Selenium-induced oxidative stress in coffee cell suspension cultures
Rui A. Gomes-Junior A , Priscila L. Gratão B , Salete A. Gaziola B , Paulo Mazzafera C , Peter J. Lea D and Ricardo A. Azevedo B EA Centro de Estudos Superiores de Balsas, Universidade Estadual do Maranhão, 65800-000, Balsas, MA, Brazil.
B Departamento de Genética, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo, 13 418-900 Piracicaba, SP, Brazil.
C Departamento de Fisiologia Vegetal, Instituto de Biologia, CP 6109, Universidade Estadual de Campinas, 13 083-970 Campinas, SP, Brazil.
D Department of Biological Sciences, University of Lancaster, Lancaster, LA1 4YQ, UK.
E Corresponding author. Email: raazeved@esalq.usp.br
Functional Plant Biology 34(5) 449-456 https://doi.org/10.1071/FP07010
Submitted: 17 January 2007 Accepted: 28 March 2007 Published: 17 May 2007
Abstract
Selenium (Se) is an essential element for humans and animals that is required for key antioxidant reactions, but can be toxic at high concentrations. We have investigated the effect of Se in the form of selenite on coffee cell suspension cultures over a 12-day period. The antioxidant defence systems were induced in coffee cells grown in the presence of 0.05 and 0.5 mm sodium selenite (Na2SeO3). Lipid peroxidation and alterations in antioxidant enzymes were the main responses observed, including a severe reduction in ascorbate peroxidase activity, even at 0.05 mm sodium selenite. Ten superoxide dismutase (SOD) isoenzymes were detected and the two major Mn-SOD isoenzymes (bands V and VI) responded more to 0.05 mm selenite. SOD band V exhibited a general decrease in activity after 12 h of treatment with 0.05 mm selenite, whereas band VI exhibited the opposite behavior and increased in activity. An extra isoenzyme of glutathione reductase (GR) was induced in the presence of selenite, which confirmed our previous results obtained with Cd and Ni indicating that this GR isoenzyme may have the potential to be a marker for oxidative stress in coffee.
Additional keywords: Coffea arabica, glutathione reductase, oxidative stress, selenium, superoxide dismutase.
Acknowledgements
This work was financed by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Grant no. 04/08444-6) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brazil, Grants no. 471814/2003-2 and 452944/2006-6). The authors also thank Dr Virgilio Nascimento Filho for technical support. RAA and PM thank CNPq for the researches fellowships.
Agalou A,
Spaink HP, Roussis A
(2006) Novel interaction of selenium-binding protein with glyceraldehyde-3-phosphate dehydrogenase and fructose-bisphosphate aldolase of Arabidopsis thaliana. Functional Plant Biology 33, 847–856.
| Crossref | GoogleScholarGoogle Scholar |
Anza M,
Riga P, Garbisu C
(2005) Time course of antioxidant responses of Capsicum annuum subjected to a progressive magnesium deficiency. Annals of Applied Biology 146, 123–134.
| Crossref | GoogleScholarGoogle Scholar |
Azevedo JA, Azevedo RA
(2006) Heavy metals and oxidative stress: where do we go from here? Communications in Biometry and Crop Science 1, 135–138.
Azevedo RA,
Alas RM,
Smith RJ, Lea PJ
(1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiologia Plantarum 104, 280–292.
| Crossref | GoogleScholarGoogle Scholar |
Bartoli CG,
Gomez F,
Martinez DE, Guianet JJ
(2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). Journal of Experimental Botany 55, 1663–1669.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bradford MM
(1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brown TA, Shrift A
(1982) Selenium: toxicity and tolerance in higher plants. Biological Reviews of the Cambridge Philosophical Society 57, 59–84.
Cançado GMA,
De Rosa VE,
Fernandez JH,
Maron LG,
Jorge RA, Menossi M
(2005) Glutathione S-transferase and aluminum toxicity in maize. Functional Plant Biology 32, 1045–1055.
| Crossref | GoogleScholarGoogle Scholar |
Carlson CL,
Adriano DC, Dixon PM
(1991) Effects of soil-applied selenium on the growth and selenium content of a forage species. Journal of Environmental Quality 20, 363–368.
