Abstract
Bio-energy crops need to be grown on marginal salt and drought lands in India as per policy. Understanding environmental stress response in bio-energy crops might help in promoting cultivation of bio-energy feedstock on marginal salty and drought land. This is one of the first report for vegetative propagation of Bamboo (Bambusa balcooa) under salt and drought stress to understand antioxidant enzymes’ gene regulations to combat stress through activation of antioxidant enzymes and osmo-protectant molecules to scavenge reactive oxygen species as measured by physiological changes. Morphological, physiological, and biochemical traits were noted as indicators of plant health upon different sodium chloride (NaCl) salt-stress while various drought conditions with correlation analysis. A significant up-regulation of genes related to most of the antioxidant enzymes was observed up to salinity of 14 mS cm− 1 electric conductivity (EC) at 150 mM NaCl experimental salt stress which declined with higher salt-stress. While in the case of drought-stress, all genes remained up-regulated while proline dehydrogenase (PDH) remained down-regulated up-to 100% drought-stress having 4% soil moisture. The gene expressions of antioxidant enzymes were significantly correlated with their corresponding gene-products namely super-oxide dismutase (SOD), catalase (CAT), glutathione reductase (GR) and ascorbate peroxidase (APX) activities. Biochemical parameters such as, soluble sugar, proline, malondialdehyde (MDA), total amino acids, hydrogen peroxide and electrolyte leakage ratio also showed positive correlation (p = 0.001) with salt condition. Genetic and biochemical test parameters were significantly correlated with physiological attributes of plant health at soil EC of 14 mS cm− 1 shown as 150 mM NaCl salt stress and 60% drought-stress having 17% soil moisture content, were the optimum stress tolerance limits observed. Application of these data would be useful to cultivate 0.63 million ha of salinity affected land and 10.05 million ha of drought affected land among wastelands in India to meet biofuel need.
Similar content being viewed by others
References
Aebi H, Lester P (1984) Catalase in-vitro. Methods Enzymol 105:121–126
Arisi AM, Cornic G, Jouanin L, Foyer CH (1998) Overexpression of iron superoxide dismutase in transformed poplar modifies the regulation of photosynthesis at low CO2 partial pressures or following exposure to the prooxidant herbicide methyl viologen. Plant Physiol 117:565–574
Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241
Astier J, Gross I, Durner J (2017) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411. https://doi.org/10.1093/jxb/erx420
Bao W, Qu Y, Shan X, Wan Y (2016) Screening and validation of housekeeping genes of the root and cotyledon of Cunninghamia lanceolata under abiotic stresses by using quantitative real-time PCR. Int J Mol Sci. https://doi.org/10.3390/ijms17081198
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline in water stress studies. Plant Soil 39:205–207
Beyer WF, Fridowich I (1987) Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Bhaumik M, Seldin MF, Stanley P (1995) Cloning and chromosomal mapping of the mouse Mgat3 gene encoding N-acetylglucosaminyltransferase III. Gene 164:295–300
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 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Chamizo-Ampudia A, Sanz-Luque E, Llamas A et al (2017) Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci 22:163–174. https://doi.org/10.1016/j.tplants.2016.12.001
Chatzidimitriadou K, Nianiou-Obeidat I, Madesis P et al (2009) Expression of SOD transgene in pepper confer stress tolerance and improve shoot regeneration. Electron J Biotechnol 12:1–9. https://doi.org/10.2225/vol12-issue4-fulltext-10
Corpas FJ (2016) Reactive nitrogen species (RNS) in plants under physiological and adverse environmental conditions: current view. In: Cánovas F, Lüttge U, Matyssek R (eds) Progress in botany. Springer, Cham, pp 97–119
Corpas FJ, Barroso JB, Palma JM, Rodriguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol 11:535–542. https://doi.org/10.1016/j.redox.2016.12.033
Dubey RS (1997) Photosynthesis in plants under stressful conditions. In: Pessarakli M (ed) Handbook of photosynthesis. Marcel Dekker, New York, pp 859–875
Ferreira AL, Lima cosata ME (2006) Metabolic responses to salt stress in cell suspension cultures of sensitive and resistant Citrus. J Hortic Sci Biotechnol 81:983–988
Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis:regulation and signaling. New Phytol 146:359–388
Garratt LC, Janagoundar BS, Lowe K et al (2002) Salinity tolerance and antioxidant status in cotton cultures. Free Radicle Biol Med 33:502–511
Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot 47:39–50
