Synergistic Effect of Melatonin and Lysinibacillus fusiformis L. (PLT16) to Mitigate Drought Stress via Regulation of Hormonal, Antioxidants System, and Physio-Molecular Responses in Soybean Plants
Abstract
:1. Introduction
2. Results
2.1. Isolation, Screening, and Identification
2.2. In Vitro IAA and Organic-Acid Production under PEG Stress
2.3. Isolate PLT16 and Melatonin to Regulate Soybean Growth under Drought Stress
2.4. Isolate PLT16 and Melatonin Scavenge Reactive Oxygen Species (ROS) and Activate Antioxidant Enzymes
2.5. Effects of Isolate PLT16 and Melatonin on Water Status (RWC) and Proline Content under Drought Stress
2.6. Effect of Isolate PLT16 and Melatonin on Phytohormones ABA, JA, and SA
2.7. Effects of Isolate PLT16 and Melatonin on Endo-Melatonin Regulation under Drought Stress
2.8. Effects of PLT16 and Melatonin on Plant Organic Acid and Micronutrient Content under Drought Stress
2.9. Effects of Isolate PLT16 and Melatonin on Transcriptional Regulation under Drought Stress
3. Discussion
4. Materials and Methods
4.1. Isolation, Screening, and Identification
4.2. Determination of In Vitro Phytohormone and Organic-Acid Production
4.3. Plant-Growth Conditions
4.4. Determination of Chlorophyll a and b, Carotenoid, Proline, and RWC (Relative Water Content)
4.5. Determination of H2O2, MDA, and Superoxide-Anion Content
4.6. Quantification of Antioxidant Enzymes and Non-Enzymatic Antioxidant-Activitiy Quantification
4.7. Endogenous Phytohormones ABA, JA, and SA
4.8. Quantification of Endogenous Melatonin
4.9. Determination of Micronutrient Uptake in Plants
4.10. RNA Extraction and Quantitative Real-Time PCR
4.11. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Yang, L.; You, J.; Wang, Y.; Li, J.; Quan, W.; Yin, M.; Wang, Q.; Chan, Z. Systematic analysis of the G-box Factor 14-3-3 gene family and functional characterization of GF14a in Brachypodium distachyon. Plant Physiol. Biochem. 2017, 117, 1–11. [Google Scholar] [CrossRef]
- Alam, M.N.; Wang, Y.; Chan, Z. Physiological and biochemical analyses reveal drought tolerance in cool-season tall fescue (Festuca arundinacea) turf grass with the application of melatonin. Crop Pasture Sci. 2018, 69, 1041–1049. [Google Scholar] [CrossRef]
- Zhou, Y.; Karl, T.; Lewis, D.H.; McGhie, T.K.; Arathoon, S.; Davies, K.M.; Ryan, K.G.; Gould, K.S.; Schwinn, K.E. Production of betacyanins in transgenic Nicotiana tabacum increases tolerance to salinity. Front. Plant Sci. 2021, 12, 653147. [Google Scholar] [CrossRef]
- Rangecroft, S.; Van Loon, A.F.; Maureira, H.; Verbist, K.; Hannah, D.M. An observation-based method to quantify the human influence on hydrological drought: Upstream–downstream comparison. Hydrol. Sci. J. 2019, 64, 276–287. [Google Scholar] [CrossRef]
- Huseynova, I.M.; Rustamova, S.M.; Aliyeva, D.R.; Babayev, H.G.; Aliyev, J.A. Photosynthesis, antioxidant protection, and drought tolerance in plants. In Drought Stress Tolerance in Plants; Springer International Publishing: Cham, Switzerland, 2016; Volume 1, pp. 349–378. [Google Scholar]