Cartes P,
Gianfreda L, Mora ML
(2005) Uptake of selenium and its antioxidant activity in ryegrass when applied as selenate and selenite forms. Plant and Soil 276, 359–367.
| Crossref | GoogleScholarGoogle Scholar |
Cartes P,
Shene C, Mora MD
(2006) Selenium distribution in ryegrass and its antioxidant role as affected by sulfur fertilization. Plant and Soil 285, 187–195.
| Crossref | GoogleScholarGoogle Scholar |
di Toppi LS,
Marabottini R,
Vattuone Z,
Musetti R,
Favali MA,
Sorgona A, Badiani M
(2005) Cell wall immobilisation and antioxidant status of Xanthoria parietina thalli exposed to cadmium. Functional Plant Biology 32, 611–618.
| Crossref | GoogleScholarGoogle Scholar |
Djanaguiraman M,
Devi D,
Shanker AK,
Sheeba JA, Bangarusamy U
(2005) Selenium – an antioxidative protectant in soybean during senescence. Plant and Soil 272, 77–86.
| Crossref | GoogleScholarGoogle Scholar |
Fecht-Christoffers MM,
Fuhrs H,
Braun H-P, Horst WJ
(2006) The role of hydrogen peroxide-producing and hydrogen peroxide-consuming peroxidases in the leaf apoplast of cowpea in manganese tolerance. Plant Physiology 140, 1451–1463.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Foyer CH, Noctor G
(2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. The Plant Cell 17, 1866–1875.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Freeman JL,
Zhang LH,
Marcus MA,
Fakra S,
McGrath SP, Pilon-Smits EAH
(2006) Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiology 142, 124–134.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gajewska E, Sklodowska M
(2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20, 27–36.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Garcia JS,
Gratão PL,
Azevedo RA, Arruda MAZ
(2006) Metal contamination effects on sunflower (Helianthus annuus L.) growth and protein expression in leaves during development. Journal of Agricultural and Food Chemistry 54, 8623–8630.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gomes-Junior RA,
Moldes CA,
Delite FS,
Gratão PL,
Mazzafera P,
Lea PJ, Azevedo RA
(2006a) Nickel elicits a fast antioxidant response in Coffea arabica cells. Plant Physiology and Biochemistry 44, 420–429.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gomes-Junior RA,
Moldes CA,
Delite FS,
Pompeu GB,
Gratão PL,
Mazzafera P,
Lea PJ, Azevedo RA
(2006b) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65, 1330–1337.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gratão PL,
Polle A,
Lea PJ, Azevedo RA
(2005) Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology 32, 481–494.
| Crossref | GoogleScholarGoogle Scholar |
Groppa MD,
Ianuzzo MP,
Tomaro ML, Benavides MP
(2007) Polyamine metabolism in sunflower plants under long-term cadmium or copper stress. Amino Acids 32, 265–275.
| Crossref | GoogleScholarGoogle Scholar |
Hartikainen H
(2005) Biogeochemistry of selenium and its impact on food chain quality and human health. Journal of Trace Elements in Medicine and Biology 18, 309–318.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hartikainen H,
Ekholm P,
Piironen V,
Xue TL,
Koivu T, Tli-Halla M
(1997) Quality of the ryegrass and lettuce yields as affected by selenium fertilization. Agricultural and Food Science in Finland 6, 381–387.
Hartikainen H,
Xue TL, Piironen V
(2000) Selenium as an anti-oxidant and pro-oxidant in ryegrass. Plant and Soil 225, 193–200.
| Crossref | GoogleScholarGoogle Scholar |
Hassan IA
(2006) Physiological and biochemical response of potato (Solanum tuberosum L. cv. Kara) to O-3 and antioxidant chemicals: possible roles of antioxidant enzymes. Annals of Applied Biology 148, 197–206.
| Crossref | GoogleScholarGoogle Scholar |
Hatfield DL,
Carlson BA,
Xu XM,
Mix H, Gladyshev VN
(2006) Selenocysteine incorporation machinery and the role of selenoproteins in development and health. Progress in Nucleic Acid Research and Molecular Biology 81, 97–142.
| Crossref |
PubMed |
Igamberdiev AU, Lea PJ
(2002) The role of peroxisomes in the integration of metabolism and evolutionary diversity of photosynthetic organism. Phytochemistry 60, 651–674.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
King BJ,
Siddiqi MY,
Ruth TJ,
Warner RL, Glass ADM
(1993) Feedback regulation of nitrate influx in barley roots by nitrate, nitrite, and ammonium. Plant Physiology 102, 1279–1286.
| PubMed |
Lea PJ, Azevedo RA
(2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Annals of Applied Biology 149, 243–247.
