Abstract
The productivity of plants is a direct variant of the countless biotic and abiotic stresses to which a plant is exposed in an environment. This study aimed to investigate the capabilities of leguminous plant garden pea (Pisum sativum L.) to resist water deficit conditions in arid and semi-arid areas when applied with varied doses of sludge for growth response. The effect of sludge doses was evaluated on crop yield, antioxidant enzymes, viz., ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR), superoxide dismutase (SOD), and glutathione reductase (GR), and metabolites (ascorbic acid, glutathione, and total protein content). The effective sludge concentrations with respect to seed weight and crop yield were found to be in the following trend: D2 (6.25%)>D3 (12.5%)>D1 (2.5%)>D0 (control) under organic amendment (OA). Conversely, a high dose of the sludge reduced the seed weight and total crop yield. The sludge doses D2 under arid and semi-arid conditions along with organic amendments (OA) significantly enhance the antioxidant enzyme activity, whereas sludge dose D3 with OA ominously regulates the activity of these enzymes. Besides, seeds depicted a considerable increase in ascorbic acid, glutathione, and total protein content in arid and semi-arid conditions upon the application of sludge with OA. Sewage sludge as a source of nutrients indirectly enhances crop yield, antioxidant enzymes, and antioxidant metabolites. Thus, it improves the defense mechanism, reduces abnormal protein glycation, and depletes the susceptibility of protein to proteolysis.
Similar content being viewed by others
Abbreviations
- PGPR:
-
Plant growth promoting rhizobacteria
- OA:
-
Organic amendment
- APX:
-
Ascorbate peroxidase
- DHAR:
-
Dehydroascorbate reductase
- SOD:
-
Superoxide dismutase
- GR:
-
Glutathione reductase
- RCBD:
-
Randomized complete block design
- HCl:
-
Hydrochloric acid
- NBT:
-
Nitroblue tetrazolium
- EDTA:
-
Ethylenediamine tetraacetic acid
- NADH:
-
Nicotinamide adenine dinucleotide hydrogen
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
- RDF:
-
Recommended dose of fertilizer
- GSSG:
-
Glutathione disulfide
- ANOVA:
-
Analysis of variance
- FW:
-
Fresh weight
- TPC:
-
Total protein content
- CAT:
-
Catalase
References
Ali MB, Hahn EJ, Paek KY (2005) Effects of temperature on oxidative stress defense systems, lipid peroxidation and lipoxygenase activity in Phalaenopsis. Plant Physiol Biochem 43:213–222. https://doi.org/10.1016/j.plaphy.2005.01.007
Aminifard MH, Aroiee H, Ameri A, Fatem H (2012) Effect of plant density and nitrogen fertilizer on growth, yield and fruit quality of sweet pepper (Capsicum annuum L.). Afr J Agric Res 7(6):859–866
Arrigoni O, De Tullio MC (2002) Ascorbic acid, much more than just an antioxidant. Biochim Biophys Acta 1569:1–9
Balawejder M, Szostek M, Gorzelany J, Antos P, Witek G, Matłok N (2020) A study on the potential fertilization effects of microgranule fertilizer based on the protein and calcined bones in maize cultivation. Sustainability 12:1343. https://doi.org/10.3390/su12041343
Bloom AJ, Frensch J, Taylor AR (2006) Influence of inorganic nitrogen and pH on the elongation of maize seminal roots. Ann Bot 97(5):867–873
Bouvier F, Backhaus RA, Camara B (1998) Induction and control of chromoplast-specific carotenoid genes by oxidative stress. J Biol Chem 273:30651–30659
Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787. https://doi.org/10.1104/pp.106.085506
Choi H (2020) Effects of organic liquid fertilizers on biological activities and fruit productivity in open-field cherry tomato. Bragantia, Campinas 79(3):447–457
Colville L, Kranner I (2010) Desiccation tolerant plants as model systems to study redox regulation of protein thiols. Plant Growth Regul 62:241–255
Costa RCL, Lobato AKS, Silveira JAG, Laughing house HD (2011) ABA-mediated proline synthesis in cowpea leaves exposed to water deficiency and rehydration. Turk J Agric For 35:309–317
Cunniff P, Association of Official Analytical Chemists (1995) Official methods of analysis of AOAC international. Washington, DC: Association of Official Analytical Chemists
Davey MW, Keulemans J (2004) Determining the potential to breed for enhanced antioxidant status in Malus: mean inter and intravarietal fruit vitamin C and glutathione contents at harvest and their evolution during storage. J Agric Food Chem 52:8031–8038
