Skip to main content

Drought Tolerance and Antioxidant Activities in Lavender Plants Colonized by Native Drought-tolerant or Drought-sensitive Glomus Species

Abstract

This study compared the effectiveness of four arbuscular mycorrhizal (AM) fungal isolates (two autochthonous presumably drought-tolerant Glomus sp and two allochthonous presumably drought-sensitive strains) on a drought-adapted plant (Lavandula spica) growing under drought conditions. The autochthonous AM fungal strains produced a higher lavender biomass, specially root biomass, and a more efficient N and K absorption than with the inoculation of similar allochthonous strains under drought conditions. The autochthonous strains of Glomus intraradices and Glomus mosseae increased root growth by 35% and 100%, respectively, when compared to similar allochthonous strains. These effects were concomitant with an increase in water content and a decline in antioxidant compounds: 25% glutathione, 7% ascorbate and 15% H2O2 by G. intraradices, and 108% glutathione, 26% ascorbate and 43% H2O2 by G. mosseae. Glutathione and ascorbate have an important role in plant protection and metabolic function under water deficit; the low cell accumulation of these compounds in plants colonized by autochthonous AM fungal strains is an indication of high drought tolerance. Non-significant differences between antioxidant activities such as glutathione reductase (GR), catalase (CAT) and superoxide dismutase (SOD) in colonized plants were found. Thus, these results do not allow the generalization that GR, CAT and SOD were correlated with the symbiotic efficiency of these AM fungi on lavender drought tolerance. Plants colonized by allochthonous G. mosseae (the less efficient strain under drought conditions) had less N and K content than those colonized by similar autochthonous strain. These ions play a key role in osmoregulation. The AM symbiosis by autochthonous adapted strains also produced the highest intraradical and arbuscular development and extraradical mycelial having the greatest fungal SDH and ALP-ase activities in the root systems. Inoculation of autochthonous drought tolerant fungal strains is an important strategy that assured the greatest tolerance water stress contributing to the best lavender growth under drought.

This is a preview of subscription content, access via your institution.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

References

  1. 1.

    Aebi, H (1984) Catalase in vitro. In: Packer, L (Ed.) Methods in Enzymology, vol 105. Oxygen Radicals in Biological Systems, Academic Press, London, pp 121–126

    Chapter  Google Scholar 

  2. 2.

    Allen, EB, Allen, MF (1986) Water relations of xeric grasses in the field: interactions of mycorrhizas and competition. New Phytol 104: 559–571

    Article  Google Scholar 

  3. 3.

    Aono, M, Kubo, A, Saji, H, Tanaka, K, Kondo, N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione-reductase activity. Plant Cell Physiol 34: 129–135

    CAS  Google Scholar 

  4. 4.

    Augé, RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11: 3–42

    Article  Google Scholar 

  5. 5.

    Azcón, R, Barea, JM (1997) Mycorrhizal dependency of a representative plant species in mediterranean shrublands (Lavandula spica) as a key factor to its use for revegetation strategies in desertification-threatened areas. Appl Soil Ecol 7:83–92

    Article  Google Scholar 

  6. 6.

    Barea, JM, Azcón, R, Azcón-Aguilar, C (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-fixing systems. In: Norris, JR, Read, DJ, Varma, A (Eds.) Methods in Microbiology, vol 24. Techniques for the Study of Mycorrhizae, Academic Press, London, pp 391–416

    Google Scholar 

  7. 7.

    Barea, JM, Azcón, R, Azcón-Aguilar, C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie Van Leeuwenhoek 81: 343–351

    PubMed  Article  CAS  Google Scholar 

  8. 8.

    Barea, JM, Jeffries, P (1995) Arbuscular mycorrhizas in sustainable soil plant systems. In: Varma, A, Hock, B (Eds.) Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology, Springer-Verlag, Heidelberg, pp 521–559

    Google Scholar 

  9. 9.

    Beyer, WF, Fridovich, I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161: 559–566

    PubMed  Article  CAS  Google Scholar 

  10. 10.

    Bowler, C, Vanmontagu, M, Inze, D (1992) Superoxide-dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43: 83–116

    Article  CAS  Google Scholar 

  11. 11.

    Bremner, JM (1996) Nitrogen total. In: Sparks, DL (Ed.) Methods of Soil Analysis. Part 3: Chemical Methods, Soil Science Society of America, American Society of Agronomy, Madison, USA, pp 1085–1121

    Google Scholar 

  12. 12.

