Advertisement

Biochar Triggers Systemic Tolerance Against Cobalt Stress in Wheat Leaves Through Regulation of Water Status and Antioxidant Metabolism

  • Aysegul Yildiztugay
  • Ceyda Ozfidan-Konakci
  • Evren YildiztugayEmail author
  • Mustafa Kucukoduk
Original Paper
  • 7 Downloads

Abstract

To eliminate the damages of metal toxicity by reducing metal uptake by plants, organic amendments are useful. The use of carbon-rich materials known as biochar (BC) is a strong candidate to enhance the plant tolerance against stress conditions. The current study examined the effects of BC in wheat hydroponically grown treated with BC (1 and 3 g L−1) alone or in combination with cobalt (Co, 150 and 300 μM). Stress reduced the relative growth rate (RGR), relative water content (RWC), osmotic potential (ΨΠ), and increased proline content (Pro). Besides, endogenous contents of Ca2+, K+, and Mn2+ in leaves decreased under stress. In response to Co stress, a decline in the activities of peroxidase (POX), ascorbate peroxidase (APX), and glutathione reductase (GR) resulted in the induction of hydrogen peroxide (H2O2) content. BC applied with stress decreased endogenous Co2+ content and increased RGR, RWC, chlorophyll fluorescence and Pro content. Also, the activities of superoxide dismutase (SOD), catalase (CAT), APX and GR were induced and the ascorbate (AsA) and glutathione (GSH) pool and their redox state were maintained by BC application under stress condition. While, with the addition of BC, H2O2 content and lipid peroxidation displayed remarkable decreased, the scavenging activity of hydroxyl radical (OH·) increased as compared to Co stress-treated wheat plants. Besides, in wheat leaves, BC application triggered AsA-GSH pathway including activities of monodehydroascorbate reductase, dehydroascorbate reductase, and the contents of dehydroascorbate, GSH, and GSH/GSSG ratio. The presented results supported the view that biochar under stress could minimize the Co-induced oxidative damages through modulation of the growth, water status, photosynthetic apparatus, and antioxidant enzyme activity found in cellular compartments and ascorbate-glutathione cycle in wheat leaves.

Keywords

Antioxidant system Biochar Cobalt stress Reactive oxygen species Triticum aestivum 

Notes

Acknowledgments

Financial support for this work was provided by Selcuk University Scientific Research Projects Coordinating Office (Project no. 17401061). We are thankful to Synpet Technology and Bahri Dagdas International Agricultural Research Institute for providing Biochar and the seeds of wheat, respectively.

