Skip to main content

Advertisement

SpringerLink
Log in

Inoculation of Cucumber (Cucumis sativus L.) Seedlings with Salt-Tolerant Plant Growth Promoting Bacteria Improves Nutrient Uptake, Plant Attributes and Physiological Profiles

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Salinity is one of the major abiotic stresses that cause retarded plant growth and crop production. It has been reported that harmful effects of salinity could be managed by application of salt-tolerant plant growth-promoting (PGP) bacteria. In this study, eight salt-tolerant bacteria were selected from an array of 150 cultures, based on salt-tolerant properties. All the isolates were identified based on 16S rRNA gene sequencing and subjected to different PGP properties. The results showed the production of indole acetic acid (28.83–62.35 µg/ml), ammonia (35.49–67.48 µg/ml), phosphate solubilization (1.45–3.42 µg/ml), and siderophores. Further, these isolates were evaluated in pot studies on their response in Cucumis sativus plants against 100 mM salinity stress and without salinity stress (normal water) along with uninoculated controls. The results revealed that bacterized seeds had enhanced plant growth parameters and there was a corresponding increase in biomass in both conditions compared to control plants. The maximum enhancement in root and shoot length under normal condition was 54.6% (SBR-4) and 69.3% (SBS-19), whereas under saline conditions it was 42.3% (SBR-5) and 100.4% (SBS-18), respectively. Further, the inoculated seedlings maximum enhanced chlorophyll a (SBS-3; 50.6% and SBR-4; 45.4%) and chlorophyll b (SBR-1; 83.6% and SBS-3; 209.6%), proline (SBS-18; 62.0% and SBR-1; 32.8%), total phenol (SBR-1; 48.2% and SBR-5; 67.8%), ascorbic acid (SBS-2; 118.6% and SBR-1; 22.4%), and shoot and root N and P contents (twofold to threefold) under both normal and saline conditions. Among the eight isolates, isolates SBS-19, SRB-5, SBS-18, and SBR-4 improved plant growth and other parameters under both conditions in C. sativus plants. Therefore, it is suggested that these salt-tolerant PGP bacteria may be used for cultivation of C. sativus in salinized agricultural lands.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbasi MK, Sharif S, Kazmi M, Sultan T, Aslam M (2011) Isolation of plant growth promoting rhizobacteria from wheat rhizosphere and their effect on improving growth, yield and nutrient uptake of plants. Plant Biosyst 145:159–168

    Article  Google Scholar 

  • Abdelgawad KF, El-Mogy MM, Mohamed MIA, Garchery C, Stevens RG (2019) Increasing ascorbic acid content and salinity tolerance of cherry tomato plants by suppressed expression of the ascorbate oxidase gene. Agronomy 9:51

    Article  CAS  Google Scholar 

  • Abdul Qados AMS (2011) Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J Saudi Soc Agric Sci 10:7–15

    Google Scholar 

  • Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23:731–744

    Article  PubMed  PubMed Central  Google Scholar 

  • Akbarimoghaddam H, Galavi M, Ghanbari A, Panjehkeh N (2011) Salinity effects on seed germination and seedling growth of bread wheat cultivars. Trakia J Sci 9:43–50

    Google Scholar 

  • Altschul SF, Maddan TL, Schaffer AA, Zang J, Zang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programmes. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amaresan N, Kumar K, Sureshbabu K, Madhuri K (2014) Plant growth-promoting potential of bacteria isolated from active volcano sites of Barren Island, India. Lett Appl Microbiol 58:130–137

    Article  CAS  PubMed  Google Scholar 

  • Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant. Commun Soil Sci Plant Anal 20:961–969

    Article  CAS  Google Scholar 

  • Baha N, Bekki A (2015) An approach of improving plant salt tolerance of Lucerne (Medicago sativa) grown under salt stress: use of bio-inoculants. J Plant Growth Regul 34:169–182

    Article  CAS  Google Scholar 

  • Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011) Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33:1103–1111

    Article  CAS  Google Scholar 

  • Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387

    Article  CAS  PubMed  Google Scholar 

  • Cai YZ, Luo Q, Sun M, Corke H (2004) Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci 74:2157–2184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cappuccino JC, Sherman N (1992) Microbiology: a laboratory manual, 3rd edn. Benjamin/Cummings Pub. Co., New York, pp 125–179

    Google Scholar 

  • Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21:613–618

    Article  CAS  PubMed  Google Scholar 

  • Coutinho FP, Felix WP, Yano-Melo AM (2012) Solubilization of phosphates in vitro by Aspergillus spp. and Penicillium spp. Ecol Eng 42:85–89

