Abstract
Salinity harms crop productivity; thereby, the management of salt-affected soils is a prerequisite to obtaining optimum crop yields and achieving UN-SDGs. The application of bio-organic amendments is an eco-friendly and cost-effective technique for the management of salt-affected soils. Therefore, this study examined the effect of salt-tolerant Bacillus subtilis strain Y16 and biogas slurry (BGS) on growth, physiology, and yield of sunflower under salt-affected soil conditions. Three levels of soil salinity (original electrical conductivity (EC): 3 dS m−1; induced EC: 6 dS m−1 and 8 dS m−1) were evaluated against three levels of BGS (0 kg ha−1, 600 kg ha−1, and 800 kg ha−1) with and without bacterial inoculation. Soil salinity (EC = 8 dS m−1) significantly (P < 0.05) increased Na+ contents (86%), which significantly (P < 0.05) reduced growth (17–56%), physiology (39–53%), and yield (58%) of sunflower. However, the combined application of BGS and B. subtilis alleviated salt stress and significantly (P < 0.05) improved sunflower growth (11–179%), physiology (10–84%), and yield (106%). The correlation analysis showed the superiority of B. subtilis for inducing salt-stress tolerance in sunflower as compared to BGS through homeostasis of K+/Na+ ratio. The tolerance indices and heat map analysis revealed an increased salt-stress tolerance in sunflower by the synergistic application of BGS and B. subtilis at original (3 dS m−1) and induced (6 dS m−1) soil salinity. Based on the results, we conclude that the combined application of B. subtilis and BGS enhanced growth and yield of sunflower by improving physiological processes and adjustment of K+/Na+ ratio in shoot under moderate salt-stress soil conditions.
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10 May 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11356-021-14344-0
References
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria. J King Saud Uni Sci 26:1–20
Ahmad I, Akhtar MJ, Zahir ZA, Mitter B (2015) Organic amendments: effects on cereals growth and cadmium remediation. Int J Environ Sci Technol 12:2919–2928
Ahmad I, Akhtar MJ, Zakir A, Hussain MB, Khaliq A, Saeed MF, Farooqi MA, Ahmed N (2020) Co-inoculation of biogas slurry and Bacillus strain CIK-515 in improving nutrient concentration and yield of potato (Solanum tuberosum). Pak J Bot. https://doi.org/10.30848/PJB2020-4(45)
Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front Plant Sci 7:2035. https://doi.org/10.3389/fpls.2016.02035
Ashraf M, Shahzad SM, Imtiaz M, Rizwan MS, Iqbal MM (2017) Ameliorative effects of potassium nutrition on yield and fiber quality characteristics of cotton (Gossypium hirsutum L.) under NaCl stress. Soil Environ 36:51–58
Aziz A, Ashraf M, Sikandar S, Asif M, Akhtar N, Shahzad SM, Wasaya A, Ali R, Babar BH (2019) Optimizing sulfur for improving salt tolerance of sunflower (Helianthus annuus L.). Soil Environ 38:222–233
Bhat MA, Kumar V, Bhat MA, Wani IA, Dar FL, Farooq I, Bhatti F, Koser R, Rahman S, Jan AT (2020) Mechanistic insights of the interaction of plant growth promoting rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front Microbiol 11:1952. https://doi.org/10.3389/fmicb.2020.01952
Egamberdieva D, Wirth S, Kimura SDB, Mishra J, Arora NK (2019) Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol 10:2791. https://doi.org/10.3389/fmicb.2019.02791
Gao C, El-Sawah AM, Ali DFI, Hamoud YA, Shaghaleh H, Sheteiwy MS (2020) The integration of bio and organic fertilizers improve plant growth, grain yield, quality and metabolism of hybrid maize (Zea mays L.). Agronomy 10: 319. https://doi.org/10.3390/agronomy10030319
Hafeez A, Arshad-Ullah M, Rasheed M, Mahmood IA, Hyder SI, Aamir SS, Shaaban M, Mahmood T (2017) Effect of soil salinity on germination and growth of sunflower (Helianthus annuus L.) cultivars. J Innov Bio-Res 1:46–51
Hussain A, Zahir ZA, Ditta A, Tahir MU, Ahmad M, Mumtaz MZ, Hayat K, Hussain S (2020) Production and implication of bio-activated organic fertilizer enriched with zinc-solubilizing bacteria to boost up maize (Zea mays L.) production and biofortification under two cropping seasons. Agronomy 10(39). https://doi.org/10.3390/agronomy10010039
Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front Plant Sci 8:1768. https://doi.org/10.3389/fpls.2017.01768
Jabeen N, Ahmad R (2017) Growth response and nitrogen metabolism of sunflower (Helianthus annuus L.) to vermicompost and biogas slurry under salinity stress. J Plant Nutr 40:104–114
Jackson ML (1962) Chemical composition of soil. In F.E. Bean (ed.) Chemistry of soil. van Nostrand Reinheld Co., New York. p:71-144.
Khan N, Bano A, Rahman MA, Guo J, Kang Z, Babar MA (2019) Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci Rep 9:2097. https://doi.org/10.1038/s41598-019-38702-8
Khan MY, Zahir ZA, Asghar HN, Waraich EA (2017) Preliminary investigations on selection of synergistic halotolerant plant growth promoting rhizobacteria for inducing salinity tolerance in wheat. Pak J Bot 49:1541–1551
Kumar A, Singh S, Gaurav AK, Srivastava S, Verma JP (2020) Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.01216
Maathuis FJM, Ahmad I, Patishtan J (2014) Regulation of Na+ fluxes in plants. Front Plant Sci 467
Mahmood S, Daur I, Al-Solaimani SG, Ahmad S, Madkour MH, Yasir M, Hirt H, Ali S, Ali Z (2016) Plant growth promoting rhizobacteria and silicon synergistically enhance salinity tolerance of mungbean. Front Plant Sci 7:876. https://doi.org/10.3389/fpls.2016.00876
Moodie CD, Smith HW, McCreery RA (1959) Laboratory manual for soil fertility. State College of Washington, Pullman. Washington, USA.
