Abstract
Soybean is one of the most important crops of economic value, and among the factors that can alter its productivity is the water-deficit. Studies show that amino acids such as proline and glutamate can help protect plants against abiotic stresses, such as water restriction. Therefore, the present study aimed to investigate the improvement of tolerance to water deficit in soybean plants when submitted to the application of proline and glutamate. The application of these amino acids was carried out as seed treatment (ST) or as foliar application (FA). Three irrigation levels (80, 60, and 40% of the pot field capacity) were used, which corresponded to treatments without water deficit, moderate, and high deficits, respectively. The high water deficit provided a significant reduction in plant growth and productivity. Under these conditions, glutamate as ST was effective in increasing the plant dry mass and yield (21% increase in relation to control). In plants without water restriction, the application of glutamate as ST reduced the lipid peroxidation and increased the dry mass of the plants, volume, and root projection area (PA). On the other hand, for plants submitted to the low water deficit, the FA of proline increased the dry mass of the plants, nitrate reductase, and PA. Therefore, in soybean plants without water restriction and with high water deficit, the best response was obtained with glutamate as ST. For plants submitted to low water deficit, the best procedure was the application of proline as FA.
Similar content being viewed by others
References
Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L. cultivar Kent). J Plant Interact 10(1):211–223
Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23(4):731–744
Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344
Ali Q, Ashraf M, Shahbaz M, Humera H (2008) Ameliorating effect of foliar applied proline on nutrient uptake in water stressed maize (Zea mays L.) plants. Pak J Bot 40:211–219
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Baroowa B, Gogoi N (2013) Biochemical changes in two Vigna spp. During drought and subsequent recovery. Indian J Plant Physiol 18:319–325
Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and applicable to acrylamide gels. Anal Biochem 44(1):276–287
Biancucci M, Mattioli R, Moubayidin L, Sabatini S, Costantino P, Trovato M (2015) Proline affects the size of the root meristematic zone in Arabidopsis. BMC Plant Biol 15:263
Bouché N, Fait A, Zik M, Fromm H (2004) The root specific glutamate decarboxylase (GAD1) is essential for sustaining GABA levels in Arabidopsis. Plant Mol Biol 55:315–325
Bouma TJ, Nielson KL, Koutstaal BAS (2000) Sample preparation and scanning protocol for computerized analysis of root length and diameter. Plant Soil 218:185–196
Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254
Carvalho K, de Campos MKF, Domingues DS, Pereira LFP, Vieira LGE (2013) The accumulation of endogenous proline induces changes in gene expression of several antioxidant enzymes in leaves of transgenic Swingle citrumelo. Mol Biol Rep 40:3269–3279
Cuin TA, Shabala S (2007) Compatible solutes reduce ROS-induced potassium efflux in Arabidopsis roots. Plant Cell Environ 30:875–885
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS, Siddique KHM (2016) Drought stress in grain legumes during reproduction and grain filling. J Agron Crop Sci 203:1–23
Forde BG (2014) Glutamate signalling in roots. J Exp Bot 65(3):779–787
Forde BG, Roberts MR (2014) Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defense? F1000Prime Rep 37:6–37
Forde BG, Walch-Liu P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant Cell Environ 32:682–693
Forde BG, Cutler SR, Zaman N, Krysan PJ (2013) Glutamate signalling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture. Plant J 75:1–10
Gadallah MAA (1999) Effects of proline and glycine betaine on Vicia faba responses to salt stress. Biol Plant 42:249–257
Gill S, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Hammad SAR, Ali OAM (2014) Physiological and biochemical studies on drought tolerance of wheat plants by application of amino acids and yeast extract. Ann Agric Sci 59:133–145
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
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hogan ME, Swift IE, Done HJ (1983) Urease assay and ammonia release from tissue. Phytochemistry 22:663–667
Hoque MAOE, Banu MNA, Nakamura Y, Shimoishi Y, Murata Y (2007) Exogenous proline mitigates the detrimental effects of salt stress more than the betaine by increasing antioxidant enzyme activities. J Plant Physiol 164:553–561
Johnson CM, Stout PR, Broyer TC, Carlton AB (1957) Comparative chlorine requirement of different plant species. Plant Soil 8:337–353
