Electrical conductivity as an indicator of damage due to low temperatures in beans leaves

Juliandra Rodrigues Rosisca, Carolina Maria Gaspar de Oliveira, Altamara Viviane de Souza Sartori, Renata Stolf-Moreira, Marcelo Augusto de Aguiar e Silva, Heverly Morais

Abstract


The electrical conductivity test indirectly evaluates cell membrane disorganization by quantifying the electrolytes released into the water after tissue imbibing. The objective of this work was to evaluate methodological variations in the electrical conductivity test, for it to serve as an indicator of low temperature-induced damages and estimate the cold tolerance of bean plants. Cultivar IPR Uirapuru plants were subjected to minimum temperatures of 4 °C, 2 °C, 0 °C, -1 °C, -2 °C, -3 °C, and -4 °C for 1 h in a growth chamber under controlled conditions. After the treatment period, the response of plants to cold stress was evaluated by determination of the total protein content, and catalase (CAT) and ascorbate peroxidase (APX) enzymatic activities, and evaluation of photosystem II (Fm/Fv) efficiency and leaf anatomy. These results were compared with those obtained in the electrical conductivity test, which was performed in plants under cold stress as well as under a non-stress environment, with 2, 4, 6, and 8 leaf discs immersed in 30 mL of distilled water for 24 h in BOD, at temperatures of 25 °C, 30 °C, and 35°C. Analysis of variance was performed using a completely randomized design, and for electrical conductivity, a number of discs × cold stress temperature combinations were used for each soak temperature. The averages were compared using the Turkey's test at 5% and 10% probability. Pearson correlation coefficient (r) between the conductivity averages and other cold stress evaluation data was also performed. The results showed a marked reduction in the ratio (Fv/Fm) only in the treatments at -3 °C and -4°C, which indicated tissue death. At temperatures below 0°C, there was a collapse of the leaf blade tissues, and it was not possible to differentiate the palisade parenchyma from the spongy parenchyma in the treatments at -2°C, -3°C, and -4°C. There was an increase in the protein content since the temperature -3°C. The enzyme activity of CAT decrease at -4°C whereas that of APX increased. In the electrical conductivity test, there was a significant interaction between soak temperature and the number of discs, and an increase in conductivity of the solution with a decrease in temperature was verified in several treatments, among which, the combination that best correlated with the other tests was 25°C with six leaf discs. It was concluded that the electrical conductivity test presents results similar to those obtained from other physiological, biochemical, and anatomical tests, and therefore, it can be used to evaluate the damage caused by low temperatures in bean plants.

Keywords


Oxidative stress; Cold; Enzymes; Membrane integrity.

Full Text:

PDF

References


ALMESELMANI, M.; DESHMUKH, P. S.; SAIRAM, R. K.; KUSHWAHA, S. R.; SINGH, T. P. Protective role of antioxidant enzymes under high temperature stress. Plant Science, Davis, v. 171, n. 3, p. 382-388, 2006. DOI: 10.1016/j.plantsci.2006.04.009

BANDURSKI, R. S.; GREINER, C. M. The enzymatic synthesis of oxalacetate from phosphoryl-enopyruvate and carbon dioxide. The Journal of Biological Chemistry, Massachusetts, v. 204, n. 1, p. 781-786, 1953.

BARRANCO, D.; RUIZ, N.; GÓMEZ-DEL CAMPO, M. Frost tolerance of eight Olive cultivars. HortScience, Baton Rouge, v. 40, n. 3, p. 558-560, 2005.

BARTOLOZZI, F.; FONTANAZZA, G. Assessment of frost tolerance in olive (Olea europaea L.). Scientia Horticulturae, Agassiz, v. 81, n. 3, p. 309-319, 1999. DOI: 10.1016/S0304-4238(99)00019-9

BERTAMINI, M.; ZULINI, L.; MUTHUCHELIAN, K.; NEDUNCHEZHIAN, N. Low night temperature effects on photosynthetic performance on two gravepine genotypes. Biologia Plantarum, Prague, v. 51, n. 2, p. 381-385, 2007.

BJÖRKMAN, O.; DEMMIG, B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta, Berlim, v. 170, n. 4, p. 489-504, 1987.

BOLHÀR-NORDENKAMPF, H. R.; ÖQUIST, G. Chlorophyll fluorescence as a tool in photosynthesis research. In: HALL, D. O.; SCURLOCK, J. M. O.; BOLHÀR-NORDENKAMPF, H. R.; LEEGOOD, R. C.; LONG, S. P. (Ed.). Photosynthesis and production in a changing environment: a field and laboratory manual. London: Chapman & Hall, 1993. p. 193-206.

