Symbiosis of Acacia auriculiformis and Acacia mangium with mycorrhizal fungi and Bradyrhizobium spp. improves salt tolerance in greenhouse conditions
Diégane Diouf A B F , Robin Duponnois C , Amadou Tidiane Ba A , Marc Neyra B D and Didier Lesueur B EA Département de Biologie Végétale, Université Cheikh Anta Diop, BP 5005, Dakar, Sénégal.
B Laboratoire Commun de Microbiologie, IRD / ISRA / UCAD, BP 1386, Dakar, Sénégal.
C UR 40, Symbioses Tropicales et Méditerranéennes, IRD, 01 BP 182, Ouagadougou, Burkina Faso.
D UR 40, Symbioses Tropicales et Méditerranéennes, IRD, BP 1386, Dakar, Sénégal.
E Forest Department of CIRAD, UPR ‘ETP’, Tropical Soil Biology and Fertility Institute of CIAT, Nairobi, Kenya.
F Corresponding author. Email: diegane.diouf@ird.sn
Functional Plant Biology 32(12) 1143-1152 https://doi.org/10.1071/FP04069
Submitted: 8 April 2004 Accepted: 25 July 2005 Published: 1 December 2005
Abstract
The aim of our work was to assess the growth and mineral nutrition of salt stressed Acacia auriculiformis A. Cunn. ex Benth. and Acacia mangium Willd. seedlings inoculated with a combination of selected microsymbionts (bradyrhizobia and mycorrhizal fungi). Plants were grown in greenhouse conditions in non-sterile soil, irrigated with a saline nutrient solution (0, 50 and 100 mm NaCl). The inoculation combinations consisted of the Bradyrhizobium strain Aust 13c for A. mangium and Aust 11c for A. auriculiformis, an arbuscular mycorrhizal fungus (Glomus intraradices, DAOM 181602) and an ectomycorrhizal fungus (Pisolithus albus, strain COI 007). The inoculation treatments were designed to identify the symbionts that might improve the salt tolerance of both Acacia species. The main effect of salinity was reduced tree growth in both acacias. However, it appeared that, compared with controls, both rhizobial and mycorrhizal inoculation improved the growth of the salt-stressed plants, while inoculation with the ectomycorrhizal fungus strain appeared to have a small effect on their growth and mineral nutrition levels. Endomycorrhizal inoculation combined with rhizobial inoculation usually gave good results. Analysis of foliar proline accumulation confirmed that dual inoculation gave the trees better tolerance to salt stress and suggested that the use of this dual inoculum might be beneficial for inoculation of both Acacia species in soils with moderate salt constraints.
Keywords: Acacia, microsymbionts, proline accumulation, salt stress.
Acknowledgments
The authors are grateful to Leon Biagui and Abdoulaye Sy for technical assistance in the nursery experiments and to Dr Antoine Galiana for helpful discussions on statistical analyses.
Abdelmoumen H,
Filali-Maltouf A,
Neyra M,
Belaleb A, Missbah El Idrissi M
(1999) Effect of high salt concentrations on the growth of rhizobia and responses to added osmotica. Journal of Applied Microbiology 86, 889–898.
| Crossref | GoogleScholarGoogle Scholar |
Ahmed M
(1995) Compatibility and co-selection of vascular arbuscular mycorrhizal fungi and rhizobia for tropical legumes. Critical Review of Biochemistry 15, 229–239.
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.
| Crossref | GoogleScholarGoogle Scholar |
Anthraper A, Dubois JD
(2003) The effect of NaCl on growth, N2 fixation (acetylene reduction), and percentage total nitrogen in Leucaena leucocephala (Leguminosae) var. K-81. American Journal of Botany 90, 683–692.
Apse MP,
Aharon GS,
Snedden WS, Blumwald E
(1999) Salt tolerance conferred by overexpression of a vacuolar Na+ / H+ antiport in Arabidopsis. Science 285, 1256–1258.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barbiéro L,
Mohamedou AO,
Laperrousaz C,
Furian S, Cunnac S
(2004) Polyphasic origin of salinity in the Senegal delta and middle valley. CATENA 58, 101–124.
Ben Khaled L,
Morte Gõmez A,
Honrubia M, Oihabi A
(2003) Effet du stress salin en milieu hydroponique sur le trèfle inoculé par le Rhizobium. Agronomie 23, 553–560.
| Crossref | GoogleScholarGoogle Scholar |
Brundett MC,
Piche Y, Petersen RL
(1985) A developmental study of the early stages of vesicular-arbuscular mycorrhizal formation. Canadian Journal of Botany 63, 184–194.
