Log in

Consortium of Endophytic Bacillus australimaris CK11 and Staphylococcus epidermidis CK9 from Commiphora gileadensis Mediates Tomato Resilience to Combined Salinity, Heat, and Drought Stresses

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

Abstract

Climate change poses a critical threat to global agriculture. Plant growth-promoting bacteria (PGPB) present a sustainable approach to increase climate resilience. The study focused on isolating and screening abiotic stress-resistant endophytic bacteria from the Arabian balsam tree (Commiphora gileadensis); these bacteria can lessen the phytotoxic impacts of heat, salinity, and drought stress. C. gileadensis is known for its resilience to diverse abiotic stresses and hosts a diverse array of PGPB. Isolated endophytic bacteria were evaluated for their growth-promoting activities, including phosphate and silicate solubilization and indole3-acetic acid production, and screened for tolerance to multiple abiotic stresses. Out of 20 distinct endophytic bacterial isolates exhibiting various plant growth-promoting (PGP) traits, the Staphylococcus epidermidis CK9 strain and the Bacillus australimaris CK11 strain demonstrated remarkable resilience to a range of abiotic stresses, including heat, salinity, and drought. Tomato inoculation with sole or a consortium of CK9 and CK11 under combined abiotic stresses led to significantly enhanced plant growth attributes and photosynthetic pigments (chlorophyll a, b and carotenoids), reduced Na+ uptake and maintained a high K+/Na+ ratio. Combined abiotic stress-induced oxidative stress (lipid peroxidation and superoxide anion) was significantly counteracted by the enhanced accumulation of antioxidant activities (catalase and peroxidase) and upregulated expression of Glutathione reductase and catalase (CAT) genes compared with noninoculated plants. Co-inoculation promoted phytohormones crosstalk by downregulating abscisic acid and jasmonic acid accumulation while stimulating salicylic acid accumulation under stress conditions. This hormonal crosstalk significantly induced abiotic stress-related heat shock protein (HSP) genes (HSP70 and HSP90) compared to noninoculated plants. This study provides valuable insights into the potential use of PGPB from C. gileadensis as a bioinoculant for enhancing tomato growth and yield under combined abiotic stress conditions. Future research will focus on the field assessment of this consortium in hot weather under saline- and drought-induced stresses to determine their effect on crop productivity.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

References

  • Abuljadayel K (2020) Antibacterial effect of extract from Commiphora gileadensis; in vitro study. University of British Columbia

  • Adhikari A, Lee K-E, Khan MA, Kang S-M, Adhikari B, Imran M, Jan R, Kim K-M, Lee I-J (2020) Effect of silicate and phosphate solubilizing rhizobacterium Enterobacter ludwigii GAK2 on Oryza sativa L. under cadmium stress. J Microbiol Biotechnol 30(1):118

    Article  CAS  PubMed  Google Scholar 

  • Alhazmi A, Aldairi AF, Alghamdi A, Alomery A, Mujalli A, Obaid AA, Farrash WF, Allahyani M, Halawani I, Aljuaid A (2022) Antibacterial effects of Commiphora gileadensis methanolic extract on wound healing. Molecules 27(10):3320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alherthi M, Aljuaid M, Alfifi O, Alshaer R, Alsaadi R, Almehmadi M, Eid E, Hawash Y (2020) In vitro and in vivo antibacterial effect of Commiphora gileadensis methanolic extract against methicillin-resistant Staphylococcus aureus (MRSA) and Pseudomonas aeruginosa. Pak J Biol Sci 23(12):1676–1680

    Article  PubMed  Google Scholar 

  • Ali A, Bilal S, Khan AL, Mabood F, Al-Harrasi A, Lee I-J (2019) Endophytic Aureobasidium pullulans BSS6 assisted developments in phytoremediation potentials of Cucumis sativus under Cd and Pb stress. J Plant Interact 14(1):303–313

    Article  CAS  Google Scholar 

  • Alsamir M, Mahmood T, Trethowan R, Ahmad N (2021) An overview of heat stress in tomato (Solanum lycopersicum L.). Saudi J Biol Sci 28(3):1654–1663