- Ashraf, M.; Harris, P. Stress environments and their impact on crop production. In Abiotic Stresses; CRC Press: Boca Raton, FL, USA, 2005; pp. 25–40. [Google Scholar]
- Yin, M.; Wang, Y.; Zhang, L.; Li, J.; Quan, W.; Yang, L.; Wang, Q.; Chan, Z. The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. J. Exp. Bot. 2017, 68, 2991–3005. [Google Scholar] [CrossRef]
- Dong, S.; Jiang, Y.; Dong, Y.; Wang, L.; Wang, W.; Ma, Z.; Yan, C.; Ma, C.; Liu, L. A study on soybean responses to drought stress and rehydration. Saudi J. Biol. Sci. 2019, 26, 2006–2017. [Google Scholar] [CrossRef]
- Ku, Y.-S.; Au-Yeung, W.-K.; Yung, Y.-L.; Li, M.-W.; Wen, C.-Q.; Liu, X.; Lam, H.-M. Drought Stress and Tolerance in Soybean. In A Comprehensive Survey of International Soybean Research—Genetics, Physiology, Agronomy and Nitrogen Relationships; IntechOpen: London, UK, 2013; pp. 209–237. [Google Scholar]
- Sobko, O.; Stahl, A.; Hahn, V.; Zikeli, S.; Claupein, W.; Gruber, S. Environmental effects on soybean (Glycine max (L.) Merr) production in central and South Germany. Agronomy 2020, 10, 1847. [Google Scholar] [CrossRef]
- Cotrim, M.F.; Gava, R.; Campos, C.N.S.; de David, C.H.O.; Reis, I.d.A.; Teodoro, L.P.R.; Teodoro, P.E. Physiological performance of soybean genotypes grown under irrigated and rainfed conditions. J. Agro. Crop Sci. 2021, 207, 34–43. [Google Scholar] [CrossRef]
- Jin, Z.; Zhuang, Q.; Wang, J.; Archontoulis, S.V.; Zobel, Z.; Kotamarthi, V.R. The combined and separate impacts of climate extremes on the current and future US rainfed maize and soybean production under elevated CO2. Glob. Chang. Biol. 2017, 23, 2687–2704. [Google Scholar] [CrossRef]
- Wei, Y.; Jin, J.; Jiang, S.; Ning, S.; Liu, L. Quantitative response of soybean development and yield to drought stress during different growth stages in the Huaibei Plain, China. Agronomy 2018, 8, 97. [Google Scholar] [CrossRef]
- Kumari, B.; Mallick, M.; Solanki, M.K.; Solanki, A.C.; Hora, A.; Guo, W. Plant growth promoting rhizobacteria (PGPR): Modern prospects for sustainable agriculture. In Plant Health Under Biotic Stress; Springer Nature: Singapore, 2019; pp. 109–127. [Google Scholar]
- Takada, K.; Tanaka, N.; Kikuno, H.; Babil, P.; Onjo, M.; Park, B.-J.; Shiwachi, H. Isolation of nitrogen-fixing bacteria from water yam (Dioscorea alata L.). Trop. Agric. Dev. 2019, 63, 198–203. [Google Scholar]
- Yan, X.; Wang, Z.; Mei, Y.; Wang, L.; Wang, X.; Xu, Q.; Peng, S.; Zhou, Y.; Wei, C. Isolation, diversity, and growth-promoting activities of endophytic bacteria from tea cultivars of Zijuan and Yunkang-10. Front. Microbiol. 2018, 9, 1848. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.; Li, X.; Shen, B.; Zhang, Z.; Wang, J.; Shang, X. Bioremediation of lead-contaminated soil by inorganic phosphate-solubilizing bacteria immobilized on biochar. Ecotoxicol. Environ. Saf. 2022, 237, 113524. [Google Scholar] [CrossRef] [PubMed]