Delfini R, Belgoff C, Fernández E, Fabra A, Castro S (2010) Symbiotic nitrogen fixation and nitrate reduction in two peanut cultivars with different growth habit and branching pattern structures. Plant Growth Regul 6:153–159
Devi SR, Prasad MNV (2005) Antioxidant capacity of Brassica juncea plants exposed to elevated levels of copper. Russ J Plant Physiol 52:205–208. https://doi.org/10.1007/s11183-005-0031-8
Dheeba B, Sampathkumar P, Kannan K (2015) Fertilizers and mixed crop cultivation of chromium tolerant and sensitive plants under chromium toxicity. J Toxicol 2015:1–9. https://doi.org/10.1155/2015/367217
Dhotre M, Mantur SM, Biradar MS (2018) Influence of irrigation regimes and fertigation levels on fruit yield and quality of polyhouse-grown bell pepper. Acta Horticult. https://doi.org/10.17660/ActaHortic.2018.1227.87
Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107
Fan HF, Ding L, Du CX, Wu X (2014) Effect of short-term water deficit stress on antioxidative systems in cucumber seedling roots. Bot Stud 55:46. https://doi.org/10.1186/s40529-014-0046-6
Food and Agriculture Organization of the United Nations (2015) World reference base for soil resources: international soil classification system for naming soils and creating legends for soil maps. http://www.fao.org/3/i3794en/I3794en.pdf
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I et al. (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212. https://doi.org/10.1016/j.plaphy.2013.05.032
Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877
Griffith OW (1980) Determination of glutathione and glutathione disulphide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212
Guilioni L, Wéry J, Lecoeur J (2003) High temperature and water deficit may reduce seed number in field pea purely by decreasing plant growth. Funct Plant Biol 30:1151–1164
Gutiérrez-Gamboa G, Garde-Cerdán T, Gonzalo-Diago A, Moreno-Simunovic Y, Martínez-Gil AM (2017) Effect of different foliar nitrogen applications on the must amino acids and glutathione composition in Cabernet Sauvignon vineyard. LWT Food Sci Technol 75:147–154
Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine, 4th edn. Oxford University Press, Oxford, UK
Han C, Liu Q, Yang Y (2009) Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Picea asperata seedlings. Plant Growth Regul 58(2):153–162
Hasanuzzaman M, Nahar K, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in abiotic stress tolerance. Physiol Mol Biol Plants 23:249–268
Hicks LM, Cahoon RE, Bonner ER, Rivard RS, Sheffield J, Jez JM (2007) Thiol-based regulation of redox-active glutamate cysteine ligase from Arabidopsis thaliana. Plant Cell 19:2653–2661
Jeuffroy MH, Vocanson A, Roger-Estrade J, Meynard JM (2012) The use of models at field and farm levels for the extant assessment of new pea genotypes. Eur J Agron 42:68–78
Jiménez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002a) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214: 751–758
Jiménez A, Gómez JM, Navarro E, Sevilla F (2002b) Changes in the antioxidative systems in mitochondria during ripening of pepper fruits. Plant Physiol Biochem 40:515–520
Khaleghi A, Naderi R, Brunetti C, Maserti BE, Salami SA, Babalar M (2019) Morphological, physiochemical and antioxidant responses of Maclura pomifera to drought stress. Sci Rep 9:19250. https://doi.org/10.1038/s41598-019-55889-y
Kramer PJ, Boyer JS (1995) Water relations of plant and soils. Academic Press, New York
Lawson DM, Smith BE (2002) Molybdenum nitrogenases: a crystallographic and mechanistic view. Met Ions Biol Syst 39:75–119
Lejeune-Hénaut I, Hanocq E, Béthencourt L, Fontaine V, Delbreil B, Morin J, Petit A, Devaux R, Boilleau M, Stempniak JJ, Thomas M, Lainé AL, Foucher F, Baranger A, Burstin J, Rameau C, Giauffret C (2008) The flowering locus Hr colocalizes with a major QTL affecting winter frost tolerance in Pisum sativum L. Theor Appl Gen 116:1105–1116
Loscos J, Matamoros MA, Becana M (2008) Ascorbate and homoglutathione metabolism in common bean nodules under stress conditions and during natural senescence. Plant Physiol 146:1282–1292
Lu P, Sang WG, Ma KP (2008) Differential responses of the activities of antioxidant enzymes to thermal stresses between two invasive Eupatorium species in China. J Integr Plant Biol 50:393–401
Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59(1):37–49
Malacrida C, Valle E, Boggio S (2006) Post harvest chilling induces oxidative stress response in the dwarf tomato cultivar Micro-Tom. Physiol Plant 127:10–18