    Article  Google Scholar 

  • Ge H, Zhang F (2019) Growth-promoting ability of Rhodopseudomonas palustris G5 and its effect on induced resistance in cucumber against salt stress. J Plant Growth Regul 38:180–188

    Article  CAS  Google Scholar 

  • Gordon SA, Paleg LG (1957) Quantitative measurement of indole acetic acid. Physiol Plant Pathol 10:347–348

    Google Scholar 

  • Hmaeid N, Wali M, Ben Mahmoud QM, Pueyo JJ, Ghnaya T, Abdelly C (2019) Efficient rhizobacteria promote growth and alleviate NaCl-induced stress in the plant species Sulla carnosa. Appl Soil Ecol 133:104–113

    Article  Google Scholar 

  • Islam MR, Madhaiyan M, Boruah HPD, Yim W, Lee G, Saravanan VS, Fu Q, Hu H, Sa T (2009) Characterization of plant growth-promoting traits of free-living diazotrophic bacteria and their inoculation effects on growth and nitrogen uptake of crop plants. J Microbiol Biotechnol 19:1213–1222

    Article  CAS  PubMed  Google Scholar 

  • Jackson ML (1967) Soil chemical analysis. Prentice Hall Inc., Engle Wood Cliff

    Google Scholar 

  • Jackson ML (1973) Soil chemical analysis. Prentice Hall of India (P) Ltd., New Delhi

    Google Scholar 

  • Jay PV, Janardan Y, Kavindra NT, Ashok K (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286

    Article  Google Scholar 

  • Kang SM, Khan AL, Waqas M, You YH, Kim JH, Kim JG, Hamayun M, Lee IJ (2014) Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J Plant Interact 9:673–682

    Article  CAS  Google Scholar 

  • Kato N, Esaka M (1999) Changes in ascorbate oxidase gene expression and ascorbate levels in cell division and cell elongation in tobacco cells. Physiol Plant 105:321–329

    Article  CAS  Google Scholar 

  • Khalifa AYZ, Alsyeeh AM, Almalki MA, Saleh FA (2016) Characterization of the plant growth promoting bacterium, Enterobacter cloacae MSR1, isolated from roots of non-nodulating Medicago sativa. Saudi J Biol Sci 23:79–86

    Article  CAS  PubMed  Google Scholar 

  • Khan F, Ahmed KBM, Shariq M, Siddiqui MA (2019) Potentiality of plant growth-promoting rhizobacteria in easing of soil salinity and environmental sustainability. In: Akhtar M (ed) Salt stress, microbes, and plant interactions: causes and solution. Springer, Singapore, pp 21–58

    Chapter  Google Scholar 

  • Khan MA, Gemenet DC, Villordon A (2016) Root system architecture and abiotic stress tolerance: current knowledge in root and tuber crops. Front Plant Sci 7:1584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khanna K, Jamwal VL, Sharma A, Gandhi SG, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Ali HM, Ahmad P (2019a) Supplementation with plant growth promoting rhizobacteria (PGPR) alleviates cadmium toxicity in Solanum lycopersicum by modulating the expression of secondary metabolites. Chemosphere 230:628–639

    Article  CAS  PubMed  Google Scholar 

  • Khanna K, Jamwal VL, Kohli SK, Gandhi SG, Ohri P, Bhardwaj R, Wijaya L, Alyemeni MN, Ahmad P (2019b) Role of plant growth promoting bacteria (PGPRs) as biocontrol agents of Meloidogyne incognita through improved plant defense of Lycopersicon esculentum. Plant Soil 463:325–345

    Article  CAS  Google Scholar 

  • Khanna K, Jamwal VL, Sharma A, Gandhi SG, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Marraiki N, Ahmad P (2019c) Evaluation of the role of rhizobacteria in controlling root-knot nematode infection in Lycopersicon esculentum plants by modulation in the secondary metabolite profiles. AoB Plants 11:plz069

    Article  CAS  Google Scholar 

  • Khanna K, Sharma A, Ohri P, Bhardwaj R, Abd_Allah EF, Hashem A, Ahmad P (2019d) Impact of plant growth promoting rhizobacteria in the rrchestration of Lycopersicon esculentum Mill. resistance to plant parasitic nematodes: a metabolomic approach to evaluate defense responses under field conditions. Biomolecules 9:676