- Khan, H.; Akbar, W.A.; Shah, Z.; Rahim, H.U.; Taj, A.; Alatalo, J.M. Coupling phosphate-solubilizing bacteria (PSB) with inorganic phosphorus fertilizer improves mungbean (Vigna radiata) phosphorus acquisition, nitrogen fixation, and yield in alkaline-calcareous soil. Heliyon 2022, 8, e09081. [Google Scholar] [CrossRef] [PubMed]
- Nadal, M.C.; Ferreira, G.M.d.R.; Andrade, G.V.S.; Buttrós, V.H.; Rodrigues, F.A.; da Silva, C.M.; Martins, A.D.; Rufato, L.; Luz, J.M.Q.; Dória, J.; et al. Endophytic Bacteria Can Replace the Need for Synthetic Auxin during In Vitro Rooting of Pyrus communis. Agronomy 2022, 12, 1226. [Google Scholar] [CrossRef]
- Chattopadhyay, P.; Banerjee, G.; Handique, P.J. Use of an abscisic acid-producing Bradyrhizobium japonicum isolate as biocontrol agent against bacterial wilt disease caused by Ralstonia solanacearum. J. Plant Dis. Prot. 2022, 129, 869–879. [Google Scholar] [CrossRef]
- Ashry, N.M.; Alaidaroos, B.A.; Mohamed, S.A.; Badr, O.A.M.; El-Saadony, M.T.; Esmael, A. Utilization of drought-tolerant bacterial strains isolated from harsh soils as a plant growth-promoting rhizobacteria (PGPR). Saudi J. Biol. Sci. 2022, 29, 1760–1769. [Google Scholar] [CrossRef]
- Sun, L.; Zhang, X.; Ouyang, W.; Yang, E.; Cao, Y.; Sun, R. Lowered Cd toxicity, uptake and expression of metal transporter genes in maize plant by ACC deaminase-producing bacteria Achromobacter sp. J. Hazard. Mater. 2022, 423, 127036. [Google Scholar] [CrossRef]
- Alinia, M.; Kazemeini, S.A.; Dadkhodaie, A.; Sepehri, M.; Mahjenabadi, V.A.J.; Amjad, S.F.; Poczai, P.; El-Ghareeb, D.; Bassouny, M.A.; Abdelhafez, A.A. Co-application of ACC deaminase-producing rhizobial bacteria and melatonin improves salt tolerance in common bean (Phaseolus vulgaris L.) through ion homeostasis. Sci. Rep. 2022, 12, 22105. [Google Scholar] [CrossRef]
- Duca, D.R.; Glick, B.R. Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria. Appl. Microbiol. Biotechnol. 2020, 104, 8607–8619. [Google Scholar] [CrossRef]
- Gupta, S.; Pandey, S. ACC deaminase producing bacteria with multifarious plant growth promoting traits alleviates salinity stress in French bean (Phaseolus vulgaris) plants. Front. Microbiol. 2019, 10, 1506. [Google Scholar] [CrossRef] [PubMed]
- Kour, D.; Rana, K.L.; Sheikh, I.; Kumar, V.; Yadav, A.N.; Dhaliwal, H.S.; Saxena, A.K. India Section B: Biological Sciences. Alleviation of drought stress and plant growth promotion by Pseudomonas libanensis EU-LWNA-33, a drought-adaptive phosphorus-solubilizing bacterium. Proc. Natl. Acad. Sci. India Sect. B Boil. Sci. 2020, 90, 785–795. [Google Scholar] [CrossRef]
- Kumar, V.; Joshi, S.; Pant, N.C.; Sangwan, P.; Yadav, A.N.; Saxena, A.; Singh, D. Molecular approaches for combating multiple abiotic stresses in crops of arid and semi-arid region. In Molecular Approaches in Plant Biology and Environmental Challenges; Springer: Berlin/Heidelberg, Germany, 2019; pp. 149–170. [Google Scholar]
- Vejan, P.; Abdullah, R.; Khadiran, T.; Ismail, S.; Nasrulhaq Boyce, A. Role of plant growth promoting rhizobacteria in agricultural sustainability—A review. Molecules 2016, 21, 573. [Google Scholar] [CrossRef] [PubMed]
