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The effect of hydro and proline seed priming on growth, proline and sugar content, and antioxidant activity of maize under cadmium stress

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Abstract

We tested the effect of seed hydro- and proline-priming on cadmium (Cd) tolerance in maize plants. Soil supplemented with two concentrations of cadmium was used for the investigation. Cadmium content, fresh and dry mass, shoot length, leaf length and width, chlorophyll, proline, sugar and protein content, and antioxidant potential in 4-week-old plants were analysed. Cadmium content in soil and maize shoots was determined by flame atomic absorption spectrometry. Accumulation of Cd was observed for all plants, and highest Cd concentration was recorded in seedlings grown from proline-primed seeds with no visual signs of Cd toxicity. In proline-primed plants, increase in leaf length, photosynthetic pigments, and sugar and proline content as well as changes in antioxidant enzyme activities was recorded. Results obtained in this study suggest that proline-priming of maize seeds induces activation of defensive mechanisms, such as proline and sugar synthesis, which in return alleviates Cd toxicity on maize growth with increased Cd accumulation comparing to control plants.

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Abbreviations

APX:

Ascorbate peroxidases

CAT:

Catalases

Car:

Carotenoids

Cd:

Cadmium

CdCl2 :

Cadmium chloride

Chl a :

Chlorophyll a

Chl b :

Chlorophyll b

DW:

Dry weight

DPPH:

2.2-Diphenyl-1-picrylhydrazyl radical

FAAS:

Flame atomic absorption spectrometry

FW:

Fresh weight

HCl:

Hydrochloric acid

HNO3 :

Nitric acid

H2O2 :

Hydrogen peroxide

LL:

Leaf length

LW:

Leaf width

SL:

Shoot length

POD:

Guaiacol peroxidases

RN:

Root necrosis

SCF:

Shoot concentration factor

SD:

Standard deviation

TChl:

Total chlorophylls

References

  • Akinyemi AJ, Faboya OL, Olayide I, Faboya OA, Ijabadeniyi T (2017) Effect of cadmium stress on non-enzymatic antioxidant and nitric oxide levels in two varieties of maize (Zea mays). Bull Environ Contam Toxicol 98(6):845–849

    Article  CAS  Google Scholar 

  • Angelini R, Manes F, Federico R (1990) Spatial and functional correlation between diamine-oxidase and peroxidase activities and their dependence upon de-etiolation and wounding in chick-pea stems. Planta 182(1):89–96

    Article  CAS  Google Scholar 

  • Anju M, Sanskriti G, Suresh BS, Nidhi S (2015) In vitro accumulation of cadmium chloride in papaya seedling and its impact on plant protein. Int J Ayur Pharm Res 2(3):54–52

    Google Scholar 

  • Anjum SA, Tanveer M, Hussain S, Bao M, Wang L, Khan I, Ullah E, Tung SA, Samad RA, Shahzad B (2015) Cadmium toxicity in maize (Zea mays L.): consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environ. Sci Pollut Res 22(21):17022–17030

    Article  CAS  Google Scholar 

  • Armas T, Pinto AP, de Varennes A, Mourato MP, Martins LL, Gonçalves MLS, Mota AM (2015) Comparison of cadmium-induced oxidative stress in Brassica juncea in soil and hydroponic cultures. Plant Soil 388(1–2):297–305

    Article  CAS  Google Scholar 

  • Asgher M, Khan MIR, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252(2):399–413

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2005) Pre-sowing seed treatment—a shotgun approach to improve germination, plant growth, and crop yield under saline and non-saline conditions. Adv Agron 88:223–271

    Article  Google Scholar 

  • Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216

    Article  CAS  Google Scholar 

  • Balestri M, Bottega S, Spanò C (2014) Response of Pteris vittata to different cadmium treatments. Acta Physiol Plant 36(3):767–775

    Article  CAS  Google Scholar 

  • Bartkienė E (2012) Plant food analysis methods: methodical book. Lietuvos sveikatos mokslų universitetas, Kaunas

    Google Scholar 

  • Bauddh K, Singh RP (2011) Differential toxicity of cadmium to mustard (Brassica juncia L.) genotypes under higher metal levels. J Exp Bot 32(3):355–362

    CAS  Google Scholar 

  • Bavi K, Kholdebarin B, Moradshahi A (2011) Effect of cadmium on growth, protein content and peroxidase activity in pea plants. Pak J Bot 43(3):1467–1470

    CAS  Google Scholar 

  • Beckers GJ, Conrath U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10(4):425–431

