Ectomycorrhizal diversity enhances growth and nitrogen fixation of Acacia mangium seedlings

Soil Biology and Biochemistry

Volumn 57, Issue , 2013, Pages 468-476

  Diagne, N ^a,b   Thioulouse, J ^c   Sanguin, H ^d   Prin, Y ^d   Krasova Wade, T ^a   Sylla, S ^a,b   Galiana, A ^d   Baudoin, E ^d   Neyra, M ^d   Svistoonoff, S ^e   Lebrun, M ^d   Duponnois, R ^d  

^a Centre IRD de Bel Air   (Senegal)

^b UNIVERSITÉ CHEIKH ANTA DIOP   (Senegal)

^c UNIVERSITÉ LYON 1   (France)

^d LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

^e INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Ectomycorrhizal fungal diversity; Nitrogen fixation; Tree growth

Indexed keywords

ACACIA MANGIUM; CONTROLLED CONDITIONS; DIVERSITY EFFECTS; ECOSYSTEM PRODUCTIVITY; ECTOMYCORRHIZAL; FOREST MANAGEMENT PRACTICES; FUNGAL DIVERSITY; FUNGAL ISOLATES; MEDITERRANEAN AREAS; MYCORRHIZAL SYMBIOSIS; NODULATION; OUTPLANTING; PLANT DIVERSITY; PLANT GROWTH; PLANT NUTRIENT UPTAKE; REAFFORESTATION; SEEDLING GROWTH; TREE GROWTH; WHOLE PLANTS;

FORESTRY; NITROGEN FIXATION; NUTRIENTS; SOILS;

FUNGI;

ABUNDANCE; AFFORESTATION; ECTOMYCORRHIZA; GROWTH RATE; INOCULATION; LEGUME; NITROGEN FIXATION; NODULATION; NUTRIENT UPTAKE; PHOSPHATE; SEEDLING; SPECIES DIVERSITY; SYMBIOSIS; TROPICAL REGION;

FORESTRY; FUNGI; GROWTH; NUTRIENTS; SOIL; TREES;

AUSTRALIA; MEDITERRANEAN REGION;

ACACIA; ACACIA MANGIUM;

EID: 84870179600     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2012.08.030     Document Type: Article

References (71)