- Yadav, A.N.; Rastegari, A.A.; Yadav, N. Microbiomes of Extreme Environments: Biodiversity and Biotechnological Applications; CRC Press: Boca Raton, FL, USA, 2021. [Google Scholar]
- Zhang, Y.; Yang, S.; Chen, Y. Effects of melatonin on photosynthetic performance and antioxidants in melon during cold and recovery. Biol. Plant. 2017, 61, 571–578. [Google Scholar] [CrossRef]
- Arnao, M.B.; Hernández-Ruiz, J. Melatonin: Plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 2014, 19, 789–797. [Google Scholar] [CrossRef]
- Arnao, M.B.; Hernández-Ruiz, J. Functions of melatonin in plants: A review. J. Pineal Res. 2015, 59, 133–150. [Google Scholar] [CrossRef]
- Zhang, N.; Sun, Q.; Zhang, H.; Cao, Y.; Weeda, S.; Ren, S.; Guo, Y.-D. Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot. 2015, 66, 647–656. [Google Scholar] [CrossRef]
- Arnao, M.B.; Hernández-Ruiz, J. Melatonin and its relationship to plant hormones. Ann. Bot. 2018, 121, 195–207. [Google Scholar] [CrossRef]
- Wang, Y.; Reiter, R.J.; Chan, Z. Phytomelatonin: A universal abiotic stress regulator. J. Exp. Bot. 2018, 69, 963–974. [Google Scholar] [CrossRef]
- Khan, M.A.; Sahile, A.A.; Jan, R.; Asaf, S.; Hamayun, M.; Imran, M.; Adhikari, A.; Kang, S.-M.; Kim, K.-M.; Lee, I.-J. Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biol. 2021, 21, 176. [Google Scholar] [CrossRef]
- Asif, M.; Pervez, A.; Ahmad, R. Role of melatonin and plant-growth-promoting rhizobacteria in the growth and development of plants. CLEAN Soil Air Water 2019, 47, 1800459. [Google Scholar] [CrossRef]
- Li, J.; Yang, Y.; Sun, K.; Chen, Y.; Chen, X.; Li, X. Exogenous melatonin enhances cold, salt and drought stress tolerance by improving antioxidant defense in tea plant (Camellia sinensis (L.) O. Kuntze). Molecules 2019, 24, 1826. [Google Scholar] [CrossRef]
- Khalilpour, M.; Mozafari, V.; Abbaszadeh-Dahaji, P. Tolerance to salinity and drought stresses in pistachio (Pistacia vera L.) seedlings inoculated with indigenous stress-tolerant PGPR isolates. Sci. Hortic. 2021, 289, 110440. [Google Scholar] [CrossRef]
- Li, C.; Tan, D.-X.; Liang, D.; Chang, C.; Jia, D.; Ma, F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. J. Exp. Bot. 2015, 66, 669–680. [Google Scholar] [CrossRef] [PubMed]
- Jiang, M.; Zhang, J. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 2002, 53, 2401–2410. [Google Scholar] [CrossRef]
- Manjunatha, B.S.; Nivetha, N.; Krishna, G.K.; Elangovan, A.; Pushkar, S.; Chandrashekar, N.; Aggarwal, C.; Asha, A.D.; Chinnusamy, V.; Raipuria, R.K.; et al. Plant growth-promoting rhizobacteria Shewanella putrefaciens and Cronobacter dublinensis enhance drought tolerance of pearl millet by modulating hormones and stress-responsive genes. Physiol. Plant. 2022, 174, e13676. [Google Scholar] [CrossRef]
- Wang, X.-R.; Wang, Y.-H.; Jia, M.; Zhang, R.-R.; Liu, H.; Xu, Z.-S.; Xiong, A.-S. The phytochrome-interacting factor DcPIF3 of carrot plays a positive role in drought stress by increasing endogenous ABA level in Arabidopsis. Plant Sci. 2022, 322, 111367. [Google Scholar] [CrossRef]