Authors’ Contributions

EY, COK, and MK conceived and designed research. AY and EY conducted experiments. EY analyzed data. COK, AY, and EY wrote the manuscript. All authors read and approved the manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. Abbas T, Rizwan M, Ali S, Adrees M, Mahmood A, Rehman MZ, Ibrahim M, Arshad M, Qayyum MF (2018) Biochar application increased the growth and yield and reduced cadmium in drought stressed wheat grown in an aged contaminated soil. Ecotoxicol Environ Saf 148:825–833CrossRefGoogle Scholar
  2. Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Mehmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut R 22(15):11679–11689CrossRefGoogle Scholar
  3. Akhtar SS, Li G, Andersen MN, Liu F (2014) Biochar enhances yield and quality of tomato under reduced irrigation. Agric Water Manag 138:37–44CrossRefGoogle Scholar
  4. Akhtar SS, Andersen MN, Naveed M, Zahir ZA, Liu F (2015) Interactive effect of biochar and plant growth-promoting bacterial endophytes on ameliorating salinity stress in maize. Funct Plant Biol 42(8):770–781CrossRefGoogle Scholar
  5. Ali S, Rizwan M, Bano R, Bharwana SA, ur Rehman MZ, Hussain MB, Al-Wabel MI (2018) Effects of biochar on growth, photosynthesis, and chromium (Cr) uptake in Brassica rapa L. under Cr stress. Arab J Geosci 11(17):507CrossRefGoogle Scholar
  6. Amin A, Eissa MA (2017) Biochar effects on nitrogen and phosphorus use efficiencies of zucchini plants grown in a calcareous sandy soil. J Soil Sci Plant Nutr 17(4):912–921CrossRefGoogle Scholar
  7. Aziz R, Rafiq MT, Li T, Liu D, He Z, Stoffella P, Sun K, Xiaoe Y (2015) Uptake of cadmium by rice grown on contaminated soils and its bioavailability/toxicity in human cell lines (Caco-2/HL-7702). J Agr Food Chem 63(13):3599–3608CrossRefGoogle Scholar
  8. Bamminger C, Poll C, Sixt C, Högy P, Wuest D, Kandeler E, Marhan S (2016) Short-term response of soil microorganisms to biochar addition in a temperate agroecosystem under soil warming. Agric Ecosyst Environ 233:308–317CrossRefGoogle Scholar
  9. Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207CrossRefGoogle Scholar
  10. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287CrossRefGoogle Scholar
  11. Begović L, Mlinarić S, Dunić JA, Katanić Z, Lončarić Z, Lepeduš H, Cesar V (2016) Response of Lemna minor L. to short-term cobalt exposure: the effect on photosynthetic electron transport chain and induction of oxidative damage. Aquat Toxicol 175:117–126CrossRefGoogle Scholar
  12. Bergmeyer HU (1970) Methoden der enzymatischen Analyse. 2. Verlag ChemieGoogle Scholar
  13. 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):248–254CrossRefGoogle Scholar
  14. Brestic M, Zivcak M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Molecular Stress Physiology of Plants. Springer, Berlin, pp 87–131CrossRefGoogle Scholar
  15. Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109(1):69–74CrossRefGoogle Scholar
  16. Chung S-K, Osawa T, Kawakishi S (1997) Hydroxyl radical-scavenging effects of spices and scavengers from brown mustard (Brassica nigra). Biosci Biotechnol Biochem 61(1):118–123Google Scholar
  17. Cornelissen G, Martinsen V, Shitumbanuma V, Alling V, Breedveld GD, Rutherford DW, Sparrevik M, Hale SE, Obia A, Mulder J (2013) Biochar effect on maize yield and soil characteristics in five conservation farming sites in Zambia. Agronomy 3(2):256–274CrossRefGoogle Scholar
  18. Cuypers A, Karen S, Jos R, Kelly O, Els K, Tony R, Nele H, Nathalie V, Yves G, Jan C (2011) The cellular redox state as a modulator in cadmium and copper responses in Arabidopsis thaliana seedlings. J Plant Physiol 168(4):309–316CrossRefGoogle Scholar
  19. Dalton DA, Russell SA, Hanus FJ, Pascoe GA, Evans HJ (1986) Enzymatic-reactions of ascorbate and glutathione that prevent peroxide damage in soybean root-nodules. P Natl Acad Sci USA 83(11):3811–3815Google Scholar
  20. de Silva NDG, Cholewa E, Ryser P (2012) Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). J Exp Bot 63(16):5957–5966CrossRefGoogle Scholar
  21. Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003) Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131(1):264–275Google Scholar
  22. Enders A, Hanley K, Whitman T, Joseph S, Lehmann J (2012) Characterization of biochars to evaluate recalcitrance and agronomic performance. Bioresour Technol 114:644–653CrossRefGoogle Scholar
  23. Farhangi-Abriz S, Faegi-Analou R, Nikpour-Rashidabad N (2017) Foliar application of sodium molybdate enhanced nitrogen uptake and translocation in soybean plants by improving nodulation process under salt stress. Cercetari Agronomice in Moldova 50(3):71–82CrossRefGoogle Scholar
  24. Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133(1):21–25CrossRefGoogle Scholar