    Article  CAS  PubMed  Google Scholar 

  • Al-Sieni AI (2014) The antibacterial activity of traditionally used Salvadora persica L. (miswak) and Commiphora gileadensis (palsam) in Saudi Arabia. Afr J Tradit Complement Altern Med 11(1):23–27

    PubMed  Google Scholar 

  • Bhandari R, Neupane N, Adhikari DP (2021) Climatic change and its impact on tomato (Lycopersicum esculentum L.) production in plain area of Nepal. Environ Chall 4:100129

    Article  CAS  Google Scholar 

  • Bilal S, Shahzad R, Khan AL, Al-Harrasi A, Kim CK, Lee I-J (2019) Phytohormones enabled endophytic Penicillium funiculosum LHL06 protects Glycine max L. from synergistic toxicity of heavy metals by hormonal and stress-responsive proteins modulation. J Hazard Mater 379:120824

    Article  CAS  PubMed  Google Scholar 

  • Bilal S, Shahzad R, Lee I-J (2021) Synergistic interaction of fungal endophytes, Paecilomyces formosus LHL10 and Penicillium funiculosum LHL06, in alleviating multi-metal toxicity stress in Glycine max L. Environ Sci Pollut Res 28(47):67429–67444

    Article  CAS  Google Scholar 

  • Bilal S, Khan A, Imran M, Khan AL, Asaf S, Al-Rawahi A, Al-Azri MSA, Al-Harrasi A, Lee I-J (2022) Silicon-and boron-induced physio-biochemical alteration and organic acid regulation mitigates aluminum phytotoxicity in date palm seedlings. Antioxidants 11(6):1063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bilal S, Khan T, Asaf S, Khan NA, Saad Jan S, Imran M, Al-Rawahi A, Khan AL, Lee I-J, Al-Harrasi A (2023) Silicon-induced morphological, biochemical and molecular regulation in Phoenix dactylifera L. under low-temperature stress. Int J Mol Sci 24(7):6036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaudhary J, Alisha A, Bhatt V, Chandanshive S, Kumar N, Mir Z, Kumar A, Yadav SK, Shivaraj S, Sonah H (2019) Mutation breeding in tomato: advances, applicability and challenges. Plants 8(5):128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coonan EC, Kirkby CA, Kirkegaard JA, Amidy MR, Strong CL, Richardson AE (2020) Microorganisms and nutrient stoichiometry as mediators of soil organic matter dynamics. Nutr Cycl Agroecosyst 117(3):273–298

    Article  CAS  Google Scholar 

  • Dai A, Zhao T, Chen J (2018) Climate change and drought: a precipitation and evaporation perspective. Curr Clim Change Rep 4:301–312

    Article  Google Scholar 

  • Divya K, Bhatnagar-Mathur P, Sharma KK, Reddy PS (2019) Heat shock proteins (Hsps) mediated signalling pathways during abiotic stress conditions. In: Plant signaling molecules. Elsevier, pp 499–516

  • Dong C-J, Li L, Shang Q-M, Liu X-Y, Zhang Z-G (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240:687–700

    Article  CAS  PubMed  Google Scholar 

  • Egamberdieva D, Wirth SJ, Alqarawi AA, Abd-Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104

    Article  PubMed  PubMed Central  Google Scholar 

  • Etesami H, Jeong BR, Glick BR (2023) Potential use of Bacillus spp. as an effective biostimulant against abiotic stresses in crops—a review. Curr Res Biotechnol 5:100128

    Article  CAS  Google Scholar 

  • Farooq A, Farooq N, Akbar H, Hassan ZU, Gheewala SH (2023) A critical review of climate change impact at a global scale on cereal crop production. Agronomy 13(1):162

    Article  Google Scholar 

  • Ferreira MJ, Cunha A, Figueiredo S, Faustino P, Patinha C, Silva H, Sierra-Garcia IN (2021) The root microbiome of Salicornia ramosissima as a seedbank for plant-growth promoting halotolerant bacteria. Appl Sci 11(5):2233

