Skip to main content
SpringerLink
Log in

Mycorrhizosphere Interactions for Legume Improvement

  • Chapter
Microbes for Legume Improvement

Abstract

Legumes, plant species of great agronomical and ecological interest, are known to establish beneficial symbiotic relationships with two types of soil-borne microorganisms: N2-fixing bacteria and arbuscular mycorrhizal fungi. Additionally, the legume rhizosphere harbors other associative beneficial microorganisms such as plant growth promoting rhizobacteria (PGPR). These microorganisms interact among themselves, and with legume roots, to develop the multifunctional legume mycorrhizosphere, a scenario of diverse activities relevant for legume productivity either in sustainable agriculture or in the maintenance of natural plant communities. This Chapter highlights strategic and applied research conducted so far, which have allowed a comprehensive understanding of the formation and functioning of the legume mycorrhizosphere. Manipulation of the microbial activities allows tailoring efficient mycorrhizosphere systems for improving legume productivity. The technology for the production of efficient rhizobial, free-living PGPR, and AM-fungal inoculants, nowadays commercially available, is likely to support sustainable and environmentally friendly low-input agrotechnological practices. The possibilities to use these bioproducts to help a sustainable development of legumes in either agrosystems or natural ecosystems are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    Article  PubMed  CAS  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929

    Article  PubMed  CAS  Google Scholar 

  • Ahmad MH (1995) Compatibility and coselection of vesicular-arbuscular mycorrhizal fungi and rhizobia for tropical legumes. Crit Rev Biotechnol 15:229–239

    Article  Google Scholar 

  • Alguacil MD, Caravaca F, Díaz G, Marín P, Roldán A (2004) Establishment of Retama sphaerocarpa L. seedlings on a degraded semiarid soil as influenced by mycorrhizal inoculation and sewage-sludge amendment. J Plant Nutr Soil Sci 167:637–644

    Article  Google Scholar 

  • Alguacil MM, Caravaca E, Roldán A (2005) Changes in rhizosphere microbial activity mediated by native or allochthonous AM fungi in the reafforestation of a Mediterranean degraded environment. Biol Fertil Soils 41:59–68

    Article  Google Scholar 

  • Alguacil MM, Caravaca F, Azcón R, Roldán A (2008) Changes in biological activity of a degraded Mediterranean soil after using microbially-treated dry olive cake as a biosolid amendment and arbuscular mycorrhizal fungi. Eur J Soil Biol 44:347–354

    Article  CAS  Google Scholar 

  • Alguacil MM, Roldán A, Torres MP (2009) Assessing the diversity of AM fungi in arid gypsophilous plant communities. Environ Microbiol 11:2649–2659

    Article  PubMed  CAS  Google Scholar 

  • Alikhani HA, Saleh-Rastin N, Antoun H (2007) Phosphate solubilisation activity of rhizobia native to Iranian soils. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Series: developments in plant and soil sciences. Springer, Dordrecht, The Netherlands, pp 35–41

    Chapter  Google Scholar 

  • Altieri MA (1994) Sustainable agriculture. In: Arntzen CJ, Ritter EM (eds) Encyclopedia of agriculture science, vol 4. Academic, San Diego, pp 239–247

    Google Scholar 

  • Ames RN, Bethlenfalvay GJ (1987) Mycorrhizal fungi and the integration of plant and soil nutrient dynamics. J Plant Nutr 10:1313–1321

    Article  CAS  Google Scholar 

  • Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 192:71–79

    Article  CAS  Google Scholar 

  • Antunes PM, de Varennes A, Zhang T, Goss MJ (2006) The tripartite symbiosis formed by indigenous arbuscular mycorrhizal fungi, Bradyrhizobium japonicum and soya bean under field conditions. J Agron Crop Sci 192:373–378

    Article  Google Scholar 

  • Aroca R, Porcel R, Ruíz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816

    Article  PubMed  CAS  Google Scholar 

  • Artursson V, Finlay DR, Jansson KJ (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  PubMed  CAS  Google Scholar 

  • Asai T (1944) Die bedeutung der mikorrhiza für das pflanzenleben. Jpn J Bot 12:359–408

    Google Scholar 

  • Asimi S, Gianinazzi-Pearson V, Gianinazzi S (1980) Influence of increasing soil-phosphorus levels on interactions between vesicular arbuscular mycorrhizae and Rhizobium in soybeans. Can J Bot–Rev Can Bot 58:2200–2205

    Article  CAS  Google Scholar 

  • Atkinson D (2009) Soil microbial resources and agricultural policies. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 33–45

    Google Scholar 

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

    Article  Google Scholar 

  • Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740

    Article  CAS  Google Scholar 

  • Azcón R (1987) Germination and hyphal growth of Glomus mosseae in vitro. Effect of rhizosphere bacteria and cell-free culture media. Soil Biol Biochem 19:417–419

    Article  Google Scholar 

  • Azcón R (1993) Growth and nutrition of nodulated mycorrhizal and non-mycorrhizal Hedysarum coronarium as a result of treatments with fractions from a plant growth-promoting rhizobacteria. Soil Biol Biochem 25:1037–1042

    Article  Google Scholar 

  • Azcón R, El-Atrach F, Barea JM (1988) Influence of mycorrhiza vs soluble phosphate on growth, nodulation, and N2 fixation (15N) in Medicago sativa at four salinity levels. Biol Fertil Soils 7:28–31

    Article  Google Scholar 

  • Azcón R, Rubio R, Barea JM (1991) Selective interactions between different species of mycorrhizal fungi and Rhizobium meliloti strains, and their effects on growth, N2 fixation (N15) in Medicago sativa at four salinity levels. New Phytol 117:399–404

    Article  Google Scholar 

  • Azcón R, Medina A, Roldán A, Biró B, Vivas A (2009a) Significance of treated agrowaste residue and autochthonous inoculates (Arbuscular mycorrhizal fungi and Bacillus cereus) on bacterial community structure and phytoextraction to remediate heavy metals contaminated soils. Chemosphere 75:327–334

    Article  PubMed  CAS  Google Scholar 

  • Azcón R, Perálvarez MD, Biró B, Roldán A, Ruíz-Lozano JM (2009b) Antioxidant activities and metal acquisition in mycorrhizal plants growing in a heavy-metal multicontaminated soil amended with treated lignocellulosic agrowaste. Appl Soil Ecol 41:168–177

