Cadmium (Cd) disrupts the normal growth and development of plants, depending on their tolerance to this toxic element. The present study was focused on the impacts of exogenous salicylic acid (SA) on the response and regulation of the antioxidant defense system and membrane lipids to 16-day-old flax plantlets under Cd stress. Exposure of flax to high Cd concentrations led to strong inhibition of root growth and enhanced lipid peroxides, membrane permeability, protein oxidation, and hydrogen peroxide (H2O2) production to varying degrees. Concomitantly, activities of the antioxidant enzymes catalase (CAT, EC 1.11.1.6), guaïcol peroxydase (GPX, EC 1.11.1.7), ascorbate peroxydase (APX, EC 1.11.1.11), and superoxide dismutase (SOD, EC 1.15.1.1), and the total antioxidant capacities (2,2’-diphenyl-1-picrylhydrazyl (DPPH) scavenging activity and ferric reducing antioxidant power (FRAP)) were significantly altered by Cd. In contrast, exogenous SA greatly reduced the toxic effects of Cd on the root growth, antioxidant system, and membrane lipid content. The Cd-treated plantlets pre-soaked with SA exhibited less lipid and protein oxidation and membrane alteration, as well as a high level of total antioxidant capacities and increased activities of antioxidant enzymes except of CAT. These results may suggest that SA plays an important role in triggering the root antioxidant system, thereby preventing membrane damage as well as the denaturation of its components.
Get full access to this article
View all access options for this article.
References
1.
AebyH. 1984. Catalase in vitro. Meth Enzymol, 105:121–126.
2.
AnanievaEA, ChristovKN, PopovaLP. 2004. Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. J Plant Physiol, 161:319–328.
3.
ApelK, HirtH. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol, 55:373–399.
4.
BalestrasseKB, GardeyL, GallegoSM, TomaroML. 2001. Response of antioxidant defense system in soybean nodules and roots subjected to cadmium stress. Aust J Plant Physiol, 28:497–504.
5.
BeauchampC, FridovichI. 1971. Superoxide dismutase, improved assays and an assay applicable to acrylamide gels. Anal Biochem, 44:276–287.
6.
BelkhadiA, HedijiH, AbbesZet al.2010. Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotox Environ Safe, 73:1004–1011.
7.
Ben YoussefN, NouairiI, Ben TemimeSet al.2005. Cadmium effects on lipid metabolism of rape (Brassica napus L.)C R Biol, 328:745–757.
8.
BenzieIFF, StrainJJ. 1996. The ferric reducing ability of plasma (FRAP) as a measure of ''antioxidant power'': The FRAP assay. Anal Biochem, 239:70–76.
9.
BradfordMM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem, 72:248–254.
10.
Brand-WilliamsW, CuveleirME, BersetC. 1995. Use of a free radical method to evaluate antioxidant activity. Lebensmittel-Wissenschaft und -Technologie, 28:25–30.
ÇagS, CevahirözG, SarsagM, Gören-SaglamN. 2009. Effect of salicylic acid on pigment, protein content and peroxides activity in excised sunflower cotyledons. Pak J Bot, 41:2297–2303.
13.
ChenZ, SilvaH, KlessingDF. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science, 262:1883–1886.
14.
ChoiSM, SongHR, HanSKet al.2012. HDA19 is required for the repression of salicylic acid biosynthesis and salicylic acid-mediated defense responses in Arabidopsis. Plant J, 71:135–146.
15.
ChoudhuryS, PandaSK. 2004. Role of salicylic acid in regulating cadmium induced oxidative stress in Oryza sativa L. roots. Bulg J Plant Physiol, 30:95–110.
16.
ConrathU, ChenZ, RiciglianoJR, KlessigDF. 1995. Two inducers of plant defense responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc Natl Acad Sci USA, 92:7143–7147.
17.
DjebaliW, ZarroukM, BrouquisseR, El KahouiS, LimamF, GhorbelMH, ChaïbiW. 2005. Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol, 7:258–368.
18.
DjebaliW, GallusciP, PolgeCet al.2008. Modifications in endopeptidase and 20S proteasome expression and activities in cadmium treated tomato (Solanum lycopersicum L.) plants. Planta, 227:625–639.
19.
DouchicheO, Soret-MorvanO, ChaïbiW, MorvanC, PaynelF. 2010. Characteristics of cadmium tolerance in 'Hermes' flax seedlings: Contribution of cell walls. Chemosphere, 81:1430–1436.
20.
DrazicG, MihailovicN. 2005. Modification of cadmium toxicity in soybean seedlings by salicylic acid. Plant Physiol, 168:511–517.