1. Allen E.B., Allen M.F., Helm D.J., Trappe J.M., Molina R., Rincon E. Patterns and regulation of mycorrhizal plant and fungal diversity. Plant and Soil 1995, 170:47-62.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997, 25:3389-3402.
3. André S., Galiana A., Le Roux C., Prin Y., Neyra M., Duponnois R. Ectomycorrhizal symbiosis enhanced the efficiency of two Bradyrhizobium inoculated on Acacia holosericea plant growth. Mycorrhiza 2005, 15:357-364.
4. Baxter J.W., Dighton J. Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions. New Phytologist 2001, 152:139-149.
5. Baxter J.W., Dighton J. Phosphorus source alters host plant response to ectomycorrhizal diversity. Mycorrhiza 2005, 15:513-523.
6. Blilou I., Ocampo J.A., Gracia-Garrido J.M. Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. Journal of Experimental Botany 1999, 50:1663-1668.
7. Bruno J.F., Stachowicz J.J., Bertness M.D. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 2003, 18:119-125.
8. Caravaca F., Barea J.M., Figueroa D., Roldan A. Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Applied Soil Ecology 2002, 20:107-118.
9. Chapin F.S. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 1980, 11:223-260.
10. Chu-Chou M., Grace L.J. Comparative efficiency of the mycorrhizal fungi Laccaria laccata, Hebeloma crustuliniforme and Rhizopogon species on growth of radiate pine seedlings. New Zealand Journal of Botany 1985, 23:417-424.
11. Clay K., Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 1999, 285:1742-1744.
12. Cornet F., Diem H.G. Etude comparative de l'efficacité des souches de Rhizobium d'Acacia isolées de sols du Sénégal et effet de la double symbiose Rhizobium - Glomus mosseae sur la croissance de Acacia holosericea et A. raddiana. Bois et Forêts des Tropiques 1982, 198:3-15.
13. Daft M.J. Influences of génotypes, rock phosphate and plant densities on mycorrhizal development and the growth-responses of 5 different crops. Agriculture Ecosystems & Environment 1991, 35:151-169.
14. Ducousso, M., 1991. Importance des symbioses racinaires pour l'utilisation des acacias d'Afrique de l'Ouest. Thèse de l'Université de Lyon 1, pp. 205.
15. Duponnois R., Bâ A.M. Growth stimulation of Acacia mangium Willd by Pisolithus sp. in some Senegalese soils. Forest Ecology and Management 1999, 119:209-215.
16. Duponnois R., Garbaye J. Techniques for controlled synthesis of the Douglas fir-Laccaria laccata ectomycorrhizal symbiosis. Annales des Sciences Forestières 1991, 48:239-251.
17. Duponnois R., Plenchette C. A mycorrhiza helper bacterium enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 2003, 13:85-91.
18. Duponnois R., Founoune H., Lesueur D. Influence of controlled dual ectomycorrhizal and rhizobial symbiosis on the growth of Acacia mangium provenances, the indigenous symbiotic microflora and the structure of plant parasitic nematode communities. Geoderma 2002, 109:85-102.
19. Duponnois R., Founoune H., Lesueur D., Thioulouse J., Neyra M. Ectomycorrhization of six Acacia auriculiformis provenances from Australia, Papua New Guinea and Senegal in glasshouse conditions: effect on the plant growth and on the multiplication of plant parasitic nematodes. Australian Journal of Experimental Agriculture 2000, 40:443-450.
20. Duponnois R., Founoune H., Masse D., Pontanier R. Inoculation of Acacia holosericea with ectomycorrhizal fungi in a semi-arid site in Senegal: growth response and influences on the mycorrhizal soil infectivity. Forest Ecology and Management 2005, 207:351-362.
21. Duponnois R., Plenchette C., Ba A.M. Growth stimulation of seventeen fallow leguminous plants inoculated with G. aggregatum in Senegal. European Journal of Soil Biology 2001, 37:181-186.
22. Duponnois R., Plenchette C., Prin Y., Ducousso M., Kisa M., Bâ A.M., Galiana A. Use of mycorrhizal inoculation to improve reafforestation process with Australian Acacia in Sahelian ecozones. Ecological Engineering 2007, 29:105-112.
23. Finlay R.D. Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. Journal of Experimental Botany 2008, 59:1115-1126.
24. Founoune H., Duponnois R., Bâ A.M. Influence of the dual arbuscular endomycorrhizal/ectomycorrhizal symbiosis on the growth of Acacia holosericea (A. Cunn. ex G. Don) in glasshouse conditions. Annals of Forest Sciences 2002, 59:93-98.