    Article  Google Scholar 

  • Azcón-Aguilar C, Barea JM (1992) Interactions between mycorrhizal fungi and other rhizosphere microorganisms. In: Allen MF (ed) Mycorrhizal functioning: an integrative plant-fungal process. Chapman & Hall, New York, pp 163–198

    Google Scholar 

  • Azcón-Aguilar C, Azcón R, Barea JM (1979) Endomycorrhizal fungi and Rhizobium as biological fertilizers for Medicago sativa in normal cultivation. Nature 279:325–327

    Article  Google Scholar 

  • Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (2009) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg

    Book  Google Scholar 

  • Baar J (2008) From production to application of arbuscular mycorrhizal fungi in agricultural systems: requirements and needs. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany, pp 361–373

    Google Scholar 

  • Babajide PA, Akanbi WB, Alamu LO, Ewetola EA, Olatunji OO (2009) Growth, nodulation and biomass yield of soybean (Glycine max L.) as influenced by bio-fertilizers under simulated eroded soil condition. Res Crops 10:29–34

    Google Scholar 

  • Bago B, Cano C (2005) Breaking myths on arbuscular mycorrhizas in vitro biology. In: Declerck S, Strullu FG, Fortin JA (eds) In vitro culture of mycorrhizas, vol 4, Soil biology. Springer-Verlag, Berlin, Heidelberg, pp 111–138

    Chapter  Google Scholar 

  • Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524

    Article  PubMed  CAS  Google Scholar 

  • Barea JM (1991) Vesicular-arbuscular mycorrhizae as modifiers of soil fertility. In: Stewart BA (ed) Advances in soil science, vol 7. New York, Springer Verlag, pp 1–40

    Chapter  Google Scholar 

  • Barea JM, Azcón-Aguilar C (1983) Mycorrhizas and their significance in nodulating nitrogen-fixing plants. In: Brady N (ed) Advances in agronomy, vol 36. Academic, New York, pp 1–54

    Google Scholar 

  • Barea JM, Azcón-Aguilar C, Azcón R (1987) Vesicular-arbuscular mycorrhiza improve both symbiotic N2-fixation and N uptake from soil as assessed with a 15N technique under field conditions. New Phytol 106:717–725

    Article  CAS  Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (1989) Time-course of N2 fixation (15N) in the field by clover growing alone or in mixture with ryegrass to improve pasture productivity, and inoculated with vesicular-arbuscular mycorrhizal fungi. New Phytol 112:399–404

    Article  Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-fixing systems. Methods Microbiol 24:391–416

    Article  Google Scholar 

  • Barea JM, Tobar RM, Azcón-Aguilar C (1996) Effect of a genetically modified Rhizobium meliloti inoculant on the development of arbuscular mycorrhizas, root morphology, nutrient uptake and biomass accumulation in Medicago sativa. New Phytol 134:361–369

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Barea JM, Gryndler M, Lemanceau P, Schüepp H, Azcón R, Gianinazzi S, Haselwandter K (2002b) The rhizosphere of mycorrhizal plants mycorrhiza technology in agriculture: from genes to bioproducts. Birkhäuser Verlag, Basel, Switzerland, pp 1–18

    Book  Google Scholar 

  • Barea JM, Toro M, Orozco MO, Campos E, Azcón R (2002c) The application of isotopic (P32 and N15) dilution techniques to evaluate the interactive effect of phosphate-solubilizing rhizobacteria, mycorrhizal fungi and Rhizobium to improve the agronomic efficiency of rock phosphate for legume crops. Nutr Cycl Agroecosyst 63:35–42

    Article  CAS  Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (2004) Mycorrhizal fungi and plant growth promoting rhizobacteria. In: Varma A, Abbott LK, Werner D, Hampp R (eds) Plant surface microbiology. Springer-Verlag, Heidelberg, Germany, pp 351–371

    Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (2005a) Interactions between mycorrhizal fungi and bacteria to improve plant nutrient cycling and soil structure. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer-Verlag, Berlin, Heidelbert, pp 195–212

    Chapter  Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005b) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Barea JM, Werner D, Azcón-Aguilar C, Azcón R (2005c) Interactions of arbuscular mycorrhiza and nitrogen fixing symbiosis in sustainable agriculture. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry, ecology and the environment. Springer, Netherlands, pp 199–222

    Chapter  Google Scholar 

  • Barea JM, Toro M, Azcón R (2007) The use of 32P isotopic dilution techniques to evaluate the interactive effects of phosphate-solubilizing bacteria and mycorrhizal fungi at increasing plant P availability. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Series: developments in plant and soil sciences. Springer, Dordrecht, The Netherlands, pp 223–227

    Chapter  Google Scholar 

  • Barea JM, Ferrol N, Azcón-Aguilar C, Azcón R (2008) Mycorrhizal symbioses. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Series: plant ecophysiology. Springer, Dordrecht, pp 143–163

    Chapter  Google Scholar 

  • Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496

    Article  CAS  Google Scholar 

  • Benabdellah K, Ruíz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70:647–661

    Article  PubMed  CAS  Google Scholar 

  • Bethlenfalvay GJ, Brown MS, Stafford AE (1985) Glycine-Glomus Rhizobium symbiosis. II. antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiol 79:1054–1058

    Article  PubMed  CAS  Google Scholar 

  • Bhatia NP, Adholeya A, Sharma A (1998) Biomass production and changes in soil productivity during longterm cultivation of Prosopis juliflora (Swartz) DC inoculated with VA mycorrhiza and Rhizobium spp. in a semi-arid wasteland. Biol Fertil Soils 26:208–214

    Article  CAS  Google Scholar 

  • Biró B, Köves-Péchy K, Vörös I, Kádár I (1998) Toxicity of some field applied heavy metal salts to the rhizobial and fungal microsymbionts of alfalfa and red clover. Agrokem Talajtan 47:265–277

    Google Scholar 

  • Bisht R, Chaturvedi S, Srivastava R, Sharma AK, Johri BN (2009) Effect of arbuscular mycorrhizal fungi, Pseudomonas fluorescens and Rhizobium leguminosarum on the growth and nutrient status of Dalbergia sissoo Roxb. Trop Ecol 50:231–242

