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Biochar Increased Plant Growth-Promoting Hormones and Helped to Alleviates Salt Stress in Common Bean Seedlings

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Abstract

Salinity seriously disrupts the growth and physiology of plants, whereas phytohormones play an important role in regulating plant responses to salinity stress. Biochar is attracting increasing attention in recent years as a potential soil amendment under stress condition. This study addressed the use of biochar to mitigate salt-stressed soil and evaluated the levels of some phytohormones in bean (Phaseolus vulgaris L.) seedlings. A pot experiment was conducted in a climate-controlled greenhouse with three biochar ratios (control, 10, and 20% mass), three salt stress treatments (non-saline, 6, 12 dS m−1 NaCl), and four replications. The results indicated that sodium (Na) concentration, polyamine oxidase (PAO) activity, the contents of polyamines (putrescine, spermidine, and spermine), abscisic acid (ABA), 1-aminocyclopropane-1-carboxylic acid (ACC), jasmonic acid (JA), and salicylic acid (SA) in bean leaf and root increased under salt stress. However, endogenous indole-3-acetic acid (IAA) content was decreased by salinity compared to the non-saline treatment. On the other hand, we observed decreases of Na concentration, PAO activity, polyamines, ABA, ACC, and JA contents in plants treated by biochar. In contrast, biochar enhanced IAA content and the growth of roots and shoots. As a result, the effectiveness of 20% biochar was superior to the 10% treatment in terms of polyamine contents, especially under saline conditions. Interestingly, there were no considerable changes in phytohormone contents by use of biochar under non-saline conditions. Overall, biochar alleviated the negative effects of salt stress on bean seedlings by reduction of Na concentration, endogenous stress hormones, and improvement of growth hormones.

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References

  • Abbas T, Rizwan M, Ali S, Adrees M, Zia-ur-Rehman M, Qayyum MF, Ok YS, Murtaza G (2017) Effect of biochar on alleviation of cadmium toxicity in wheat (Triticum aestivum L.) grown on Cd-contaminated saline soil. Environ Sci Pollut Res 1–13

  • Ahmed AA, Roosens N, Dewaele E, Jacobs M, Angenon G (2015) Overexpression of a novel feedback-desensitized ∆1-pyrroline-5-carboxylate synthetase increases proline accumulation and confers salt tolerance in transgenic Nicotiana plumbaginifolia. Plant Cell Tissue Organ Cult 122:383–393

    Article  CAS  Google Scholar 

  • Akhtar SS, Andersen MN, Liu F (2015) Biochar mitigates salinity stress in potato. J Agron Crop Sci 201:368–378

    Article  CAS  Google Scholar 

  • Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Rizwan M, Qayyum MF, Ok YS, Ibrahim M, Riaz M, Arif MS, Hafeez F, Al-Wabel MI, Shahzad AN (2017) Biochar soil amendment on alleviation of drought and salt stress in plants: a critical review. Environ Sci Pollut Res 24:12700–12712

    Article  CAS  Google Scholar 

  • Ashraf M (2009) Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotech Adv 27:84–93

    Article  CAS  Google Scholar 

  • Aziz A, Larher F (1995) Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stresses. Plant Sci 112:175–186

    Article  CAS  Google Scholar 

  • Babu MA, Singh D, Gothandam KM (2012) The effect of salinity on growth, hormones and mineral elements in leaf and fruit of tomato cultivar PKM1. J Anim Plant Sci 22:159–164

    CAS  Google Scholar 

  • Bankaji I, Sleimi N, López-Climent MF, Perez-Clemente RM, Gomez-Cadenas A (2014) Effects of combined abiotic stresses on growth, trace element accumulation, and phytohormone regulation in two halophytic species. J Plant Growth Regul 33:632–643

    Article  CAS  Google Scholar 

  • Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman HD (1965) Cation-exchange capacity. Methods of soil analysis. Part 2. Chemical and microbiological properties, (methods of soil anb), pp 891–901

