyidogan, F., Afsar, N., Oktem, H.A., Yucel, M.: Cu/Zn superoxide dismutase activity and respective gene expression during cold acclimation and freezing stress in barley cultivars. - Biol Plant 56: 693-698, 2012.
Go to original source... - Lima, A.L., DaMatta, F.M., Pinheiro, H.A., Totola, M.R., Loureiro, M.E.: Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions. - Environ. exp. Bot. 47: 239-247, 2002.
Go to original source... - Logan, B.A.: Reactive oxygen species and photosynthesis. - In: Smirnoff, N. (ed.): Antioxidants and Reactive Oxygen in Plants. Pp. 250-267. Blackwell Publishing, Oxford 2005.
Go to original source... - Lynch, J.P., St. Clair, S.B.: Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. - Field Crops Res. 90: 101-115, 2004.
Go to original source... - Malavolta, E.: Nutrição Mineral e Adubação do Cafeeiro - Colheitas Económicas Máximas. [Mineral Nutrition and Fertilization of Coffee - Maximal Economical Yield.] - Editora Agronômica Ceres, São Paulo 1993.
- Marschner, H.: Mineral Nutrition of Higher Plants, 2nd Ed. - Academic Press, London 1995.
- McGrath, S.P., Zhao, F.J.: Sulphur uptake, yield responses and the interactions between nitrogen and sulphur in winter oilseed rape (Brassica napus). - J. agr. Sci. 126: 53-62, 1996.
Go to original source... - Mengel, K., Kirkby, E.A.: Principles of Plant Nutrition. 5th Ed. - Kluwer Academic Publishers, Dordrecht 2001.
Go to original source... - Mills, R.F., Doherty, M.L., López-Marqués, R.L., Weimar, T., Dupree, P., Palmgren, M.G., Pittman, J.K., Williams, L.E.: ECA3, a Golgi-localized P2A-type ATPase, plays a crucial role in manganese nutrition in Arabidopsis. - Plant Physiol. 146: 116-128, 2008.
Go to original source... - Monroy, A.F., Dhindsa, R.S.: Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 °C. - Plant Cell 7: 321-331, 1995.
- Morcuende, R., Pérez, P., Martínez-Carrasco, R., Molino, I.M., Puente, L.S.: Long- and short-term responses of leaf carbohydrate levels and photosynthesis to decreased sink demand in soybean. - Plant Cell Environ. 19: 976-982, 1996.
Go to original source... - Öncel, I.: A study on the relation of cold acclimation and hardiness to mineral nutritional and biochemical fluctuations of three agricultural forms of Brassica oleracea L. - III. Mineral nutrients. - Commun. Fac. Sci. Univ. Ank??. Serie C 6: 101-131, 1988.
Go to original source... - Öquist, G.: Seasonally induced changes in acyl lipids and fatty acids of chloroplast thylakoids of Pinus silvestris. A correlation between the level of unsaturation of monogalatosyldiglyceride and the rate of electron transport. - Plant Physiol. 69: 869-875, 1982.
Go to original source... - Paal, Z., Ertl, G., Lee, S.B.: Interactions of potassium, oxygen and nitrogen with polycrystalline iron surfaces. - Appl. Surface Sci. 8: 231-249, 1981.
Go to original source... - Partelli, F.L., Batista-Santos, P., Campos, P.S., Pais, I.P., Quartin, V.L., Vieira, H.D., Ramalho, J.C.: Characterization of the main lipid components of chloroplast membranes and cold induced changes in Coffea spp. - Environ. exp. Bot. 74: 194-204, 2011.
Go to original source... - Pedas, P., Ytting, C.K., Fuglsang, A.T., Jahn, T.P., Schjoerring, J.K., Husted, S.: Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. - Plant Physiol. 148: 455-466, 2008.
Go to original source... - Perl-Treves, R., Perl, A.: Oxidative stress: an introduction. - In: Inzé, D., Van Montagu, M. (ed.): Oxidative Stress in Plants. Pp. 1-32, Taylor & Francis, London 2002.
- Pompelli, M.F., Martins, S.C.V., Antunes, W.C., Chaves, A.R.M., DaMatta, F.M.: Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. - J. Plant Physiol. 167: 1052-1060, 2010.
