Mycorrhiza

, Volume 24, Issue 2, pp 121–129

Relationship between genetic variability in Rhizophagus irregularis and tolerance to saline conditions

Original Paper

Abstract

Reclamation of saline soils produced by extraction of bitumen from oil sands is challenging. The main objective of this study was to select a salt-tolerant arbuscular mycorrhizal (AM) fungal isolate that could, in the future, be used to pre-inoculate plants used in reclamation of saline substrates produced by oil sand industry. To achieve this, the effects of NaCl, Na2SO4, and saline release water from composite tailings (CT) on hyphal growth of two AM fungal isolates from non-saline (Rhizophagus irregularis DAOM 181602, Rhizophagus sp. DAOM 227023) and three isolates of R. irregularis isolated from saline or sodic soils (DAOM 234181, DAOM241558, and DAOM241559) were tested in vitro. Pre-symbiotic hyphal growth of the five isolates, in absence of a host plant, decreased with increasing salt stress and no spores germinated in CT. The symbiotic extraradical phase of the four isolates of R. irregularis developed well in saline media compared to the Rhizophagus sp. Nevertheless, fungal development of the four R. irregularis isolates differed in saline media indicating phenotypic variations between isolates.

Keywords

Arbuscular mycorrhizal fungi Rhizophagus Salt stress Spore germination Extraradical hyphae Intraspecificity 