Cordovilla MP,
Ocana A,
Ligero F, Lluch C
(1995) Salinity effect on growth analysis and nutrient composition in four grain legumes–Rhizobium symbiosis. Journal of Plant Nutrition 18, 1595–1609.
De Oliveira VL,
Schmidt VDB, Bellei MM
(1997) Patterns of arbuscular and ectomycorrhizal colonisation of Eucalyptus dunnii in southern Brazil. Annals of Science 54, 473–481.
Delauney AJ, Verma DPS
(1993) Proline biosynthesis and osmoregulation in plant. The Plant Journal 4, 215–223.
| Crossref | GoogleScholarGoogle Scholar |
Dixon RK,
Rao MV, Garg VK
(1993) Inoculation of Leucaena leucocephala and Prosopis seedlings with Glomus and Rhizobium species in saline soil: rhizosphere relations and seedling growth. Arid Soil Research and Rehabilitation 7, 133–144.
Doran, JC ,
and
Turnbull, JW (1997).
Duponnois R, Bâ AM
(1999) Growth stimulation of Acacia mangium Willd by Pisolithus sp. in some Senegalese soils. Forest Ecology and Management 119, 209–215.
| Crossref | GoogleScholarGoogle Scholar |
Duponnois R,
Founoune H, Lesueur D
(2002) Influence of the 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 109, 85–102.
| Crossref | GoogleScholarGoogle Scholar |
Duponnois R,
Founoune H,
Lesueur D,
Thioulouse J, Neyra M
(2000) 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 40, 443–450.
Founoune H,
Duponnois R,
Bâ AM, Bouami F
(2002) Influence of the dual arbuscular endomycorrhizal / ectomycorrhizal symbiosis on the growth of Acacia holosericea (A. Cunn. ex G. Don) in glasshouse conditions. Annals of Science 59, 93–98.
| Crossref | GoogleScholarGoogle Scholar |
Fowler, J ,
and
Cohen, L (1992).
Galiana A,
Chaumont J,
Diem HG, Dommergues YR
(1990) Nitrogen-fixing potential of Acacia mangium and Acacia auriculiformis seedlings inoculated with Bradyrhizobium and Rhizobium spp. Biology and Fertility of Soils 9, 261–267.
| Crossref | GoogleScholarGoogle Scholar |
Galiana A,
Gnahoua GM,
Chaumont J,
Lesueur D,
Prin Y, Mallet B
(1998) Improvement of nitrogen fixation in Acacia mangium through inoculation with rhizobia. Agroforestry Systems 40, 297–307.
| Crossref | GoogleScholarGoogle Scholar |
Giri B,
Kapoor R, Mukerji KG
(2003) Influence of arbuscular mycorrhizal fungi and salinity on growth, biomass, and mineral nutrition of Acacia auriculiformis. Biology and Fertility of Soils 38, 170–175.
| Crossref | GoogleScholarGoogle Scholar |
Habte M, Soedarjo M
(1996) Response of Acacia mangium to vesicular-arbuscular mycorrhizal inoculation, soil pH, and soil P concentration in an oxisol. Canadian Journal of Botany 74, 155–161.
Hatimi A
(1999) Effect of salinity on the association between root symbionts and Acacia cyanophylla Lind.: growth and nutrition. Plant and Soil 216, 93–101.
| Crossref | GoogleScholarGoogle Scholar |
Herrera MA,
Salamanca CP, Barea JM
(1993) Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified mediterranean ecosystems. Applied and Environmental Microbiology 59, 129–133.
Hussain G,
Al-Jaloud AA,
Al-Shammary SF, Karimulla S
(1995) Effect of saline irrigation on the biomass yield, and the protein, nitrogen and phosphorus, and potassium composition of alfalfa in pot experiment. Journal of Plant Nutrition 18, 2289–2298.
Jain M,
Mathur G,
Koul S, Sarin NB
(2001) Ameliorative effects of proline on salt stress-induced lipid peroxidation in cell lines of groundnut (Arachis hypogea L.). Plant Cell Reports 20, 463–468.
| Crossref | GoogleScholarGoogle Scholar |
John MK
(1970) Colorimetric determination in soil and plant material with ascorbic acid. Soil Science 68, 171–177.
