Skip to main content

Advertisement

SpringerLink
Log in

Mechanisms of halotolerant plant growth promoting Alcaligenes sp. involved in salt tolerance and enhancement of the growth of rice under salinity stress

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

In the present study halotolerant bacteria were isolated from saline soil (EC ~ 11.9). Based on salt tolerance and plant growth promoting characteristics isolate AF7 was selected for further study. It was identified as Alcaligenes sp. on the basis of protein profiling and 16S rRNA sequence homology. Interestingly, AF7 showed diverse PGP characters at different salinity levels. While phosphate solubilization activity was expressed up to 300 mM NaCl, siderophore production was shown up to 700 mM, zinc solubilization up to 1000 mM and indole acetic acid (IAA), gibberellic acid (GA) and exopolysaccharides (EPS) production were depicted till 1400 mM. Correlative and regression analysis suggested positive relation between IAA, GA, EPS, siderophore production and zinc solubilization capability of AF7 and salinity up to 300 mM NaCl. EPS was found to be the most significant response and there was 263% increment in presence of 300 mM NaCl when compared to non-saline control. Analysis also showed that while growth promoting attributes were significant up to a threshold salinity level, further increasing the stress deviates the mechanism towards survival involving proline, antioxidant and hydroxyl scavenging activities. Combination of halotolerant AF7 and EPS showed more than twofold increase in the vegetative growth parameters of rice at ~ 170 mM NaCl (EC 9 dS/m). The study shows the mechanisms/metabolites of the plant growth promoting bacterium (PGPB) AF7 prominently involved during the salinity stress. Study also proves that novel bioformulations can be developed by integrative use of EPS and salt tolerant-PGPB which can be effective for saline soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbas M, Hernández-García J, Pollmann S, Samodelov SL, Kolb M, Friml J, Alabadí D (2018) Auxin methylation is required for differential growth in Arabidopsis. Proc Natl Acad Sci 115(26):6864–6869

    CAS  PubMed  PubMed Central  Google Scholar 

  • Addinsoft (2020) XLSTAT statistical and data analysis solution. New York, USA. https://www.xlstat.com

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163(2):173–181

    CAS  PubMed  Google Scholar 

  • Akintokun AK, Ezaka E, Akintokun PO, Shittu OB, Taiwo LB (2019) Isolation, screening and response of maize to plant growth promoting rhizobacteria inoculants. Sci Agric bohem 50(3):181–190

    Google Scholar 

  • Altschul FS, Warren G, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Amna BUD, Sarfraz B, Xia Y, Kamran MA, Javed MT, Sultan T, Munis MFH, Chaudhary HJ (2019) Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC-deaminase producing Bacillus strains under induced salinity stress. Ecotoxicol Environ Saf 183:109466

    CAS  PubMed  Google Scholar 

  • Arora NK, Fatima T, Mishra I, Verma M, Mishra J, Mishra V (2018) Environmental sustainability: challenges and viable solutions. Environ Sustain 1(4):309–340

    Google Scholar 

  • Arora NK, Mishra J (2016) Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl Soil Ecol 107:405–407

    Google Scholar 

  • Arora NK, Verma M (2017) Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 7(381):1–9

    Google Scholar 

  • Arora NK, Fatima T, Mishra J, Mishra I, Verma S, Verma R, Verma M, Bhattacharya A, Verma P, Mishra P, Bharti C (2020) Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. J Adv Res. https://doi.org/10.1016/j.jare.2020.07.003

    Article  Google Scholar 

  • Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 18:509

    Google Scholar 

  • Bakhsh K, Akram W, Jahanzeb A, Khan M (2016) Estimating productivity of Bt cotton and its impact on pesticide use in Punjab, Pakistan. Pak Econ Soc Rev 54(1):15–24

    Google Scholar 

  • Bal HB, Nayak L, Das S, Adhya TK (2013) Isolation of ACC deaminase PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366:93–105

    CAS  Google Scholar 

  • Bargaz A, Lyamlouli K, Chtouki M, Zeroual Y, Dhiba D (2018) Soil microbial resources for improving fertilizers efficiency in an integrated plant nutrient management system. Front Microbiol 9:1606

    PubMed  PubMed Central  Google Scholar 

  • Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Behera BK, Das P, Maharana J, Meena DK, Sahu TK, Rao AR, Chatterjee S, Mohanty BP, Sharma AP (2015) Functional screening and molecular characterization of halophilic and halotolerant bacteria by 16S rRNA gene sequence analysis. Proc Natl Acad Sci India B Biol Sci 85:957–964

