Advertisement

Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth

  • Shweta Tiwari
  • Pratibha Singh
  • Rameshwar Tiwari
  • Kamlesh K. Meena
  • Mahesh Yandigeri
  • Dhananjaya P. SinghEmail author
  • Dilip K. Arora
Original Paper

Abstract

Salt-tolerant isolates Bacillus pumilus, Pseudomonas mendocina, Arthrobacter sp., Halomonas sp., and Nitrinicola lacisaponensis isolated from high saline habitats exhibited plant growth-promoting traits like P solubilization and indole acetic acid (IAA), siderophore, and ammonia production. These isolates were inoculated in wheat to assess microbe-mediated responses and plant growth promotion in salt affected soil. Maximum shoot and root length (33.8 and 13.6 cm) and shoot and root biomass (2.73 and 4.48 g dry weight) was recorded in plants inoculated with B. pumilus after 30 days. Total chlorophyll content was maximum in the leaves of the plants treated with Halomonas sp. (24.22 mg g−1 dry weight) followed by B. pumilus (23.41 mg g−1 dry weight) as compared to control (18.21 mg g−1 dry weight) after 30 days. Total protein content was maximum in Arthrobacter sp. inoculated plant leaves (3.19 mg g−1 dry weight) followed by B. pumilus (2.47 mg g−1 dry weight) as compared to control (2.15 mg g−1 dry weight) after 30 days. Total carotenoid content was maximum in plants inoculated with Halomonas sp. (1,075.45 and 1,113.29 μg g−1 dry weight) in comparison to control (837.32 and 885.85 μg g−1 dry weight) after 15 and 30 days. Inoculation of bacterial isolates increased presence of individual phenolics (gallic, caffeic, syringic, vanillic, ferulic, and cinnamic acids) and flavonoid quercetin in the rhizosphere soil. The concentration of IAA in rhizosphere soil and root exudates was also higher in all treatments than in control. Accumulation of phenolics and quercetin in the plants played a cumulative synergistic role that supported enhanced plant growth promotion of wheat in the stressed soil.

Keywords

Plant growth promotion Stress tolerance Bacillus pumilus Phenolics Flavonoids 

Notes

Acknowledgment

Authors are thankful to the Indian Council of Agricultural Research (ICAR), New Delhi, India for financial assistance under the Network project “Application of Microorganisms in Agriculture and Allied Sectors” (AMAAS).