25. Founoune H., Duponnois R., Bâ A.M., Sall S., Branger I., Lorquin J., Neyra M., Chotte J.L. Mycorrhiza helper bacteria stimulate ectomycorrhizal symbiosis of Acacia holosericea with Pisolithus albus. New Phytologist 2002, 153:81-89.
26. Founoune H., Duponnois R., Meyer J.M., Thioulouse J., Masse D., Chotte J.L., Neyra M. Interactions between ectomycorrhizal symbiosis and fluorescent pseudomonads on Acacia holosericea: isolation of mycorrhiza helper bacteria (MHB) from a soudano-Sahelian soil. FEMS Microbiology Ecology 2002, 41:37-46.
27. Frey P., Frey-Klett P., Garbaye J., Berge O., Heulin T. Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas fir Laccaria bicolor mycorrhizosphere. Applied and Environmental Microbiology 1997, 63:1852-1860.
28. Frey-Klett P., Chavatte M., Clausse M.L., Courrier S., Le Roux C., Raaijmakers J., Martinotti M.G., Pierrat J.P., Garbaye J. Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytologist 2005, 165:317-328.
29. Galiana A., Chaumont J., Diem H.G., Dommergues Y.R. Nitrogen-fixing potential of Acacia mangium and Acacia auriculiformis seedlings inoculated with Bradyrhizobium and Rhizobium spp. Biology and Fertility of Soils 1990, 9:261-267.
30. Galiana A., Prin Y., Mallet B., Gnahoua G.M., Poitel M., Diem H.G. Inoculation of A. mangium with alginate beads containing selected Bradyrhizobium strains under field conditions: long-term effect on plant growth and persistence of the introduced strains in soil. Applied and Environmental Microbiology 1994, 60:3974-3980.
31. Garbaye J. Biological interactions in the mycorrhizosphere. Experientia 1991, 47:370-375.
32. Garbaye J., Bowen G.D. Ectomycorrhizal infection of Pinus radiata by Rhizopogon luteolus is stimulated by microorganisms naturally present in the mantle of ectomycorrhizas. New Phytologist 1989, 112:383-388.
33. Garbaye J., Delwaulle J., Diangana D. Growth response of eucalyptus to ectomycorrhizal inoculation in the Congo. Forest Ecology and Management 1988, 24:151-157.
34. Garnier E., Navas M.L., Austin M.P., Lilley J.M., Gifford R.M. A problem for biodiversity-productivity studies: how to compare the productivity of multispecific plant mixtures to that of monocultures. Acta Oecologica 1997, 18:657-670.
35. Grime J.P. Biodiversity and ecosystem function: the debate deepens. Science 1997, 277:1260-1261.
36. Hector A., Schmid B., Beierkuhnlein C., Caldeira M.C., Diemer M., Dimitrakopoulos P.G., Finn J.A., Freitas H., Giller P.S., Good J., Harris R., Högberg P., Huss-Danell K., Joshi J., Jumpponen A., Körner C., Leadley P.W., Loreau M., Minns A., Mulder C.P.H., O'Donovan G., Otway S.J., Pereira J.S., Prinz A., Read D.J., Scherer-Lorenzen M., Schulze E.D., Siamantziouras A.S.D., Spehn E.M., Terry A.C., Troumbis A.Y., Woodward F.I., Yachi S., Lawton J.H. Plant diversity and productivity in European grasslands. Science 1999, 286:1123-1127.
37. Hector A., Schmid B., Beierkuhnlein C., Caldeira M.C., Diemer M., Dimitrakopoulos P.G., Finn J.A., Freitas H., Giller P.S., Good J., Harris R., Högberg P., Huss-Danell K., Joshi J., Jumpponen A., Körner C., Leadley P.W., Loreau M., Minns A., Mulder C.P.H., O'Donovan G., Otway S.J., Pereira J.S., Prinz A., Read D.J., Scherer-Lorenzen M., Schulze E.D., Siamantziouras A.S.D., Spehn E.M., Terry A.C., Troumbis A.Y., Woodward F.I., Yachi S., Lawton J.H. No consistent effects of plant diversity on productivity (response). Science 2000, 289:1255.
38. Högberg P., Nordgren A., Buchmann N., Taylor A.F.S., Ekblad A., Högberg M.N., Nyberg G., Ottosson-Löfvenius M., Read D.J. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 2001, 411:789-792.
39. Hooper D.U., Vitousek P.M. The effects of plant composition and diversity on ecosystem processes. Science 1997, 277:1302-1305.
40. Hooper D.U., Vitousek P.M. Effects of plant composition and diversity on nutrient cycling. Ecological Monographs 1998, 68:121-149.
41. Huston M.A. Hidden treatments in ecological experiments: re-evaluation the ecosystem function of biodiversity. Oecologia 1997, 110:449-460.
42. Huston M.A., Aarssen L.W., Austin M.P., Cade B.S., Fridley J.D., Garnier E., Grime J.P., Hodgson J., Lauenroth W.K., Thompson K., Vandermeer J.H., Wardle D.A. No consistent effect of plant diversity on productivity. Science 2000, 289:1255.
43. John M.K. Colorimetric determination of phosphorus in soil and plant material with ascorbic acid. Soil Science 1970, 68:171-177.
44. Jonsson L.M., Nilsson M.C., Wardle D.A., Zackrisson O. Context dependent of ectomycorrhizal species richness on tree seedling productivity. Oikos 2001, 93:353-364.