    Brennan, T, Frenkel, C (1977) Involvement of hydrogen-peroxide in regulation of senescence in pear. Plant Physiol 59: 411–416

    PubMed  CAS  Google Scholar 

  13. 13.

    Bryla, DR, Duniway, JM (1997) Growth, phosphorus uptake, and water relations of safflower and wheat infected with an arbuscular mycorrhizal fungus. New Phytol 136: 581–590

    Article  Google Scholar 

  14. 14.

    Bryla, DR, Duniway, JM (1997) Water uptake by safflower and wheat roots infected with arbuscular mycorrhizal fungi. New Phytol 136: 591–601

    Article  Google Scholar 

  15. 15.

    Burrit, DJ, Larkindale, J, Hurd, CL (2002). Antioxidant metabolism in the intertidal red seaweed stictosiphonia arbuscular following desiccation. Planta 215: 829–838

    Article  CAS  Google Scholar 

  16. 16.

    Caravaca, F, Barea, JM, Palenzuela, J, Figueroa, D, Alguacil, MD, Roldan, A (2002) Establishment of shrubs species in a degraded semiarid site after inoculation with native or allochtohonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22: 103–111

    Article  Google Scholar 

  17. 17.

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

    PubMed  CAS  Article  Google Scholar 

  18. 18.

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

    Article  Google Scholar 

  19. 19.

    Essington, ME (2004) Soil and Water Chemistry: an Integrative Approach. CRC Press, Boca Raton, Florida

    Google Scholar 

  20. 20.

    Foyer, CH, López-Delgado, H, Dat, JF, Scott, IM (1997) Hydrogen peroxide and glutathiones-associated mechanisms of acclimatory stress tolerance and signalling. Physiol Plant 100: 241–254

    Article  CAS  Google Scholar 

  21. 21.

    Foyer, CH, Souriau, N, Perret, S, Lelandais, M, Kunert, KJ, Pruvost, C, Jouanin, L (1995) Overexpression of glutathione-reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109: 1047–1057

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Goicoechea, N, Szalai, G, Antolín, MC, Sánchez-Díaz, M, Paldi, E (1998) Influence of arbuscular mycorrhizar and Rhizobium on free polyamines and proline levels in water-stressed alfalfa. J Plant Physiol 153: 706–711

    CAS  Google Scholar 

  23. 23.

    Koide, RT (1993) Physiology of the mycorrhizal plant. Adv Plant Pathol 9: 33–54

    Google Scholar 

  24. 24.

    Lachica, M, Aguilar, A, Yañez, J (1973) Análisis foliar, métodos utilizados en la Estación Experimental del Zaidín. An Edafol Agrobiol 32: 1033–1047

    CAS  Google Scholar 

  25. 25.

    Law, MY, Charles, SA, Halliwell, B (1992) Glutathione and ascorbic acid in spinach (Spicacea oleracea) choloplast. The effect of hydrogen peroxide and Paraquat. Biochem J 210: 899–903

    Google Scholar 

  26. 26.

    Levine, A, Tenhaken, R, Dixon, R, Lamb, C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593

    PubMed  Article  CAS  Google Scholar 

  27. 27.

    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

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    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 

  29. 29.

    Monzón, A, Azcón, R (1996) Relevance of mycorrhizal fungal origin and host plant genotype to inducing growth and nutrient uptake in Medicago species. Agric Ecosyst Environ 60: 9–15

    Article  Google Scholar 

  30. 30.

    Niu, DK, Wang, MG, Wang, YF (1997) Plant cellular osmotic. Acta Biotheor 45: 161–169

    Article  Google Scholar 

  31. 31.

    Noctor, G, Foyer, CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49: 249–279

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    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 

  33. 33.

    Porcel, R, Barea, JM, Ruíz-Lozano, JM (2003) Antioxidant activities in mycorrhizal soybean under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157: 135–143

    Article  CAS  Google Scholar 

  34. 34.

    Requena, N, Jeffries, P, Barea, JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62: 842–847

    PubMed  CAS  Google Scholar 

  35. 35.

    Rontein, D, Basset, G, Hanson, AD (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4: 49–56

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    Roth, CH, Malicki, MA, Plagge, R (1992) Empirical evaluation of the relationship between soil dielectric constant and volumetric water content as the basis for calibrating soil moisture measurements. J Soil Sci 43: 1–13

    Article  Google Scholar 

  37. 37.

