Abstract
Salinity has become one of the major factors limiting agricultural production. In this regard, different cost-effective management strategies such as the use of plant growth-promoting bacteria (PGPB) as inoculants to alleviate salt-stress conditions and minimize plant productivity losses have been used in agricultural systems. The aim of this study was to characterize induced antioxidant responses in corn through inoculation with Azospirillum brasilense and examine the relationship between these responses and the acquired salt-stress tolerance. Treatments were performed by combining sodium chloride (0 and 100 mM NaCl) through irrigation water with absence and presence of A. brasilense inoculation. The experiment was performed in a completely randomized design with four replications. Lipid peroxidation (malondialdehyde [MDA]), and nitrogen (N), sodium (Na+) and potassium (K+) contents, as well as dry biomass, glycine betaine, and antioxidant enzymes activities such as of superoxide dismutase (SOD, EC 1. 15. 1. 1), glutathione reductase (GR, EC 1. 6. 4. 2), guaiacol peroxidase (GPOX, EC 1. 11. 1. 7), and glutathione peroxidase (GSH-PX, EC 1. 11. 1. 9) were determined. Overall results indicated that plants treated with 100 mM NaCl showed the most pronounced salt-stress damages with consequent increase in MDA content. However, inoculated plants showed an enhanced capacity to withstand or avoid salt-stress damages. These results could be attributed, at least in part, to the increased activity of antioxidant enzymes. Our results suggest that A. brasilense may confer tolerance to salt stress in corn plants enhancing antioxidant responses, primarily by the enzymes GSH-PX and GPOX, and the osmolyte glycine betaine.
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Ahmed M, Rauf M, Mukhtar Z, Saeed NA (2017) Excessive use of nitrogenous fertilizers: an unawareness causing serious threats to environment and human health. Environ Sci Pollut Res 24:26983–26987
Alves RC, Medeiros AS, Nicolau MCM, Neto AP, Oliveira FA, Lima LW, Tezotto T, Gratão PL (2018) The partial root-zone saline irrigation system and antioxidant responses in tomato plants. Plant Physiol Biochem 127:366–379
Anderson JV, Davis DG (2004) Abiotic stress alters transcript profiles activity of gluthatione S tranferase, gluthatione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Planta 120:421–433
Barbosa JC, Junior WM (2015) Experimentação agronômica and AgroEstat: Sistemas para Análises Estatísticas de Ensaios Agronômicos. FCAV/UNESP, Jaboticabal, p 396
Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by anindonle-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107
Boaretto LF, Carvalho G, Borgo L, Creste S, Landell MGA, Mazzafera P, Azevedo RA (2014) Water stress reveals differential antioxidant responses of tolerant and non- tolerant sugarcane genotypes. Plant Physiol Biochem 74:165–175
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Carvalho RF, Monteiro CC, Caetano AC, Dourado MN, Gratão PL, Haddad CKB, Peres LEP, Azevedo RA (2013) Leaf senescence in tomato mutants as affected by irradiance and phytohormones. Biol Planta 57:749–757
Chen THH, Murata N (2008) Glycine betaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505
DeBruin JL, Schussler JR, Mo H, Cooper M (2017) Grain Yield and Nitrogen accumulation in maize hybrids released during 1934 to 2013 in the US Midwet. Crop Sci 57:1431
Epstein E, Bloom AJ (2005) Mineral nutrition of plants principles and perspectives, vol 2. Oxford University Press, Sunderland, p 400
Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environ Saf 156:225–246
Farooq M, Hussain M, Wakeel A, Siddique KHM (2015) Salt stress in maize: effects resistance mechanisms, and management. A review. Agron Sustain Dev 35:461–481
Farooq MA, Niazi AK, Ullah S (2019) Acquiring control: the evolution of ROS-induced and redox signaling pathways in plant-stress responses. Plant Physiol Biochem 141:353–369
Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18:2087–2090
Fukami J, Ollero FJ, Megías M, Hungria M (2017) Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth. AMB Express 7:153
Fukami J, Osa CI, Ollero FJ, Megías M, Hungria M (2018a) Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress. Funct Plant Biol 45:328–339
Fukami J, Ollero AJ, Osa CI, Valderrama-Fernandez R, Nogueira MA, Megías M, Hungria M (2018b) Antioxidant activity and induction of mechanisms of resistance to stresses related to the inoculation with Azospirillum brasilense. Arch Microbiol 200:1191–1203
Fukami J, Cerezini P, Hungria M (2018) Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Exp 8:73