  25. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48(12):909–930Google Scholar
  26. Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase-mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut R 22(14):10375–10394Google Scholar
  27. Gopal R (2014) Antioxidant defense mechanism in pigeon pea under cobalt stress. J Plant Nutr 37(1):136–145CrossRefGoogle Scholar
  28. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32(6):481–494CrossRefGoogle Scholar
  29. Haider G, Koyro H-W, Azam F, Steffens D, Müller C, Kammann C (2015) Biochar but not humic acid product amendment affected maize yields via improving plant-soil moisture relations. Plant Soil 395(1–2):141–157CrossRefGoogle Scholar
  30. Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Crop stress and its management: perspectives and strategies. Springer, Berlin, pp 261–315CrossRefGoogle Scholar
  31. Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Anal Biochem 55(554):e62Google Scholar
  32. Houben D, Sonnet P, Cornelis J-T (2014) Biochar from Miscanthus: a potential silicon fertilizer. Plant Soil 374(1–2):871–882CrossRefGoogle Scholar
  33. Hu Z, Lv X, Xia X, Zhou J, Shi K, Yu J, Zhou Y (2016) Genome-wide identification and expression analysis of calcium-dependent protein kinase in tomato. Front Plant Sci 7:469Google Scholar
  34. Inyang MI, Gao B, Yao Y, Xue Y, Zimmerman A, Mosa A, Pullammanappallil P, Ok YS, Cao X (2016) A review of biochar as a low-cost adsorbent for aqueous heavy metal removal. Crit Rev Environ Sci Technol 46(4):406–433CrossRefGoogle Scholar
  35. Jayakumar K (2019) Antioxidant enzyme mechanism of cluster bean (Cyamopsis tetragonaloba (L.) Taub). under cobalt stress. World News Nat Sci 24:64–70Google Scholar
  36. Jiang M, Zhang J (2002) Involvement of plasma-membrane NADPH oxidase in abscisic acid- and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215(6):1022–1030Google Scholar
  37. Kabata-Pendias A (2010) Trace elements in soils and plants. CRC press, Boca RatonCrossRefGoogle Scholar
  38. Kandil H (2007) Effect of cobalt fertilizer on growth, yield and nutrients status of faba bean (Vicia faba L.) plants. J Appl Sci Res 3(9):867–872Google Scholar
  39. Keshavarz Afshar R, Hashemi M, DaCosta M, Spargo J, Sadeghpour A (2016) Biochar application and drought stress effects on physiological characteristics of Silybum marianum. Commun Soil Sci Plant Anal 47(6):743–752CrossRefGoogle Scholar
  40. Kim H-S, Kim K-R, Yang JE, Ok YS, Owens G, Nehls T, Wessolek G, Kim K-H (2016) Effect of biochar on reclaimed tidal land soil properties and maize (Zea mays L.) response. Chemosphere 142:153–159CrossRefGoogle Scholar
  41. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefGoogle Scholar
  42. Liu ZJ, Guo YK, Bai JG (2010) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two Cucumber ecotypes under osmotic stress. J Plant Growth Regul 29(2):171–183Google Scholar
  43. Lwalaba JL, Zwobgo G, Fu L, Zhang X, Mwamba TM, Muhammad N, Mundende RP, Zhang G (2017) Alleviating effects of calcium on cobalt toxicity in two barley genotypes differing in cobalt tolerance. Ecotoxicol Environ Saf 139:488–495CrossRefGoogle Scholar
  44. Lyu S, Du G, Liu Z, Zhao L, Lyu D (2016) Effects of biochar on photosystem function and activities of protective enzymes in Pyrus ussuriensis Maxim. under drought stress. Acta Physiol Plant 38(9):220CrossRefGoogle Scholar
  45. Maksymiec W, Krupa Z (2006) The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ Exp Bot 57(1–2):187–194CrossRefGoogle Scholar
  46. Mehdizadeh L, Moghaddam M, Lakzian A (2019) Response of summer savory at two different growth stages to biochar amendment under NaCl stress. Arch Agron Soil Sci 65:1120–1133CrossRefGoogle Scholar
  47. Micó C, Li H, Zhao F, McGrath S (2008) Use of Co speciation and soil properties to explain variation in Co toxicity to root growth of barley (Hordeum vulgare L.) in different soils. Environ Pollut 156(3):883–890CrossRefGoogle Scholar
  48. Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase-activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem 212(2):540–546Google Scholar
  49. Miyake C, Asada K (1992) Thylakoid-bound ascorbate peroxidase in spinach-chloroplasts and photoreduction of its primary oxidation-product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol 33(5):541–553Google Scholar
  50. Mohamedin A, El-Kader AA, Badran NM (2006) Response of sunflower (Helianthus annuus L.) to plants salt stress under different water table depths. J Appl Sci Res 2(12):1175Google Scholar
  51. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880Google Scholar