- Li, R.; Yang, R.; Zheng, W.; Wu, L.; Zhang, C.; Zhang, H. Melatonin Promotes SGT1-Involved Signals to Ameliorate Drought Stress Adaption in Rice. Int. J. Mol. Sci. 2022, 23, 599. [Google Scholar] [CrossRef]
- Chai, M.; Fan, R.; Huang, Y.; Jiang, X.; Wai, M.H.; Yang, Q.; Su, H.; Liu, K.; Ma, S.; Chen, Z.; et al. GmbZIP152, a Soybean bZIP Transcription Factor, Confers Multiple Biotic and Abiotic Stress Responses in Plant. Int. J. Mol. Sci. 2022, 23, 10935. [Google Scholar] [CrossRef]
- Aihebaier, S.; Muhammad, T.; Wei, A.; Mamat, A.; Abuduaini, M.; Pataer, P.; Yigaimu, A.; Yimit, A. Membrane-Protected Molecularly Imprinted Polymer for the Microextraction of Indole-3-butyric Acid in Mung Bean Sprouts. ACS Omega 2019, 4, 16789–16793. [Google Scholar] [CrossRef]
- Mukherjee, A.; Lal, R.; Zimmerman, A. Effects of biochar and other amendments on the physical properties and greenhouse gas emissions of an artificially degraded soil. Sci. Total. Environ. 2014, 487, 26–36. [Google Scholar] [CrossRef] [PubMed]
- Gao, Q.-H.; Wu, C.-S.; Wang, M.; Xu, B.-N.; Du, L.-J. Effect of drying of jujubes (Ziziphus jujuba Mill.) on the contents of sugars, organic acids, α-tocopherol, β-carotene, and phenolic compounds. J. Agric. Food Chem. 2012, 60, 9642–9648. [Google Scholar] [CrossRef] [PubMed]
- Ashrafi, M.; Azimi-Moqadam, M.-R.; Moradi, P.; MohseniFard, E.; Shekari, F.; Kompany-Zareh, M. Effect of drought stress on metabolite adjustments in drought tolerant and sensitive thyme. Plant Physiol. Biochem. 2018, 132, 391–399. [Google Scholar] [CrossRef] [PubMed]
- Dimkpa, C.O.; Bindraban, P.S.; Fugice, J.; Agyin-Birikorang, S.; Singh, U.; Hellums, D. Composite micronutrient nanoparticles and salts decrease drought stress in soybean. Agron. Sustain. Dev. 2017, 37, 5. [Google Scholar] [CrossRef]
- Panchal, P.; Miller, A.J.; Giri, J. Organic acids: Versatile stress-response roles in plants. J. Exp. Bot. 2021, 72, 4038–4052. [Google Scholar] [CrossRef]
- Igamberdiev, A.U.; Eprintsev, A.T. Organic acids: The pools of fixed carbon involved in redox regulation and energy balance in higher plants. Front. Plant Sci. 2016, 7, 1042. [Google Scholar] [CrossRef]
- Shahbaz, A.M.; Oki, Y.; Adachi, T.; Murata, Y.; Khan, M.H.R. Phosphorus starvation induced root-mediated pH changes in solublization and acquisition of sparingly soluble P sources and organic acids exudation by Brassica cultivars. Soil Sci. Plant Nutr. 2006, 52, 623–633. [Google Scholar] [CrossRef]
- Kim, J.-M.; To, T.K.; Matsui, A.; Tanoi, K.; Kobayashi, N.I.; Matsuda, F.; Habu, Y.; Ogawa, D.; Sakamoto, T.; Matsunaga, S. Acetate-mediated novel survival strategy against drought in plants. Nat. Plants 2017, 3, 17119. [Google Scholar] [CrossRef]
- Maruyama, K.; Todaka, D.; Mizoi, J.; Yoshida, T.; Kidokoro, S.; Matsukura, S.; Takasaki, H.; Sakurai, T.; Yamamoto, Y.Y.; Yoshiwara, K.; et al. Identification of cis-acting promoter elements in cold-and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res. 2012, 19, 37–49. [Google Scholar] [CrossRef]