Ghorbani A, Razavi SM, Ghasemi Omran VO, Pirdashti H (2018) Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biol (Stuttg) 20:729–736
Giannopolitis CN, Ries SK (1977) Superoxide Dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314
Giri J (2011) Glycine betaine and abiotic stress tolerance in plants. Plant Signal Behav 6:1746–1751
Gratão PL, Monteiro CC, Carvalho RF, Tezzoto T, Piotto FA, Peres LEP, Azevedo RA (2012) Biochemical dissection of diageotropica and never ripe tomato mutants to Cd-stressful conditions. Plant Physiol Biochem 56:79–96
Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peter LJ, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
Han HS, Lee KD (2005) Plant growth-promoting rhizobacteria: effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1:210–215
Hasanuzzaman M, Hossain MA, Fujita M (2012) Exogenous selenium pretreatment protects rapeseed seedlings from cadmium-induced oxidative stress by upregulating antioxidant defense and methylglyoxal detoxification systems. Biol Trace Elem Res 149:248–261
Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468
Hungria M (2011) Inoculação com Azospirillum brasilense: inovação em rendimento a baixo custo, vol 325. Embrapa Soja, Londrina, p 36
Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768
Kuhn H, Borchert A (2002) Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. Free Radic Biol Med 33:154–172
Kumar A, Verma JP (2018) Does plant–microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52
Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics and ionomics perspectives of salinity tolerance in halophytes. Front Plant Sci 6:537
Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophy Res Commun 495:286–291
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382
Lim JH, Park HJ, Kim BK, Jeong JW, Kim HJ (2012) Effect of salinity stress on phenolic compounds and carotenoids in buckwheat (Fagopyrum esculentum M.) sprouts. Food Chem 135:1065–1070
Miyazawa M, Pavan MA, Muraoka T, Carmo CAF, de Do S, de Mello WJ (1999) Análises químicas de tecido vegetal. In: da Silva FC (ed) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Comunicação para Transferência de Tecnologia, Rio de Janeiro, pp 171–223
Monteiro CC, Carvalho RF, Gratão PL, Carvalho G, Tezoto T, Medici LO, Peres LEP, Azevedo RA (2011) Biochemical responses of the ethylene-insensitive never ripe tomato mutant subjected to cadmium and sodium stresses. Environ Exp Bot 71:306–320
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Pii Y, Aldrighetti A, Valentinuzzi F, Mimmo T, Cesco S (2019) Azospirillum brasilense inoculation counteracts the induction of nitrate uptake in maize plants. J Exp Bot 70:1313–1324
Radhakrishnan R, Baek KH (2017) Physiological and biochemical perspectives of non-salt tolerant plants during bacterial interaction against soil salinity. Plant Physiol Biochem 116:116–126
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidant defense mechanism in plants under stressful conditions. J Bot 2012:1–26 (ID 217037)
Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14:605–611
Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14
Wang QY, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-amnocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct Plant Biol 43:161–172
Wu H (2018) Plant salt tolerance and Na+ sensing and transport. Crop J 6:215–225
Xiong X, Liu N, Wei Y, Bi Y, Luo J, Xu R, Zhou J, Zhang Y (2018) Effects of non-uniform root zone salinity on growth, ion regulation, and antioxidant defense system in two alfafa cultivars. Plant Physiol Biochem 132:434–444
Yadav S, Irfan M, Ahmad A, Hayat S (2011) Causes of salinity and plant manifestations to salt stress: a review. J Environ Biol 32:667
Zhai CZ, Zhao L, Yin LJ, Chen M, Wang QY, Li LC, Xu SC, Ma YZ (2013) Two wheat gluthathione peroxidase genes whose products are located in chloroplasts improve salt and H2O2 tolerances in Arabidopsis. Plos One 8:73989
Acknowledgements
We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (MVC) for the scholarship granted (Finance Code 001). PLG also thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research fellowship (Grant nº 314380/2018-3) - Brazil. This work was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP - Grant n° 2017/04787-6).
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Checchio, M.V., de Cássia Alves, R., de Oliveira, K.R. et al. Enhancement of salt tolerance in corn using Azospirillum brasilense: an approach on antioxidant systems. J Plant Res 134, 1279–1289 (2021). https://doi.org/10.1007/s10265-021-01332-1
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DOI: https://doi.org/10.1007/s10265-021-01332-1