Guerrier G (1996) Fluxes of Na+, K + and Cl- -and osmotic adjustment in Lycopersicon pimpinellifolium and L. esculentum during short and long term exposures to NaCL. Physiol Plant 97:5587–5394
Hasthanasombut S, Paisarnwipatpong N, Triwitayakorn K (2011) Expression of OsBADH1 gene in Indica rice (Oryza sativa L.) in correlation with salt, plasmolysis, temperature and light stresses. Plant Omics J 4:400–407
Hazzoumi Z, Moustakime Y, hassan Elharchli E, Joutei KA (2015) Effect of arbuscular mycorrhizal fungi (AMF) and water stress on growth, phenolic compounds, glandular hairs, and yield of essential oil in basil (Ocimum gratissimum L.). Chem Biol Technol Agric. https://doi.org/10.1186/s40538-015-0035-3
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–190
IBM (2019) SPSS-statistics software. http://ibm-spss-statistics.soft32.com/. Accessed 22 Aug 2019
Khan MA, Ungar IA, Showalter AM (2000) Effects of sodium chloride treatments on growth and ion accumulation of the halophyte Haloxylon recurvum. Commun Soil Sci Plant Anal 31:2763–2774
Krishnaveni S, Balasubramaniam T, Sadasivam S (1984) Sugar distribution is sweet stalk sorghum. Food Chem 15:229–282
Levitt J (1980) Responses of plants to environmental stresses: water, radiation, salt and other stresses. Academic Press, New York
Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787
Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398
MAFW-GOI (2016) Manual for drought management. New Delhi, India. https://www.preventionweb.net/files/57453_indiadroughtmanual2016.pdf. Accessed 23 Jan 2020
Mahajan G, Das B, Morajkar S et al (2020) Soil quality assessment of coastal salt-affected acid soils of India. Environ Sci Pollut Res 27:26221–26238. https://doi.org/10.1007/s11356-020-09010-w
Mandal AK, Sharma RC, Singh G, Dagar J (2010) Computerized database on salt affected soils in India. Technical Bulletin No. CSSRI/Karnal/2/2010, Karnal, p 28
Ministry of New & Renewable Energy- Government of India Ministry (2009) National policy on biofuels. pp 1–18. http://mnre.gov.in/file-manager/UserFiles/biofuel_policy.pdf. Accessed 26 Mar 2020
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663
Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Aust J Plant Physiol 22:561–569
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate peroxidase in spinach chloroplasts. Plant Cell Physiol 21:867–880
NRSC - Goverment of India (2019) Wastelands atlas of India-2019. National remote sensing centre ISRO, Govt. of India, Hyderabad. http://dolr.gov.in/sites/default/files/Wastelands_Atlas_2011.pdf. Accessed 2 Apr 2020
Patankar HV, Assaha DVM, Al-Yahyai R et al (2016) Identification of reference genes for quantitative real-time PCR in date palm (Phoenix dactylifera L.) subjected to drought and salinity. PLoS One 11:1–21. https://doi.org/10.1371/journal.pone.0166216
Patel AD, Lacheta K, Gill S, Tuneja N (2013) Salinity tolerance of Avicennia officinalis L. (Acanthaceae) from Gujarat coasts of India. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley-VCH Verlag GmbH & Co., Weinheim
Patel MP, Gami B, Patel B (2015) Seasonal impact on physical-chemical properties of soil in north and south Gujarat. IOSR J Agric Vet Sci Version II 8:2319–2372. https://doi.org/10.9790/2380-08622636
Patel B, Gami B, Patel P (2017) Carbon sequestration by bamboo farming on marginal land and sustainable use of wood waste for wioenergy: case studies from abellon clean energy. In: Krishna K, Pandey V, Ramakantha SS et al (eds) Wood is good current trends and future prospects in wood utilization. Springer Nature Singapore Pte Ltd, Singapore, pp 451–467
Patel B, Gami B, Patel A, Patel P (2019) Wasteland utilization for B. balcooa cultivation: socio-economic and environmental impacts through bamboo-based product development. Eur J Sustain Dev Res 3:1–11. https://doi.org/10.29333/ejosdr/5957
Patel B, Patel A, Gami B, Patel P (2020a) Energy balance, GHG emission and economy for cultivation of high biomass verities of bamboo, sorghum and pearl millet as energy crops at marginal ecologies of Gujarat state in India. Renew Energy 148:816–823. https://doi.org/10.1016/j.renene.2019.10.167
Patel MP, Gami B, Patel A et al (2020b) Climatic and anthropogenic impact on groundwater quality of agriculture dominated areas of southern and central Gujarat, India. Groundw Sustain Dev 10:100306. https://doi.org/10.1016/j.gsd.2019.100306
Perez -Al focea F, Bal Ibrea ME, Santa Cruz A, Estan MT (1996) Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid. Plant Soil 180:251–257
Rao R, Patil P (2012) In vitro selection of salt tolerant calli lines and regeneration of salt tolerant plantlets in mung bean (Vigna radiata L. Wilczek). In: Sammour R (ed) Biotechnology - molecular studies and novel applications for improved quality of human life. InTech, Rijeka, Croatia, pp 197–212.
