Advertisement

Annals of Forest Science

, 75:72 | Cite as

Selection of arbuscular mycorrhizal fungal strains to improve Casuarina equisetifolia L. and Casuarina glauca Sieb. tolerance to salinity

  • Pape Ibrahima Djighaly
  • Nathalie Diagne
  • Mariama Ngom
  • Daouda Ngom
  • Valérie Hocher
  • Dioumacor Fall
  • Diégane Diouf
  • Laurent Laplaze
  • Sergio Svistoonoff
  • Antony Champion
Research Paper

Abstract

Key message

Selection of the best salt-tolerant combination of Casuarina sp. and arbuscular mycorrhizal fungi (AMF) is one of the key criteria for successful setup of saline land rehabilitation program.

Context

Land salinization is a serious problem worldwide that mainly leads to soil degradation and reduces crop productivity. These degraded areas could be rehabilitated by planting salt-tolerant species like Casuarina glauca Sieb. and Casuarina equisetifolia L. These are pioneer plants, able to form symbiotic associations with arbuscular mycorrhizal fungi (AMF), ectomycorrhizal fungi (EMF), and nitrogen-fixing bacteria.

Aims

The aim of this study was to select the highest salt-tolerant combination of Casuarina/AMF that can be used for the rehabilitation of lands degraded by salinity.

Methods

C. equisetifolia and C. glauca were grown in sandy sterile soil in the greenhouse and inoculated separately with Rhizophagus fasciculatus (Thaxt.) C. Walker & A. Schüßler, Rhizophagus aggregatus (N.C. Schenck & G.S. Sm.) C. Walker, and Rhizophagus intraradices (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler. After confirming the establishment of a symbiosis, the plants were watered with gradually increasing concentrations of saline solution. After harvest, size and biomass of the seedlings, root colonization by AMF, and AMF metabolic activities were evaluated.

Results

A larger growth was obtained in the two species when the individuals were inoculated with R. fasciculatus. Root colonization rates did not differ among fungal species, but fungal metabolic activities were higher in mycorrhizal roots of C. glauca plants inoculated with R. fasciculatus.

Conclusion

Among the three mycorrhizal fungi, R. fasciculatus was more efficient in association with Casuarinaceae species under salt stress. Our results suggest that selection of appropriate fungal strains is crucial to improve plant performance in saline soils.

Keywords

Salinity Arbuscular mycorrhizal fungi C. glauca C. equisetifolia Rehabilitation Salt-affected land 

Notes

Acknowledgments

This work was supported by the International Foundation for Sciences (IFS, no. AD/22680), the Academy of Sciences for the Developing World (TWAS, no. 11-214 RG/BIO/AF/AC I), The “Fonds d’Impulsion de la Recherche Scientifique et Technique” (FIRST) of the Ministry of Higher Education and Research of Senegal, and the “Laboratoire Mixte International Adaptation des Plantes et microorganismes associés aux Stress Environnementaux” (LAPSE). P. I. Djighaly was granted by “Institut de Recherche pour le Développement” (IRD) through its ARTS PhD program.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13595_2018_747_Fig5_ESM.png (1.3 mb)
Supplemental fig. 1

Effect of NaCl on root colonization of Casuarina a. Staining of Uvitex 2B in Casuarina roots not exposed to NaCl (arrow indicates arbuscular mycorrhizae); b. Casuarina roots subjected to 150 mM NaCl; c. Plant subjected to 300 mM NaCl, cw: cell wall, h: intracellular hyphae, Bars=100μM. (PNG 1367 kb)

13595_2018_747_MOESM1_ESM.eps (462 kb)
High resolution image (EPS 462 kb)