References

  1. Al Karaki G (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hortic 109:1–7CrossRefGoogle Scholar
  2. Al Karaki G, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47CrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schaeffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCentralPubMedCrossRefGoogle Scholar
  4. Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schäffer AA, Yu YK (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J 272:5101–5109PubMedCentralPubMedCrossRefGoogle Scholar
  5. Azcòn-Aguilar C, Barea JM (1997) Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci Hortic 68:1–24CrossRefGoogle Scholar
  6. Bécard G, Fortin JA (1988) Early events of vesicular–arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108:211–218CrossRefGoogle Scholar
  7. Bois G, Piché Y, Fung M, Khasa DP (2005) Mycorrhizal inoculum potentials of pure reclamation materials and revegetated tailing sands from the Canadian oil sand industry. Mycorrhiza 15:149–158PubMedCrossRefGoogle Scholar
  8. Copeman R, Martin C, Stutz J (1996) Tomato growth in response to salinity and mycorrhizal fungi from saline or nonsaline soils. HortSci 31:341–344Google Scholar
  9. Daniels BA, Graham SO (1976) Effects of nutrition and soil extracts on germination of Glomus mossae spores. Mycologia 68:108–116CrossRefGoogle Scholar
  10. Daniels BA, Trappe JM (1980) Factors affecting spore germination of the vesicular–arbuscular mycorrhizal fungus Glomus epigeus. Mycologia 72:457–471CrossRefGoogle Scholar
  11. Danielson RM (1991) Temporal changes and effects of amendments on the occurrence of sheathing (ecto-) mycorrhizas of conifers growing in oil sands tailings and coal spoil. Agric Ecosyst Environ 35:261–281CrossRefGoogle Scholar
  12. Del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy metal contaminated soils. Appl Environ Microbiol 65:718–723PubMedCentralPubMedGoogle Scholar
  13. Ehinger M, Koch AM, Sanders IR (2009) Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. New Phytol 184:412–423PubMedCrossRefGoogle Scholar
  14. Estaun MV (1989) Effect of sodium chloride and mannitol on germination and hyphal growth of the vesicular–arbuscular mycorrhizal fungus Glomus mossae. Agric Ecosyst Environ 29:123–129CrossRefGoogle Scholar
  15. Estaun MV (1991) Effect of NaCl and mannitol on the germination of two isolates of the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Abstracts, 3rd European Symposium on Mycorrhizas. University of Sheffield, Sheffield, UKGoogle Scholar
  16. Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013a) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201–202:42–51PubMedCrossRefGoogle Scholar
  17. Estrada B, Barea JM, Aroca R, Ruiz-Lozano JM (2013b) A native Glomus intraradices strain from a Mediterranean saline area exhibits salt tolerance and enhanced symbiotic efficiency with maize plants under salt stress conditions. Plant Soil 366:333–349CrossRefGoogle Scholar
  18. Estrada B, Aroca R, Azcón-Aguilar C, Barea JM, Ruiz-Lozano JM (2013c) Importance of native arbuscular mycorrhizal inoculation in the halophyte Asteriscus maritimus for successful establishment and growth under saline conditions. Plant Soil. doi:10.1007/s11104-013-1635-y Google Scholar
  19. Fontaine J, Grandmougin-Ferjani A, Glorian V, Durand R (2004) 24-methyl/methylene sterols increase in monoxenic roots after colonization by arbuscular mycorrhizal fungi. New Phytol 163:159–167CrossRefGoogle Scholar
  20. FTFC (Fine Tailings Fundamentals Consortium) (1995) Volume II: Fine Tails and Process Water Reclamation. In: Advances in Oil Sands Tailings Research. Alberta Department of Energy, Oil Sands and Research Division, Edmonton, AB, CanadaGoogle Scholar
  21. Hepper CM, Smith GA (1976) Observations on the germination of Endogone spores. Trans Br Mycol Soc 66:189–194CrossRefGoogle Scholar
  22. Hirrel MC (1981) The effect of sodium and chloride salts on the germination of Gigaspora margarita. Mycologia 73:610–617CrossRefGoogle Scholar
  23. Hirrel MC, Gerdemann JW (1980) Improved growth of onion and bell pepper in saline soils by two vesicular–arbuscular mycorrhizal fungi collected from saline soils. Soil Sci Soc Am J 44:654–655CrossRefGoogle Scholar
  24. Jahromi F, Aroca R, Porcel R, Ruiz-Lozano JM (2008) Influence of salinity on the in vitro development of Glomus intraradices and on the in vivo physiological and molecular responses of mycorrhizal lettuce plants. Microb Ecol 55:45–53PubMedCrossRefGoogle Scholar
  25. Juniper S, Abbott L (1993) Vesicular–arbuscular mycorrhizas and soil salinity. Mycorrhiza 4:45–57CrossRefGoogle Scholar
  26. Juniper S, Abbott L (2004) A change in the concentration of NaCl in soil alters the rate of hyphal extension of some arbuscular mycorrhizal fungi. Can J Bot 82:1235–1242CrossRefGoogle Scholar
  27. Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna LA, Cullu AM (2009) The influence of arbuscular mycorrhizal colonization on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hortic 121:1–6CrossRefGoogle Scholar
  28. Khasa DP, Hambling B, Kernaghan G, Fung M, Ngimbi E (2002) Genetic variability in salt tolerance of selected boreal woody seedlings. For Ecol Manag 165:257–269CrossRefGoogle Scholar
  29. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Ecol Lett 101:2369–2374Google Scholar
  30. Koch AM, Croll D, Sanders IR (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Proc Natl Acad Sci 9:103–110Google Scholar
  31. MacKinnon MD, Matthews JG, Shaw WH, Cuddy RG (2001) Water quality issues associated with of composite tailings (CT) technology for managing oil sands tailings. Int J Surf Min Reclam Environ 15:235–256CrossRefGoogle Scholar
  32. McMillen BG, Juniper S, Abbott LK (1998) Inhibition of hyphal growth of a vesicular–arbuscular mycorrhizal fungus in soil containing sodium chloride limits the spread of infection from spores. Soil Biol Biochem 30:1639–1646CrossRefGoogle Scholar
  33. Mosse B (1959) The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular–arbuscular mycorrhiza. Trans Br Mycol Soc 42:273–286CrossRefGoogle Scholar
  34. Mosse B, Philipps JM (1971) The influence of phosphate and other nutrients on the development of vesicular–arbuscular mycorrhiza in culture. J Gen Microbiol 69:157–166CrossRefGoogle Scholar
  35. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  36. Renault S, Qualizza C, MacKinnon M (2004) Suitability of altai wildrye (Elymus angustus) and slender wheatgrass (Agropyron trachycaulum) for initial reclamation of saline composite tailings of oil sands. Environ Pollut 128:339–349PubMedCrossRefGoogle Scholar
  37. Ruiz-Lozano J, Azcòn R, Gomez M (1996) Alleviation of salt stress by arbuscular mycorrhizal Glomus species in Lactuca sativa plants. Physiol Plant 98:767–772CrossRefGoogle Scholar
  38. Schüßler A, Walker C (2010) The glomeromycota: a species list with new families and new genera 1–58. Libraries at The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University. Available at: www.amf-phylogeny.com
  39. Sharifi M, Ghorbanli M, Ebrahimzadeh H (2007) Improved growth of salinity stressed soybean after inoculation with salt pretreated mycorrhizal fungi. J Plant Physiol 164:1144–1151PubMedCrossRefGoogle Scholar
  40. Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  41. Sokolski S, Dalpé Y, Seguin S, Khasa D, Lévesque CA, Piché Y (2010) Conspecificity of DAOM 197198, the model arbuscular mycorrhizal fungus, with Glomus irregulare: molecular evidence with three protein-encoding genes. Botany 88:829–838CrossRefGoogle Scholar
  42. Sokolski S, Dalpé Y, Piché Y (2011) Phosphate transporter genes as reliable gene markers for the identification and discrimination of arbuscular mycorrhizal fungi in the genus Glomus. Appl Environ Microbiol 77:1888–1891PubMedCentralPubMedCrossRefGoogle Scholar
  43. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332CrossRefGoogle Scholar
  44. Stockinger H, Walker C, Schüßler A (2009) Glomus intraradices DAOM197198, a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytol 183:1176–1187PubMedCrossRefGoogle Scholar
  45. Szabolics I (1994) Soils and salinization. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 3–11Google Scholar
  46. Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001CrossRefGoogle Scholar
  47. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCentralPubMedCrossRefGoogle Scholar
  48. Tian CY, Feng G, Li XL, Zhang FS (2004) Different effects of arbuscular mycorrhizal fungal isolates from saline or non-saline soil on salinity tolerance of plants. Appl Soil Ecol 26:143–148CrossRefGoogle Scholar
  49. Tommerup I (1984) Effect of soil water potential on spore germination by vesicular–arbuscular mycorrhizal fungi. Trans Br Mycol Soc 83:193–202CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Centre d’étude de la forêt et Institut de biologie intégrative et des systèmesUniversité LavalQuebecCanada

Personalised recommendations