    CAS  Google Scholar 

  • Brito I, Goss MJ, de Carvalho M, van Tuinen D, Antunes PM (2008) Agronomic management of indigenous mycorrhizas. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany, pp 375–402

    Google Scholar 

  • Brown MS, Bethlenfalvay GJ (1988) The Glycine Glomus Rhizobium symbiosis. 7. Photosynthetic nutrient use efficiency in nodulated, mycorrhizal soybeans. Plant Physiol 86:1292–1297

    Article  PubMed  CAS  Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304

    Article  Google Scholar 

  • Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212

    Article  CAS  Google Scholar 

  • Buscot F (2005) What are soils? In: Buscot F, Varma S (eds) Microorganisms in soils: roles in genesis and functions. Heidelbert, Germany, Springer-Verlag, pp 3–18

    Chapter  Google Scholar 

  • Caravaca F, Alguacil MM, Figueroa D, Barea JM, Roldán A (2003a) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. For Ecol Manage 182:49–58

    Article  Google Scholar 

  • Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldán A (2003b) Establishment of shrubs species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111

    Article  Google Scholar 

  • Caravaca F, Figueroa D, Alguacil MM, Roldán A (2003c) Application of composted urban residue enhanced the performance of afforested shrub species in a degraded semiarid land. Bioresour Technol 90:65–70

    Article  PubMed  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Azcón R, Díaz G, Roldán A (2004a) Comparing the effectiveness of mycorrhizal inoculation and amendment with sugar beet, rock phosphate and Aspergillus niger to enhance field performance of the leguminous shrub Dorycnium pentaphyllum L. Appl Soil Ecol 25:169–180

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Vassileva M, Díaz G, Roldán A (2004b) AM fungi inoculation and addition of microbially-treated dry olive cake-enhanced afforestation of a desertified Mediterranean site. Land Degrad Dev 15:153–161

    Article  Google Scholar 

  • Caravaca F, Figueroa D, Barea JM, Azcon-Aguilar C, Roldan A (2004c) Effect of mycorrhizal inoculation on nutrient acquisition, gas exchange, and nitrate reductase activity of two Mediterranean-autochthonous shrub species under drought stress. J Plant Nutr 27:57–74

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Barea JM, Roldán A (2005a) Survival of inocula and native AM fungi species associated with shrubs in a degraded Mediterranean ecosystem. Soil Biol Biochem 37:227–233

    Article  CAS  Google Scholar 

  • Caravaca F, Alguacil MM, Diaz G, Marin P, Roldán A (2005b) Nutrient acquisition and nitrate reductase activity of mycorrhizal Retama sphaerocarpa L. seedlings afforested in an amended semiarid soil under two water regimes. Soil Use Manage 21:10–16

    Article  Google Scholar 

  • Caravaca F, Tortosa G, Carrasco L, Cegarra J, Roldán A (2006) Interaction between AM fungi and a liquid organic amendment with respect to enhancement of the performance of the leguminous shrub Retama sphaerocarpa. Biol Fertil Soils 43:30–38

    Article  Google Scholar 

  • Chalk PM, Souza RD, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951

    Article  CAS  Google Scholar 

  • Chaudhary VB, Bowker MA, O'Dell TE, Grace JB, Redman AE, Rillig MC, Johnson NC (2009) Untangling the biological contributions to soil stability in semiarid shrublands. Ecol Appl 19:110–122

    Article  PubMed  Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytol 157:503–523

    Article  CAS  Google Scholar 

  • Cornejo P, Azcón-Aguilar C, Barea JM, Ferrol N (2004) Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol Lett 241:265–270

    Article  PubMed  CAS  Google Scholar 

  • Croll D, Wille L, Gamper HA, Mathimaran N, Lammers PJ, Corradi N, Sanders IR (2008) Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 178:672–687

    Article  PubMed  CAS  Google Scholar 

  • Cuenca G, Cáceres A, González MG (2008) AM inoculation in tropical agriculture: field results. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany, pp 403–417

    Google Scholar 

  • Danso SKA (1988) The use of 15N enriched fertilizers for estimating nitrogen fixation in grain and pasture legumes. In: Beck DP, Materon L (eds) Nitrogen fixation by legumes in Mediterranean agriculture. Martinus Nijhoff Publishers, Dordrecht, pp 345–358

    Chapter  Google Scholar 

  • de Boer W, Verheggen P, Gunnewiek P, Kowalchuk GA, van Veen JA (2003) Microbial community composition affects soil fungistasis. Appl Environ Microbiol 69:835–844

    Article  PubMed  CAS  Google Scholar 

  • de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  CAS  Google Scholar 

  • Dessaux Y, Hinsinger P, Lemanceau P (2010) Rhizosphere: achievements and challenges. Springer, New York

    Google Scholar 

  • Díaz G, Azcón-Aguilar C, Honrubia M (1996) Influence of arbuscular mycorrhizae on heavy metal (Zn and Pb) uptake and growth of Lygeum spartum and Anthyllis cytisoides. Plant Soil 180:241–249

    Article  Google Scholar 

  • Dong Y, Zhu YG, Smith FA, Wang YS, Chen BD (2008) Arbuscular mycorrhiza enhanced arsenic resistance of both white clover (Trifolium repens Linn.) and ryegrass (Lolium perenne L.) plants in an arsenic-contaminated soil. Environ Pollut 155:174–181

    Article  PubMed  CAS  Google Scholar 

  • Douglas AE (2008) Conflict, cheats and the persistence of symbioses. New Phytol 177:849–858

    Article  PubMed  Google Scholar 

  • Echeverria M, Scambato AA, Sannazzaro AI, Maiale S, Ruíz OA, Menéndez AB (2008) Phenotypic plasticity with respect to salt stress response by Lotus glaber: the role of its AM fungal and rhizobial symbionts. Mycorrhiza 18:317–329

    Article  PubMed  Google Scholar 

  • 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 184:412–423

    Article  PubMed  CAS  Google Scholar 

  • Estaún V, Camprubí A, Joner EJ (2002) Selecting arbuscular mycorrhizal fungi for field application. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhiza technology in agriculture, from genes to bioproducts. Birkhauser Verlag, Basel, Switzerland, pp 249–259