    Article  CAS  PubMed Central  Google Scholar 

  • Kumar D, Al Hassan M, Naranjo MA, Agrawal V, Boscaiu M, Vicente O (2017a) Effects of salinity and drought on growth, ionic relations, compatible solutes and activation of antioxidant systems in oleander (Nerium oleander L.). PLoS One 12:e0185017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar K, Amaresan N, Madhuri K (2017b) Alleviation of the adverse effect of salinity stress by inoculation of plant growth promoting rhizobacteria isolated from hot humid tropical climate. Ecol Eng 102:361–366

    Article  Google Scholar 

  • Li Y, Shi H, Zhang H, Chen S (2019) Amelioration of drought effects in wheat and cucumber by the combined application of super absorbent polymer and potential biofertilizer. Peer J 7:e6073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, Khan A, Al-Harrasi A (2018) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32

    Article  CAS  PubMed  Google Scholar 

  • Oberbacher MF, Vines HM (1963) Spectrophotometric assay of ascorbic acid oxidase. Nature 197:1203–1204

    Article  CAS  PubMed  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda D, Sharma SG, Sarkar RK (2008) Chlorophyll fluorescence parameters, CO2 photosynthetic rate and regeneration capacity as a result of complete submergence and subsequent re-emergence in rice (Oryza sativa L.). Aquat Bot 88:127–133

    Article  CAS  Google Scholar 

  • Pandey P, Irulappan V, Bagavathiannan MV, Senthilkumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

    PubMed  PubMed Central  Google Scholar 

  • Panwar M, Tewari R, Nayyar H (2016) Native halo-tolerant plant growth promoting rhizobacteria Enterococcus and Pantoea sp. improve seed yield of Mungbean (Vigna radiata L.) under soil salinity by reducing sodium uptake and stress injury. Physiol Mol Biol Plants 22:445–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel S, Jinal HN, Amaresan N (2017) Isolation and characterization of drought resistance bacteria for plant growth promoting properties and their effect on chilli (Capsicum annuum) seedling under salt stress. Biocatal Agric Biotechnol 12:85–89

    Article  Google Scholar 

  • Patel VK, Srivastava R, Sharma A, Srivastava AK, Singh S, Srivastava AK, Kashyap PL, Chakdar H, Pandiyan K, Kalra A, Saxena AK (2018) Halotolerant Exiguobacterium profundum PHM11 tolerate salinity by accumulating L-proline and fine-tuning gene expression profiles of related metabolic pathways. Front Microbiol 9:423

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul D, Lade H (2014) Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review. Agron Sustain Dev 34:737–752

    Article  Google Scholar 

  • Ploegman J, Bierhuizen CF (1970) Salt tolerance in cucumber. Bedrijfsontwikkeling Editie Tuinbouw 1:32–39

  • Prittesh P, Avnika P, Kinjal P, Jinal HN, Saktivel K, Amaresan N (2020) Amelioration effect of salt-tolerant plant growth-promoting bacteria on growth and physiological properties of rice (Oryza sativa) under salt-stressed conditions. Arch Microbiol. https://doi.org/10.1007/s00203-020-01962-4

    Article  PubMed  Google Scholar 

  • Parray JA, Jan S, Kamili AN, Qadri RA, Egamberdieva D, Ahmad P (2016) Current perspectives on plant growth promoting rhizobacteria. J Plant Growth Regul 35:877–902

    Article  CAS  Google Scholar 

  • Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Plant growth-promoting traits in Enterobacter cloacae subsp. dissolvens MDSR9 isolated from soybean rhizosphere and its impact on growth and nutrition of soybean and wheat upon inoculation. Agric Res 3:53–66

    Article  CAS  Google Scholar 

  • Sambrook J, Fritschi EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Sayed E, Ahmed HES, Baziad SAM, Basaba RAAS (2015) Application of exogenous ascorbic acid on tomato (Solanum lycopersicum L.) seeds under NaCl salinity stress. Int J Curr Res Biosci Plant Biol 2:33–46

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shahid SA, Zaman M, Heng L (2018) Introduction to soil salinity, sodicity and diagnostics techniques. In: Zaman M, Shahid SA, Heng L (eds) Guideline for salinity assessment, mitigation and adaptation using nuclear and related techniques. Springer, Cham, pp 1–42

    Google Scholar 

  • Singh JS, Kaushal S, Kumar A, Vimal SR, Gupta VK (2016) Book review: microbial inoculants in sustainable agricultural productivity—Vol II: functional application. Front Microbiol 7:2015

    Google Scholar 

  • Sukweenadhi J, Balusamy SR, Kim YJ, Lee CH, Kim YJ, Koh SC, Yang DC (2018) A growth-promoting bacteria, Paenibacillus yonginensis DCY84T enhanced salt stress tolerance by activating defense-related systems in Panax ginseng. Front Plant Sci 9:813