References

  1. Amirjani MR (2010) Effect of salinity stress on growth, mineral composition, proline content, antioxidant enzymes of soybean. Am J Plant Physiol 5:350–360CrossRefGoogle Scholar
  2. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  3. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway? Trends Plant Sci 9:26–32PubMedCrossRefGoogle Scholar
  4. Bano A, Fatima M (2009) Salt tolerance in Zea mays L. following inoculation with Rhizobium and Pseudomonas. Biol Fert Soils 45:405–413CrossRefGoogle Scholar
  5. Barriuso J, Ramos Solano B, Gutiérrez Mañero FJ (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathol 98:666–672CrossRefGoogle Scholar
  6. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  7. Bhattacharya A, Sood P, Citovsky V (2010) The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11:705–719PubMedGoogle Scholar
  8. Brencic A, Winans SC (2005) Detection of and response to signals involved in host–microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194PubMedCrossRefGoogle Scholar
  9. Brick JM, Bostock RM, Silverstone SE (1991) Rapid in-situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Appl Environ Microbiol 57:535–538Google Scholar
  10. Castro-Sowinski S, Herschkovitz Y, Okon Y, Jurkevitch E (2007) Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms. FEMS Microbiol Lett 276:1–11PubMedCrossRefGoogle Scholar
  11. Cogdel RJ, Frank HA (1987) How carotenoids function in photosynthetic bacteria. Biochim Biophys Acta 895:63–79Google Scholar
  12. Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: further prospects. Aust J Exp Agr 45:1425–1443CrossRefGoogle Scholar
  13. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18PubMedCrossRefGoogle Scholar
  14. Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206PubMedCrossRefGoogle Scholar
  15. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L) by application of plant growth promoting rhizobacteria. Microbiol Res 159:371–394PubMedCrossRefGoogle Scholar
  16. Dey C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694CrossRefGoogle Scholar
  17. Edwards U, Rogall TH, Blocker H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853PubMedCrossRefGoogle Scholar
  18. Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fert Soils 45:563–571CrossRefGoogle Scholar
  19. Egamberdieva D, Kucharova Z, Davranov K, Berg G, Makarova N, Azarova T, Chetobar V, Tikhonovich I, Kamilova F, Validov SZ, Lugtenberg B (2011) Bacteria able to control foot and root rot and to promote growth of cucumber in salinated soils. Biol Fert Soils 47:197–205CrossRefGoogle Scholar
  20. Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003) Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637PubMedCrossRefGoogle Scholar
  21. Gaur AC (1990) Physiological functions of phosphate solubilizing micro-organisms. In: Gaur AC (ed) Phosphate solubilizing micro-organisms as biofertilizers. Omega Scientific, New Delhi, pp 16–72Google Scholar
  22. Graham HN (1992) Green tea composition, consumption and polyphenol chemistry. Prev Med 21:334–350PubMedCrossRefGoogle Scholar
  23. Ikuta SK, Matuura S, Imamura H, Misaki HY (1977) Oxidative pathway of choline to betaine in the soluble fraction prepared from Arthrobacter globiformis. J Biochem 82:157–163PubMedGoogle Scholar
  24. Jones MG (2009) Using resources from the model plant Arabidopsis thaliana to understand effects of abiotic stress. Salinity Water Stress 44:129–132CrossRefGoogle Scholar
  25. Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487CrossRefGoogle Scholar
  26. Kerepesi I, Galiba G, Banyai E (1998) Osmotic and salt stresses induced differential alteration in water-soluble carbohydrate content in wheat seedlings. J Agr Food Chem 46:5347–5354CrossRefGoogle Scholar
  27. Kim D, Jeong SW, Lee CY (2003) Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81:321–326CrossRefGoogle Scholar
  28. Kothandaraman N, Chanbasha B, Vladimir BB, Swarup S (2003) Enhancement of plant–microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153CrossRefGoogle Scholar
  29. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  30. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556PubMedCrossRefGoogle Scholar
  31. Maness N (2010) Extraction and analysis of soluble carbohydrates. Methods Mol Biol 639:341–370PubMedCrossRefGoogle Scholar
  32. Meena KK, Mesapogu S, Kumar M, Yandigeri MS, Singh G, Saxena AK (2010) Co-inoculation of the endophytic fungus Piriformospora indica with the P-solubilizing bacteria Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol Fert Soils 46:169–174CrossRefGoogle Scholar
  33. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149PubMedCrossRefGoogle Scholar
  34. Naz I, Bano A, Ul-Hassan T (2009) Isolation of phytohormones producing plant growth promoting rhizobacteria from weeds growing in Khewra salt range, Pakistan and their implication in providing salt tolerance to Glycine max. L. Afr J Biotech 8:5762–5766Google Scholar
  35. Neelam T, Meenu S (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5:51–58CrossRefGoogle Scholar
  36. Nelson EB (2004) Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol 42:271–309PubMedCrossRefGoogle Scholar
  37. O'Callaghan KJ, Stone PJ, Hu X, Griffiths DW, Davey MR, Cocking EC (2000) Effects of glucosinolates and flavonoids on colonization of the roots of Brassica napus by Azorhizobium caulinodans ORS571. Appl Environ Microbiol 66:2185–2191PubMedCrossRefGoogle Scholar
  38. Ortíz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, López-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712PubMedCrossRefGoogle Scholar
  39. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15PubMedCrossRefGoogle Scholar
  40. Pospiech A, Neumann B (1995) A versatile quick-prep of genomic DNA from gram-positive bacteria. Trends Genet 11:217–218PubMedCrossRefGoogle Scholar
  41. Rabie GG, Almandini AM (2005) Role of bioinoculants in development of salt-tolerance of Vicia faba plants under salinity stress. Afr J Biotech 4:210–223Google Scholar
  42. Sadasivam S, Manikam A (1992) Biochemical methods. Wiley Port of University Grants Commission, New DelhiGoogle Scholar
  43. Sairam RK, Shukla DS, Saxena DC (1997) Stress induced injury and antioxidant enzymes in relation to drought tolerance in wheat genotypes. Biol Plant 40:357–364CrossRefGoogle Scholar
  44. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophore. Anal Biochem 160:47–56PubMedCrossRefGoogle Scholar
  45. Scurtz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30CrossRefGoogle Scholar
  46. Siddikee MA, Chauhan PS, Anandham R, Han GH, Sa T (2010) Isolation, characterization and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584PubMedCrossRefGoogle Scholar
  47. Singh UP, Sarma BK, Singh DP (2003) Effect of plant growth-promoting rhizobacteria and culture filtrate of Sclerotium rolfsii on phenolic and salicylic acid contents in chickpea (Cicer arietinum). Curr Microbiol 44:131–140CrossRefGoogle Scholar
  48. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Smalla G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shift revealed. Appl Environ Microbiol 67:4742–4751PubMedCrossRefGoogle Scholar
  49. Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190CrossRefGoogle Scholar
  50. Sutee C, Cha-um S, Sompornpailin K (2009) Differential accumulations of proline and flavonoids in indica rice varieties against salinity. Pak J Bot 41:2497–2506Google Scholar
  51. Tripathi AK, Mishra BM, Tripathi P (1998) Salinity stress responses in the plant growth promoting rhizobacteria, Azospirillum spp. J Biosci 23:463–471CrossRefGoogle Scholar
  52. Umbrient WW, Burris RH, Stauffer J, Cohen P, Johnson WJ, Leepxgi GA, Patter VR, Schneider WCI (1959) Monometric Techniques, a manual describing methods applicable to the study of tissue metabolism. Burgess, MinneapolisGoogle Scholar
  53. Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479PubMedCrossRefGoogle Scholar
  54. Whips JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511Google Scholar
  55. Wu CH, Bernard SM, Anderson GL, Chen W (2009) Developing microbe–plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microb Biotechnol 2:428–440PubMedCrossRefGoogle Scholar
  56. Yang J, Kloepper JW, Ryu C-M (2008) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4PubMedCrossRefGoogle Scholar
  57. Yang CH, Chai Q, Huang GB (2010) Root distribution and yield responses of wheat/maize intercropping to alternate irrigation in the arid areas of northwest China. Plant Soil Environ 56:253–262Google Scholar
  58. Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Shweta Tiwari
    • 1
  • Pratibha Singh
    • 1
  • Rameshwar Tiwari
    • 1
  • Kamlesh K. Meena
    • 1
  • Mahesh Yandigeri
    • 1
  • Dhananjaya P. Singh
    • 1
    Email author
  • Dilip K. Arora
    • 1
  1. 1.National Bureau of Agriculturally Important MicroorganismsKushmaurIndia

Personalised recommendations