    Chapter  Google Scholar 

  • Estaún V, Vicente S, Calvet C, Camprubí A, Busquets M (2007) Integration of arbuscular mycorrhiza inoculation in hydroseeding technology. Effects on plant growth and inter-species competition. Land Degrad Dev 18:621–630

    Article  Google Scholar 

  • Facelli E, Smith SE, Smith FA (2009) Mycorrhizal symbiosis – overview and new insights into roles of arbuscular mycorrhizas in agro and natural ecosystems. Australas Plant Pathol 38:338–344

    Article  Google Scholar 

  • Farhat MB, Farhat A, Bejar W, Kammoun R, Bouchaala K, Fourati A, Antoun A, Bejar S, Chouayekh H (2009) Characterization of the mineral phosphate solubilizing activity of Serratia marcescens CTM 50650 isolated from the phosphate mine of Gafsa. Arch Microbiol 191:815–824

    Article  PubMed  CAS  Google Scholar 

  • Faure D, Vereecke D, Leveau JHJ (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303

    Article  CAS  Google Scholar 

  • Ferrol N, Pérez-Tienda J (2009) Coordinated nutrient exchange in arbuscular mycorrhiza. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 73–87

    Chapter  Google Scholar 

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126

    Article  PubMed  CAS  Google Scholar 

  • Francis DF, Thornes JB (1990) Matorral, erosion and reclamation. In: Albaladejo J, Stocking MA, Díaz E (eds) Soil degradation and rehabilitation in mediterranean environmental conditions. CSIC, Murcia, Spain, pp 87–115

    Google Scholar 

  • Franzini VI, Azcón R, Latanze-Mendes F, Aroca R (2009) Interaction between Glomus species and Rhizobium strains affect the nutritional physiology of drought stressed legume hosts. J Plant Physiol. doi:j.jplph.2009.11.010

    PubMed  Google Scholar 

  • Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328

    Article  PubMed  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  • Galleguillos C, Aguirre C, Barea JM, Azcón R (2000) Growth promoting effect of two Sinorhizobium meliloti strains (a wild type and its genetically modified derivative) on a non-legume plant species in specific interaction with two arbuscular mycorrhizal fungi. Plant Sci 159:57–63

    Article  PubMed  CAS  Google Scholar 

  • Gamalero E, Lingua G, Capri FG, Fusconi A, Berta G, Lemanceau P (2004) Colonization pattern of primary tomato roots by Pseudomonas fluorescens A6RI characterized by dilution plating, flow cytometry, fluorescence, confocal and scanning electron microscopy. FEMS Microbiol Ecol 48:79–87

    Article  PubMed  CAS  Google Scholar 

  • Gamper HA, van der Heijden MGA, Kowalchuk GA (2010) Molecular trait indicators: moving beyond phylogeny in arbuscular mycorrhizal ecology. New Phytol 185:67–82

    Article  PubMed  CAS  Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Garcia-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459

    Article  PubMed  CAS  Google Scholar 

  • Gavito ME, Schweiger P, Jakobsen I (2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Glob Chang Biol 9:106–116

    Article  Google Scholar 

  • George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions, vol 7, Series: plant ecophysiology. Springer, Dordrecht, pp 247–270

    Chapter  Google Scholar 

  • Gianinazzi S, Vosátka M (2004) Inoculum of arbuscular mycorrhizal fungi for production systems: science meets business. Can J Bot–Rev Can Bot 82:1264–1271

    Article  Google Scholar 

  • Gianinazzi-Pearson V, Brechenmacher L (2004) Functional genomics of arbuscular mycorrhiza: decoding the symbiotic cell programme. Can J Bot–Rev Can Bot 82:1228–1234

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Azcón-Aguilar C, Bécard G, Bonfante P, Ferrol N, Franken P, Gollote A, Harrier L, Lanfranco L, van Tuinen D (2004) Structural and functional genomics of symbiotic arbuscular mycorrhizal fungi. In: Tkacz JS, Lange L (eds) Advances in fungal biotechnology for industry, medicine and agriculture. Kluwer Academic/Plenum Publishers, New York, Boston, pp 405–424

    Chapter  Google Scholar 

  • Gianinazzi-Pearson V, Tollot M, Seddas PMA (2009) Dissection of genetic cell programmes driving early arbuscular mycorrhiza interactions. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 33–45

    Chapter  Google Scholar 

  • Giri B, Giang PH, Kumari R, Prasad R (2005) Microbial diversity in soils. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions. Springer-Verlag, Heidelbert, Germany, pp 195–212

    Google Scholar 

  • Goicoechea N, Antolín MC, Sánchez-Díaz M (2000) The role of plant size and nutrient concentrations in associations between Medicago, and Rhizobium and/or Glomus. Biol Plant 43:221–226

    Article  Google Scholar 

  • González-Guerrero M, Benabdellah K, Ferrol N, Azcón-Aguilar C (2009) Mechanisms underlying heavy metal tolerance in arbuscular mycorrhizas. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 107–122

    Chapter  Google Scholar 

  • Gryndler M (2000) Interactions of arbuscular mycorrhizal fungi with other soil organisms. In: Kapulnik Y, Douds DDJ (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 239–262

    Google Scholar 

  • Gryndler M, Hrselova H, Cajthaml T, Havrankova M, Rezacova V, Gryndlerova H, Larsen J (2009) Influence of soil organic matter decomposition on arbuscular mycorrhizal fungi in terms of asymbiotic hyphal growth and root colonization. Mycorrhiza 19:255–266

    Article  PubMed  Google Scholar 

  • Ha Y, Gray VM (2008) Growth yield of Vicia faba L in response to microbial symbiotic associations. S Afr J Bot 74:25–32

    Article  Google Scholar 

  • Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species – opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    Article  PubMed  CAS  Google Scholar 

  • Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

  • Hayman DS (1986) Mycorrhizae of nitrogen-fixing legumes. MIRCEN J 2:121–145

    Article  Google Scholar 

  • Haystead A, Malajczuk N, Grove TS (1988) Underground transfer of nitrogen between pasture plants infected with vesicular arbuscular mycorrhizal fungi. New Phytol 108:417–423