Niamat B, Naveed M, Ahmad Z, Yaseen M, Ditta A, Mustafa A, Rafique M, Bibi R, Minggang X (2019) Calcium-enriched animal manure alleviates the adverse effects of salt stress on growth, physiology and nutrients homeostasis of Zea mays L. MDPI-Plants 8(11):480. https://doi.org/10.3390/plants8110480
Niyungeko C, Liang X, Liu C, Liu ZW, Sheteiwy M, Zhang H, Zhou J, Tian G (2018) Effect of biogas slurry application rate on colloidal phosphorus leaching in paddy soil: a column study. Geoderma. 325:117–124
Richards LA, (1954) Diagnosis and improvement of saline and alkali soils. US Salinity Lab., US Department of Agriculture Handbook 60. California, USA.
Saqib AI, Ahmed K, Qadir G, Nawaz MQ, Rizwan M, Zaka MA, Warraich IA (2017) Comparison the efficient reclamation of different inorganic materials with organic amendments to rice-wheat crop sustainable production in salt-affected soils. Cercetari Agronomice in Moldova 1:19–29. https://doi.org/10.1515/cerce-2017-0002
Scotti R, Scelza GR, Zoina A, Rao MA (2015) Organic amendments as sustainable tool to recovery fertility in intensive agricultural systems. J Soil Sci Plant Nutr 15:333–352
Shahzad H, Ullah S, Iqbal M, Bilal HM, Shah GM, Ahmad S, Zakir A, Ditta A, Farooqi MA, Ahmad I (2019) Effects of salinity sources and levels on growth, physiology and nutrient contents of maize crop. Ital J Agron 14:199–207. https://doi.org/10.4081/ija.2019.1326
Sheteiwy MS, An J, Yin M, Jia X, Guan Y, He F, Hu J (2019) Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma 256:79–99
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Bio Sci 22:123–131
Shultana R, Zuan ATK, Yusop MR, Saud HM (2020) Characterization of salt-tolerant plant growth promoting rhizobacteria and the effect on growth and yield of saline-affected rice. PLoS One 15:e0238537. https://doi.org/10.1371/journal.pone.0238537
Singh I (2018) Plant growth promoting rhizobacteria (PGPR) and their various mechanisms for plant growth enhancement in stressful conditions: a review. Europ J Biol Res 8:191–213. https://doi.org/10.5281/zenodo.1455995
Sohaib M, Zahir ZA, Khan MY, Ans M, Asghar HN, Yasin S, Al-Barakaha FNI (2020) Comparative evaluation of different carrier-based multistrain bacterial formulations to mitigate the salt stress in wheat. Saudi J Biol Sci 27:777–787
Syed A, Sarwar G, Shah SH, Muhammad S (2021) Soil salinity research in 21st century in Pakistan: its impact on availability of plant nutrients, growth and yield of crops. Commun Soil Sci Plant Anal 52:183–200. https://doi.org/10.1080/00103624.2020.1854294
Tahir M, Ahmad I, Shahid M, Shah GM, Farooq ABU, Akram M, Tabassum SA, Naeem MA, Khalid U, Ahmad S, Zakir A (2019) Regulation of antioxidant production, ion uptake and productivity in potato (Solanum tuberosum L.) plant inoculated with growth promoting salt tolerant Bacillus strains. Ecotoxicol Environ Saf 178:33–42
Tahir M, Naeem MA, Shahid M, Khalid U, Farooq ABU, Ahmad N, Ahmad I, Arshad M, Waqar A (2020) Inoculation of pqqE gene inhabiting Pantoea and Pseudomonas strains improve the growth and grain yield of wheat with a reduced amount of chemical fertilizer. J Appl Microbiol 129:575–589. https://doi.org/10.1111/jam.14630
Walkley AJ, Black IA (1934) Estimation of soil organic carbon by the chromic acid titration method. Soil Sci 37:29–38
Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts. Soil Sci Soc Am Proc 29:677–678
Yaseen R, Zafar-ul-Hye M, Hussain M (2019) Integrated application of ACC-deaminase containing plant growth promoting rhizobacteria and biogas slurry improves the growth and productivity of wheat under drought stress. Int J Agric Biol 21:869–878
Zahir ZA, Shah MK, Naveed M, Akhter MJ (2010) Substrate-dependent auxin production by Rhizobium phaseoli improves the growth and yield of Vigna radiata L. under salt stress conditions. J Microbiol Biotechnol 20:1288–1294
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The work is partially supported by the Higher Education Commission of Pakistan (Grant No. NRPU3899) and Shanghai Science and Technology Committee (Grant No. 19390743300).
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SH, IA, and MJA: writing–original draft preparation, methodology, and investigation; MNI and MS: methodology and investigation; MT and AR: methodology; AS and MK: resources and analysis; AD and BZ: writing–reviewing and editing; IA and MJA: conceptualization, resources, and supervision.
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Hamid, S., Ahmad, I., Akhtar, M.J. et al. Bacillus subtilis Y16 and biogas slurry enhanced potassium to sodium ratio and physiology of sunflower (Helianthus annuus L.) to mitigate salt stress. Environ Sci Pollut Res 28, 38637–38647 (2021). https://doi.org/10.1007/s11356-021-13419-2
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DOI: https://doi.org/10.1007/s11356-021-13419-2