Juniper S, Abbott L
(1993) Vesicular arbuscular mycorrhizas and soil salinity. Mycorrhiza 4, 45–57.
| Crossref | GoogleScholarGoogle Scholar |
Lambers H
(2003) Dryland salinity: a key environmental issue in southern Australia. Plant and Soil 257, v–vii.
| Crossref | GoogleScholarGoogle Scholar |
Lin CC, Kao CH
(1996) Proline accumulation is associated with inhibition of rice seedling root growth caused by NaCl. Plant Science 114, 121–128.
| Crossref | GoogleScholarGoogle Scholar |
Liu J, Zhu JK
(1997) Proline accumulation and salt-stressed-induced gene expression in salt-hypersensitive mutant of Arabidopsis. Plant Physiology 114, 591–596.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Marcar NE,
Dart P, Sweeney C
(1991) Effect of root-zone salinity on growth and chemical composition of Acacia ampliceps BR Maslin, A. auriculiformis A. Cunn. ex Benth. and A. mangium Willd. at two nitrogen levels. New Phytologist 119, 567–573.
Martin-Laurent F,
Lee SK,
Tham FY,
Jie H, Diem HG
(1999) Aeroponic production of Acacia mangium saplings inoculated with AM fungi for reforestation in the tropics. Forest Ecology and Management 122, 199–207.
| Crossref | GoogleScholarGoogle Scholar |
Marx DH
(1969) The influence of ectotropic mycorrhizal fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59, 153–163.
Monnevaux P, Nemmar M
(1986) Contribution à l’étude de la résistance à la sécheresse chez le blé tendre (Triticum aestivum L.) et le blé dur (Triticum durum Desf.). Étude de l’accumulation de la proline au cours du cycle de développement. Agronomie 6, 583–590.
Müller J
(2003) Artificial infection by endophytes affects growth and mycorrhizal colonisation of Lolium perenne. Functional Plant Biology 30, 419–424.
| Crossref | GoogleScholarGoogle Scholar |
Olsen, SR ,
Cole, CV ,
Watanabe, FS ,
and
Dean, LA (1954).
Phillips JM, Hayman DS
(1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Plenchette C,
Perrin R, Duvert P
(1989) The concept of soil infectivity and method for its determination as applied to endomycorrhizas. Canadian Journal of Botany 67, 112–115.
Ruiz-Lozano JM, Azcon R
(2000) Symbiotic efficiency and infectivity of an autochthonous arbuscular mycorrhizal Glomus sp. from saline soils and Glomus deserticola under salinity. Mycorrhiza 10, 137–143.
| Crossref | GoogleScholarGoogle Scholar |
Saadallah K,
Drevon JJ, Abdelly C
(2001) Nodulation et croissance nodulaire chez le haricot (Phaseolus vulgaris) sous contrainte saline. Agronomie 21, 627–634.
| Crossref | GoogleScholarGoogle Scholar |
Santiago GM,
Garcia Q, Scotti MR
(2002) Effect of pot-planting inoculation with Bradyrhizobium sp. and mycorrhizal fungi on the growth of Brazilian rosewood, Dalbergia nigra Allem. ex Benth., in two tropical soils. New Forests 24, 15–25.
| Crossref | GoogleScholarGoogle Scholar |
Shamseldin A, Werner D
(2005) High salt and high pH tolerance of new isolates Rhizobium etli strains from Egyptian soils. Current Microbiology 50, 11–16.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smith, MD ,
and
Read, DJ (1997).
Sprent, JI ,
and
Zahran, HH (1988). Infection, development and functioning of nodules under drought and salinity. In ‘Nitrogen fixation by legumes in Mediterranean agriculture’. pp. 145–151. (Martinus Nijhoff: Dordrecht)
Vincent, JM (1970). ‘A manual for the practical study of root-nodule bacteria.’ International biological programme handbook number 15. (Blackwell Scientific Publications: Oxford)
Weber J,
Ducousso M,
Tham FY,
Nourissier-Mountou S,
Galiana A,
Prin Y, Lee SK
(2005) Co-inoculation of Acacia mangium with Glomus intraradices and Bradyrhizobium sp. in aeroponic culture. Biology and Fertility of Soils 41, 233–239.
| Crossref | GoogleScholarGoogle Scholar |
Yokota S
(2003) Relationship between salt tolerance and proline accumulation in Australian acacia species. Journal of Forest Research 8, 89–93.
| Crossref | GoogleScholarGoogle Scholar |
Zahran HH
(1999)
Rhizobium–legume symbiosis and nitrogen fixation under severe conditions and in arid climate. Microbial Molecular Biology Review 63, 968–989.