Skip to main content
SpringerLink
Log in

Differential Activity of Autochthonous Bacteria in Controlling Drought Stress in Native Lavandula and Salvia Plants Species Under Drought Conditions in Natural Arid Soil

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The effectiveness of autochthonous plant growth-promoting rhizobacteria was studied in Lavandula dentata and Salvia officinalis growing in a natural arid Mediterranean soil under drought conditions. These bacteria identified as Bacillus megaterium (Bm), Enterobacter sp. (E), Bacillus thuringiensis (Bt), and Bacillus sp. (Bsp). Each bacteria has different potential to meliorate water limitation and alleviating drought stress in these two plant species. B. thuringiensis promoted growth and drought avoidance in Lavandula by increasing K content, by depressing stomatal conductance, and it controlled shoot proline accumulation. This bacterial effect on increasing drought tolerance was related to the decrease of glutathione reductase (GR) and ascorbate peroxidase (APX) that resulted sensitive indexes of lower cellular oxidative damage involved in the adaptative drought response in B. thuringiensis-inoculated Lavandula plants. In contrast, in Salvia, having intrinsic lower shoot/root ratio, higher stomatal conductance and lower APX and GR activities than Lavandula, the bacterial effects on nutritional, physiological and antioxidant enzymatic systems were lower. The benefit of bacteria depended on intrinsic stress tolerance of plant involved. Lavadula demonstrated a greater benefit than Salvia to control drought stress when inoculated with B. thuringiensis. The bacterial drought tolerance assessed as survival, proline, and indolacetic acid production showed the potential of this bacteria to help plants to grow under drought conditions. B. thuringiensis may be used for Lavandula plant establishment in arid environments. Particular characteristic of the plant species as low shoot/root ratio and high stomatal conductance are important factors controlling the bacterial effectiveness improving nutritional, physiological, and metabolic plant activities.

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

Similar content being viewed by others

Abbreviations

PGPR:

Plant growth promoting rhizobacteria

GR:

Glutathione reductase

APX:

Ascorbate peroxidase

SOD:

Superoxide dismutase

CAT:

Catalase

IAA:

Indolacetic acid

Bm:

Bacillus megaterium

E:

Enterobacter sp.

Bt:

Bacillus thuringiensis

Bsp:

Bacillus sp.

References

  1. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  CAS  PubMed  Google Scholar 

  2. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47:453–467

    Article  CAS  PubMed  Google Scholar 

  3. Marulanda A, Barea JM, Azcón R (2006) An indigenous drought-tolerant strain of Glomus intraradices associated with a native bacterium improves water transport and root development in Retama sphaerocarpa. Microb Ecol 52:670–678

    Article  CAS  PubMed  Google Scholar 

  4. Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments. Mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124

    Article  CAS  Google Scholar 

  5. Kasim WA, Osman ME, Omar MN, Abd El-Daim IA, Bejai S, Meijer J (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32:122–130

    Article  CAS  Google Scholar 

  6. Barea JM, Azcón R, Azcón-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Anton Leeuw Int J G 81:343–351

    Article  CAS  Google Scholar 

  7. Medina A, Azcón R (2012) Reclamation strategies of semiarid Mediterranean soil: improvement of the efficiency of arbuscular mycorrhizal fungi by inoculation of plant growth promoting microorganisms and organic amendments. In: Hafidi M, Duponnois R (eds) The mycorrhizal symbiosis in Mediterranean environment: importance in ecosystem stability and in soil rehabilitation strategies. Nova Science, New York, pp 87–106

    Google Scholar 

  8. Marulanda A, Azcón R, Ruíz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533

    Article  CAS  Google Scholar 

  9. Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168

    Article  CAS  Google Scholar 

  10. Nowak J (1998) Benefits of in vitro “biotization” of plant tissue cultures with microbial inoculants. In Vitro Cell Dev Biol Plant 34:122–130

    Article  Google Scholar 

  11. Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology—a charging concept. Plant Physiol Biochemistry 48:292–300

    Article  CAS  Google Scholar 

  12. Benabdellah K, Abbas Y, Abourouh M, Aroca R, Azcon R (2011) Influence of two bacterial isolates from degraded and non-degraded soils and arbuscular mycorrhizae fungi isolated from semi-arid zone on the growth of Trifolium repens under drought conditions: mechanisms related to bacterial effectiveness. Eur J Soil Biol 47:303–309

    Article  Google Scholar 

  13. Ruíz-Sánchez M, Aroca R, Munoz Y, Polon R, Ruíz-Lozano JM (2010) The arbuscular mycorrhizal symbiosis enhances the photosynthetic efficiency and the antioxidative response of rice plants subjected to drought stress. J Plant Physiol 167:862–869

    Article  PubMed  Google Scholar 

  14. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic-stress. Microbiol Rev 53:121–147

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Glick BR (1995) The enhancement of plant-growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  16. Phillips JM, Hayman DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:159–161