References

  1. Abdel-Fattah GM, Asrar A-WA (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance of wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol Plant 34:267–277.  https://doi.org/10.1007/s11738-011-0825-6 CrossRefGoogle Scholar
  2. Abeer H, Alterami Salwa A, Alqarawi AA, ABD_Allah EF, Egamberdieva D (2016) Arbuscular mycorrhizal fungi enhance basil tolerance to salt stress through improved physiological and nutritional status. Pak J Bot 48(1):37–45Google Scholar
  3. Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Sci Hort 109:1–7.  https://doi.org/10.1016/j.scienta.2006.02.019 CrossRefGoogle Scholar
  4. Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47.  https://doi.org/10.1007/s005720100098 CrossRefGoogle Scholar
  5. Al-Karaki GN (2000) Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza 10:51–54.  https://doi.org/10.1007/s005720000055 CrossRefGoogle Scholar
  6. Alqarawi AA, Allah EFA, Hashem A (2014) Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. J Plant Interact 9:802–810.  https://doi.org/10.1080/17429145.2014.949886 CrossRefGoogle Scholar
  7. Barrow J, Aaltonen R (2001) Evaluation of the internal colonization of Atriplex canescens (Pursh) Nutt. roots by dark septate fungi and the influence of host physiological activity. Mycorrhiza 11:199–205.  https://doi.org/10.1007/s005720100111 CrossRefGoogle Scholar
  8. Beltrano J, Ruscitti M, Arango MC, Ronco M (2013) Effects of arbuscular mycorrhiza inoculation on plant growth, biological and physiological parameters and mineral nutrition in pepper grown under different salinity and p levels. J Soil Sci Plant Nutr 13:123–141.  https://doi.org/10.4067/S0718-95162013005000012 Google Scholar
  9. Campanelli A, Ruta C, De Mastro G, Morone-Fortunato I (2012) The role of arbuscular mycorrhizal fungi in alleviating salt stress in Medicago sativa L. var. icon. Symbiosis 59:65–76.  https://doi.org/10.1007/s13199-012-0191-1 CrossRefGoogle Scholar
  10. Carvalho LM, Caçador I, Martins-Loução M (2001) Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11:303–309.  https://doi.org/10.1007/s00572-001-0137-6 CrossRefPubMedGoogle Scholar
  11. Diagne N, Djighaly P. I, Ngom M, Prodjinoto H, NGOM D, Hocher V, Fall D, Diouf D Nambiar-Veetil M, Sy M O, Ndoye I, Franche C, Bogusz D, Laplaze L (2014) Rehabilitation of saline lands using selected salt-tolerant Casuarina-microorganisms combinations. Proceedings of 5th International Casuarina workshop Chennai India 3–7 February 2014Google Scholar
  12. Diagne N, Diouf D, Svistoonoff S, Kane A, Noba K, Franche C, Bogusz D, Duponnois R (2013) Casuarina in Africa: distribution, role and importance of arbuscular mycorrhizal, ectomycorrhizal fungi and Frankia on plant development. J Environ Manag 128:204–209.  https://doi.org/10.1016/j.jenvman.2013.05.009 CrossRefGoogle Scholar
  13. Diagne N, Escoute J, Lartaud M, Verdeil JL, Franche C, Kane A, Bogusz D, Diouf D, Duponnois R, Svistoonoff S (2011) Uvitex2B: a rapid and efficient stain for detection of arbuscular mycorrhizal fungi within plant roots. Mycorrhiza 21:315–321.  https://doi.org/10.1007/s00572-010-0357-8 CrossRefPubMedGoogle Scholar
  14. Diem HG, Duhoux E, Zaid H, Arahou M (2000) Cluster roots in Casuarinaceae: role and relationship to soil nutrient factors. Ann of Bot 85:929–936CrossRefGoogle Scholar
  15. Diouf D, Duponnois R, Ba AT, Neyra M, Lesueur D (2005) Symbiosis of Acacia auriculiformis and Acacia mangium with mycorrhizal fungi and Bradyrhizobium spp. improves salt tolerance in greenhouse conditions. Functional Plant Biol 32:1143–1152.  https://doi.org/10.1071/FP04069 CrossRefGoogle Scholar