    Article  Google Scholar 

  • Ben Ahmed C, Ben Rouina B, Sensoy S, Boukhriss M, Ben Abdullah F (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58(7):4216–4222

    Article  CAS  Google Scholar 

  • Borges KLR, Salvato F, Alcântara BK, Nalin RS, Piotto FÂ, Azevedo RA (2018) Temporal dynamic responses of roots in contrasting tomato genotypes to cadmium tolerance. Ecotoxicology 27(3):245–258

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254

    Article  CAS  Google Scholar 

  • Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35:412–426

    Article  CAS  Google Scholar 

  • Carvalho RF, Piotto FA, Schmidt D, Peters LP, Monteiro CC, Azevedo RA (2011) Seed priming with hormones does not alleviate induced oxidative stress in maize seedlings subjected to salt stress. Sci Agric 68(5):598–602

    Article  CAS  Google Scholar 

  • Charest C, Ton Phan C (1990) Cold acclimation of wheat (Triticum aestivum): properties of enzymes involved in proline metabolism. Physiol Plant 80(2):159–168

    Article  CAS  Google Scholar 

  • Chen H, Wang A (2009) Adsorption characteristics of Cu (II) from aqueous solution onto poly (acrylamide)/attapulgite composite. J Hazard Mater 165(1):223–231

    Article  CAS  Google Scholar 

  • Đogić S, Džubur N, Karalija E, Parić A (2017) Biochemical responses of basil to aluminium and cadmium stresses. Acta Agriculturae Serbica 22(43):57–651

    Article  Google Scholar 

  • Foti R, Abureni K, Tigere A, Gotosa J, Gere J (2008) The efficacy of different seed priming osmotica on the establishment of maize (Zea mays L.) caryopses. J Arid Environ 72(6):1127–1130

    Article  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  CAS  Google Scholar 

  • Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42(2):249–257

    Article  CAS  Google Scholar 

  • Gadapati WR, Macfie SM (2006) Phytochelatins are only partially correlated with Cd-stress in two species of Brassica. Plant Sci 170(3):471–480

    Article  CAS  Google Scholar 

  • Giuliano S, Ryan MR, Véricel G, Rametti G, Perdrieux F, Justes E, Alletto L (2016) Low-input cropping systems to reduce input dependency and environmental impacts in maize production: a multi-criteria assessment. Eur J Agron 76:160–175

    Article  Google Scholar 

  • Góth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196(2–3):143–151

    Article  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Palaeontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Hanson AD (1973) The effects of imbibition drying treatments on wheat seeds. New Phytol 72(5):1063–1073

    Article  CAS  Google Scholar 

  • Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84(10):1446–1451

    Article  CAS  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466

    Article  CAS  Google Scholar 

  • Hernández LE, Cooke DT (1997) Modification of the root plasma membrane lipid composition of cadmium-treated Pisum sativum. J Exp Bot 48(7):1375–1381

    Article  Google Scholar 

  • Iqbal M, Ashraf M (2007) Seed treatment with auxins modulates growth and ion partitioning in salt-stressed wheat plants. J Integr Plant Biol 49(7):1003–1015

    Article  CAS  Google Scholar 

  • ISO 11466 (1995) Soil quality—extraction of trace elements soluble in aqua regia. International standard. Croatian Standards Institute, Zagreb

  • John R, Ahmad P, Gadgil K, Sharma S (2008) Effect of cadmium and lead on growth, biochemical parameters and uptake in Lemna polyrrhiza L. Plant Soil Environ 54(6):262–270

    Article  CAS  Google Scholar 

  • Kalra YP, Maynard DG (1997) Microwave digestion of plant tissue in an open vessel. In: Handbook of reference methods for plant analysis. CRC Press, Boca Raton, pp 75–79

    Chapter  Google Scholar 

  • Kaur S, Gupta AK, Kaur N (2002) Effect of osmo-and hydropriming of chickpea seeds on seedling growth and carbohydrate metabolism under water deficit stress. Plant Growth Regul 37(1):17–22

    Article  CAS  Google Scholar 

  • Kaya MD, Okçu G, Atak M, Çıkılı Y, Kolsarıcı Ö (2006) Seed treatments to overcome salt and drought stress during germination in sunflower (Helianthus annuus L.). Eur J Agron 24(4):291–295

    Article  CAS  Google Scholar 

  • Kučerová D, Kollárová K, Zelko I, Vatehová Z, Lišková D (2014) Galactoglucomannan oligosaccharides alleviate cadmium stress in Arabidopsis. J Plant Physiol 171(7):518–524