    Ruíz-Lozano, JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13: 309–317

    PubMed  Article  Google Scholar 

  38. 38.

    Ruíz-Lozano, JM, Azcón, R (1995) Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiol Plant 95: 472–478

    Article  Google Scholar 

  39. 39.

    Ruíz-Lozano, JM, Azcón, R (1996) Mycorrhizal colonization and drought stress as factors affecting nitrate reductase activity in lettuce plants. Agric Ecosyst Environ 60: 175–181

    Article  Google Scholar 

  40. 40.

    Ruíz-Lozano, JM, Azcón, R, Gómez, M (1995) Effects of arbuscular-mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61: 456–460

    PubMed  Google Scholar 

  41. 41.

    Smith, SE, Gianinazzi-Pearson, V (1990) Phosphate uptake and arbuscular activity in mycorrhizal Allium cepa L. Effects of photon irradiance and phosphate nutrition. Aust J Plant Physiol 17: 177–188

    CAS  Google Scholar 

  42. 42.

    Sumner, ME, Miller, WP (2007) Cation exchange capacity and exchange coefficients. In: Sparks, DL (Ed.) Methods of Soil Analysis. Part 3: Chemical Methods, Soil Science Society of America, American Society of Agronomy, Madison, USA, pp 1201–1229

    Google Scholar 

  43. 43.

    Thomas, HM, Morgan, WG, Humphreys, MW (2003) Designing grasses with a future—combining the attributes of Lolium and Festuca. Euphytica 133: 19–26

    Article  Google Scholar 

  44. 44.

    Tisserant, B, Gianinazzi-Pearson, V, Gianinazzi, S, Gollotte, A (1993) In Planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97: 245–250

    CAS  Article  Google Scholar 

  45. 45.

    Trouvelot, A, Fardeau, JC, Plenchette, C, Gianinazzi, S, Gianinazzi-Pearson, V (1986) Nutritional balance and symbiotic expression in mycorrhizal wheat. Physiol Veg 24: 300

    Google Scholar 

  46. 46.

    Vilariño, A, Arines, J (1990) An instrumental modification of Gerdeman and Nicolson’s method for extracting VAM fungal spores from soil samples. Plant Soil 121: 211–215

    Article  Google Scholar 

  47. 47.

    Vivas, A, Azcón, R, Biró, B, Barea, JM, Ruíz-Lozano, JM (2003) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pratense L. under lead toxicity. Can J Microbiol 49: 577–588

    PubMed  Article  CAS  Google Scholar 

  48. 48.

    White, I, Knight, J.H., Zegelin, SJ, Topp, GC (1994) Comments to “Considerations on the use of time-domain reflectometry (TDR) for measuring soil water content” by WR Whalley. J Soil Sci 45: 503–508

    Article  Google Scholar 

  49. 49.

    Wright, SF, Franckee-Snyder, M, Morton, M, Upadhyaya, A (1998) Time-course study and partial characterization of a protein on arbuscular mycorrhizal hyphae during active colonization of roots. Plant Soil 181: 193–203

    Article  Google Scholar 

  50. 50.

    Wright, SF, Nichols, KA, Schmidt, WF (2006) Comparison of efficacy of three extractants to solubilize glomalin on hyphae and soil. Chemosphere 64(7): 1219–1224

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    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: 1–12

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by GLO FEDER-National Plan (REN2003-00968). A. M. acknowledges AECI for financial support through a MAE Fellowship. We thank Dra. C. Lluch Plá and her group for the help in the determination of antioxidant activities, C. Cano who give inoculants of fungi AM from de E.E.Z collection and R. Aroca, R. Blanco, and F. Jahromi for correcting the English text.

Author information

Affiliations

Authors

Corresponding author

Correspondence to R. Azcón.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Marulanda, A., Porcel, R., Barea, J.M. et al. Drought Tolerance and Antioxidant Activities in Lavender Plants Colonized by Native Drought-tolerant or Drought-sensitive Glomus Species. Microb Ecol 54, 543 (2007). https://doi.org/10.1007/s00248-007-9237-y

Download citation

Keywords

  • Glutathione Reductase
  • Autochthonous
  • Volumetric Soil Moisture
  • Extraradical Mycelium
  • Plant Water Uptake