Romero-Aranda R, Soria T, Cuartero S (2001) Tomato plant-water uptake and plant-water relationships under saline growth conditions. Plant Sci 160:265–272
Sadasivam S, Manickam A (1992) Biochemical methods for agricultural sciences. Wiley Eastern Ltd., New Delhi
Sharma D, Singh A (2015) Salinity research in India-achievements, challenges and future prospects. Water Energy Int 58:35–45
Sharma R, Wahono J, Baral H (2018) Bamboo as an alternative bioenergy crop and powerful ally for land restoration in Indonesia. Sustainability 10:1–10. https://doi.org/10.3390/su10124367
Smith I, Vierheller T, Thorne C (1988) Assay of glutathione reductase in crude tissue homogenates using 5,5’-dithiobis(2-nitrobenzoic acid). Anal Biochem 175:408–413
Sohan D, Nasoni R, Zajicek J (1999) Plant-water relations of NaCl and calcium-treated sunflower plants. Environ Exp Bot 42:105–111
Syed BA, Patel B (2014) Investigation and correlation of soil biotic and abiotic factors affecting agricultural productivity in semi-arid regions of Noth Gujarat, India. Int J Res Stud Biosci 2:18–29
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Turan S, Tripathy BC (2012) Salt and genotype impact on antioxidative enzymes and lipid peroxidation in two rice cultivars during de-etiolation. Protoplasma. https://doi.org/10.1007/s00709-012-0395-5
Vandelle E, Delledonne M (2011) Peroxynitrite formation and function in plants. Plant Sci 181:534–539. https://doi.org/10.1016/j.plantsci.2011.05.002
Wahome P, Jesch H, Grittner I (2001) Mechanisms of salt stress tolerance in two rose rootstocks: Rosa chinensis “Major” and R. rubiginosa. Sci Hortic 876:207–216
Wang M, Le, Li QH, Xin HH et al (2017) Reliable reference genes for normalization of gene expression data in tea plants (Camellia sinensis) exposed to metal stresses. PLoS One 12:1–13. https://doi.org/10.1371/journal.pone.0175863
Yeo AR (1998) Molecular biology of salt tolerance in the context of whole plant physiology. J Exp Bot 49:915–929
Yiping L, Yanxia L, Buckingham K et al (2010) Bamboo and climate change mitigation: a comparative analysis of carbon sequestration. p 47. International Network for Bamboo and Rattan (INBAR), Beijing, China. http://forestindustries.eu/sites/default/files/userfiles/1file/bamboo-TR32.pdf
Yooyongwech S, Cha-um S, Supaibulwatana K (2006) Proline related genes expression and physiological changes in indica rice response to water- deficit stress. Plant Omics J 5:597–603
Zhifang G, Loescher WH (2003) Expression of a celery mannose-6-phosphate reductase in Arabidopsos thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimmer. Plant Cell Environ 26:275–283
Acknowledgements
All authors are thankful to Abellon CleanEnergy Ltd. and Xcelris Labs Ltd. for financial support to accomplish this work.
Author information
Authors and Affiliations
Contributions
BAS designed the experiments, studied gene expression, antioxidant enzyme activities, biochemical parameters and morphological parameters, performed statistical analysis and prepared the manuscript. BP conceptualized and coordinated the study and manuscript design. BG helped in biochemical studies. MP helped in statistical analysis of the data. AP helped in manuscript editing, proofreading and reference citation.
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Syed, B.A., Patel, M., Patel, A. et al. Regulation of antioxidant enzymes and osmo-protectant molecules by salt and drought responsive genes in Bambusa balcooa. J Plant Res 134, 165–175 (2021). https://doi.org/10.1007/s10265-020-01242-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-020-01242-8