    Article  PubMed  PubMed Central  Google Scholar 

  • Tajini F, Mustapha TM, Drevon JJ (2012) Combined inoculation with Glomus intraradices and Rhizobium tropici CIAT899 increases phosphorus use efficiency for symbiotic nitrogen fixation in common bean (Phaseolus vulgaris L.). Saudi J Biol Sci 19:157–163

    Article  CAS  PubMed  Google Scholar 

  • Torre-Ruiza NDL, Ruiz-Valdiviezob VM, Rincón-Molinab CI, Rodríguez-Mendiolaa M, Arias-Castroa C, Gutiérrez-Micelib FA, Palomeque-Dominguezb H, Rincón-Rosales R (2016) Effect of plant growth-promoting bacteria on the growth and fructan production of Agave americana L. Braz J Microbiol 47:587–596

    Article  CAS  Google Scholar 

  • Ullah A, Mushtaq H, Fahad Sh, Hakim SA, Chaudhary HJ (2017) Plant growth promoting potential of bacterial endophytes in novel association with Olea ferruginea and Withania coagulans. Microbiology 86:119–127

    Article  CAS  Google Scholar 

  • Upadhyay SK, Singh DP (2015) Effect of salt-tolerant plant growth-promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol 17:288–293

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol 14:605–611

    Article  CAS  PubMed  Google Scholar 

  • Usanmaz S, Abak K (2019) Plant growth and yield of cucumber plants grafted on different commercial and local rootstocks grown under salinity stress. Saudi J Biol Sci 26:1134–1139

    Article  CAS  PubMed  Google Scholar 

  • Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286

    Article  Google Scholar 

  • Vimal SR, Patel VK, Singh JS (2019) Plant growth promoting Curtobacterium albidum strain SRV4: an agriculturally important microbe to alleviate salinity stress in paddy plants. Ecol Indic 105:553–562

    Article  CAS  Google Scholar 

  • Wolf B (1982) The comprehensive system of leaf analysis and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 3:1035–1059

    Article  Google Scholar 

  • Yamamoto A, Bhuiyan MN, Waditee R, Tanaka Y, Esaka M, Oba K, Jagendorf AT, Takabe T (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. J Exp Bot 56:1785–1796

    Article  CAS  PubMed  Google Scholar 

  • Yoo SJ, Weon HY, Song J, Sang MK (2019) Induced tolerance to salinity stress by halotolerant bacteria Bacillus aryabhattai H19-1 and B. mesonae H20-5 in tomato plants. J Microbiol Biotechnol 29:1124–1136

    Article  CAS  PubMed  Google Scholar 

  • Zahid M, Abbasi MK, Hameed S, Rahim N (2015) Isolation and identification of indigenous plant growth promoting rhizobacteria from Himalayan region of Kashmir and their effect on improving growth and nutrient contents of maize (Zea mays L.). Front Microbiol 6:207

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou T, Chen D, Li C, Sun Q, Li L, Liu F, Shen Q, Shen B (2012) Isolation and characterization of Pseudomonas brassicacearum J12 as an antagonist against Ralstonia solanacearum and identification of its antimicrobial components. Microbiol Res 167:388–394

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Head, Department of Biosciences, Veer Narmad South Gujarat University, Surat, and Uka Tarsadia University management, and Director, C.G. Bhakta Institute of Biotechnology, for constant support and providing necessary facilities to carry out the work.

Author information

Authors and Affiliations

  1. Department of Biosciences, Veer Narmad South Gujarat University, Surat, Gujarat, India

    Vinodbhai Patel Kartik

  2. C. G. Bhakta Institute of Biotechnology, Uka Tarsadia University, Maliba Campus, Bardoli, Surat, Gujarat, 394 350, India

    Hardik Naik Jinal & Natarajan Amaresan

Authors
  1. Vinodbhai Patel Kartik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hardik Naik Jinal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natarajan Amaresan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NA-Conceived and designed the experiments; VPK, HNJ-Performed all experiments, statistical analysis, tables and figures; VPK, NA wrote the paper.

Corresponding author

Correspondence to Natarajan Amaresan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kartik, V.P., Jinal, H.N. & Amaresan, N. Inoculation of Cucumber (Cucumis sativus L.) Seedlings with Salt-Tolerant Plant Growth Promoting Bacteria Improves Nutrient Uptake, Plant Attributes and Physiological Profiles. J Plant Growth Regul 40, 1728–1740 (2021). https://doi.org/10.1007/s00344-020-10226-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10226-w

Keywords

Search

Navigation