  • Cheng Y, Cai ZC, Chang S, Wang J, Zhang JB (2012) Wheat straw and its biochar have contrasting effects on inorganic N retention and N2O production in a cultivated Black Chernozem. Biol Fertil Soil 48:941–946

    Article  CAS  Google Scholar 

  • Concepcion M, Lizada C, Yang SF (1979) A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Anal Biochem 100:140–145

    Article  Google Scholar 

  • Djanaguiraman M, Sheeba JA, Durga DD, Bangarusamy U (2009) Cotton leaf senescence can be delayed by nitrophenolate spray through enhanced antioxidant defence system. J Agron Crop Sci 195:213–224

    Article  CAS  Google Scholar 

  • Downie A, Crosky A, Munroe P (2009) Physical properties of biochar. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology, 2nd edn. Earthscan, London, pp 13–32

    Google Scholar 

  • Du H, Wu N, Chang Y, Li X, **ao J, **ong L (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Mol Biol 83:475–488

    Article  CAS  PubMed  Google Scholar 

  • Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635

    Article  CAS  PubMed  Google Scholar 

  • Enders A, Hanley K, Whitman T, Joseph S, Lehmann J (2012) Characterization of biochars to evaluate recalcitrance and agronomic performance. Bioresour Technol 114:644–653

    Article  CAS  PubMed  Google Scholar 

  • Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70

    Article  CAS  PubMed  Google Scholar 

  • Flores HE (1991) Changes in polyamine metabolism in response to abiotic stress. In: Slocum RM, Flores HE (eds) Biochemistry and Physiology of Polyamines Plants. CRC Press, Boca Raton, pp 213–228

    Google Scholar 

  • George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Article  CAS  PubMed  Google Scholar 

  • Ghanem ME, Albacete A, Martínez-Andújar C, Acosta M, Romero-Aranda R, Ian CD, Lutts S, Pérez-Alfocea F (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grattan SR, Grieve CM (1998) Salinity–mineral nutrient relations in horticultural crops. Sci Hortic 78:127–157

    Article  Google Scholar 

  • Grieve CM, Grattan SR, Maas EV (2012) Plant salt tolerance. Agricultural salinity assessment and management, 2nd edn. ASCE Manual Reports on Engineering Practice, vol 71, pp 405–459

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate saltinduced damages. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87

    Chapter  Google Scholar 

  • Horvath E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300

    Article  CAS  Google Scholar 

  • Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42

    Article  CAS  Google Scholar 

  • Javid MG, Sorooshzadeh A, Moradi F, Modarres Sanavy S, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 5:726–734

    CAS  Google Scholar 

  • Jia W, Wang Y, Zhang S, Zhang J (2002) Salt-stress-induced ABA, accumulation is more sensitively triggered in roots than in shoots. J Exp Bot 53:2201–2206

    Article  CAS  PubMed  Google Scholar 

  • Jimenez-Bremont JF, Ruiz OA (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    Article  CAS  PubMed  Google Scholar 

  • Kazan K, Manners JM (2009) Linking development to defense: auxin in plant pathogen interactions. Trends Plant Sci 14:1360–1385

    Article  Google Scholar 

  • Keskin BC, Sarikaya AT, Yuksel B, Memon AR (2010) Abscisic acid regulated gene expression in bread wheat. Aust J Crop Sci 4:617–625

    CAS  Google Scholar 

  • Khan NA, Khan MIR (2014) The ethylene: from senescence hormone to key player in plant metabolism. J Plant Biochem Physiol 2, e124

    Article  Google Scholar 

  • Kim HS, Kim KR, Yang JE, Ok YS, Owens G, Nehls T, Wessolek G, Kim KH (2016) Effect of biochar on reclaimed tidal land soil properties and maize (Zea mays L.) response. Chemosphere 142:153–159

    Article  CAS  PubMed  Google Scholar 

  • Kovac M, Piskernik D, Ravnikar M (2003) Jasmonic acid-induced morphological changes are reflected in auxin metabolism of beans grown in vitro. Biol Plant 47:273–275