    Article  Google Scholar 

  • Kurtyka R, Małkowski E, Kita A, Karcz W (2008) Effect of calcium and cadmium on growth and accumulation of cadmium, calcium, potassium and sodium in maize seedlings. Pol J Environ Stud 17(1):51–56

    CAS  Google Scholar 

  • Latef AA, Tran LSP (2016) Impacts of priming with silicon on the growth and tolerance of maize plants to alkaline stress. Front Plant Sci 7:243

    Google Scholar 

  • Lefèvre I, Vogel-Mikuš K, Arčon I, Lutts S (2016) How do roots of the metal-resistant perennial bush Zygophyllum fabago cope with cadmium and zinc toxicities? Plant Soil 404(1–2):193–207

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Methods in enzymology Academic Press 148: 350–382

  • Lichtfouse E, Navarrete M, Debaeke P, Souchère V, Alberola C, Ménassieu J (2009) Agronomy for sustainable agriculture: a review. Agron Sustain Dev 29:1–6

    Article  Google Scholar 

  • Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N (2008) Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils. Environ Res 106(3):326–332

    Article  CAS  Google Scholar 

  • Marshall JD (1986) Drought and shade interact to cause fine-root mortality in Douglas-fir seedlings. Plant Soil 91(1):51–60

    Article  Google Scholar 

  • Matysik J, Alia Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82(5):525–532

    CAS  Google Scholar 

  • Meda A, Lamien CE, Romito M, Millogo J, Nacoulma OG (2005) Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem 91(3):571–577

    Article  CAS  Google Scholar 

  • Mohan BS, Hosetti BB (1997) Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization ponds. Environ Pollut 98(2):233–238

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  Google Scholar 

  • Nogueirol RC, Monteiro FA, Gratão PL, da Silva BKDA, Azevedo RA (2016) Cadmium application in tomato: nutritional imbalance and oxidative stress. Water Air Soil Pollut 227(6):210

    Article  Google Scholar 

  • Pourrut B, Shahid M, Douay F, Dumat C, Pinelli E (2013) Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In: Corpas FJ, Palma JM, Gupta DK (eds) Heavy metal stress in plants. Springer, Berlin, pp 121–147

    Chapter  Google Scholar 

  • Roychoudhury A, Ghosh S, Paul S, Mazumdar S, Das G, Das S (2016) Pre-treatment of seeds with salicylic acid attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean (Vigna radiata L. Wilczek). Acta Physiol Plant 38(1):11

    Article  Google Scholar 

  • Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109(4):1427–1433

    Article  CAS  Google Scholar 

  • Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    CAS  Google Scholar 

  • Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4(2):272

    Article  Google Scholar 

  • Shahid M, Dumat C, Pourrut B, Silvestre J, Laplanche C, Pinelli E (2014) Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J Soils Sediments 14(4):835–843

    Article  Google Scholar 

  • Stoyanova S, Geuns J, Hideg E, Van den Ende W (2011) The food additives inulin and stevioside counteract oxidative stress. Int J Food Sci Nutr 62:207–214

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97

    Article  CAS  Google Scholar 

  • Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103(3):771–781

    Article  CAS  Google Scholar 

  • Wang SH, Yang ZM, Yang H, Lu B, Li SQ, Lu YP (2004) Copper-induced stress and antioxidative responses in roots of Brassica juncea L. Bot Bull Acad Sin 45:203–212

    CAS  Google Scholar 

  • Yagmur M, Kaydan D (2008) Alleviation of osmotic stress of water and salt in germination and seedling growth of triticale with seed priming treatments. Afr J Biotechnol 7(13):2156–2162

    CAS  Google Scholar 

  • Zacchini M, Iori V, Mugnozza GS, Pietrini F, Massacci A (2011) Cadmium accumulation and tolerance in Populus nigra and Salix alba. Biol Plant 55(2):383–386

    Article  CAS  Google Scholar 

  • Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252(3):911–924

    Article  CAS  Google Scholar 

  • Zouari M, Elloumi N, Ahmed CB, Delmail D, Rouina BB, Abdallah FB, Labrousse P (2016) Exogenous proline enhances growth, mineral uptake, antioxidant defense, and reduces cadmium-induced oxidative damage in young date palm (Phoenix dactylifera L.). Ecol Eng 86:202–209

    Article  Google Scholar 

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Correspondence to Erna Karalija.

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Karalija, E., Selović, A. The effect of hydro and proline seed priming on growth, proline and sugar content, and antioxidant activity of maize under cadmium stress. Environ Sci Pollut Res 25, 33370–33380 (2018). https://doi.org/10.1007/s11356-018-3220-7

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