Matamoros MA, Moran JF, Iturbe-Ormaetxe I, Rubio MC, Becana M (1999) Glutathione and homoglutathione synthesis in legume root nodules. Plant Physiol 121:879–888
Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia–legume symbiosis. Plant Physiol 133:499–509
Matamoros MA, Loscos J, Dietz K, Aparicio-Tejo PM, Becana M (2010) Function of antioxidant enzymes and metabolites during maturation of pea fruits. J Exp Bot 61:87–97
Meyer AJ, Hell R (2005) Glutathione homeostasis and redox regulation by sulfhydryl groups. Photosynth Res 86:435–457
Mishra A, Prasad K, Rai G (2010) Effect of bio-fertilizer inoculations on growth and yield of dwarf field pea (Pisum sativum L.) in conjunction with different doses of chemical fertilizers. J Agron 9:163–168
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379
Nielsen D (1998) Food analysis. Aspen Publishers, Inc. Gaithersburg, Maryland United State Department of Agriculture Nutrient base
Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. J Exp Bot 53:1283–1304
Palma JM, Jiménez A, Sandalio LM, Corpas FJ, Lundqvist M, Gómez M, Sevilla F, del Río A (2006) Antioxidative enzymes from chloroplasts, mitochondria, and peroxisomes during leaf senescence of nodulated pea plants. J Exp Bot 57:1747–1758
Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. Met Ions Biol Syst 39:31–74
Razaq M, Zhang P, Shen H, Salahuddin (2017) Influence of nitrogen and phosphorous on the growth and root morphology of Acer mono. PLoS ONE 12(2):e0171321. https://doi.org/10.1371/journal.pone.0171321
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 16:1189–1202
Rouached H, Pal S, Rachmilevitch S, Libault M, Tran LP (2015) Plants coping abiotic and biotic stresses: a tale of diligent management. BioMed Research International. https://doi.org/10.1155/2015/754754
Rubio MC, González EM, Minchin FR, Webb KJ, Arrese-Igor C, Ramos J, Becana M (2002) Effects of water stress on antioxidant enzymes of leaves and nodules of transgenic alfalfa overexpressing superoxide dismutases. Physiol Plant 115:531–540
Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012
Soumare A, Diedhiou AG, Thuita M, Hafidi M, Ouhdouch Y, Gopalakrishnan S, Kouisni L (2020) Exploiting biological nitrogen fixation: a route towards a sustainable agriculture. Plants 9(8):1011. https://doi.org/10.3390/plants9081011
Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31:1086–1096
Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984
Voisin AS, Gastal F (2015) In: Schneider A, Huygues C (eds) Les légumineuses pour des systèmes agricoles et alimentaires durables. QUAE Editions, France
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179
Ye XD, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P et al (2000) Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305. https://doi.org/10.1126/science.287.5451.303
Yousuf PY, Hakeem K, Chandna R, Ahmad P (2012) Role of glutathione reductase in plant abiotic stress. In: Ahmad P, MNV P (eds) Abiotic stress responses in plants. Springer, New York, pp 149–158
Acknowledgements
This project was funded by the Deanship of Scientific Research (DSR), King Abdulaziz University, Jeddah, under the grant no. G: 460-130-1440. The authors, therefore, acknowledge with thanks the DSR technical and financial support.
Funding
This project was funded by the Deanship of Scientific Research (DSR) at King Abdulaziz University, Jeddah, under grant no. G: 460-130-1440.
Author information
Authors and Affiliations
Contributions
Khalid Rehman Hakeem and Rouf Ahmad Bhat have designed and performed the experiments. They have also written the original manuscript and analyzed the data. Hesham F. Alharby and Khalid M. Alghamdi have analyzed the data, interpreted the results, and critically edited the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
All authors confirm consent to participate in this journal.
Consent for publication
All authors accept to publishing.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Gangrong Shi
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
Hakeem, .R., Alharby, H.F., Alghamdi, K.M. et al. Antioxidant enzyme responses and metabolite functioning of Pisum sativum L. to sewage sludge in arid and semi-arid environments. Environ Sci Pollut Res 29, 13201–13210 (2022). https://doi.org/10.1007/s11356-021-16620-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16620-5