    Article  Google Scholar 

  • Helgason T, Fitter AH (2009) Natural selection and the evolutionary ecology of the arbuscular mycorrhizal fungi (Phylum Glomeromycota). J Exp Bot 60:2465–2480

    Article  PubMed  CAS  Google Scholar 

  • Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9:1930–1938

    Article  PubMed  CAS  Google Scholar 

  • Herrera MA, Salamanca CP, Barea JM (1993) Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified Mediterranean ecosystems. Appl Environ Microbiol 59:129–133

    PubMed  CAS  Google Scholar 

  • Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium–legume symbiosis. Fungal Genet Biol 23:205–212

    Article  PubMed  CAS  Google Scholar 

  • Jaderlund L, Arthurson V, Granhall U, Jansson JK (2008) Specific interactions between arbuscular mycorrhizal fungi and plant growth-promoting bacteria: as revealed by different combinations. FEMS Microbiol Lett 287:174–180

    Article  PubMed  CAS  Google Scholar 

  • Janse JM (1896) Les endophytes radicaux des quelques plantes Javanaises. Annales du Jardin Botanique Buitenzorg 14:53–212

    Google Scholar 

  • Jasper DA (2007) Beneficial soil microorganisms of the Jarrah forest and their recovery in bauxite Southwestern Australia. Restor Ecol 15:S74–S84

    Article  Google Scholar 

  • Jeffries P, Barea JM (2001) Arbuscular Mycorrhiza – a key component of sustainable plant-soil ecosystems. In: Hock B (ed) The mycota, vol 9, Fungal associations. Springer-Verlag, Berlin, Heidelberg, pp 95–113

    Google Scholar 

  • Jones FR (1924) A mycorrhizal fungus in the roots of legumes and some other plant. J Agric Res 29:459–470

    Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33

    Article  CAS  Google Scholar 

  • Khan MS, Zaidi A, Wani PA (2007) Role of phosphate solubilizing microorganisms in sustainable agriculture – a review. Agron Sustain Dev 27:29–43

    Article  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi – current perspective. Arch Agron Soil Sci 56(1):73–98

    Article  CAS  Google Scholar 

  • Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215–236

    Article  Google Scholar 

  • Kloepper JW (1994) Plant growth-promoting rhizobacteria (other systems). In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, Florida, pp 111–118

    Google Scholar 

  • Kloepper JW, Zablotowicz RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, pp 315–326

    Google Scholar 

  • Koltai H, Meir D, Shlomo E, Resnick N, Ziv O, Wininger S, Ben-Dor B, Kapulnik Y (2008) Exploiting arbuscular mycorrhizal technology in different cropping systems under greenhouse conditions in semi-arid regions. In: Kubota C, Kacira M (eds) Book series. Acta horticulturae. Proceedings of the international workshop on greenhouse environmental control and crop production in semi-arid regions. ISHS publishes, Tucson, AZ, USA, pp 223–228

    Google Scholar 

  • Kucey RMN, Janzen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:199–228

    Article  CAS  Google Scholar 

  • Lambais MR (2006) Unraveling the signaling and signal transduction mechanisms controlling arbuscular mycorrhiza development. Sci Agric 63:405–413

    Article  CAS  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant–microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  • Leigh G (2002) Nitrogen fixation at the millennium. Elsevier Science, London

    Google Scholar 

  • Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    Article  PubMed  CAS  Google Scholar 

  • Lesueur D, Sarr A (2008) Effects of single and dual inoculation with selected microsymbionts (rhizobia and arbuscular mycorrhizal fungi) on field growth and nitrogen fixation of Calliandra calothyrsus Meissn. Agroforest Syst 73:37–45

    Article  Google Scholar 

  • Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153

    Article  CAS  Google Scholar 

  • Leyval C, Joner EJ, del Val C, Haselwandter K (2002) Potential of arbuscular mycorrhizal fungi for bioremediation. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. Birkhäuser Verlag, Basel, Switzerland, pp 175–186

    Chapter  Google Scholar 

  • Lin AJ, Zhang XH, Wong MH, Ye ZH, Lou LQ, Wang YS, Zhu YG (2007) Increase of multi-metal tolerance of three leguminous plants by arbuscular mycorrhizal fungi colonization. Environ Geochem Health 29:473–481

    Article  PubMed  CAS  Google Scholar 

  • Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora. The mycorrhizosphere effects. Phytopathology 78:366–371

    Google Scholar 

  • López-Sánchez ME, Díaz G, Honrubia M (1992) Influence of vesicular-arbuscular mycorrhizal infection and P addition on growth and P nutrition of Anthyllis cytisoides L. and Brachypodium retusum (Pers.) Beauv. Mycorrhiza 2:41–45

    Article  Google Scholar 

  • Lucas-Garcia JA, Probanza A, Ramos B, Colón-Flores JJ, Gutierrez-Mañero FJ (2004) Effects of plant growth promoting rhizobateria (PGPRs) on the biological nitrogen fixation, nodulation and growth of Lupinus albus I. cv. Multolupa. Eng Life Sci 4:71–77

    Article  CAS  Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 86:1–25

    Article  CAS  Google Scholar 

  • Lupwayi NZ, Kennedy AC (2007) Grain legumes in northern Great Plains: impacts on selected biological soil processes. Agron J 99:1700–1709

    Article  CAS  Google Scholar 

  • Maki T, Nomachi M, Yoshida S, Ezawa T (2008) Plant symbiotic microorganisms in acid sulfate soil: significance in the growth of pioneer plants. Plant Soil 310:55–65

    Article  CAS  Google Scholar 

  • Mallik MAB, Williams RD (2008) Plant growth promoting rhizobacteria and mycorrhizal fungi in sustainable agriculture and forestry. In: Zeng RS, Mallik AU, Luo SM (eds) Allelopathy in sustainable agriculture and forestry. Springer, New York, pp 321–345

    Chapter  Google Scholar 

  • Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86

    Article  PubMed  CAS  Google Scholar 

  • Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:497–506

    Article  CAS  Google Scholar 

  • Marschner P (2008) The role of rhizosphere microorganisms in relation to P uptake by plants. In: White PJ, Hammond J (eds) The ecophysiology of plant–phosphorus interactions, vol 7, Series: plant ecophysiology. Springer, Dordrecht, pp 165–176