    Article  CAS  Google Scholar 

  • Kramell R, Atzorn R, Schneider G, Miersch O, Bruckner C, Schmidt J, Sembdner G, Parthier B (1995) Occurrence and identification of jasmonic acid and its amino acid conjugates induced by osmotic stress in barley leaf tissue. J Plant Growth Regul 14:29–36

    Article  CAS  Google Scholar 

  • Lashari MS, Liu Y, Li L, Pan W, Fu J, Pan G, Zheng J, Zheng J, Zhang X, Yu X (2013) Effects of amendment of biochar-manure compost in conjunction with pyroligneous solution on soil quality and wheat yield of a salt-stressed cropland from Central China Great Plain. Field Crop Res 144:113–118

    Article  Google Scholar 

  • Lashari MS, Ye Y, Ji H, Li L, Kibue GW, Lu H, Zheng J, Pan G (2014) Biocharmanure compost in conjunction with pyroligneous solution alleviated salt stress and improved leaf bioactivity of maize in a saline soil from Central China: a twoyear field experiment. J Sci Food Agric 95:1321–1327

    Article  PubMed  Google Scholar 

  • Lashari MS, Ye Y, Ji H, Li L, Kibue GW, Lu H, Zheng J, Pan G (2015) Biochar–manure compost in conjunction with pyroligneous solution alleviated salt stress and improved leaf bioactivity of maize in a saline soil from central China: a 2-year field experiment. J Sci Food Agric 95:1321–1327

    Article  CAS  PubMed  Google Scholar 

  • Lehmann J, Joseph S (2015) Biochar for environmental management: science, technology and implementation. Routledge, London

    Google Scholar 

  • Li XJ, Meng FJ (1996) Study on the photoperiodic-induced flowering in soybean: changes of plant hormones and assimilates of the first leaves. J China Agric Univ 1:35–39

    Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    Article  CAS  PubMed  Google Scholar 

  • Monteiro CC, Rolão MB, Franco MR, Peters LP, Cia MC, Capaldi FR, Carvalho RF, Gratão PL, Rossi ML, Martinelli AP, Peres LEP, Azevedo RA (2012) Biochemical and histological characterization of tomato mutants. An Acad Bras Cienc 84:573–585

    Article  CAS  PubMed  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Montagu M (1997) Antagonistic effects of abscisic acid and jasmonate on salt stress inducible transcripts in rice roots. Plant Cell 12:2243–2259

    Article  Google Scholar 

  • Munns R, Tester M (2008) Mechanism of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nadeem SM, Zahir ZA, Naveed M, Ashraf M (2010) Microbial ACC-deaminase: prospectsand applications for inducing salt tolerance in plants. Crit Rev Plant Sci 29:360–393

    Article  CAS  Google Scholar 

  • Nazar R, Iqbal N, Masood A, Syeed S, Khan NA (2011) Understanding the significance of sulfur in improving salinity tolerance in plants. Environ Exp Bot 70:80–87

    Article  CAS  Google Scholar 

  • Nazar R, Khan MIR, Iqbal N, Masood A, Khan NA (2014) Involvement of ethylene in reversal of salt-inhibited photosynthesis by sulphur in mustard. Physiol Plant 152:331–344

    Article  CAS  PubMed  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (2005) Polyamines inhibit NADPH oxidase-mediated superoxide generation and putrescine prevents programmed cell death induced by polyamine oxidase generated hydrogen peroxide. Planta 220:826–837

    Article  CAS  PubMed  Google Scholar 

  • Peng F, He PW, Luo Y, Lu X, Liang Y, Fu J (2012) Adsorption of phosphate by biomass char deriving from fast pyrolysis of biomass waste. Clean 40:493–498

    CAS  Google Scholar 

  • Qian L, Chen B (2013) Dual role of biochars as adsorbents for aluminum: the effects of oxygen-containing organic components and the scattering of silicate particles. Environ Sci Technol 47:8759–8768