- Kim, J.-S.; Mizoi, J.; Yoshida, T.; Fujita, Y.; Nakajima, J.; Ohori, T.; Todaka, D.; Nakashima, K.; Hirayama, T.; Shinozaki, K.; et al. An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol. 2011, 52, 2136–2146. [Google Scholar] [CrossRef]
- Nakashima, K.; Kiyosue, T.; Yamaguchi-Shinozaki, K.; Shinozaki, K. A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J. 1997, 12, 851–861. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Yu, T.-F.; Ma, J.; Chen, J.; Zhou, Y.-B.; Chen, M.; Ma, Y.-Z.; Wei, W.-L.; Xu, Z.-S. The soybean bZIP transcription factor gene GmbZIP2 confers drought and salt resistances in transgenic plants. Int. J. Mol. Sci. 2020, 21, 670. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.; Su, X.; Chen, Y.; Fan, X.; He, L.; Guo, J.; Wang, Y.; Yang, Q. Melatonin improves drought resistance in maize seedlings by enhancing the antioxidant system and regulating abscisic acid metabolism to maintain stomatal opening under PEG-induced drought. J. Plant Biol. 2021, 64, 299–312. [Google Scholar] [CrossRef]
- Sharma, A.; Wang, J.; Xu, D.; Tao, S.; Chong, S.; Yan, D.; Li, Z.; Yuan, H.; Zheng, B. Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Sci. Total Environ. 2020, 713, 136675. [Google Scholar] [CrossRef] [PubMed]
- Glickmann, E.; Dessaux, Y. A critical examination of the specificity of the salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 1995, 61, 793–796. [Google Scholar] [CrossRef]
- Kim, Y.-N.; Khan, M.A.; Kang, S.-M.; Hamayun, M.; Lee, I.-J. Enhancement of drought-stress tolerance of Brassica oleracea var. italica L. by newly isolated Variovorax sp. YNA59. J. Microbiol. Biotechnol. 2020, 30, 1500–1509. [Google Scholar] [CrossRef]
- Schwyn, B.; Neilands, J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987, 160, 47–56. [Google Scholar] [CrossRef]
- Khan, A.L.; Halo, B.A.; Elyassi, A.; Ali, S.; Al-Hosni, K.; Hussain, J.; Al-Harrasi, A.; Lee, I.-J. Indole acetic acid and ACC deaminase from endophytic bacteria improves the growth of Solanum lycopersicum. Electron. J. Biotechnol. 2016, 21, 58–64. [Google Scholar] [CrossRef]
- Bilal, S.; Khan, A.; Imran, M.; Khan, A.L.; Asaf, S.; Al-Rawahi, A.; Al-Azri, M.S.A.; Al-Harrasi, A.; Lee, I.-J. Silicon-and Boron-Induced Physio-Biochemical Alteration and Organic Acid Regulation Mitigates Aluminum Phytotoxicity in Date Palm Seedlings. Antioxidants 2022, 11, 1063. [Google Scholar] [CrossRef]
- Imran, M.; Shazad, R.; Bilal, S.; Imran, Q.M.; Khan, M.; Kang, S.-M.; Khan, A.L.; Yun, B.-W.; Lee, I.-J. Exogenous Melatonin mediates the regulation of endogenous nitric oxide in Glycine max L. to reduce effects of drought stress. Environ. Exp. Bot. 2021, 188, 104511. [Google Scholar] [CrossRef]
- Lichtenthaler, H.K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. In Methods in Enzymology; Elsevier: Amsterdam, The Netherlands, 1987; Volume 148, pp. 350–382. [Google Scholar]