    CAS  Google Scholar 

  • Bhalodia NR, Nariya PB, Acharya RN, Shukla VJ (2013) In vitro antioxidant activity of hydro alcoholic extract from the fruit pulp of Cassia fistula Linn. Ayu 34:209–214

    PubMed  PubMed Central  Google Scholar 

  • Boukhelata N, Taguett F, Kaci Y (0201M) Characterization of an extracellular polysaccharide produced by Saharan bacterium Paenibacillus tarimensis REG 0201M. Ann Microbiol 69:93–106

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Dar MH, Waza SA, Shukla S, Zaidi NW, Nayak S, Hossain M, Kumar A, Ismail AM, Singh US (2020) Drought tolerant rice for ensuring food security in Eastern India. Sustainability 12:2214

    Google Scholar 

  • Ding P, Song W, Yang Z, Jian J (2018) Influence of Zn(II) stress-induction on component variation and sorption performance of extracellular polymeric substances (EPS) from Bacillus vallismortis. Bioprocess Biosyst Eng 41:781–791

    CAS  PubMed  Google Scholar 

  • Dixit VK, Misra S, Mishra SK, Joshi N, Chauhan PS (2020) Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays. Antonie Van Leeuwenhoek 113:889–905

    CAS  PubMed  Google Scholar 

  • Donati AJ, Lee HI, Leveau JH, Chang WS (2013) Effects of indole -3-acetic acid on the transcriptional activities and stress tolerance of Bradyrhizobium japonicum. PLoS ONE 8:e76559

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Gilles K, Hamilton J, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • Durán RE, Barra-Sanhuez B, Salvà-Serra F, Méndez V, Jaén-Luchoro D, Moore ERB, Seeger M (2019) Complete genome sequence of the marine hydrocarbon degrader Alcaligenes aquatilis QD168, isolated from crude oil-polluted sediment of Quintero Bay, Central Chile. Microbiol Resour Announc 8:e01664–e1718

    PubMed  PubMed Central  Google Scholar 

  • Egamberdieva D, Wirth S, Bellingrath-Kimura SD, Mishra J, Arora NK (2019) Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Front Microbiol 10:2791

    PubMed  PubMed Central  Google Scholar 

  • Etesami H, Glick BR (2020) Halotolerant plant growth–promoting bacteria: prospects for alleviating salinity stress in plants. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2020.104124

    Article  Google Scholar 

  • FAO (2015) Global soil partnership- world soil charter. https://www.fao.org/3/a-mn442e.pdf

  • Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol Lett 213:1–6

    CAS  PubMed  Google Scholar 

  • Fathalla AM (2018) Effectiveness of exopolysaccharides and biofilm forming plant growth promoting rhizobacteria on salinity tolerance of faba bean (Vicia faba L.). Afr J Microbiol Res 12:399–404

    Google Scholar 

  • Fatima T, Arora NK (2019) Plant growth-promoting rhizospheric microbes for remediation of saline soils. In: Arora NK, Kumar N (eds) Phyto and Rhizo Remediation. Springer, Singapore, pp 121–146

    Google Scholar 

  • Ferreira MJ, Silva H, Cunha A (2019) Siderophore producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: a review. Pedosphere 29(4):409–420

    Google Scholar 

  • Garrity G (2005) The proteobacteria, Part B the gammaproteobacteria. In: Garrity G, Brenner DJ, Krieg NR, Staley JR (eds) Bergey’s manual of systematic bacteriology, vol 2. Springer, New York, pp 323–337

    Google Scholar 

  • Ghosh B, Ali MN, Saikat G (2016) Response of rice under salinity stress: a review update. J Res Rice 4:167

    Google Scholar 

  • Giri DD, Kumar A, Shukla PN, Singh R, Singh PK, Pandey KD (2013) Salt stress tolerance of methylotrophic bacteria Methylophilus sp. and Methylobacterium sp. isolated from coal mine spoils. Pol J Microbiol 62(3):273–280

    CAS  PubMed  Google Scholar 

  • Hoang TM, Tran TN, Nguyen TK, Williams B, Wurm P, Bellairs S, Mundree S (2016) Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6:54

    Google Scholar 

  • Ibal JC, Jung BK, Park CE, Shin JH (2018) Plant growth-promoting rhizobacteria used in South Korea. Appl Biol Chem. https://doi.org/10.1007/s13765-018-0406-0

    Article  Google Scholar 

  • Inostroza NG, Barra PJ, Wick LY, Mora ML, Jorquera MA (2016) Effect of rhizobacterial consortia from undisturbed arid- and agro-ecosystems on wheat growth under differing conditions. Lett Appl Microbiol 64:158–163