BRADFORD, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, Bethesda, v. 72, n. 1, p. 248-254, 1976. DOI: 10.1016/0003-2697(76)90527-3

CALATAYUD, Á.; GORBE, E.; ROCA, D.; MARTÍNEZ, P. F. Effect of two nutrient solution temperatures on nitrate uptake, nitrate reductase activity, NH4+ concentration and chlorophyll a fluorescence in rose plants. Environmental and Experimental Botany, Barcelona, v. 64, n. 1, p. 65-74, 2008. DOI: 10.1016/j.envexpbot.2008.02.003

CHINNUSAMY, V.; ZHU, J.; ZHU, J. K. Cold stress regulation of gene expression in plants. Trends in Plant Science, Massachusetts, v. 12, n. 10, p. 444-451, 2007. DOI: 10.1016/j.tplants.2007.07.002

DAT, J.; VANDENABEELE, S.; VRANOVÁ, E.; VAN MONTAGU, M.; INZÉ, D.; VAN BREUSEGEM, F. Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences, Freiburg, v. 57, n. 5, p. 779-795, 2000.

ENNAHLI, S.; EARL, H. J. Physiological limitations to photosynthetic carbon assimilation in cotton under water stress. Crop Science, Washington, v. 45, n. 6, p. 2374-2382, 2005.

FILGUEIRA, F. A. R. Novo manual de olericultura: agrotecnologia moderna na produção e comercialização de hortaliças. 2. ed. Viçosa, MG: UFV, 2008. 421 p.

FLOWERS, M. D.; FISCUS, E. L.; BURKEY, K. O.; BOOKER, F. L.; DUBOIS, J. J. B. Photosynthesis, chlorophyll fluorescence, and yield of snap bean (Phaseolus vulgaris L.) genotypes differing in sensitivity to ozone. Environmental and Experimental Botany, Barcelona, v. 61, n. 2, p. 190-198, 2008.

GUYE, M. G.; VIGH, L.; WILSON, J. M. Recovery after chilling: an assessment of chill-tolerance in Phaseolus spp. Journal of Experimental Botany, Colchester, v. 38, n. 4, p. 691-701, 1987. DOI:10.1093/jxb/38.4.691

HUANG, M.; GUO, Z. Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity. Biologia Plantarum, Prague, v. 49, n. 1, p. 81-84, 2005.

JOHANSEN, D. A. Plant microtechnique. New York: Mc Graw- Hill Book Company, 1940. 523 p.

KOTAK, S.; LARKINDALE, J.; LEE, U.; VON KOSKULL-DÖRING, P.; VIERLING, E.; SCHARF, K. D. Complexity of the heat stress response in plants. Current Opinion in Plant Biology, London, v. 10, n. 3, p. 310-316, 2007. DOI: 10.1016/j.pbi.2007.04.011

KRAUSE, G. H.; WEIS, E. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Biology, Berkeley, v. 42, n. 1, p. 313-349, 1991.

LUO, Q. Temperature thresholds and crop production: a review. Climatic Change, Princenton, v. 109, n. 3-4, p. 583-598, 2011. DOI 10.1007/s10584-011-0028-6

MANETTI FILHO, J.; OLIVEIRA, C. M. G.; CARAMORI, P. H.; NAGASHIMA, G. T.; HERNANDEZ, F. B. T. Cold tolerance of forage plant species. Semina: Ciências Agrárias, Londrina, v. 39, n. 4, p. 1469-1476, 2018. DOI: 10.5433/1679-0359.2018v39n4p1469

MASSACCI, A.; NABIEV, S. M.; PIETROSANTI, L.; NEMATOV, S. K.; CHERNIKOVA, T. N.; THOR, K.; LEIPNER, J. Response of the photosynthetic apparatus of cotton (Gossypium hirsutum) to the onset of drought stress under field conditions studied by gas-exchange analysis and chlorophyll fluorescence imaging. Plant Physiology and Biochemistry, Bari, v. 46, n. 2, p. 189-195, 2008. DOI:10.1016/j.plaphy.2007.10.006

McCONNELL, D. B.; SHEEHAN, T. J. Anatomical aspects of chilling injury to leaves of Phalaenopsis. HortScience, Baton Rouge, v. 13, n. 1, p. 705-706, 1978.

MITTLER, R. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, Massachusetts, v. 7, n. 9, p. 405-410, 2002. DOI: 10.1016/S1360-1385(02)02312-9

MOSHTAGHI, E. A.; SHAHSAVAR, A. R.; TASLIMPOUR, M. R. Ionic leakage as indicators of cold hardiness in olive (Olea europaea L.). World Applied Sciences Journal, Babol, v. 7, n. 10, p. 1308-1310, 2009.

