Abstract
Intensive cultivation increases the salinity and alkalinity of soil leading to its degradation. Such soil lead to abiotic stress conditions in plants causing ROS-mediated cellular damage. Microbes constitute an important group of bio-stimulants, which are promising alternatives to reduce ROS-mediated abiotic stresses and improve plant growth. In the present study synergistic activity of stress-tolerant Trichoderma koningiopsis NBRI-PR5 (MTCC 25372) and T. asperellum NBRI-K14 (MTCC 25373) (TrichoMix) was assessed in paddy crop under salt stress conditions. Improved soil microbial biomass carbon (MBC), total organic carbon (TOC), and available nutrients N/P/K by 2–3 folds was observed in the pot experiment using the TrichoMix. It restored the heterogeneous microbial population of the paddy rhizosphere during salt stress and modulated the soil enzyme activities. The anatomical distortions in rice roots due to salt stress were stabilized in presence of the TrichoMix. Different stress marker genes (OsMAPK5, OsAPX, OsGST, OsUSP, OsBADH, OsLYSO, OsNRAMP6, and OsBz8) were differentially modulated by the TrichoMix in presence of salt stress as compared to the control. The TrichoMix increased the yield by 10% in marginally stressed fields; however, it enhanced the yield by approximately 60% when used with the 50% recommended dose of NPK. In the integrated treatment, Fe and Zn were fortified by approximately 40% and 29% respectively in the grains. From the present study, it was concluded that the TrichoMix stimulated the rice plants to accumulate osmoprotectants, improved the anatomical features, modulated the plant defense system, and improved the grain yield and quality. Therefore, the NBRI-PR5 and NBRI-K14 mixture may be used as a bio-stimulant to increase productivity in the rapidly deteriorating soil and reduce the NPK inputs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References:
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Agarwal P, Singh PC, Chaudhry V, Shirke PA, Chakrabarty D, Farooqui A, Nautiyal CS, Sane AP, Sane VA (2019) PGPR-induced OsASR6 improves plant growth and yield by altering root auxin sensitivity and the xylem structure in transgenic Arabidopsis thaliana. J Plant Physiol 240:153010. https://doi.org/10.1016/j.jplph.2019.153010
Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal R (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. https://doi.org/10.1007/s12298-017-0462-7
Ahmed S, Heo TY, Roy Choudhury A, Walitang DI, Choi J, Sa T (2021) Accumulation of compatible solutes in rice (Oryza sativa L.) cultivars by inoculation of endophytic plant growth promoting bacteria to alleviate salt stress. App Biol Chem 64(1):1–14
Ainsworth EA, Gillespie KM (2007) Nature protocols 2(4):875–7. https://doi.org/10.1038/nprot.2007.101
Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry (No. 631.46 M592ma). Academic Press. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. https://doi.org/10.1038/nprot.2007.102
Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol 8:971. https://doi.org/10.3389/fmicb.2017.00971
Berg G, Alavi M, Schmidt CS, Zachow C, Egamberdieva D, Kamilova F, Lugtenberg B (2013) Biocontrol and osmoprotectants for plants under salinated conditions. Mol Microbial Ecol Rhizosphere 1:561–573
Blake GR (1965) Bulk density. Methods of soil analysis: part 1 physical and mineralogical properties. Stat Meas Sampl 9:374–390. https://doi.org/10.2134/agronmonogr9.1.c30
Bremner JM (1965) Total nitrogen. Methods of soil analysis: part 2. Chemical and Microbiological Properties. J Res 9:1149–1178. https://doi.org/10.2134/agronmonogr9.2.c32
Bruuinsma J (1963) The quantitative analysis of chlorophylls a and b in plant extracts. Photochem Photobiol 2(2):241–249. https://doi.org/10.1111/j.1751-1097.1963.tb08220.x
Carillo P, Woo SL, Comite E, El-Nakhel A, Rouphael Y, Fusco GM, Vinale F (2020) Application of Trichoderma harzianum, 6-pentyl-α-pyrone and plant biopolymer formulations modulate plant metabolism and fruit quality of plum tomatoes. Plants 9(6):771. https://doi.org/10.3390/plants9060771
Chauhan PS, Lata C, Tiwari S, Chauhan AS, Mishra SK, Agrawal L, Chakrabarty D, Nautiyal CS (2019) Transcriptional alterations reveal Bacillus amyloliquefaciens-rice cooperation under salt stress. Sci Rep 9(1):1–3. https://doi.org/10.1038/s41598-019-48309-8
Chen J, Sun X, Zheng J, Zhang X, Liu X, Bian R, Li L, Cheng K, Zheng J, Pan G (2018) Biochar amendment changes temperature sensitivity of soil respiration and composition of microbial communities 3 years after incorporation in an organic carbon-poor dry cropland soil. Biol Fertil Soils 54(2):175–188. https://doi.org/10.1007/s00374-017-1253-6