- Cawley, S.; Bekiranov, S.; Ng, H.H.; Kapranov, P.; Sekinger, E.A.; Kampa, D.; Piccolboni, A.; Sementchenko, V.; Cheng, J.; Williams, A.J.; et al. Unbiased Mapping of Transcription Factor Binding Sites along Human Chromosomes 21 and 22 Points to Widespread Regulation of Noncoding RNAs. Cell 2004, 116, 499–509. [Google Scholar] [CrossRef] [PubMed]
- Tiwari, J.K.; Munshi, A.D.; Kumar, R.; Pandey, R.N.; Arora, A.; Bhat, J.S.; Sureja, A.K. Effect of salt stress on cucumber: Na+–K+ ratio, osmolyte concentration, phenols and chlorophyll content. Acta Physiol. Plant. 2010, 32, 103–114. [Google Scholar] [CrossRef]
- Velikova, V.; Yordanov, I.; Edreva, A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Sci. 2000, 151, 59–66. [Google Scholar] [CrossRef]
- Huang, B.; Chen, Y.-E.; Zhao, Y.-Q.; Ding, C.-B.; Liao, J.-Q.; Hu, C.; Zhou, L.-J.; Zhang, Z.-W.; Yuan, S.; Yuan, M. Exogenous melatonin alleviates oxidative damages and protects photosystem II in maize seedlings under drought stress. Front. Plant Sci. 2019, 10, 677. [Google Scholar] [CrossRef] [PubMed]
- Halo, B.A.; Khan, A.L.; Waqas, M.; Al-Harrasi, A.; Hussain, J.; Ali, L.; Adnan, M.; Lee, I.-J. Endophytic bacteria (Sphingomonas sp. LK11) and gibberellin can improve Solanum lycopersicum growth and oxidative stress under salinity. J. Plant Interact. 2015, 10, 117–125. [Google Scholar] [CrossRef]
- Nakano, Y.; Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22, 867–880. [Google Scholar]
- Giannopolitis, C.N.; Ries, S.K. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 1977, 59, 309–314. [Google Scholar] [CrossRef]
- Zhang, J.; Kirkham, M. Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol. 1994, 35, 785–791. [Google Scholar] [CrossRef]
- Asaf, S.; Khan, A.L.; Khan, M.A.; Imran, Q.M.; Yun, B.-W.; Lee, I.-J. Osmoprotective functions conferred to soybean plants via inoculation with Sphingomonas sp. LK11 and exogenous trehalose. Microbiol. Res. 2017, 205, 135–145. [Google Scholar] [CrossRef]
- Qi, Q.; Rose, P.A.; Abrams, G.D.; Taylor, D.C.; Abrams, S.R.; Cutler, A.J. (+)-Abscisic acid metabolism, 3-ketoacyl-coenzyme A synthase gene expression, and very-long-chain monounsaturated fatty acid biosynthesis in Brassica napus embryos. Plant Physiol. 1998, 117, 979–987. [Google Scholar] [CrossRef]
- Kim, Y.-H.; Hwang, S.-J.; Waqas, M.; Khan, A.; Lee, J.-H.; Lee, J.-D.; Nguyen, H.; Lee, I.-J. Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front. Plant Sci. 2015, 6, 714. [Google Scholar] [CrossRef] [PubMed]
- Antoniou, C.; Chatzimichail, G.; Xenofontos, R.; Pavlou, J.J.; Panagiotou, E.; Christou, A.; Fotopoulos, V. Melatonin systemically ameliorates drought stress-induced damage in M edicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J. Pineal Res. 2017, 62, e12401. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Shi, Y.; Zhang, X.; Du, H.; Xu, B.; Huang, B. Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ. Exp. Bot. 2017, 138, 36–45. [Google Scholar] [CrossRef]