    Article  CAS  Google Scholar 

  • Genest O, Wickner S, Doyle SM (2019) Hsp90 and Hsp70 chaperones: collaborators in protein remodeling. J Biol Chem 294(6):2109–2120

    Article  CAS  PubMed  Google Scholar 

  • Gharsallah C, Fakhfakh H, Grubb D, Gorsane F (2016) Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AoB Plants 8:plw055

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo T, Gull S, Ali MM, Yousef AF, Ercisli S, Kalaji HM, Telesiński A, Auriga A, Wróbel J, Radwan NS (2022) Heat stress mitigation in tomato (Solanum lycopersicum L.) through foliar application of gibberellic acid. Sci Rep 12(1):1–13

    Google Scholar 

  • Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiol Mol Biol Plants 23:249–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igiehon NO, Babalola OO, Cheseto X, Torto B (2021) Effects of rhizobia and arbuscular mycorrhizal fungi on yield, size distribution and fatty acid of soybean seeds grown under drought stress. Microbiol Res 242:126640

    Article  CAS  PubMed  Google Scholar 

  • Ihsan MZ, Daur I, Alghabari F, Alzamanan S, Rizwan S, Ahmad M, Waqas M, Shafqat W (2019) Heat stress and plant development: role of sulphur metabolites and management strategies. Acta Agric Scand Sect B Soil Plant Sci 69(4):332–342

    CAS  Google Scholar 

  • Imran M, Mpovo CL, Aaqil Khan M, Shaffique S, Ninson D, Bilal S, Khan M, Kwon E-H, Kang S-M, Yun B-W (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. Int J Mol Sci 24(10):8489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jogawat A, Yadav B, Chhaya LN, Singh AK, Narayan OP (2021) Crosstalk between phytohormones and secondary metabolites in the drought stress tolerance of crop plants: a review. Physiol Plant 172(2):1106–1132

    Article  CAS  PubMed  Google Scholar 

  • Kapadia C, Sayyed R, El Enshasy HA, Vaidya H, Sharma D, Patel N, Malek RA, Syed A, Elgorban AM, Ahmad K (2021) Halotolerant microbial consortia for sustainable mitigation of salinity stress, growth promotion, and mineral uptake in tomato plants and soil nutrient enrichment. Sustainability 13(15):8369

    Article  CAS  Google Scholar 

  • Karkute SG, Ansari WA, Singh AK, Singh PM, Rai N, Bahadur A, Singh J (2021) Characterization of high-temperature stress-tolerant tomato (Solanum lycopersicum L.) genotypes by biochemical analysis and expression profiling of heat-responsive genes. 3 Biotech 11:1–10

    Article  Google Scholar 

  • Khan A, Kamran M, Imran M, Al-Harrasi A, Al-Rawahi A, Al-Amri I, Lee I-J, Khan AL (2019) Silicon and salicylic acid confer high-pH stress tolerance in tomato seedlings. Sci Rep 9(1):1–16

    Article  Google Scholar 

  • Khan MA, Asaf S, Khan AL, Jan R, Kang S-M, Kim K-M, Lee I-J (2020a) Extending thermotolerance to tomato seedlings by inoculation with SA1 isolate of Bacillus cereus and comparison with exogenous humic acid application. PLoS ONE 15(4):e0232228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MA, Asaf S, Khan AL, Jan R, Kang S-M, Kim K-M, Lee I-J (2020b) Thermotolerance effect of plant growth-promoting Bacillus cereus SA1 on soybean during heat stress. BMC Microbiol 20(1):1–14

    Article  Google Scholar 

  • Khan MIR, Ashfaque F, Chhillar H, Irfan M, Khan NA (2021) The intricacy of silicon, plant growth regulators and other signaling molecules for abiotic stress tolerance: an entrancing crosstalk between stress alleviators. Plant Physiol Biochem 162:36–47

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Numan M, Bilal S, Asaf S, Crafword K, Imran M, Al-Harrasi A, Al-Sabahi JN, ur Rehman N, Ahmed A (2022a) Mangrove’s rhizospheric engineering with bacterial inoculation improve degradation of diesel contamination. J Hazard Mater 423:127046

    Article  CAS  PubMed  Google Scholar 

  • Khan T, Bilal S, Asaf S, Alamri SS, Imran M, Khan AL, Al-Rawahi A, Lee I-J, Al-Harrasi A (2022b) Silicon-induced tolerance against arsenic toxicity by activating physiological, anatomical and biochemical regulation in Phoenix dactylifera (date palm). Plants 11(17):2263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koza NA, Adedayo AA, Babalola OO, Kappo AP (2022) Microorganisms in plant growth and development: roles in abiotic stress tolerance and secondary metabolites secretion. Microorganisms 10 (8):1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar N, Dubey RC (2022) Plant growth promoting endophytic bacteria Bacillus australimaris BLR41 and Enterobacter kobei BLR45 enhance the growth of medicinal plant Barleria lupulina Lindl. Journal of Pure & Applied Microbiology 16(4):2647–2658 https://doi.org/10.22207/JPAM.16.4.32

    Article  Google Scholar 

  • Kusale SP, Attar YC, Sayyed R, Malek RA, Ilyas N, Suriani NL, Khan N, El Enshasy HA (2021) Production of plant beneficial and antioxidants metabolites by Klebsiella variicola under salinity stress. Molecules 26(7):1894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale J, Huang B (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for cree** bentgrass. Plant Growth Regul 47:17–28

    Article  CAS  Google Scholar 

  • Liu Y, Nessa A, Zheng Q, Hu D, Zhang W, Zhang M (2023) Inoculations of phosphate-solubilizing bacteria alter soil microbial community and improve phosphorus bioavailability for moso bamboo (Phyllostachys edulis) growth. Appl Soil Ecol 189:104911

    Article  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42(6):565–572

    Article  CAS  PubMed  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166(2):525–530

    Article  CAS  Google Scholar 

  • Msimbira LA, Smith DL (2020) The roles of plant growth promoting microbes in enhancing plant tolerance to acidity and alkalinity stresses. Front Sustain Food Syst 4:106

    Article  Google Scholar 

  • Narayanan Z, Glick BR (2022) Secondary metabolites produced by plant growth-promoting bacterial endophytes. Microorganisms 10(10):2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathan SI, Ceccherini MT, Sunseri F, Lupini A (2020) Rhizosphere as hotspot for plant-soil-microbe interaction. In: Datta R, Meena RS, Pathan SI, Ceccherini MT (eds) Carbon and nitrogen cycling in soil. Springer Singapore, Singapore, pp 17–43. https://doi.org/10.1007/978-981-13-7264-3_2

    Chapter  Google Scholar 

  • Per TS, Khan MIR, Anjum NA, Masood A, Hussain SJ, Khan NA (2018) Jasmonates in plants under abiotic stresses: crosstalk with other phytohormones matters. Environ Exp Bot 145:104–120

    Article  CAS  Google Scholar 

  • Rai AC, Singh M, Shah K (2012) Effect of water withdrawal on formation of free radical, proline accumulation and activities of antioxidant enzymes in ZAT12-transformed transgenic tomato plants. Plant Physiol Biochem 61:108–114

    Article  Google Scholar 

  • Ramasamy M (2020) Role of fungi in agriculture. biostimulants in plant science, Intech. Open Vol 12 https://doi.org/10.5772/intechopen.89718

  • Rana KL, Kour D, Kaur T, Devi R, Yadav AN, Yadav N, Dhaliwal HS, Saxena AK (2020) Endophytic microbes: biodiversity, plant growth-promoting mechanisms and potential applications for agricultural sustainability. Antonie Van Leeuwenhoek 113:1075–1107

    Article  CAS  PubMed  Google Scholar 

  • Reis MNO, Vitorino LC, Lourenço LL, Bessa LA (2022) Microbial inoculation improves growth, nutritional and physiological aspects of Glycine max (L.) Merr. Microorganisms 10(7):1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riva V, Mapelli F, Dragonetti G, Elfahl M, Vergani L, Crepaldi P, La Maddalena N, Borin S (2021) Bacterial inoculants mitigating water scarcity in tomato: the importance of long-term in vivo experiments. Front Microbiol 12:675552

    Article  PubMed  PubMed Central  Google Scholar 

  • Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues, Francisca, (2024) Are tomato plants co-exposed to heat and salinity able to ensure a proper carbon metabolism?–An insight into the photosynthetic hub. Plant Physiology and Biochemistry 206:108270

    Article  CAS  PubMed  Google Scholar 

  • Shahzad R, Khan AL, Bilal S, Waqas M, Kang S-M, Lee I-J (2017) Inoculation of abscisic acid-producing endophytic bacteria enhances salinity stress tolerance in Oryza sativa. Environ Exp Bot 136:68–77

    Article  CAS  Google Scholar 

  • Shahzad R, Khan AL, Bilal S, Asaf S, Lee I-J (2018) What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci 9:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Shamshiri RR, Jones JW, Thorp KR, Ahmad D, Man HC, Taheri S (2018) Review of optimum temperature, humidity, and vapour pressure deficit for microclimate evaluation and control in greenhouse cultivation of tomato: a review. Int Agrophys 32(2):287–302

    Article  Google Scholar 

  • Sheahan M, Gould CA, Neumann JE, Kinney PL, Hoffmann S, Fant C, Wang X, Kolian M (2022) Examining the relationship between climate change and vibriosis in the United States: projected health and economic impacts for the 21st century. Environ Health Perspect 130(8):087007

    Article  PubMed  PubMed Central  Google Scholar 

  • Snowdon RJ, Wittkop B, Chen T-W, Stahl A (2021) Crop adaptation to climate change as a consequence of long-term breeding. Theor Appl Genet 134(6):1613–1623

    Article  PubMed  Google Scholar 

  • Sousa, Bruno, (2022) Impact of combined heat and salt stresses on tomato plants—insights into nutrient uptake and redox homeostasis. Antioxidants1 11(3):478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sumanta N, Haque CI, Nishika J, Suprakash R (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 2231:606X

    Google Scholar 

  • Teshome DT, Zharare GE, Naidoo S (2020) The threat of the combined effect of biotic and abiotic stress factors in forestry under a changing climate. Front Plant Sci 11:1874

    Article  Google Scholar 

  • Tokić M, Leljak Levanić D, Ludwig-Müller J, Bauer N (2023) Growth and molecular responses of tomato to prolonged and short-term heat exposure. Int J Mol Sci 24(5):4456

    Article  PubMed  PubMed Central  Google Scholar 

  • Verma D, Singh K (2021) Understanding role of glutathione reductase gene family in drought and heat stresses in Brassica juncea and B. rapa. Environ Exp Bot 190:104595

    Article  CAS  Google Scholar 

  • Zandalinas SI, Fritschi FB, Mittler R (2021) Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci 26(6):588–599

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Lu Z, Wang L, ** B (2020) Plant responses to heat stress: physiology, transcription, noncoding RNAs, and epigenetics. Int J Mol Sci 22(1):117

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou R, Yu X, Ottosen C-O, Rosenqvist E, Zhao L, Wang Y, Yu W, Zhao T, Wu Z (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biol 17(1):1–13

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Research Foundation of Korea (NRF)grant funded by the Korea government (MSIT) (No. 2022R1A2C1008993).

Author information

Authors and Affiliations

Authors

Contributions

SSJ, NAK, MI, and L performed experimental and analysis. SA, SB, RS performed Biochemical analysis and wrote the draft manuscript and statistical analysis. SA, L, performed hormonal analysis and statistical analysis of data. SB, I-J.L and AA-H, supervision and arranging resources.

Corresponding authors

Correspondence to Saqib Bilal or Ahmed Al-Harrasi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Handling Editor: Axel Mithöfer.

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.

Supplementary file1 (DOCX 625 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jan, S.S., Khan, N.A., Asaf, S. et al. Consortium of Endophytic Bacillus australimaris CK11 and Staphylococcus epidermidis CK9 from Commiphora gileadensis Mediates Tomato Resilience to Combined Salinity, Heat, and Drought Stresses. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11394-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00344-024-11394-9

Keywords

Navigation