21.
DurrantWE, DongX. 2004. Systemic acquired resistance. Annu Rev Phytopath, 42:185–209.
22.
FerreresF, SousaC, ValentaoP, SeabraRM, PereiraJA, AndradePB. 2007. Tronchuda cabbage (Brassica oleracea L. var. costata DC) seeds: Phytochemical characterization and antioxidant potential. Food Chem, 101:549–558.
23.
FobertPR, DespresC. 2005. Redox control of systemic acquired resistance. Curr Opin Plant Biol, 8:378–382.
24.
FoyerCH, NoctorG. 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell, 17:1866–1875.
25.
GallegoSM, PenaLB, BarciaRAet al.2012. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ Exp Bot, 83:33–46.
26.
GarcésR, ManchaM. 1993. One-step lipid extraction and fatty acid methyl esters preparation from fresh plant tissues. Anal Biochem, 211:139–143.
27.
GichnerT, PatkovaZ, SzakovaJ, DemnerovaK. 2004. Cadmium induces DNA damages in tobacco roots, but no DNA damage, somatic mutations orhomologous recombinations in tobacco leaves. Mutat Res Genet Toxicol Environ Mut, 559:49–57.
28.
GonçalvesJF, TabaldiLA, CargneluttiDet al.2009. Cadmium-induced oxidative stress in two potato cultivars. Biometals, 22:779–792.
29.
GratãoPL, PolleA, LeaPJ, AzevedoRA. 2005. Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol, 32:481–494.
30.
GratãoPL, MonteiroCC, CarvalhoRFet al.2012. Biochemical dissection of diageotropica and Never ripe tomato mutants to Cd stressful conditions. Plant Physiol Biochem, 56:79–96.
31.
GuoT, ZhangG, ZhouM, WuF, ChenJ. 2004. Effect of aluminium and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil, 258:241–248.
32.
GuoB, LiangYC, ZhuYG, ZhaoFJ. 2007. Role of salicylic acid in alleviating oxidative damage in rice roots (Oryza sativa) subjected to cadmium stress. Environ Pollut, 147:743–749.
33.
HanzelJR, WilliamsEE. 1990. The role of alteration in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res, 29:167–227.
34.
HaoL, ZhaoY, JinDDet al.2012. Salicylic acid-altering Arabidopsis mutants response to salt stress. Plant Soil, 354:81–95.
35.
HassanMJ, ZhangG, ZhuZ. 2008. Influence of cadmium toxicity on plant growth and nitrogen uptake in rice as affected by nitrogen form. J Plant Nutr, 31:251–262.
36.
HayatS, HasanSA, FariduddinQ, AhmadA. 2008. Growth of tomato (Lycopersicon esculentum) in response to salicylic acid under water stress. J Plant Int, 3:297–304.
37.
HédijiH, DjebaliW, CabassonCet al.2010. Effects of long-term cadmium exposure on growth and metabolomic profile of tomato plants. Ecotox Environ Safe, 73:1965–1974.
38.
HendryGAF, BakerAJM, EwartCF. 1992. Cadmium tolerance and toxicity, oxygen radical processes and molecular damages in Cd tolerant and Cd sensitive clones of Holcus lanatus. Acta Bot Neert, 40:271–281.
39.
HernándezLE, CookeDT. 1997. Modifications of the root plasma membrane lipid composition of cadmium-treated Pisum sativum. J Exp Bot, 48:1375–1381.
40.
HorváthDM, HuangDJ, ChuaNH. 1998. Four classes of salicylate-induced tobacco genes. Mol Plant Micro Inter, 11:895–905.
41.
HsuYT, KaoCH. 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul, 42:227–238.
42.
JandaT, SzalaiG, TariI, PáldiE. 1999. Hydroponic treatment with salicylic acid decreases the effect of chilling injury in maize (Zea mays L.) plants. Planta, 208:175–180.
43.
JandaT, SzalaiG, Rios-GonzalezK, VeiszO, PáldiE. 2003. Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci, 164:301–306.
44.
KatochR. 2007. Induction of apathogenesis-related protein in pea after treatment with inducers or inoculation with Erysiphe polygoni. J Veg Sci, 12:15–25.
45.
KhanNA, SamiullahSS, NazarR. 2007. Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. J Agron Crop Sci, 193:435–444.
46.
KrantevA, YordanovaR, JandaT, SzalaiG, PopovaL. 2008. Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol, 165:920–931.
47.