    Chapter  Google Scholar 

  • Martin F (2008) Orchestrating morphogenesis in mycorrhizal symbioses. New Phytol 177:839–841

    Article  PubMed  Google Scholar 

  • Martin F, Gianinazzi-Pearson V, Hijri M, Lammers P, Requena N, Sanders IR, Shachar-Hill Y, Shapiro H, Tuskan GA, Young JPW (2008) The long hard road to a completed Glomus intraradices genome. New Phytol 180:747–750

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Romero E (2009) Coevolution in Rhizobium–Legume symbiosis? DNA Cell Biol 28:361–370

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Matias SR, Pagano MC, Muzzi FC, Oliveira CA, Carneiro AA, Horta SN, Scotti MR (2009) Effect of rhizobia, mycorrhizal fungi and phosphate-solubilizing microorganisms in the rhizosphere of native plants used to recover an iron ore area in Brazil. Eur J Soil Biol 45:259–266

    Article  CAS  Google Scholar 

  • Medina A, Vassileva M, Caravaca F, Roldán A, Azcón R (2004) Improvement of soil characteristics and growth of Dorycnium pentaphyllum by amendment with agrowastes and inoculation with AM fungi and/or the yeast Yarowia lipolytica. Chemosphere 56:449–456

    Article  PubMed  CAS  Google Scholar 

  • Medina A, Vassilev N, Barea JM, Azcón R (2005) Application of Aspergillus niger-treated agrowaste residue and Glomus mosseae for improving growth and nutrition of Trifolium repens in a Cd-contaminated soil. J Biotechnol 116:369–378

    Article  PubMed  CAS  Google Scholar 

  • Medina A, Vassileva M, Barea JM, Azcón R (2006) The growth-enhancement of clover by Aspergillus-treated sugar beet waste and Glomus mosseae inoculation in Zn-contaminated soil. Appl Soil Ecol 33:87–98

    Article  Google Scholar 

  • Miller RM, Jastrow JD (2000) Mycorrhizal fungi influence soil structure. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 3–18

    Google Scholar 

  • 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 

  • Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019–1027

    Article  CAS  Google Scholar 

  • Morton JB (2009) Reconciliation of conflicting phenotypic and rRNA gene phylogenies of fungi in glomeromycota based on underlying patterns and processes. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 137–154

    Chapter  Google Scholar 

  • Mosse B (1986) Mycorrhiza in a sustainable agriculture. Biol Agric 3:191–209

    Article  Google Scholar 

  • Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364

    Article  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mader P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agric Ecosyst Environ 134:257–268

    Article  Google Scholar 

  • Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008a) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876

    Article  PubMed  CAS  Google Scholar 

  • Öpik M, Saks Ü, Kennedy J, Daniell T (2008b) Global diversity patterns of arbuscular mycorrhizal fungi-community composition and links with functionality. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany, pp 89–111

    Google Scholar 

  • Pagano MC, Cabello MN, Bellote AF, Sa NM, Scotti MR (2008) Intercropping system of tropical leguminous species and Eucalyptus camaldulensis, inoculated with rhizobia and/or mycorrhizal fungi in semiarid Brazil. Agroforest Syst 74:231–242

    Article  Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    Article  PubMed  CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775

    Article  PubMed  CAS  Google Scholar 

  • Pivato B, Offre P, Marchelli S, Barbonaglia B, Mougel C, Lemanceau P, Berta G (2009) Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19:81–90

    Article  PubMed  Google Scholar 

  • Porcel R, Ruíz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Porcel R, Aroca R, Azcón R, Ruíz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404

    Article  PubMed  CAS  Google Scholar 

  • Postgate J (1998) The origins of the unit of nitrogen fixation at the University of Sussex. Notes Rec R Soc Lond 52:355–362

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Verhage A, García-Andrade J, García JM, A-A C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 123–135

    Chapter  Google Scholar 

  • Provorov NA, Vorobyov NI (2009a) Host plant as an organizer of microbial evolution in the beneficial symbioses. Phytochem Rev 8:519–534

    Article  CAS  Google Scholar 

  • Provorov NA, Vorobyov NI (2009b) Interspecies altruism in plant–microbe symbioses: use of group selection models to resolve the evolutionary paradoxes. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas functional processes and ecological impact. Springer-Verlag, Berlin, Heidelberg, pp 17–31

    Chapter  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000a) Glomalean fungi from the Ordovician. Science 289:1920–1921

    Article  PubMed  CAS  Google Scholar 

  • Redecker D, Morton JB, Bruns TD (2000b) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14:276–284

    Article  PubMed  CAS  Google Scholar 

  • Redon PO, Beguiristain T, Leyval C (2009) Differential effects of AM fungal isolates on Medicago truncatula growth and metal uptake in a multimetallic (Cd, Zn, Pb) contaminated agricultural soil. Mycorrhiza 19:187–195

    Article  PubMed  CAS  Google Scholar 

  • Reinhardt D (2007) Programming good relations – development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 10:98–105

    Article  PubMed  Google Scholar 

  • Requena N, Jiménez I, Toro M, Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136:667–677

    Article  Google Scholar 

  • Requena N, Pérez-Solis E, Azcón-Aguilar C, Jeffries P, Barea JM (2001) Management of indigenous plant–microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498

    Article  PubMed  CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Article  PubMed  CAS  Google Scholar 

  • Rinu K, Pandey A (2009) Bacillus subtilis NRRL B-30408 inoculation enhances the symbiotic efficiency of Lens esculenta Moench at a Himalayan location. J Plant Nutr Soil Sci 172:134–139

    Article  CAS  Google Scholar 

  • Rivas R, Peix A, Mateos P, Trujillo M, Martínez-Molina E, Velázquez E (2007) Biodiversity of populations of phosphate solubilizing rhizobia that nodulates chickpea in different Spanish soils. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Series: developments in plant and soil sciences. Springer, Dordrecht, The Netherlands, pp 23–33

    Chapter  Google Scholar 

  • Rosendahl S (2008) Communities, populations and individuals of arbuscular mycorrhizal fungi. New Phytol 178:253–266