| Crossref | GoogleScholarGoogle Scholar |
LeDuc DL,
AbdelSamie M,
Montes-Bayon M,
Wu CP,
Reisinger SJ, Terry N
(2006) Overexpressing both ATP sulfurylase and selenocysteine methyltransferase enhances selenium phytoremediation traits in Indian mustard. Environmental Pollution (Barking, Essex : 1987) 144, 70–76.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
LeDuc DL, Terry N
(2005) Phytoremediation of toxic elements in soil and water. Journal of Industrial Microbiology & Biotechnology 32, 514–520.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lynch JM, Moffat AJ
(2005) Bioremediation – prospects for the future application of innovative applied biological research. Annals of Applied Biology 146, 217–221.
| Crossref | GoogleScholarGoogle Scholar |
Mazzafera P
(1998) Growth and biochemical alterations in coffee due to selenite toxicity. Plant and Soil 201, 189–196.
| Crossref | GoogleScholarGoogle Scholar |
Meija J,
Bryson JM,
Vonderheide AP,
Montes-Bayon M, Caruso JA
(2003) Studies of selenium-containing volatiles in roasted coffee. Journal of Agricultural and Food Chemistry 51, 5116–5122.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neuenschwander B, Baumann TW
(1992) A novel type of somatic embryogenesis in Coffea arabica. Plant Cell Reports 10, 608–612.
| Crossref | GoogleScholarGoogle Scholar |
Nowak J,
Kaklewski K, Ligocki M
(2004) Influence of selenium on oxidoreductive enzymes activity in soil and in plants. Soil Biology & Biochemistry 36, 1553–1558.
| Crossref | GoogleScholarGoogle Scholar |
Praxedes SC,
DaMatta FM,
Loureiro ME,
Ferrao MAG, Cordeiro AT
(2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environmental and Experimental Botany 56, 263–273.
| Crossref | GoogleScholarGoogle Scholar |
Ronchi CP,
DaMatta FM,
Batista KD,
Moraes GABK,
Loureiro ME, Ducatti C
(2006) Growth and photosynthetic down-regulation in Coffea arabica in response to restricted root volume. Functional Plant Biology 33, 1013–1023.
| Crossref | GoogleScholarGoogle Scholar |
Saeidi-Sar S,
Khavari-Nejad RA,
Fahimi H,
Ghorbanli M, Majd A
(2007) Interactive effects of gibberellin A(3) and ascorbic acid on lipid peroxidation and antioxidant enzyme activities in Glycine max seedlings under nickel stress. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 54, 74–79.
| Crossref | GoogleScholarGoogle Scholar |
Santosh TR,
Sreekala M, Lalitha K
(1999) Oxidative stress during selenium deficiency in seedlings of Trigonella foenum-graecum and mitigation by mimosine – Part II. Glutathione metabolism. Biological Trace Element Research 70, 209–222.
| PubMed |
Seppänen M,
Turakainen M, Hartikainen H
(2003) Selenium effects on oxidative stress in potato. Plant Science 165, 311–319.
| Crossref | GoogleScholarGoogle Scholar |
Sreekala M,
Santosh TR, Lalitha K
(1999) Oxidative stress during selenium deficiency in seedlings of Trigonella foenum-graecum and mitigation by mimosine – Part I. Hydroperoxide metabolism. Biological Trace Element Research 70, 193–207.
| PubMed |
Van Hoewyk D,
Garifullina GF,
Ackley AR,
Abdel-Ghany SE, Marcus MA , et al.
(2005) Overexpression of AtCpNifS enhances selenium tolerance and accumulation in Arabidopsis. Plant Physiology 139, 1518–1528.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Van-Huysen T,
Terry N, Pilon-Smits EAH
(2004) Exploring the selenium phytoremediation potential of transgenic Indian mustard overexpressing ATP sulfurylase or cystathionine-γ-synthase. International Journal of Phytoremediation 6, 111–118.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vitória AP,
Lea PJ, Azevedo RA
(2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57, 701–710.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
White PJ,
Bowen HC,
Parmaguru P,
Fritz M, Spracklen WP , et al.
(2004) Interactions between selenium and sulphur nutrition in Arabidopsis thaliana. Journal of Experimental Botany 55, 1927–1937.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xue TL,
Hartikainen H, Piironen V
(2001) Antioxidative and growth-promoting effect of selenium on senescing lettuce. Plant and Soil 237, 55–61.
| Crossref | GoogleScholarGoogle Scholar |
Zhang L,
Ackley AR, Pilon-Smits EAH
(2007) Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. Journal of Plant Physiology 164, 327–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zoller T,
Skroppa T,
Johnsen O, Polle A
(2003) Apoplastic peroxidases in needles of Norway spruce (Picea abies) progenies from different crossing environments. Forstwissenschaftliches Centralblatt 122, 153–159.
| Crossref | GoogleScholarGoogle Scholar |