  52. Nyomora A, Sah R, Brown P, Miller R (1997) Boron determination in biological materials by inductively coupled plasma atomic emission and mass spectrometry: effects of sample dissolution methods. Fresenius J Anal Chem 357(8):1185–1191CrossRefGoogle Scholar
  53. Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60(2):149–181CrossRefGoogle Scholar
  54. Paneque M, José M, Franco-Navarro JD, Colmenero-Flores JM, Knicker H (2016) Effect of biochar amendment on morphology, productivity and water relations of sunflower plants under non-irrigation conditions. Catena 147:280–287CrossRefGoogle Scholar
  55. Paradiso A, Berardino R, de Pinto MC, Sanita di Toppi L, Storelli MM, Tommasi F, De Gara L (2008) Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. Plant Cell Physiol 49(3):362–374Google Scholar
  56. Puga A, Abreu C, Melo L, Beesley L (2015) Biochar application to a contaminated soil reduces the availability and plant uptake of zinc, lead and cadmium. J Environ Manag 159:86–93CrossRefGoogle Scholar
  57. Ramzani PMA, Iqbal M, Kausar S, Ali S, Rizwan M, Virk ZA (2016) Effect of different amendments on rice (Oryza sativa L.) growth, yield, nutrient uptake and grain quality in Ni-contaminated soil. Environ Sci Pollut R 23(18):18585–18595CrossRefGoogle Scholar
  58. Ramzani PMA, Khalid M, Anjum S, Ali S, Hannan F, Iqbal M (2017) Cost-effective enhanced iron bioavailability in rice grain grown on calcareous soil by sulfur mediation and its effect on heavy metals mineralization. Environ Sci Pollut R 24(2):1219–1228CrossRefGoogle Scholar
  59. Rao KM, Sresty T (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh) in response to Zn and Ni stresses. Plant Sci 157(1):113–128CrossRefGoogle Scholar
  60. Rizwan M, Ali S, Abbas T, Adrees M, Zia-ur-Rehman M, Ibrahim M, Abbas F, Qayyum MF, Nawaz R (2018) Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions. J Environ Manag 206:676–683CrossRefGoogle Scholar
  61. Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126(3):1281–1290CrossRefGoogle Scholar
  62. Sakamoto A, Murata N (2000) Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J Exp Bot 51(342):81–88CrossRefGoogle Scholar
  63. Santa-Cruz A, Martinez-Rodriguez MM, Perez-Alfocea F, Romero-Aranda R, Bolarin MC (2002) The rootstock effect on the tomato salinity response depends on the shoot genotype. Plant Sci 162(5):825–831CrossRefGoogle Scholar
  64. Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570CrossRefGoogle Scholar
  65. Seevers P, Daly J, Catedral F (1971) The role of peroxidase isozymes in resistance to wheat stem rust disease. Plant Physiol 48(3):353–360CrossRefGoogle Scholar
  66. Sinclair T, Ludlow M (1986) Influence of soil water supply on the plant water balance of four tropical grain legumes. Funct Plant Biol 13(3):329–341CrossRefGoogle Scholar
  67. Singh Mavi M, Singh G, Singh BP, Singh Sekhon B, Choudhary OP, Sagi S, Berry R (2018) Interactive effects of rice-residue biochar and N-fertilizer on soil functions and crop biomass in contrasting soils. J Soil Sci Plant Nutr 18(1):41–45Google Scholar
  68. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53(2):258–260CrossRefGoogle Scholar
  69. Srivastava RK, Pandey P, Rajpoot R, Rani A, Gautam A, Dubey R (2015) Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 252(4):959–975CrossRefGoogle Scholar
  70. Tripathi SK, Ahmadi Z, Gupta KC, Kumar P (2016) Polyethylenimine-polyacrylic acid nanocomposites: type of bonding does influence the gene transfer efficacy and cytotoxicity. Colloids Surf B: Biointerfaces 140:117–120CrossRefGoogle Scholar
  71. Wang L-f (2014) Physiological and molecular responses to drought stress in rubber tree (Hevea brasiliensis Muell. Arg.). Plant Physiol Bioch 83:243–249CrossRefGoogle Scholar
  72. Woodbury W, Spencer A, Stahmann M (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44(1):301–305CrossRefGoogle Scholar
  73. Younis U, Malik SA, Rizwan M, Qayyum MF, Ok YS, Shah MHR, Rehman RA, Ahmad N (2016) Biochar enhances the cadmium tolerance in spinach (Spinacia oleracea) through modification of cd uptake and physiological and biochemical attributes. Environ Sci Pollut R 23(21):21385–21394CrossRefGoogle Scholar
  74. Yuan HM, Huang X (2016) Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant Cell Environ 39(1):120–135CrossRefGoogle Scholar
  75. Zeid I, Ghazi S, Nabawy D (2013) Alleviation of Co and Cr toxic effects on alfalfa. Int J Agron Plant Prod 4(5):984–993Google Scholar

Copyright information

© Sociedad Chilena de la Ciencia del Suelo 2019

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceSelcuk UniversityKonyaTurkey
  2. 2.Department of Molecular Biology and Genetics, Faculty of ScienceNecmettin Erbakan UniversityKonyaTurkey
  3. 3.Department of Biotechnology, Faculty of ScienceSelcuk UniversityKonyaTurkey

Personalised recommendations