    Article  PubMed  Google Scholar 

  • Rosendahl S, McGee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ruíz-Lozano JM, Aroca R (2008) Last insights into the role of aquaporins in the alleviation of osmotic stress by arbuscular mycorrhizal symbiosis. In: Van Dijk T (ed) Microbial ecology research trends. Nova Science Publishers, Inc., New York, pp 139–154

    Google Scholar 

  • Ruíz-Lozano JM, Azcón R (1993) Specificity and functional compatibility of VA mycorrhizal endophytes in association with Bradyrhizobium strains in Cicer arietinum. Symbiosis 15:217–226

    Google Scholar 

  • Ruíz-Lozano JM, Azcón R (1994) Development and activity of the symbiosis between Bradyrhizobium strains, Glomus species and Cicer arietinum: effect of timing of inoculation and photon irradiance. Symbiosis 16:249–265

    Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Arbuscular mycorrhizal symbiosis can alleviate drought-induced nodule senescence in soybean plants. New Phytol 151:493–502

    Article  CAS  Google Scholar 

  • Ruíz-Lozano JM, Porcel R, Aroca R (2008) Evaluation of the possible participation of drought-induced genes in the enhanced tolerance of arbuscular mycorrhizal plants to water deficit. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer-Verlag, Berlin, Heidelberg, Germany, pp 185–207

    Google Scholar 

  • Sabannavar SJ, Lakshman HC (2008) Interactions between Azotobacter, Pseudomonas and arbuscular mycorrhizal fungi on two varieties of Sesamum indicum L. J Agron Crop Sci 194:470–478

    Google Scholar 

  • Santos-González JC, Finlay RD, Tehler A (2007) Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Appl Environ Microbiol 73:5613–5623

    Article  PubMed  CAS  Google Scholar 

  • Schiavo JA, Busato JG, Martins MA, Canellas LP (2009) Recovery of degraded areas revegeted with Acacia mangium and Eucalyptus with special reference to organic matter humification. Sci Agric 66:353–360

    Article  CAS  Google Scholar 

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota, phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Siviero MA, Motta AM, Lima DDS, Birolli RR, Huh SY, Santinoni IA, Murate LS, de Castro CMA, Miyauchi MYH, Zangaro W, Nogueira MA, Andrade G (2008) Interaction among N-fixing bacteria and AM fungi in Amazonian legume tree (Schizolobium amazonicum) in field conditions. Appl Soil Ecol 39:144–152

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, Academic, New York

    Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    Article  PubMed  CAS  Google Scholar 

  • Sonjak S, Beguiristain T, Leyval C, Regvar M (2009) Temporal temperature gradient gel electrophoresis (TTGE) analysis of arbuscular mycorrhizal fungi associated with selected plants from saline and metal polluted environments. Plant Soil 314:25–34

    Article  CAS  Google Scholar 

  • Staddon PL, Thompson K, Jakobsen I, Grime JP, Askew AP, Fitter AH (2003) Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob Chang Biol 9:186–194

    Article  Google Scholar 

  • Teng Y, Y-m L, Gao J, Z-g L (2008) Combined remediation effects of arbuscular mycorrhizal fungi–legumes–rhizobium symbiosis on PCBs contaminated soils. Huan Jing Ke Xue 29:2925–2930

    PubMed  CAS  Google Scholar 

  • Tobar RM, Azcón R, Barea JM (1994a) Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol 126:119–122

    Article  Google Scholar 

  • Tobar RM, Azcón R, Barea JM (1994b) The improvement of plant N acquisition from an ammonium-treated, drought-stressed soil by the fungal symbiont in arbuscular mycorrhizae. Mycorrhiza 4:105–108

    Article  Google Scholar 

  • Tobar RM, Azcón-Aguilar C, Sanjuan J, Barea JM (1996) Impact of a genetically modified Rhizobium strain with improved nodulation competitiveness on the early stages of arbuscular mycorrhiza formation. Appl Soil Ecol 4:15–21

    Article  Google Scholar 

  • Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338

    Article  PubMed  CAS  Google Scholar 

  • Toro M, Azcón R, Barea JM (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate-solubilizing rhizobacteria to improve rock phosphate bioavailability (P32) and nutrient cycling. Appl Environ Microbiol 63:4408–4412

    PubMed  CAS  Google Scholar 

  • Toro M, Azcón R, Barea JM (1998) The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytol 138:265–273

    Article  CAS  Google Scholar 

  • Turnau K, Jurkiewicz A, Língua G, Barea JM, Gianinazzi-Pearson V (2006) Role of arbuscular mycorrhiza and associated microorganisms in phytoremediation of heavy metal-polluted sites. In: Prasad MNV, Sajwan KS, Naidu R (eds) Trace elements in the environment. Biogeochemistry, biotechnology and bioremediation. CRC/Taylor & Francis, Boca Raton, Florida, pp 235–252

    Google Scholar 

  • Uyanoz R, Akbulut M, Cetin U, Gultepe N (2007) Effects of microbial inoculation, organic and chemical fertilizer on yield and physicochemical and cookability properties of bean (Phaseolus vulgaris L.) seeds. Philipp Agric Sci 90:168–172

    Google Scholar 

  • van Loon WKP, de Kreuk MK, Hamelers HVM, Bot GPA (1998) Water regulated air flow controller for permeability measurements. In: Farkas I (ed) Control applications in post-harvest and processing technology. Published for the international federation of automatic control. Pergamon Oxford, Tarrytown, NY, USA, pp 43–47

    Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    Article  PubMed  CAS  Google Scholar 

  • Vargas R, Baldocchi DD, Querejeta JI, Curtis PS, Hasselquist NJ, Janssens IA, Allen MF, Montagnani L (2010) Ecosystem CO2 fluxes of arbuscular and ectomycorrhizal dominated vegetation types are differentially influenced by precipitation and temperature. New Phytol 185:226–236

    Article  PubMed  CAS  Google Scholar 

  • Varma A (2008) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany

    Google Scholar 

  • Vassilev N, Vassileva M, Azcón R, Barea JM (2002) The use of 32P dilution techniques to evaluate the effect of mycorrhizal inoculation on plant uptake of P from products of fermentation mixtures including agrowastes Aspergillus niger and rock phosphate. Assessment of soil phosphorus status and management of phosphatic fertilisers to optimise crop production. IAEA, Vienna, pp 47–53