    Article  Google Scholar 

  17. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  18. Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586

    Article  CAS  Google Scholar 

  19. Aroca R, Irigoyen JJ, Sánchez-Díaz M (2003) Drought enhances maize chilling tolerance. II. Photosynthetic traits and protective mechanisms against oxidative stress. Physiol Plant 117:540–549

    Article  CAS  PubMed  Google Scholar 

  20. Burd GI, Dixon DG, Glick BR (2000) Plant growth promoting bacteria that decreased heavy metal toxicity in plants. Can J Microbiol 46:237–245

    Article  CAS  PubMed  Google Scholar 

  21. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  22. Amako K, Chen GX, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35:497–504

    CAS  Google Scholar 

  23. Carlberg I, Mannervik B (1985) Glutathione reductase. Methods Enzymol 113:484–489

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Gordon SA, Paleg LG (1957) Observations on the quantitative determination of indoleacetic acid. Physiol Plant 10:39–47

    Article  CAS  Google Scholar 

  28. Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42

    Article  Google Scholar 

  29. Loutfy N, El-Tayeb MA, Hassanen AM, Moustafa MFM, Sakuma Y, Inouhe M (2012) Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). J Plant Res 125:173–184

    Article  CAS  PubMed  Google Scholar 

  30. Shaul-Keinan O, Gadkar V, Ginzberg I, Grunzweig JM, Chet I, Elad Y, Wininger S, Belausov E, Eshed Y, Arzmon N, Ben-Tal Y, Kapulnik Y (2002) Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomus intraradices. New Phytol 154:501–507

    Article  CAS  Google Scholar 

  31. Rodríguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y-O, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416

    Article  PubMed  Google Scholar 

  32. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  33. Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ Microbiol 10:1–9

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  35. Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181:413–423

    Article  CAS  PubMed  Google Scholar 

  36. Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agric Res 56:715–721

    Article  Google Scholar 

  37. Sakamoto M, Munemura I, Tomita R, Kobayashi K (2008) Involvement of hydrogen peroxide in leaf abscission signaling, revealed by analysis with an in vitro abscission system in Capsicum plants. Plant J 56:13–27

    Article  CAS  PubMed  Google Scholar 

  38. Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4

    Article  CAS  PubMed  Google Scholar 

  39. Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Can J Bot 82:273–281

    Article  Google Scholar 

  40. Zhang Y, Wang Z, Zhang L, Cao Y, Huang D, Tang K (2006) Molecular cloning and stress-dependent regulation of potassium channel gene in Chinese cabbage (Brassica rapa ssp Pekinensis). J Plant Physiol 163:968–978

    Article  CAS  PubMed  Google Scholar 

  41. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Gong HJ, Zhu XY, Chen KM, Wang SM, Zhang CL (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321

    Article  CAS  Google Scholar 

  43. Orvar BL, Ellis BE (1997) Transgenic tobacco plants expressing antisense RNA for cytosolic ascorbate peroxidase show increased susceptibility to ozone injury. Plant J 11:1297–1305

    Article  CAS  Google Scholar 

  44. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agron Sustain Dev 29:185–212

    Article  Google Scholar 

  45. Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136

    Article  CAS  PubMed  Google Scholar 

  46. Jiménez A, Hernández JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    PubMed Central  PubMed  Google Scholar 

  47. Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  48. Kohler J, Hernández JA, Caravaca F, Roldán A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151

    Article  CAS  Google Scholar 

  49. Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  50. Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Correa Molinari HB, Marur CJ, Esteves Vieira LG (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376

    Article  CAS  PubMed  Google Scholar 

  51. Azcón R, Medina A, Aroca R, Ruíz-Lozano R (2013) Abiotic stress remediation by the arbuscular mycorrhizal symbiosis and rhizosphere bacteria/yeast interactions. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Wiley, Hoboken, pp 991–1002

    Chapter  Google Scholar 

Download references

Acknowledgments

E. Armada was financed by Ministerio de Ciencia e Innovación. This work was carried out in the framework of the project reference AGL2009-12530-C02-02. We thank the Instrumentation Service (EEZ) for the plant analysis.

Author information

Authors and Affiliations

  1. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, Prof. Albareda 1, 18008, Granada, Spain

    Elisabeth Armada & Rosario Azcon

  2. Department of Soil and Water Conservation, Centro de Edafología y Biología Aplicada del Segura, CSIC, P.O. Box 164, Campus de Espinardo, 30100, Murcia, Spain

    Antonio Roldán

Authors
  1. Elisabeth Armada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Antonio Roldán
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rosario Azcon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosario Azcon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Armada, E., Roldán, A. & Azcon, R. Differential Activity of Autochthonous Bacteria in Controlling Drought Stress in Native Lavandula and Salvia Plants Species Under Drought Conditions in Natural Arid Soil. Microb Ecol 67, 410–420 (2014). https://doi.org/10.1007/s00248-013-0326-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0326-9

Keywords

Search

Navigation