  16. Duponnois R, Diedhiou S, Chotte JL, Sy MO (2003) Relative importance of the endomycorrhizal and (or) ectomycorrhizal associations in Allocasuarina and Casuarina genera. Can J Microbiol 49:281–287.  https://doi.org/10.1139/w03-038 CrossRefPubMedGoogle Scholar
  17. Duro N, Batista-Santos P, da CM, Maia R, Castro IV, Ramos M, Ramalho JC, Pawlowski K, Máguas C, Ribeiro-Barros A (2015) The impact of salinity on the symbiosis between Casuarina glauca Sieb. ex Spreng. and N2-fixing Frankia bacteria based on the analysis of nitrogen and carbon metabolism. Plant Soil 398:327–337.  https://doi.org/10.1007/s11104-015-2666-3 CrossRefGoogle Scholar
  18. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280.  https://doi.org/10.1093/aob/mcp251 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Feng G, Zhang F, Li X, Tian C, Tang C, Rengel Z (2002) Improved tolerance of maize plants to salt stress by arbuscular mycorrhiza is related to higher accumulation of soluble sugars in roots. Mycorrhiza 12:185–190.  https://doi.org/10.1007/s00572-002-0170-0 CrossRefPubMedGoogle Scholar
  20. Fisher RA, Yates F (1948) Statistical tables for biological agriculture and medical research, sixth ed. Hafner Publ Comp, DavienGoogle Scholar
  21. Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal endogone species extracted from soil by wet-sieving and decanting. Trans Br Mycol Soc p 46:235–244CrossRefGoogle Scholar
  22. Giri B, Mukerji KG (2004) Mycorrhizal inoculant alleviates salt stressing Sesbania aegyptiaca and Sesbania grandiflora under field conditions: evidence for reduced sodium and improved magnesium uptake. Mycorrhiza 14:307–312.  https://doi.org/10.1007/s00572-003-0274-1 CrossRefPubMedGoogle Scholar
  23. Giri B, Kapoor R, Mukerji KG (2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biol Fertil Soils 38:170–175.  https://doi.org/10.1007/s00374-003-0636-z CrossRefGoogle Scholar
  24. Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1664–1462.  https://doi.org/10.3389/fpls.2016.01787 CrossRefGoogle Scholar
  25. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments a review. Plant Signal Behav 7(11):1456–1466.  https://doi.org/10.4161/psb.21949 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kaya C, Ashraf M, Sonmez O, Aydemir S, Tuna AL, Cullu MA (2009) The influence of arbuscular mycorrhizal colonisation on key growth parameters and fruit yield of pepper plants grown at high salinity. Sci Hort 121:1–6.  https://doi.org/10.1016/j.scienta.2009.01.001 CrossRefGoogle Scholar
  27. Kough JL, Gianinazzi-Pearson V, Gianinazzi S (1987) Depressed metabolic activity of vesicular arbuscular mycorrhizal fungi after fungicide application. New Phytol 106:707–715.  https://doi.org/10.1111/j.1469-8137.1987-x CrossRefGoogle Scholar
  28. Krishnamoorthy R, Kim K, Subramanian P, Senthilkumar M, Anandham R, Sa T (2016) Arbuscular mycorrhizal fungi and associated bacteria isolated from salt-affected soil enhances the tolerance of maize to salinity in coastal reclamation soil. Agric Ecosyst Environ 231:233–239.  https://doi.org/10.1016/j.agee.2016.05.037 CrossRefGoogle Scholar
  29. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713.  https://doi.org/10.1093/aob/mcl114 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Latef AAH, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hort 127:228–233.  https://doi.org/10.1016/j.scienta.2010.09.020 CrossRefGoogle Scholar