    Google Scholar 

  • Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80

    PubMed  PubMed Central  Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice Hall of India Pvt. Ltd., New Delhi, pp 38–56

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Khare E, Singh S, Maheshwari DK, Arora NK (2011) Suppression of charcoal rot of chickpea by fluorescent Pseudomonas under saline stress condition. Curr Microbiol 62:1548–1553

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larsen H (1986) Halophilic and halotolerant microorganisms- an overview and historical perspective. FEMS Microbiol Rev 39:3–7

    CAS  Google Scholar 

  • Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3(2):30

    Google Scholar 

  • Mendi A, Aslim B (2014) Antioxidant lactobacilli could protect gingival fibroblasts against hydrogen peroxide: a preliminary in vitro study. Probiot Antimicrob Proteins 6:157–164

    Google Scholar 

  • Meneses CHSG, Rouws LFM, Araújo JLS, Vidal MS, Baldani JI (2011) Exopolysaccharide production is required for biofilm formation and plant colonization by the nitrogen-fixing endophyte Gluconacetobacter diazotrophicus. Mol Plant Microbe Interact 24(12):1448–1458

    CAS  PubMed  Google Scholar 

  • Miceli A, Vetrano F, Sabatino L, D’Anna F, Moncada A (2019) Influence of preharvest gibberellic acid treatments on postharvest quality of minimally processed leaf lettuce and rocket. Horticulturae 5:63

    Google Scholar 

  • Mody B, Bindra M, Modi V (1989) Extracellular polysaccharides of cowpeas rhizobia; compositional and functional studies. Arch Microbiol 153:33–42

    Google Scholar 

  • Morillo Pérez JA, García-Ribera R, Quesada T, Aguilera M, Ramos-Cormenzana A, Monteoliva-Sánchez M (2008) Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J Microbiol Biotechnol 24:2699

    Google Scholar 

  • Mukherjee P, Mitra A, Roy M (2019) Halomonas rhizobacteria of Avicennia marina of Indian Sundarbans promote rice growth under saline and heavy metal stresses through exopolysaccharide production. Front Microbiol 10:1207

    PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681

    CAS  Google Scholar 

  • Nandakumar R, Babu S, Viswanathan R, Sheela J, Raguchander T, Samiyappan R (2001) A new bio-formulation containing plant growth promoting rhizobacterial mixture for the management of sheath blight and enhanced grain yield in rice. Biocontrol 46:493–510

    Google Scholar 

  • Ngonda F (2013) In vitro anti-oxidant activity and free radical scavenging potential of roots of Malawian Trichodesma zeylanicumm (burm. f.). Asian J Biomed Pharma Sci 3(20):21–25

    Google Scholar 

  • Omer AM (2017) Inducing plant resistance against salinity using some rhizobacteria. Egypt J Desert Res 67(1):185–206

    Google Scholar 

  • Orhan F (2016) Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz J Microbiol 47:621–627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Osman KT (2018) Saline and sodic soils. In: Osman KT (ed) Management of soil problems. Springer, Cham, pp 255–298

    Google Scholar 

  • Paleg LG (1965) Physiological effects of gibberellins. Ann Rev Plant Physiol 16:291–322

    CAS  Google Scholar 

  • Pan J, Peng F, Xue X, You Q, Zhang W, Wang T, Huang C (2019) The growth promotion of two salt-tolerant plant groups with PGPR inoculation: a meta-analysis. Sustainability 11:378

    CAS  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiology 17:362–370

    CAS  Google Scholar 

  • Prakash J, Arora NK (2019) Phosphate-solubilizing Bacillus sp. enhances growth, phosphorus uptake and oil yield of Mentha arvensis L. 3 Biotech 9(4):126

    PubMed  PubMed Central  Google Scholar 

  • Rahi P, Prakash O, Shouche YS (2016) Matrix assisted laser desorption/ionization time-of-flight mass-spectrometry (MALDI-TOF MS) based microbial identifications: challenges and scopes for microbial ecologists. Front Microbiol 7:1359

    PubMed  PubMed Central  Google Scholar 

  • Rahneshan Z, Nasibi F, Moghadam AA (2018) Effects of salinity stress on some growth, physiological, biochemical parameters and nutrients in two pistachio (Pistacia vera L.) rootstocks. J Plant Interact 13(1):73–82

    CAS  Google Scholar 

  • Rodriguez PA, Rothballer M, Chowdhury SP, Nussbaumer T, Gutjahr C, Falter-Braun P (2019) Systems biology of plant-microbiome interactions. Mol Plant 12:804–821