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analyt Chem 28(3):350–356. https://doi.org/10.1021/ac60111a017
Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20(5):601–606. https://doi.org/10.1016/0038-0717(88)90141-1
Elad Y, Chet I (1983) Improved selective media for isolation of Trichoderma spp. or Fusarium spp. Phytoparasitica 11(1):55. https://doi.org/10.1007/BF02980712
Fiorentino N, Ventorino V, Woo SL, Pepe O, De Rosa A, Gioia L, Romano I, Lombardi N, Napolitano M, Colla G, Rouphael Y (2018) Trichoderma-based bio stimulants modulate rhizosphere microbial populations and improve N uptake efficiency, yield, and nutritional quality of leafy vegetables. Front Plant Sci 9:743. https://doi.org/10.3389/fpls.2018.00743
Grieve CM, Grattan SR (1983) Rapid assay for determination of water-soluble quaternary ammonium compounds. Plant Soil 70(2):303–307. https://doi.org/10.1007/BF02374789
Hashem A, AbdAllah EF, Alqarawi A, Al Huqail A, Egamberdieva D (2014) Alleviation of abiotic salt stress in Ochradenus baccatus (Del.) by Trichoderma hamatum (Bonord.) Bainier. J Plant Interact 9(1):857–868. https://doi.org/10.1080/17429145.2014.983568
Hemeda HM, Klein BP (1990) Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. J Food Sci 55(1):184–185. https://doi.org/10.1111/j.1365-2621.1990.tb06048.x
Jaemsaeng R, Jantasuriyarat C, Thamchaipenet A (2018) Molecular interaction of 1-aminocyclopropane-1-carboxylate deaminase (ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards salt-stress resistance of Oryza sativa L. cv. KDML105. Sci Rep 8(1):1–15. https://doi.org/10.1038/s41598-018-19799-9
Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30(5):435–458. https://doi.org/10.1080/07352689.2011.605739
Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48(1):1–13. https://doi.org/10.1016/j.femsec.2003.11.012
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6(1):68–72. https://doi.org/10.1007/BF00257924
Kaur J, Anand V, Srivastava S, Bist V, Tripathi P, Naseem M, Nand S, Khare P, Srivastava PK, Bisht S, Srivastava S (2020) Yeast strain Debaryomyces hansenii for amelioration of arsenic stress in rice. Ecotoxicol Environ Saf 95:110480. https://doi.org/10.1016/j.ecoenv.2020.110480
Kumar P, Sharma PK (2020) Soil salinity and food Security in India. Front Sustain Food Syst 4:174. https://doi.org/10.3389/fsufs.2020.533781
Kumar K, Manigundan K, Amaresan N (2017) Influence of salt tolerant Trichoderma spp. on growth of maize (Zea mays) under different salinity conditions. J Basic Microbiol 57(2):141–150. https://doi.org/10.1002/jobm.201600369
Ladd JN, Butler JHA (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4(1):19–30. https://doi.org/10.1016/0038-0717(72)90038-7
Lakhdar A, Rabhi M, Ghnaya T, Montemurro F, Jedidi N, Abdelly C (2009) Effectiveness of compost use in salt-affected soil. J Hazard Mater 171(1–3):29–37. https://doi.org/10.1016/j.jhazmat.2009.05.132
Li LY, WM, and Wang W, (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63(1–3):378–384. https://doi.org/10.1016/j.envexpbot.2007.11.016
Liang Y, Yang Y, Yang C, Shen Q, Zhou J, Yang L (2003) Soil enzymatic activity and growth of rice and barley as influenced by organic manure in an anthropogenic soil. Geoderma 115(1–2):149–160. https://doi.org/10.1016/S0016-7061(03)00084-3
Liao W, Ning Z, Chen L, Wei Q, Yuan E, Yang J, Ren J (2014) Intracellular antioxidant detoxifying effects of diosmetin on 2, 2-azobis (2-amidinopropane) dihydrochloride (AAPH)-induced oxidative stress through inhibition of reactive oxygen species generation. J Agric Food Chem 62(34):8648–8654. https://doi.org/10.1021/jf502359x
Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulture 3(2):30. https://doi.org/10.3390/horticulturae3020030
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Mohammadi M, Kazemi H (2002) Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium gramine arum and induced resistance. Plant Sci 162(4):491–498. https://doi.org/10.1016/S0168-9452(01)00538-6
Naik SK, Maurya S, Kumar R, Sadhna K, Gagrai S, Das B, Kumar S, Bhatt BP (2013) Inorganic phosphate solubilization by phosphate solubilizing fungi isolated from acidic soils. Afr J Microbiol Res 7(34):4310–4316. https://doi.org/10.5897/AJMR2013.5947
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate (No. 939). US Department of Agriculture
Per TS, Khan NA, Reddy PS, Masood A, Khan HM (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140. https://doi.org/10.1016/j.plaphy.2017.03.018