LandbergT, GregerM. 2002. Differences in oxidative stress in heavy metal resistant and sensitive clones of Salix viminalis. J Plant Physiol, 159:69–75.
48.
LiuXL, ZhangSZ, ShanXQ, ChristieP. 2007. Combined toxicity of cadmium and arsenate to wheat seedlings and plant uptake and antioxidative enzyme responses to cadmium and arsenate co-contamination. Ecotox Environ Safe, 68:305–313.
49.
LiuKL, ShenL, WangJQ, ShengJP. 2008. Rapid inactivation of chloroplastic ascorbate peroxidase is responsible for oxidative modification to rubisco in tomato (Lycopersicon esculentum) under cadmium stress. J Integrat Plant Biol, 50:415–426.
50.
MetwallyA, FinkemeierI, GeorgiM, DietzKJ. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol, 132:272–281.
51.
MishraS, SrivastavaS, TripathiRD, KumarR, SethCS, GuptaDK. 2006. Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere, 65:1027–1039.
52.
MobinM, KhanNA. 2007. Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol, 164:601–610.
53.
NakanoY, AsadaK. 1981. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. Plant Cell Physiol, 22:676–690.
54.
O'KaneD, GillV, BoydP, BurdonR. 1996. Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta, 198:371–377.
55.
Ortega-VillasanteC, HernandezLE, Rellan-AlvarezR, Del CampoFF, Carpena-RuizRO. 2007. Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol, 176:96–107.
56.
PandaSK, PatraHK. 2007. Effect of salicylic acid potentiates cadmium-induced oxidative damage in Oryza sativa L. Leaves. Acta Physiol Plant, 29:567–575.
57.
PopovaLP, MaslenkovaLT, YordanovaRY, IvanovaAP, KrantevAP, SzalaiG, JandaT. 2009. Exogenous treatment with salicylic acid attenuates cadmium toxicity in pea seedlings. Plant Physiol Biochem, 47:224–231.
58.
RadwanDEM. 2012. Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays L.) leaves. Pest Biochem Physiol, 102:182–188.
59.
ReznickAZ, PackerL. 1994. Oxidative damage to protein: Spectrophotometric method for carbonyl assay. Methods Enzymol, 233:357–363.
60.
Rodriguez-SerranoM, Romero-PuertasMC, PazminoDMet al.2009. Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol, 150:229–243.
61.
Romero-PuertasMC, PalmaJM, GomezM, Del RíoLA, SandalioLM. 2002. Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ, 25:677–686.
62.
Sánchez-CasasP, KlessigDF. 1994. A salicylic acid-binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol, 106:1675–1679.
63.
SaruhanN, SaglamA, KadiogluA. 2012. Salicylic acid pretreatment induces drought tolerance and delays leaf rolling by inducing antioxidant systems in maize genotypes. Acta Physiol Plant, 34:97–106.
64.
SchützendübelA, PolleA. 2002. Plant responses to abiotic stresses: Heavy metal induced oxidative stress and protection by mycorrhization. J Exp Bot, 53:1351–1365.
65.
ShiGR, CaiQS, LiuQQ, WuL. 2009. Salicylic acid-mediated alleviation of cadmium toxicity in hemp plants in relation to cadmium uptake, photosynthesis and antioxidant enzymes. Acta Physiol Plant, 31:969–977.
66.
SinghS, KhanNA, NazarR, AnjumNA. 2008. Photosynthetic traits and activities of antioxidant enzymes in blackgram (Vigna mungo L. Hepper) under cadmium stress. Am J Plant Physiol, 3:25–32.
67.
SmeetsK, RuytnxJ, SemaneBet al.2008. Cadmium induced transcriptional and enzymatic alterations related to oxidative stress. Environ Exp Bot, 63:1–8.
68.
TamásL, DurcekovaK, HaluskovaL, HuttovaJ, MistrikI, OlleM. 2007. Rhizosphere localized cationic peroxidase from barley roots is strongly activated by cadmium and correlated with root growth inhibition. Chemosphere, 66:1292–1300.
ZhangF, ZhangH, XiaY, WangG, XuL, ShenZ. 2011. Exogenous application of salicylic acid alleviates cadmium toxicity and reduces hydrogen peroxide accumulation in root apoplasts of Phaseolus aureus and Vicia sativa. Plant Cell Rep, 30:1475–1483.
72.
ZhangWN, ChenWL. 2011. Role of salicylic acid in alleviating photochemical damage and autophagic cell death induction of cadmium stress in Arabidopsis thaliana. Photochem Photobiol Sci, 10:947–955.