Kan CC, Chung TY, Wu HY, Juo YA, Hsieh MH (2017) Exogenous glutamate rapidly induces the expression of genes involved in metabolism and defense responses in rice roots. BMC Genom 18:186
Kang JM, Turano FJ (2003) The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6872–6877
Kang JM, Mehta S, Turano FJ (2004) The putative glutamate receptor 1.1 (AtGLR1.1) in Arabidopsis thaliana regulates abscisic acid biosynthesis and signaling to control development and water loss. Plant Cell Physiol 45:1380–1389
Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenol oxidase activities during rice leaf senescence. Plant Physiol 57:315–319
Kibria MG, Farzana K, Matin MdA, Hoque MdA (2016) Mitigating water stress in wheat (BARI Gom-26) by exogenous application of proline. Fundam Appl Agric 1(3):118–123
Kim SA, Kwak JM, Jae SK, Wang MH, Nam HG (2001) Overexpression of the AtGluR2 gene encoding an arabidopsis homolog of mammalian glutamate receptors impairs calcium utilization and sensitivity to ionic stress in transgenic plants. Plant Cell Physiol 42:74–84
Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011
McCullough H (1967) The determination of ammonia in whole blood by direct colorimetric method. Clin Chim Acta 17:297–298
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mulder EG, Boxma R, Veen WLV (1959) The effect of molybdenum and nitrogen deficiencies on nitrate reduction in plant tissues. Plant Soil 10:335–355
Peixoto HPP, Cambraia J, Sant’ana R, Mosquim PR, Moreira AM (1999) Aluminum effects on lipid peroxidation and the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal 11(3):137–143
Sas Institute (2011) SAS/STAT statistical analysis system manual (v.9.3). SAS Institute, Cary
Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V et al (2015) GABA signaling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6:7879
Rejeb KB, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284
Roychoudhury A, Chakraborty M (2013) Biochemical and molecular basis of varietal difference in plant salt tolerance. Annu Rev Res Biol 3:422–454
Roychoudhury A, Banerjee A, Lahiri V (2015) Metabolic and molecular-genetic regulation of proline signalling and its cross-talk with major effectors mediates abiotic stress tolerance in plants. Turk J Bot 39:887–910
Sharma P, Dubey RS (2005) Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant. J Plant Physiol 162:854–864
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060
Soares LH, Dourado-Neto D, Fagan EB, Teixeira WF, Reis MR, Reichardt K (2016) Soybean seed treatment with micronutrients, hormones and amino acids on physiological characteristics of plants. Afr J Agric Res 11(35):3314–3319
Teisseire H, Guy V (2000) Copper-induced changes in antioxidant enzymes activities in fronds of duckweed (Lemna minor). Plant Sci 153:65–72
Teixeira WF, Fagan EB, Soares LH, Umburanas RC, Reichardt K, Dourado-Neto D (2017a) Foliar and seed application of amino acids affects the antioxidant metabolism of the soybean crop. Front Plant Sci 8:1–14
Teixeira WF, Fagan EB, Soares LH, Soares JN, Reichardt K, Dourado-Neto D (2017b) Seed and foliar application of amino acids improve variables of nitrogen metabolism and productivity in soybean crop. Front Plant Sci 9:1–12
Teixeira WF, Fagan EB, Soares LH, Cabral EMA, Dourado-Neto D (2018) Changes in root architecture after amino acid application in a soybean crop. J Agric Sci 11(1):325–334
Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 14(361):1112–1115
Vincill ED, Bieck AM, Spalding EP (2012) Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159:40–46
Walch-Liu P, Forde BG (2007) L-Glutamate as a novel modifier of root growth and branching: what’s the sensor? Plant Signal Behav 2:284–286
Walch-Liu P, Forde BG (2008) Nitrate signaling mediated by the NRT1.1 nitrate transporter antagonises l-glutamate-induced changes in root architecture. Plant J 54:820–828
Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol 47(8):1045–1057
Weiland M, Mancuso S, Baluska F (2015) Signalling via glutamate and GLRs in Arabidopsis thaliana. Funct Plant Biol 43:1–25
YoshibaY Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38(10):1095–1102
Acknowledgements
The authors want to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES), for funding this research-Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Teixeira, W.F., Soares, L.H., Fagan, E.B. et al. Amino Acids as Stress Reducers in Soybean Plant Growth Under Different Water-Deficit Conditions. J Plant Growth Regul 39, 905–919 (2020). https://doi.org/10.1007/s00344-019-10032-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-019-10032-z