45. Katznelson H., Rouatt J.W., Peterson E.A. The rhizosphere effect of mycorrhizal and non-mycorrhizal roots of yellow birch seedlings. Canadian Journal of Botany 1962, 40:377-382.
46. Kowalchuk G.A., Stephen J.R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Review of Microbiology 2001, 55:485-529.
47. Linderman R.G. Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 1988, 78:366-371.
48. Marshner P., Crowley D.E., Lieberei R. Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize. Mycorrhiza 2001, 11:297-302.
49. Martin F., Diez J., Dell B., Delaruelle C. Phylogeography of the ectomycorrhizal Pisolithus species as inferred from the ribosomal DNA ITS sequences. New Phytologist 2002, 153:345-358.
50. Molina R., Massicotte H., Trappe J.M. Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. Mycorrhizal Functioning: an Integrative Plant-fungal Process 1992, 357-423. Chapman & Hall, New York, USA. M.F. Allen (Ed.).
51. Parlade J., Alvarez I.F. Coinoculation of aseptically grown Douglas-fir with pairs or ectomycorrhizal fungi. Mycorrhiza 1993, 3:93-96.
52. Parniske M. Intracellular accommodation of microbes by plant: a common developmental program for symbiosis and disease?. Current Opinion in Plant Biology 2000, 3:320-3208.
53. R Development Core Team R: a Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna, Austria, URL:. http://www.R-project.org/.
54. Reddy M.S., Natarajan K. Coinoculation efficacy of ectomycorrhizal fungi on Pinus patula seedlings in a nursery. Mycorrhiza 1997, 7:133-138.
55. Rillig M.C., Mummey D.L. Mycorrhiza and soil structure. New Phytologist 2006, 171:41-43.
56. Rudgers J.A., Koslow J.M., Clay K. Endophytic fungi alter relationships between diversity and ecosystem properties. Ecology Letters 2004, 7:42-51.
57. Smith S.E., Read D.J. Mycorrhizal Symbiosis 2008, Academic Press, London, UK. third ed.
58. Sprent J.I. Nodulation in Legumes 2001, Royal Bot. Gardens, Kew, UK.
59. Thioulouse J., Dray S. Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. Journal of Statistical Software 2007, 22:1-14.
60. Tilman D., Wedin D., Knops J. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 1996, 379:718-720.
61. Valentine L.L., Fieldler T.L., Hart A.A., Petersen C.A., Berninghausen H.K., Southworth D. Diversity of ectomycorrhizas associated with Quercus garryana in southern Oregon. Canadian Journal of Botany 2004, 82:123-135.
62. van der Heijden M.G.A., Cornelissen J.H.C. The critical role of plant-microbe interactions on biodiversity and ecosystem functioning: arbuscular mycorrhizal associations as an example. Biodiversity and Ecosystem Functioning: Synthesis and Perspectives 2002, 181-194. Oxford University Press, London. M. Loreau, S. Naeem, P. Inchausti (Eds.).
63. van der Heijden M.G.A., Bakker R., Verwaal J., Scheublin T.R., Rutten M., van Logtestijn R., Staehelin C. Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiology Ecology 2006, 56:178-187.
64. van der Heijden M.G.A., Bardgett R.D., van Straalen N.M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 2008, 11:296-310.
65. van der Heijden M.G.A., Klironomos J.N., Ursic M., Moutoglis P., Streitwolf-Engel R., Boller T., Wiemken A., Sanders I.R. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 1998, 396:72-75.
66. van der Heijden M.G.A., Klironomos J.N., Ursic M., Moutoglis P., Streitwolf-Engel R., Boller T., Wiemken A., Sanders I.R. " Sampling effect" , a problem in biodiversity manipulation? A reply to David A. Wardle. Oikos 1999, 87:408-410.
67. van der Heijden M.G.A., Wiemken A., Sanders I.R. Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytologist 2003, 157:569-578.
68. van Rhijn P., Fang Y., Galili S., Shaul O., Atzon N., Wininger S., Eshed Y., Lum M., Li Y., To V., Fujishige N., Kapulik Y., Hirsch A.M. Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae and Rhizobium-induced nodules may be conserved. Plant Biology 1997, 94:5467-5472.
69. Vincent J.M. A Manual for the Practical Study of the Root Nodule Bacteria. International Biological Program 1970, Blackwell, Oxford, Handbook no. 15.
70. Wardle D.A. Is " sampling effect" a problem for experiments investigating biodiversity-ecosystem function relationships?. Oikos 1999, 87:403-407.
71. Wardle D.A., Bonner K.I., Barker G.M. Stability of ecosystem properties in response to above ground functional group richness and composition. Oikos 2000, 89:11-23.