Reyt G, Ramakrishna P, Salas-González I, Fujita S, Love A, Tiemessen D, Lapierre C, Morreel K, Calvo-Polanco M, Flis P, Geldner N (2021) Two chemically distinct root lignin barriers control solute and water balance. Nat Commun 12(1):1–15. https://doi.org/10.1038/s41467-021-22550-0
Rouphael Y, Carillo P, Colla G, Fiorentino N, Sabatino L, El-Nakhel C, Giordano M, Pannico A, Cirillo V, Shabani E, Cozzolino E (2020) Appraisal of combined applications of Trichoderma virens and a biopolymer-based bio stimulant on lettuce agronomical, physiological, and qualitative properties under variable N regimes. Agronomy 10(2):196. https://doi.org/10.3390/agronomy10020196
Schmidt A, Kunert KJ (1986) Lipid peroxidation in higher plants: the role of glutathione reductase. Plant Physiol 2(3):700–702. https://doi.org/10.1104/pp.82.3.700
Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409(12):2430–2442. https://doi.org/10.1016/j.scitotenv.2011.03.002
Srivastava S, Srivastava S, Bist V, Awasthi S, Chauhan R, Chaudhry V, Singh PC, Dwivedi S, Niranjan A, Agrawal L, Chauhan PS (2018) Chlorella vulgaris and Pseudomonas putida interaction modulates phosphate trafficking for reduced arsenic uptake in rice (Oryza sativa L.). J Hazard Mater 351:177–187. https://doi.org/10.1016/j.jhazmat.2018.02.039
Stubberfield LCF, Shaw PJA (1990) A comparison of tetrazolium reduction and FDA hydrolysis with other measures of microbial activity. J Microbiol Methods 12(3–4):151–162. https://doi.org/10.1016/0167-7012(90)90026-3
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1(4):301–307. https://doi.org/10.1016/0038-0717(69)90012-1
Tandon A, Fatima T, Gautam A, Yadav U, Srivastava S, Singh PC (2018) Effect of Trichoderma koningiopsis on chickpea rhizosphere activities under different fertilization regimes. Open J Soil Sci 8(10):261
Tandon A, Fatima T, Shukla D, Tripathi P, Srivastava S, Singh PC (2020) Phosphate solubilization by Trichoderma koningiopsis (NBRI-PR5) under abiotic stress conditions. J King Saud Univ Sci 32(1):791–798. https://doi.org/10.1016/j.jksus.2019.02.001
Tandon A, Anshu A, Kumar S, Yadav U, Mishra SK, Srivastava S, Chauhan PS, Srivastava PK, Bahadur L, Shirke PA, Srivastava M et al (2022) Trichoderma-primed rice straw alters structural and functional properties of sodic soil. Land Degrad Dev 33(5):698–709. https://doi.org/10.1002/ldr.4151
Teulat B, Zoumarou-Wallis N, Rotter B, Salem MB, Bahri H, This D (2003) QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theor Appl Genet 108(1):181–188. https://doi.org/10.1007/s00122-003-1417-7
Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicerarietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j.plaphy.2015.11.001
Tiwari P, Srivastava D, Chauhan AS, Indoliya Y, Singh PK, Tiwari S, Fatima T, Mishra SK, Dwivedi S, Agarwal L, Singh PC et al (2021) Root system architecture, physiological analysis and dynamic transcriptomics unravel the drought-responsive traits in rice genotypes. Ecotoxicol Environ Saf 207:111252. https://doi.org/10.1016/j.ecoenv.2020.111252
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37(1):29–38
Yanai J, Nakata S, Funakawa S, Nawata E, Katawatin R, Kosaki T (2010) Effect of NPK application on growth, yield and nutrient uptake by sugarcane on a sandy soil in Northeast Thailand. Trop Agric Dev 54(4):113–118
Yin A, Zhang M, Gao C, Yang X, Xu Y, Wu P, Zhang H (2016) Salinity evolution of coastal soils following reclamation and intensive usage, Eastern China. Environ Earth Sci 5(18):1–1. https://doi.org/10.1007/s12665-016-6095-2
Zhang F, Wang Y, Liu C, Chen F, Ge H, Tian F, Zhang Y (2019) Trichoderma harzianum mitigates salt stress in cucumber via multiple responses. Ecotoxicol Environ Saf 170:436–445. https://doi.org/10.1016/j.ecoenv.2018.11.084
Zhu J, Brown KM, Lynch JP (2010) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ 3(5):740–749. https://doi.org/10.1111/j.1365-3040.2009.02099.x
Acknowledgements
We thank Director, CSIR-NBRI, for his support and providing the necessary facilities at the institute. This study was financially supported by Council of Scientific & Industrial Research funded project, MLP-49 and Department of Science &Technology funded project (DST-SEED), GAP-3487. UY and IV acknowledge AcSIR and fellowship from UGC, PA acknowledges DST-SEED for fellowship.
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.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Anshu, A., Agarwal, P., Mishra, K. et al. Synergistic action of Trichoderma koningiopsis and T. asperellum mitigates salt stress in paddy. Physiol Mol Biol Plants 28, 987–1004 (2022). https://doi.org/10.1007/s12298-022-01192-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-022-01192-6