NAUMANN, J. C.; YOUNG, D. R.; ANDERSON, J. E. Leaf chlorophyll fluorescence, reflectance, and physiological response to fresh water and salt water flooding in the evergreen shrub, Myrica Cerifera. Environment Experimental Botany, Barcelona, v. 63, n. 1-3, p. 402-409, 2008. DOI:10.1016/j.envexpbot.2007.12.008

NIR, G.; SHULMAN, Y.; FANBERSTEIN, L.; LAVEE, S. Changes in the activity of catalase (EC. 1.11.1.6) in relation to the dormancy of grapevine (Vitis vinifera L.). Plant Physiology, Glasgow, v. 81, n. 4, p. 1140-1142, 1986. DOI: 10.1104/pp.81.4.1140

O’BRIEN, T. P.; FEDER, N.; MCCULLY, M. E. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma, Verlag, v. 59, n. 2, p. 368-373, 1964.

PEISKER, M.; TICHÁ, I. Effects of chilling on CO2 Gas Exchange in two cultivars of Phaseolus vulgaris L. Journal of Plant Physiology, New York, v. 138, n. 1, p. 12-16, 1991. DOI: 10.1016/S0176-1617(11)80722-4

PEIXOTO, P. H. P.; CAMBRAIA, J.; SANT'ANNA, R.; MOSQUIM, P. R.; MOREIRA, M. A. Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal, Campinas, v. 11, n. 3, p. 137-143, 1999.

PEÑA-VALDIVIA, C. B.; LAGUNES E, L. del C.; PERALES R, H. R. Chilling effects on leaf photosynthesis and seed yields of Phaseolus vulgaris. Canadian Journal of Botany, Soskatchewan, v. 72, n. 1, p. 1403-1411, 1994. DOI: 10.1139/b94-173

PERCIVAL, G. C.; FRASER, G. A.; OXENHAM, G. Foliar salt tolerance of Acer genotypes using chlorophyll fluorescence. Journal of Arboriculture, Urbana, v. 29, n. 2, p. 61-65, 2003.

RAPACZ, M.; GA?SIOR, D.; KOS´CIELNIAK, J.; KOSMALA, A.; ZWIERZYKOWSKI, Z.; HUMPHREYS, M. W. The role of the photosynthetic apparatus in cold acclimation of Lolium multiflorum: characteristics of novel genotypes low-sensitive to PSII over-reduction. Acta Physiologiae Plantarum, Pozna?, v. 29, n. 4, p. 309-316, 2007.

SANGHERA, G. S.; WANI, S. H.; HUSSAIN, W.; SINGH, N. B. Engineering cold stress tolerance in crop plants. Current Genomics, Bentham, v. 12, n. 1, p. 30-43, 2011. DOI: 10.2174/138920211794520178

SIEGEL, V.; JONGENS, T. A.; JAN, L. Y.; JAN, Y. N. Pipsqueak, an early acting member of the posterior group of genes, affects vasa level and germ cell-somatic cell interaction in the developing egg chamber. Development, London, v. 119, n. 4, p. 1187-1202, 1993.

SILVA, A. L. L. da; OLIVEIRA, Y. de; ALCANTARA, G. B. de; SANTOS, M. dos; QUOIRIN, M. Tolerância ao resfriamento e congelamento de folhas de eucalipto. Biociências, Porto Alegre, v. 17, n. 1, p. 86-90, 2009.

STIRBET, A.; GOVINDJEE. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology, Debrecen, v. 104, n. 2, p. 236-257, 2011. DOI:10.1016/j.jphotobiol.2010.12.010

TAIZ, L.; ZEIGER, E. Fisiologia vegetal. 6. ed. Porto Alegre: Artmed, 2017. 858 p.

TSENG, M. J.; LI, P. H. Changes in protein synthesis and translatable messenger RNA populations associated with ABA induced cold hardiness in potato (Solanum commersonii). Physiologia Plantarum, Umeå, v. 81, n. 3, p. 349-358, 1991. DOI: 10.1111/j.1399-3054.1991.tb08743.x

YUSUF, M. A.; KUMAR, D.; RAJWANSHI, R.; STRASSER, R. J.; TSIMILLI-MICHAEL, M.; GOVINDJEE; SARIN, N. B. Overexpression of y-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Amsterdam, v. 1797, n. 8, p. 1428-1438, 2010. DOI: 10.1016/j.bbabio.2010.02.002

ZABOT, L.; DUTRA, L. M. C.; JAUER, A.; LUCCA FILHO, O. A.; UHRY, D.; STEFANELO, C.; LOSEKAN, M. E.; FARIAS, J. R.; LUDWIG, M. P. Análise de crescimento da cultivar de feijão BR IPAGRO 44 Guapo Brilhante cultivada na safrinha, em quatro densidades de semeadura em Santa Maria - RS. Revista de Ciências Agroveterinárias, Lages, v. 3, n. 2, p. 105-115, 2004.




DOI: http://dx.doi.org/10.5433/1679-0359.2019v40n3p1011

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional