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Plant Growth Promotion at Low Temperature by Phosphate-Solubilizing Pseudomonas Spp. Isolated from High-Altitude Himalayan Soil

Abstract

Scarcity of arable land, limited soil nutrient availability, and low-temperature conditions in the Himalayan regions need to be smartly managed using sustainable approaches for better crop yields. Microorganisms, able to efficiently solubilize phosphate at low temperatures, provide an opportunity to promote plant growth in an ecofriendly way. In this study, we have investigated the ability of psychrotolerant Pseudomonas spp., isolated from high altitudes of Indian Himalaya to solubilize P at low temperature. Quantitative estimation of phosphate solubilization and production of relevant enzymes at two different temperatures (15 and 25 °C) was performed for 4 out of 11 selected isolates, namely, GBPI_506 (Pseudomonas sp.), GBPI_508 (Pseudomonas palleroniana), GBPI_Hb61 (Pseudomonas proteolytica), and GBPI_CDB143 (Pseudomonas azotoformans). Among all, isolate GBPI_CDB143 showed highest efficiency to solubilize tri-calcium phosphate (110.50 ± 3.44 μg/mL) at 25 °C after 6 days while the culture supernatants of isolate GBPI_506 displayed the highest phytase activity (15.91 ± 0.35 U/mL) at 15 °C and alkaline phosphatase (3.09 ± 0.07 U/mL) at 25 °C in 6 and 9 days, respectively. Out of five different organic acids quantified, oxalic acid and malic acid were produced in maximum quantity by all four isolates. With the exception of GBPI_508, inoculation of bacteria promoted overall growth (rosette diameter, leaf area, and biomass) of Arabidopsis thaliana plants as compared to uninoculated control plants in growth chamber conditions. The plant growth promotion by each bacterial isolate was further validated by monitoring root colonization in the inoculated plants. These bacterial isolates with low-temperature phosphate solubilization potential along with phosphatases and phytase activity at low temperature could be harnessed for sustainable crop production in P-deficient agricultural soils under mountain ecosystems.

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References

  1. 1.

    Stigter KA, Plaxton WC (2015) Molecular mechanisms of phosphorus metabolism and transport during leaf senescence. Plants (Basel) 4(4):773–798. https://doi.org/10.3390/plants4040773

    CAS  Article  Google Scholar 

  2. 2.

    Rychter AM, Rao IM, Cardoso JA (2016) Role of phosphorus in photosynthetic carbon assimilation and partitioning. In: Pessarakli M (ed) Handbook of photosynthesis. CRC Press, Boca Raton. https://doi.org/10.1201/9781315372136

    Chapter  Google Scholar 

  3. 3.

    Malhotra H, Vandana Sharma S, Pandey R (2018) Phosphorus nutrition: plant growth in response to deficiency and excess. In: Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B (eds) Plant nutrients and abiotic stress tolerance. Springer, Singapore, pp 171–190

    Chapter  Google Scholar 

  4. 4.

    Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol 8:971. https://doi.org/10.3389/fmicb.2017.00971

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996. https://doi.org/10.1104/pp.111.175448

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18:607–621. https://doi.org/10.1038/s41579-020-0412-1

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int J Agron 4917256:1–7

    Article  Google Scholar 

  8. 8.

    Rinu K, Pandey A, Palni LMS (2012) Utilization of psychrotolerant phosphate solubilizing fungi under low temperature conditions of the mountain ecosystem. In: Satyanarayana T, Johri B, Prakash A (eds) Microorganisms in sustainable agriculture and biotechnology. Springer, Dordrecht, pp 77–90. https://doi.org/10.1007/978-94-007-2214-9_5

  9. 9.

    Liu J, Qi W, Li Q, Wang SG, Song C, Yuan XZ (2020) Exogenous phosphorus-solubilizing bacteria changed the rhizosphere microbial community indirectly. 3 Biotech 10:164

    Article  Google Scholar 

  10. 10.

    Liu L, Li A, Chen J, Su X, Li Y, Ma A (2018) Isolation of a phytase-producing bacterial strain from agricultural soil and its characterization and application as an effective eco-friendly phosphate solubilizing bioinoculant. Commun Soil Sci Plant Anal 49(8):984–994

    CAS  Article  Google Scholar 

  11. 11.

    Singh B, Satyanarayana T (2011) Microbial phytases in phosphorus acquisition and plant growth promotion. Physiol Mol Biol Plants 17(2):93–103. https://doi.org/10.1007/s12298-011-0062-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Trivedi P, Pandey A, Palni LMS (2012) Bacterial inoculants for field applications under Mountain Ecosystem: present initiatives and future prospects. In: Maheshwari DK (ed) Bacteria in agrobiology: plant probiotics. Springer, Berlin Heidelberg, pp 15–44. https://doi.org/10.1007/978-3-542-27515-9_2

  13. 13.

    Yarzábal LA (2014) Cold-tolerant phosphate-solubilizing microorganisms and agriculture development in mountainous regions of the world. In: Khan MS, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms. Springer International Publishing, Switzerland, pp 113–136

    Google Scholar 

  14. 14.

    Jain R, Pandey A (2016) A phenazine-1 carboxylic acid producing polyextremophilic Pseudomonas chlororaphis (MCC2693) strain, isolated from mountain ecosystem, possesses biocontrol and plant growth promotion abilities. Microbiol Res 190:63–71

    CAS  Article  Google Scholar 

  15. 15.

    Adhikari P, Pandey A (2019) Phosphate solubilization potential of endophytic fungi isolated from Taxus wallichiana Zucc. roots. Rhizosphere 9:2–9

    Article  Google Scholar 

  16. 16.

    Pandey A, Yarzabal LA (2019) Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl Microbiol Biotechnol 103(2):643–657

    CAS  Article  Google Scholar 

  17. 17.

    Yarzábal LA (2020) Perspectives for using glacial and periglacial microorganisms for plant growth promotion at low temperatures. Appl Microbiol Biotechnol 104:3267–3278. https://doi.org/10.1007/s00253-020-10468-4

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Pandey A, Sharma E, Palni LMS (1998) Influence of bacterial inoculation on maize in upland farming systems of the Sikkim Himalaya. Soil Biol Biochem 30:379–384

    CAS  Article  Google Scholar 

  19. 19.

    Jain R, Pandey N, Pandey A (2020) Aggregation properties of cold-active lipase produced by a psychrotolerant strain of Pseudomonas palleroniana (GBPI_508). Biocatal Biotransform 38(4):263–273

    CAS  Google Scholar 

  20. 20.

    Pandey A, Jain R, Sharma A, Dhakar K, Kaira GS, Rahi P, Dhyani A, Pandey N, Adhikari P, Shouche YS (2019) 16S rRNA gene sequencing and MALDI-TOF mass spectrometry based comparative assessment and bioprospection of psychrotolerant bacteria isolates from high altitudes under mountain ecosystem. SN Appl Sci 1:278

    CAS  Article  Google Scholar 

  21. 21.

    Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    CAS  Article  Google Scholar 

  22. 22.

    Chen W, Kuo T (1993) A simple and rapid method for the preparation of gram-negative bacterial genomic DNA. Nucleic Acids Res 21(9):2260. https://doi.org/10.1093/nar/21.9.2260

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–34

    Article  Google Scholar 

  24. 24.

    Khabarov N, Obersteiner M (2017) Global phosphorus fertilizer market and national policies: a case study revisiting the 2008 price peak. Front Nutr 4:22. https://doi.org/10.3389/fnut.2017.00022

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Praveen KV, Singh A (2019) Realizing the potential of a low-cost technology to enhance crop yields: evidence from a meta-analysis of biofertilizers in India. Agric Econ Res Rev 32:77–91. https://doi.org/10.5958/0974-0279.2019.00018.1

    Article  Google Scholar 

  26. 26.

    Sah S, Singh R (2016) Phylogenetical coherence of Pseudomonas in unexplored soils of Himalayan region. 3 Biotech 6:170–180

    Article  Google Scholar 

  27. 27.

    Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174–189

    Article  Google Scholar 

  28. 28.

    Yarzábal LA, Chica EJ (2019) Role of rhizobacterial secondary metabolites in crop protection against agricultural pests and diseases. In: Gupta VK, Pandey A (eds) New and future developments in microbial biotechnology and bioengineering. Elsevier, pp 31–53. https://doi.org/10.1016/B978-0-444-63504-4.00003-7

  29. 29.

    Kumar B, Trivedi P, Pandey A (2007) Pseudomonas corrugata: a suitable bacterial inoculant for maize grown under rainfed conditions of Himalayan region. Soil Biol Biochem 39:3093–3100

    CAS  Article  Google Scholar 

  30. 30.

    Selvakumar G, Joshi P, Suyal P, Mishra PK, Joshi GK, Venugopalan R, Bisht JK, Bhatt JC, Gupta HS (2013) Rock phosphate solubilization by psychrotolerant Pseudomonas spp. and their effect on lentil growth and nutrient uptake under polyhouse conditions. Ann Microbiol 63:1353–1362

    CAS  Article  Google Scholar 

  31. 31.

    Tomer S, Suyal DC, Shukla A, Rajwar J, Yadav A, Shouche Y, Goel R (2017) Isolation and characterization of phosphate solubilizing bacteria from Western Indian Himalayan soils. 3 Biotech 7(2):95–100

    Google Scholar 

  32. 32.

    Yarzábal LA, Monserrate L, Buela L, Chica E (2018) Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biol 41:2343–2354

    Article  Google Scholar 

  33. 33.

    Gulati A, Rahi P, Vyas P (2008) Characterization of phosphate-solubilizing fluorescent pseudomonads from the rhizosphere of seabuckthorn growing in the cold deserts of Himalayas. Curr Microbiol 56:73–79. https://doi.org/10.1007/s00284-007-9042-3

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Emami S, Alikhani HA, Pourbabaee AA, Etesami H, Motasharezadeh B, Sarmadian F (2020) Consortium of endophyte and rhizosphere phosphate solubilizing bacteria improve phosphorus use efficiency in wheat cultivars in phosphorus deficient soils. Rhizosphere 14:100196. https://doi.org/10.1016/j.rhisph.2020.100196

    Article  Google Scholar 

  35. 35.

    Perez E, Sulbaran M, Ball MM, Yarzabal LA (2007) Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biol Biochem 39:2905–2914

    CAS  Article  Google Scholar 

  36. 36.

    Behera BC, Yadav H, Singh SK, Mishra RR, Sethi BK, Dutta SK, Thatoi HN (2017) Phosphate solubilization and acid phosphatase activity of Serratia sp. isolated from mangrove soil of Mahanadi river delta, Odisha, India. J Genet Eng Biotechnol 15:169–178

    CAS  Article  Google Scholar 

  37. 37.

    Suleman M, Yasmin S, Rasul M, Yahya M, Atta BM, Mirza MS (2018) Phosphate solubilizing bacteria with glucose dehydrogenase gene for phosphorus uptake and beneficial effects on wheat. PLoS ONE 13(9):e0204408. https://doi.org/10.1371/journal.pone.0204408

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    de Amaral Leite A, de Souza Cardoso AA, de Almeida Leite R, de Oliveira-Longatti SM, Filho JFL, de Souza Moreira FM, Melo LCA (2020) Selected bacterial strains enhance phosphorus availability from biochar-based rock phosphate fertilizer. Ann Microbiol 70(6). https://doi.org/10.1186/s13213-020-01550-3

  39. 39.

    Srivastava S, Kausalya MT, Archana G, Rupela OP, Kumar NG (2007) Efficacy of organic acid secreting bacteria in solubilization of rock phosphate in acidic alfisols. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Developments in Plant and Soil Sciences, vol 102. Springer, Dordrecht

    Google Scholar 

  40. 40.

    Panhwar QA, Jusop S, Naher UA, Othman R, Razi MA (2013) Application of potential phosphate-solubilizing bacteria and organic acids on phosphate solubilization from phosphate rock in aerobic rice. Sci World J 272409:1–10

    Article  Google Scholar 

  41. 41.

    Yadav K, Kumar C, Archana G, Kumar N (2014) Pseudomonas fluorescens ATCC 13525 containing an artificial oxalate operon and vitreoscilla hemoglobin secretes oxalic acid and solubilizes rock phosphate in acidic alfisols. PLoSONE 9(4):e92400. https://doi.org/10.1371/journal.pone.0092400

    CAS  Article  Google Scholar 

  42. 42.

    Chen W, Yang F, Zhang L, Wang J (2016) Organic acid secretion and phosphate solubilizing efficiency of Pseudomonas sp. PSB12: effects of phosphorus forms and carbon sources. Geomicrobiol J 33(10):870–877

    CAS  Article  Google Scholar 

  43. 43.

    Shulse CN, Chovatia M, Agosto C, Wang G, Hamilton M, Deutsch S, Yoshikuni Y, Blow MJ (2019) Engineered root bacteria release plant-available phosphate from phytate. Appl Environ Microbiol 85:e01210–e01219. https://doi.org/10.1128/AEM.01210-19

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Valeeva LR, Nyamsuren C, Sharipova MR, Shakirov EV (2018) Heterologous expression of secreted bacterial BPP and HAP phytases in plants stimulates Arabidopsis thaliana growth on phytate. Front Plant Sci 9:186. https://doi.org/10.3389/fpls.2018.00186

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Chen Q, Liu S (2019) Identification and characterization of the phosphate solubilizing bacterium Pantoea sp. S32 in reclamation soil in Shanxi, China. Front Microbiol 10:2171. https://doi.org/10.3389/fmicb.2019.02171

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745. https://doi.org/10.3389/fmicb.2015.00745

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Wu F, Li J, Chen Y, Zhang L, ZhangY WS, Shi X, Li L, Liang J (2019) Effects of phosphate solubilizing bacteria on the growth, photosynthesis, and nutrient uptake of Camellia oleifera Abel. Forests 10:348. https://doi.org/10.3390/f10040348

    Article  Google Scholar 

  48. 48.

    Sachdev S, Singh RP (2018) Root colonization: imperative mechanism for efficient plant protection and growth. MOJ Ecol Environ Sci 3(4):240–242

    Google Scholar 

  49. 49.

    Zabihi HR, Savaghebi GR, Khavazi K (2011) Pseudomonas bacteria and phosphorus fertilization, affecting wheat (Triticum aestivum L.) yield and P uptake under greenhouse and field conditions. Acta Physiol Plant 33:145–152

    Article  Google Scholar 

  50. 50.

    Irshad U, Yergeau E (2018) Bacterial subspecies variation and nematode grazing change p dynamics in the wheat rhizosphere. Front Microbiol 9:1990–2001

    Article  Google Scholar 

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Acknowledgements

Directors, GB Pant National Institute of Himalayan Environment, Almora, Uttarakhand, CSIR – Institute of Himalayan Bioresource Technology, Palampur, Himachal Pradesh and National Centre for Cell Science, Pune are gratefully acknowledged for extending the facilities. PA thanks award of the National Mission on Himalayan Studies Fellowship under Ministry of Environment, Forest and Climate Change, Govt. of India, New Delhi.

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Correspondence to Anita Pandey.

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Adhikari, P., Jain, R., Sharma, A. et al. Plant Growth Promotion at Low Temperature by Phosphate-Solubilizing Pseudomonas Spp. Isolated from High-Altitude Himalayan Soil. Microb Ecol 82, 677–687 (2021). https://doi.org/10.1007/s00248-021-01702-1

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Keywords

  • Low temperature
  • Plant growth promotion
  • Arabidopsis thaliana
  • Fluorescence microscopy
  • Indian Himalayan region