- Kang, S.-M.; Waqas, M.; Shahzad, R.; You, Y.-H.; Asaf, S.; Khan, M.A.; Lee, K.-E.; Joo, G.-J.; Kim, S.-J.; Lee, I.-J. Isolation and characterization of a novel silicate-solubilizing bacterial strain Burkholderia eburnea CS4-2 that promotes growth of japonica rice (Oryza sativa L. cv. Dongjin). Soil Sci. Plant Nutr. 2017, 63, 233–241. [Google Scholar]
- Khan, M.; Imran, Q.M.; Shahid, M.; Mun, B.-G.; Lee, S.-U.; Khan, M.A.; Hussain, A.; Lee, I.-J.; Yun, B.-W. Nitric oxide-induced AtAO3 differentially regulates plant defense and drought tolerance in Arabidopsis thaliana. BMC Plant Biol. 2019, 19, 602–619. [Google Scholar] [CrossRef] [PubMed]
- Chan, C.-X.; Teo, S.-S.; Ho, C.-L.; Othman, R.Y.; Phang, S.-M. Optimisation of RNA extraction from Gracilaria changii (Gracilariales, Rhodophyta). J. Appl. Phycol. 2004, 16, 297–301. [Google Scholar] [CrossRef]
Treatment | SL (cm) | RL (cm) | FW (g) | DW (g) | Total Chl (mg/g−1 DW) |
---|---|---|---|---|---|
Control (normal condition) | |||||
Cont | 18.5 ± 0.21 b | 17.8 ± 0.31 c | 8.7 ± 0.14 c | 5.8 ± 0.13 c | 35.2 ± 0.28 c |
MET | 19.2 ± 0.25 b | 20.2 ± 0.27 b | 10.2 ± 0.14 b | 7.1 ± 0.14 b | 39.4 ± 0.41 b |
PLT16 | 19.0 ± 0.21 b | 19.5 ± 0.21 b | 10.7 ± 0.16 b | 7.6 ± 0.14 b | 38.7 ± 0.34 b |
MET/PLT16 | 21.5 ± 0.33 a | 23.5 ± 0.35 a | 12.8 ± 0.21 a | 8.9 ± 0.17 a | 43.8 ± 0.51 a |
Drought | |||||
Cont | 11.2 ± 0.15 e | 12.6 ± 0.19 e | 6.02 ± 0.1 e | 3.1 ± 0.12 e | 20.2 ± 0.31 f |
MET | 14.0 ± 0.21 d | 15.6 ± 0.24 d | 7.3 ± 0.22 d | 4.3 ± 0.15 d | 28.0 ± 0.0.23 e |
PLT16 | 14.2 ± 0.22 d | 15.3 ± 0.25 d | 7.1 ± 0.14 d | 4.1 ± 0.15 d | 26.5 ± 0.28 e |
MET/PLT16 | 16.5 ± 0.24 c | 17.0 ± 0.21 c | 8.5 ± 0.16 c | 5.2 ± 0.15 c | 32.4 ± 0.34 d |
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Imran, M.; Mpovo, C.L.; Aaqil Khan, M.; Shaffique, S.; Ninson, D.; Bilal, S.; Khan, M.; Kwon, E.-H.; Kang, S.-M.; Yun, B.-W.; et al. Synergistic Effect of Melatonin and Lysinibacillus fusiformis L. (PLT16) to Mitigate Drought Stress via Regulation of Hormonal, Antioxidants System, and Physio-Molecular Responses in Soybean Plants. Int. J. Mol. Sci. 2023, 24, 8489. https://doi.org/10.3390/ijms24108489
Imran M, Mpovo CL, Aaqil Khan M, Shaffique S, Ninson D, Bilal S, Khan M, Kwon E-H, Kang S-M, Yun B-W, et al. Synergistic Effect of Melatonin and Lysinibacillus fusiformis L. (PLT16) to Mitigate Drought Stress via Regulation of Hormonal, Antioxidants System, and Physio-Molecular Responses in Soybean Plants. International Journal of Molecular Sciences. 2023; 24(10):8489. https://doi.org/10.3390/ijms24108489
Chicago/Turabian StyleImran, Muhammad, Clems Luzolo Mpovo, Muhammad Aaqil Khan, Shifa Shaffique, Daniel Ninson, Saqib Bilal, Murtaza Khan, Eun-Hae Kwon, Sang-Mo Kang, Byung-Wook Yun, and et al. 2023. "Synergistic Effect of Melatonin and Lysinibacillus fusiformis L. (PLT16) to Mitigate Drought Stress via Regulation of Hormonal, Antioxidants System, and Physio-Molecular Responses in Soybean Plants" International Journal of Molecular Sciences 24, no. 10: 8489. https://doi.org/10.3390/ijms24108489