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sandhya V, Ali SZ (2015) The production of exopolysaccharide by Pseudomonas putida gap_p45 under various abiotic stress conditions and its role in soil aggregation. Microbiology 84:512–519

    CAS  Google Scholar 

  • Sayyed RZ, Chincholkar SB (2009) Siderophore-producing Alcaligenes feacalis exhibited more biocontrol potential Vis-a`-Vis chemical fungicide. Curr Microbiol 58:47–51

    CAS  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    CAS  PubMed  Google Scholar 

  • Shahid SA, Zaman M, Heng L (2018) Soil salinity: historical perspectives and a world overview of the problem. In: Zaman M, Shahid S, Heng L (eds) Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer, Cham, pp 43–53

    Google Scholar 

  • Srinivasan R, Karaoz U, Volegova M, MacKichan J, Kato-Maeda M, Miller S, Nadarajan R, Brodie EL, Lynch SV (2015) Use of 16S rRNA gene for identification of a broad range of clinically relevant bacterial pathogens. PLoS ONE 10:e0117617

    PubMed  PubMed Central  Google Scholar 

  • Tewari S, Arora NK (2016) Fluorescent Pseudomonas sp. PF17 as an efficient plant growth regulator and biocontrol agent for sunflower crop under saline conditions. Symbiosis 68(1–3):99–108

    CAS  Google Scholar 

  • Tewari S, Sharma S (2020) Rhizobial exopolysaccharides as supplement for enhancing nodulation and growth attributes of Cajanus cajan under multi-stress conditions: a study from lab to field. Soil Till Res 198:104545

    Google Scholar 

  • Timmusk S, Seisenbaeva G, Behers L (2018) Titania (TiO2) nanoparticles enhance the performance of growth-promoting rhizobacteria. Sci Rep 8:617

    PubMed  PubMed Central  Google Scholar 

  • Umali DL (1993) Irrigation induced salinity: a growing problem for development and the environment (English). World Bank technical paper; no. WTP 215. Washington, DC: TheWorld Bank

  • Upadhyay SK, Singh DP, Saikia R (2009) Genetic diversity of plant growth promoting rhizobacteria from rhizospheric soil of wheat under saline conditions. Curr Microbiol 59(5):489–496

    CAS  PubMed  Google Scholar 

  • Wang W, Wu Z, He Y, Huang Y, Li X, Ye B (2018) Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. Ecotoxicol Environ Saf 164:520–529

    CAS  PubMed  Google Scholar 

  • WeinischKu¨hner LS, Roth R, Grimm M, Roth T, Netz DJA, Pierik AJ, Filker S (2018) Identification of osmoadaptive strategies in the halophile, heterotrophic ciliate Schmidingerothrix salinarum. PLoS Biol 16(1):e2003892

    Google Scholar 

  • Xing J, Wang G, Zhang Q, Liu X, Gu Z, Zhang H, Chen YQ, Chen W (2015) Determining antioxidant activities of lactobacilli cell-free supernatants by cellular antioxidant assay: a comparison with traditional methods. PLoS ONE 10(3):e0119058

    PubMed  PubMed Central  Google Scholar 

  • Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:14

    Google Scholar 

  • Yi Y, Huang W, Ge Y (2008) Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J Microbiol Biotechnol 24:1059–1065

    CAS  Google Scholar 

  • Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    CAS  PubMed  Google Scholar 

  • Yousef NMH (2018) Capability of plant growth-promoting rhizobacteria (PGPR) for producing indole acetic acid (IAA) under extreme conditions. Eur J Biol Res 8:174–182

    CAS  Google Scholar 

  • Zeigler RS, Barclay A (2008) The relevance of rice. Rice 1(1):3–10

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Babasaheb Bhimrao Ambedkar University, Lucknow, India

    Tahmish Fatima, Isha Mishra & Renu Verma

  2. Department of Environmental Science, School for Environmental Sciences, Babasaheb Bhimrao Ambedkar University, Lucknow, India

    Naveen Kumar Arora

Authors
  1. Tahmish Fatima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isha Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Renu Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naveen Kumar Arora
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naveen Kumar Arora.

Ethics declarations

Conflict of interest

All authors declare that there is no conflict of interest in this original article.

Ethical approval

The study does not involve any work on humans or animals hence do not require any ethical clearance.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fatima, T., Mishra, I., Verma, R. et al. Mechanisms of halotolerant plant growth promoting Alcaligenes sp. involved in salt tolerance and enhancement of the growth of rice under salinity stress. 3 Biotech 10, 361 (2020). https://doi.org/10.1007/s13205-020-02348-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-020-02348-5

Keywords

Search

Navigation