  31. Makeen K, Suresh Babu G, Lavanya GR, Grard A (2007) Studies of chlorophyll content by different methods in black gram (Vigna mungo L.). Int J Agric Res 2(7):651–654.  https://doi.org/10.3923/ijar.2007.651.654 CrossRefGoogle Scholar
  32. Monneveux P, Nemmar M (1986) Contribution à l’étude de la résistance à la sécheresse chez le blé tendre (Triticum aestivum L.) et chez le blé dur (Triticum durum Desf.): Etude de l’accumulation de la proline au cours du cycle de développement. Agronomie 6:583–590CrossRefGoogle Scholar
  33. National Research Council (1984) Casuarinas: nitrogen-fixing trees for adverse sites. Office of International Affairs, Washington DC  https://doi.org/10.17226/19415
  34. Ngom M, Oshone R, Diagne N, Cissoko M, Svistoonoff S, Tisa LS, Laplaze L, Sy MO, Champion A (2016) Tolerance to environmental stress by the nitrogen-fixing actinobacterium Frankia and its role in actinorhizal plants adaptation. Symbiosis 70:17–29.  https://doi.org/10.1007/s13199-016-0396-9 CrossRefGoogle Scholar
  35. Péret B, Svistoonoff S, Laplaze L (2009) When plants socialize symbioses and root development. Annu Plant Rev 37:209–238Google Scholar
  36. Porras-Soriano A, Soriano-Martín ML, Porras-Piedra A, Azcón R (2009) Arbuscular mycorrhizal fungi increased growth, nutrient uptake and tolerance to salinity in olive trees under nursery conditions. J Plant Physiol 166:1350–1359.  https://doi.org/10.1016/j.jplph.2009.02.010 CrossRefPubMedGoogle Scholar
  37. Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124.  https://doi.org/10.1016/j.copbio.2013.12.004 CrossRefPubMedGoogle Scholar
  38. Saint-Etienne L, Paul S, Imbert D, Dulormne M, Muller F, Toribio A, Plenchette C, Bâ AM (2006) Arbuscular mycorrhizal soil infectivity in a stand of the wetland tree Pterocarpus officinalis along a salinity gradient. For Ecol Manag 232:86–89.  https://doi.org/10.1016/j.foreco.2006.05.046 CrossRefGoogle Scholar
  39. Sayed WF (2011) Improving Casuarina growth and symbiosis with Frankia under different soil and environmental conditions—review. Folia Microbiol (Praha) 56:1–9.  https://doi.org/10.1007/s12223-011-0002-8 CrossRefGoogle Scholar
  40. Sieverding E (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. GTZ Germany 371 ppGoogle Scholar
  41. Shekoofeh E, Sepideh H, Roya R (2012) Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. Afr J Biotechnol 11:2223–2235.  https://doi.org/10.5897/AJB11.1672 Google Scholar
  42. Sheng M, Tang M, Chan B, Yang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296.  https://doi.org/10.1007/s00572-008-0180-7 CrossRefPubMedGoogle Scholar
  43. Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. Arthur Schüßler & Christopher Walker, Gloucester. Published in December 2010 in libraries at The Royal Botanic Garden Edinburgh, The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University. Printed copy available under ISBN-13: 978–1466388048, ISBN-10: 1466388048 Available at http://www.amf-phylogeny.com
  44. Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057.  https://doi.org/10.1104/pp.111.174581 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Talaat NB, Shawky BT (2011) Influence of arbuscular mycorrhizae on yield, nutrients, organic solutes, and antioxidant enzymes of two wheat cultivars under salt stress. J Plant Nutr Soil Sci 174:283–291.  https://doi.org/10.1002/jpln.201000051 CrossRefGoogle Scholar