    CAS  PubMed  Google Scholar 

  • Ramzani PMA, Shan L, Anjum S, Ronggui H, Iqbal M, Virk ZA, Kausar S (2017) Improved quinoa growth, physiological response, and seed nutritional quality in three soils having different stresses by the application of acidified biochar and compost. Plant Physiol Bioch 116:127–138

    Article  CAS  Google Scholar 

  • Rhodes D, Nadolska-Orczyk A, Rich PJ (2004) Salinity, osmolytes and compatible solutes. In: Läuchli A, Lüttge U (eds) Salinity: environment-plants-molecules. Kluwer Academic Publishers, Dordrecht, pp 181–204

    Chapter  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    Article  CAS  PubMed  Google Scholar 

  • Shaharoona B, Arshad M, Zahir ZA, Khalid A (2006) Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol Biochem 38:2971–2975

    Article  CAS  Google Scholar 

  • Shi H, Chen L, Ye T, Liu X, Ding K, Chan Z (2014) Modulation of auxin content in Arabidopsis confers improved drought stress resistance. Plant Physiol Biochem 82:209–217

    Article  CAS  PubMed  Google Scholar 

  • Shim IS, Momose Y, Yamamoto A, Kim DW, Usui K (2003) Inhibition of catalase activity by oxidative stress and its relationship to salicylic acid accumulation in plants. Plant Growth Regul 39:285–292

    Article  CAS  Google Scholar 

  • Smith TA (1972) Purification and properties of the polyamine oxidase of barley plants. Phytochemistry 11:899–910

    Article  CAS  Google Scholar 

  • Thomas SC, Frye S, Gale N, Garmon M, Launchbury R, Machado N, Melamed S, Murray J, Petroff A, Winsborough C (2013) Biochar mitigates negative effects of salt additions on two herbaceous plant species. J Environ Manage 129:62–68

    Article  CAS  PubMed  Google Scholar 

  • Tognetti VB, Mühlenbock P, Van Breusegem F (2011) Stress homeostasis—the redox and auxin perspective. Plant Cell Environ 35:321–333

    Article  PubMed  Google Scholar 

  • Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and hormonal crosstalk in vegetative growth and development. Plant Physiol 169:61–72

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang S, Xu L, Li G, Chen P, **a K, Zhou X (2002) An ELISA for the determination of salicylic acid in plants using a monoclonal antibody. Plant Sci 162:529–535

    Article  CAS  Google Scholar 

  • Wang H, Liang X, Wan Q, Wang X, Bi Y (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307

    Article  CAS  PubMed  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Q, Burgess P, Xu J, Meyer W, Huang B (2016) Osmotic stress-and salt stress-inhibition and gibberellin-mitigation of leaf elongation associated with up-regulation of genes controlling cell expansion. Environ Exp Bot 131:101–109

    Article  CAS  Google Scholar 

  • Zhang C, Huang Z (2013) Effects of endogenous abscisic acid, jasmonic acid, polyamines, and polyamine oxidase activity in tomato seedlings under drought stress. Sci Hort 159:172–177

    Article  CAS  Google Scholar 

  • Zorb C, Geilfus CM, Muhling KH, Jutta Ludwig-Muller J (2013) The influence of salt stress on ABA and auxin concentrations in two maize cultivars differing in salt resistance. J Plant Physiol 170:220–224

    Article  PubMed  Google Scholar 

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Acknowledgements

We appreciate the University of Tabriz for providing greenhouse and laboratory.

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Authors and Affiliations

  1. Department of Plant Eco-physiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

    Salar Farhangi-Abriz

  2. Department of Agronomy, College of Agriculture, Isfahan University of Technology, Isfahan, Iran

    Shahram Torabian

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  1. Salar Farhangi-Abriz
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Farhangi-Abriz, S., Torabian, S. Biochar Increased Plant Growth-Promoting Hormones and Helped to Alleviates Salt Stress in Common Bean Seedlings. J Plant Growth Regul 37, 591–601 (2018). https://doi.org/10.1007/s00344-017-9756-9

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