Go to original source... - Ramalho, J.C., Campos, P.S., Quartin, V.L., Silva, M.J., Nunes, M.A.: High irradiance impairments on photosynthetic electron transport, ribulose-1,5-bisphosphate carboxylase/oxygenase and N assimilation as a function of N availability in Coffea arabica L. plants. J. Plant Physiol. 154: 319-326, 1999.
Go to original source... - Ramalho, J.C., Campos, P.S., Teixeira, M., Nunes, M.A.: Nitrogen dependent changes in antioxidant systems and in fatty acid composition of chloroplast membranes from Coffea arabica L. plants submitted to high irradiance. - Plant Sci. 135: 115-124, 1998.
Go to original source... - Ramalho, J.C., Pons, T.L., Groeneveld, H.W., Azinheira, H.G., Nunes, M.A.: Photosynthetic acclimation to high light conditions in mature leaves of Coffea arabica L.: role of xanthophylls, quenching mechanisms and nitrogen nutrition. - Aust. J. Plant Physiol. 27: 43-51, 2000.
- Ramalho, J.C., Quartin, V., Fahl, J.I., Carelli, M.L., Leitão, A.E., Nunes, M.A.: Cold acclimation ability of photosynthesis among species of the tropical Coffea genus. - Plant Biol. 5: 631-641, 2003.
Go to original source... - Ramalho, J.C., Rebelo, M.C., Santos, M.E., Antunes, M.L., Nunes, M.A.: Effects of calcium deficiency on Coffea arabica - nutrient changes and correlation of calcium levels with some photosynthetic parameters. - Plant Soil 172: 87-96, 1995.
Go to original source... - Raven, J.A.: Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. - New Phytol. 116: 1-18, 1990.
Go to original source... - Raven, J.A., Evans, M.C.W., Korb, R.E.: The role of trace metals in photosynthetic electron transport in O2-evolving organisms. - Photosynt. Res. 60: 111-149, 1999.
Go to original source... - Röhl, R., Hoffmann, H.-J., Besler, W.: Sulfur analysis of conifer needles by inductively coupled plasma atomic emission spectrometry. - Fresenius J. anal. Chem. 317: 872, 1984.
- Rolf, F.J.: NTSYS-pc: Numerical Taxonomy and Multivariate Analysis System. - Exeter Publishing, New York 1989.
- Song, W.-I., Zhang, Z.-B., Shao, H.-B., Guo, X.-L., Cao, H.-X., Zhao, H.-B., Fu, Z.-Y., Hu, X.-J.: Relationship between calcium decoding elements and plant abiotic-stress resistance. - Int. J. biol. Sci. 4: 116-125, 2008.
Go to original source... - Tähtiharju, S., Sangwan, V., Monroy, A.F., Dhindsa, R.S., Borg, M.: The induction of kin genes in cold-acclimating Arabidopsis thaliana. Evidence of a role for calcium. - Planta 203: 442-447, 1997.
Go to original source... - Vandecasteele, C., Block, C.B.: Modern Methods for Trace Element Determination. - John Willey & Sons, Chichester 1993.
- Vansuyt, G., Lopez, F., Inze, D., Briat, J.-F., Fourcroy, P.: Iron triggers a rapid induction of ascorbate peroxidase gene expression in Brassica napus. - FEBS Lett. 410: 195-200, 1997.
Go to original source... - Walker, D.J., Romero, P., Hoyos, A., Correal, E.: Seasonal changes in cold tolerance, water relations and accumulation of cations and compatible solutes in Atriplex halimus L. - Environ. exp. Bot. 64: 217-224, 2008.
Go to original source... - Waraich, E.A., Ahmad, R., Saifullah, Ashraf, M.Y., Ehsanullah: Role of mineral nutrition in alleviation of drought stress in plants. - Aust. J. Crop Sci. 5: 764-777, 2011.
- Xin, Z., Browse, J.: Cold comfort farm: the acclimation of plants to freezing temperatures. - Plant Cell Environ. 23: 893-902, 2000.
Go to original source...