  46. Tani C, Sasakawa H (2006) Proline accumulates in Casuarina equisetifolia seedlings under salt stress. Soil Sci Plant Nutr 52:21–25.  https://doi.org/10.1111/j.1747-0765.2006.00005.x CrossRefGoogle Scholar
  47. Tani C, Sasakawa H (2003) Salt tolerance of Casuarina equisetifolia and Frankia Ceq1 strain isolated from the root nodules of C. equisetifolia. Soil Sci Plant Nutr 49(2):215–222.  https://doi.org/10.1080/00380768.2003.10410000 CrossRefGoogle Scholar
  48. Tamba A (2000) Aménagement des peuplements forestiers pour la protection des cuvettes maraîchères le long du Nord littoral du Sénégal. ISRA/DRPF (DEFCCS) Projet FNRAA 16 pGoogle Scholar
  49. Tester M, Davenport RJ (2003) Na+ transport and Na+ tolerance in higher plants. Ann Bot 91:503–527.  https://doi.org/10.1093/aob/mcg058 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherches et méthodes d’estimation ayant une signification fonctionnelle. Dans : Aspects physiologiques et génétiques des mycorhizes, Dijon 1985. INRA (éd):217–221Google Scholar
  51. Vierheilig H, Knoblauch M, Juergensen K, van Bel AJ, Grundler FM, Piché Y (2001) Imaging arbuscular mycorrhizal structures in living roots of Nicotiana tabacum by light, epifluorescence, and confocal laser scanning microscopy. Can J Bot 79:231–237.  https://doi.org/10.1139/b00-156 Google Scholar
  52. Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots†. Physiol Plant 125:393–404.  https://doi.org/10.1111/j.1399-3054.2005.00564.x Google Scholar
  53. Watanabe S, Kojima K, Ide Y, Satohiko S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tiss Org 63:199–206CrossRefGoogle Scholar
  54. Wu Q-S, Zou Y-N, He X-H (2010) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plant 32:297–304.  https://doi.org/10.1007/s11738-009-0407-z CrossRefGoogle Scholar
  55. Zou Y-N, Wu Q-S (2011) Sodium chloride stress induced changes in leaf osmotic adjustment of trifoliate orange (Poncirus trifoliata) seedlings inoculated with mycorrhizal fungi. Not Bot Horti Agrobo 39(2):64–69CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  • Pape Ibrahima Djighaly
    • 1
    • 2
    • 3
    • 4
  • Nathalie Diagne
    • 2
    • 4
  • Mariama Ngom
    • 1
    • 2
    • 5
  • Daouda Ngom
    • 3
  • Valérie Hocher
    • 6
  • Dioumacor Fall
    • 1
    • 2
    • 7
  • Diégane Diouf
    • 1
    • 2
    • 5
  • Laurent Laplaze
    • 2
    • 8
  • Sergio Svistoonoff
    • 1
    • 2
    • 6
  • Antony Champion
    • 1
    • 2
    • 8
  1. 1.Laboratoire Commun de Microbiologie (LCM) Institut de Recherche pour le Développement/Institut Sénégalais de Recherches Agricoles/Université Cheikh Anta Diop, (IRD/ISRA/UCAD), Centre de Recherche de Bel AirDakarSenegal
  2. 2.Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés aux Stress Environnementaux (LAPSE), Centre de Recherche de Bel AirDakarSenegal
  3. 3.Département d’AgroforesterieUniversité Assane Seck de ZiguinchorZiguinchorSenegal
  4. 4.Centre National de Recherches Agronomiques (ISRA/CNRA)BambeySenegal
  5. 5.Département de Biologie VégétaleUniversité Cheikh Anta Diop de DakarDakarSenegal
  6. 6.Laboratoire des Symbioses Tropicales et Méditerranéennes (LSTM), (IRD/INRA/CIRAD/Université de Montpellier/Supagro), IRD TA A-82/JCampus International de BaillarguetMontpellier CEDEX 5France
  7. 7.Centre National de Recherches Forestières (ISRA/CNRF)DakarSenegal
  8. 8.Institut de Recherche pour le Développement (IRD), Unité Mixte de Recherche DIADE (Diversité Adaptation et Développement des plantes)Montpellier CEDEX 5France

Personalised recommendations