    Google Scholar 

  • Vassilev N, Medina A, Azcón R, Vassileva M (2007) Microbial solubilization of rock phosphate on media containing agro-industrial wastes and effect of the resulting products on plant growth and P uptake. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Series: developments in plant and soil sciences. Springer, Dordrecht, The Netherlands, pp 77–84

    Chapter  Google Scholar 

  • Vázquez MM, Bejarano C, Azcón R, Barea JM (2000) The effect of a genetically modified Rhizobium meliloti inoculant on fungal alkaline phosphatase and succinate dehydrogenase activities in mycorrhizal alfalfa plants as affected by the water status in soil. Symbiosis 29:49–58

    Google Scholar 

  • Vázquez MM, Barea JM, Azcón R (2002) Influence of arbuscular mycorrhizae and a genetically modified strain of Sinorhizobium on growth, nitrate reductase activity and protein content in shoots and roots of Medicago sativa as affected by nitrogen concentrations. Soil Biol Biochem 34:899–905

    Article  Google Scholar 

  • Vessey JK, Pawlowski K, Bergman B (2004) Root-based N2-fixing symbioses: legumes, actinorhizal plants, Parasponia sp and cycads. Plant Soil 266:205–230

    Article  CAS  Google Scholar 

  • Vivas A, Azcón R, Biró B, Barea JM, Ruíz-Lozano JM (2003a) 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

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Biró B, Campos E, Barea JM, Azcón R (2003b) Symbiotic efficiency of autochthonous arbuscular mycorrhizal fungus (G. mosseae) and Brevibacillus sp isolated from cadmium polluted soil under increasing cadmium levels. Environ Pollut 126:179–189

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Marulanda A, Gómez M, Barea JM, Azcón R (2003c) Physiological characteristics (SDH and ALP activities) of arbuscular mycorrhizal colonization as affected by Bacillus thuringiensis inoculation under two phosphorus levels. Soil Biol Biochem 35:987–996

    Article  CAS  Google Scholar 

  • Vivas A, Marulanda A, Ruíz-Lozano JM, Barea JM, Azcón R (2003d) Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress. Mycorrhiza 13:249–256

    Article  PubMed  Google Scholar 

  • Vivas A, Vörös A, Biró B, Barea JM, Ruíz-Lozano JM, Azcón R (2003e) Beneficial effects of indigenous Cd-tolerant and Cd-sensitive Glomus mosseae associated with a Cd-adapted strain of Brevibacillus sp. in improving plant tolerance to Cd contamination. Appl Soil Ecol 24:177–186

    Article  Google Scholar 

  • Vivas A, Barea JM, Azcón R (2005a) Brevibacillus brevis isolated from cadmium- or zinc-contaminated soils improves in vitro spore germination and growth of Glomus mosseae under high Cd or Zn concentrations. Microb Ecol 49:416–424

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Barea JM, Azcón R (2005b) Interactive effect of Brevibacillus brevis and Glomus mosseae, both isolated from Cd contaminated soil, on plant growth, physiological mycorrhizal fungal characteristics and soil enzymatic activities in Cd polluted soil. Environ Pollut 134:257–266

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Barea JM, Biro B, Azcon R (2006a) Effectiveness of autochthonous bacterium and mycorrhizal fungus on Trifolium growth, symbiotic development and soil enzymatic activities in Zn contaminated soil. J Appl Microbiol 100:587–598

    Article  PubMed  CAS  Google Scholar 

  • Vivas A, Biro B, Nemeth T, Barea JM, Azcon R (2006b) Nickel-tolerant Brevibacillus brevis and arbuscular mycorrhizal fungus can reduce metal acquisition and nickel toxicity effects in plant growing in nickel supplemented soil. Soil Biol Biochem 38:2694–2704

    Article  CAS  Google Scholar 

  • Vivas A, Biró B, Ruíz-Lozano JM, Barea JM, Azcón R (2006c) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62:1523–1533

    Article  PubMed  CAS  Google Scholar 

  • von Alten H, Blal B, Dodd JC, Feldman F, Vosátka M (2002) Quality control of arbuscular mycorrhizal fungi inoculum in Europe. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhiza technology in agriculture, from genes to bioproducts. Birkhauser Verlag, Basel, Switzerland, pp 281–296

    Chapter  Google Scholar 

  • Vosátka M, Albrechtová J, Patten R (2008) The international marked development for mycorrhizal technology. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3rd edn. Springer-Verlag, Berlin, Heidelberg, Germany, pp 419–438

    Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287

    Article  CAS  Google Scholar 

  • Willems A (2007) The taxonomy of rhizobia: an overview. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Series: developments in plant and soil sciences. Springer, Dordrecht, The Netherlands, pp 3–14

    Chapter  Google Scholar 

  • Xiao C, Chi R, He H, Zhang W (2009) Characterization of tricalcium phosphate solubilization by Stenotrophomonas maltophilia YC isolated from phosphate. J Cent S Univ Technol 16:581–587

    Article  CAS  Google Scholar 

  • Yamada S, Bohnert HJ (2000) Expression of the PIP aquaporin promoter-MipA from the common ice plant in tobacco. Plant Cell Physiol 41:719–725

    Article  PubMed  CAS  Google Scholar 

  • Zahir ZA, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS (2007) Stimulatory effects of dual inoculation with phosphate solubilising microorganisms and arbuscular mycorrhizal fungus on chickpea. Aust J Exp Agric 47:1016–1022

    Article  CAS  Google Scholar 

  • Zaidi A, Khan MS, Amil M (2003) Interactive effect of rhizotrophic microorganisms on yield and nutrient uptake of chickpea (Cicer arietinum L.). Eur J Agron 19:15–21

    Article  Google Scholar 

  • Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284

    Article  PubMed  CAS  Google Scholar 

  • Zapata F, Axmann H (1995) P32 isotopic techniques for evaluating the agronomic effectiveness of rock phosphate materials. Fertil Res 41:189–195

    Article  Google Scholar 

  • Zapata F, Danso SKA, Hardanson G, Fried M (1987) Nitrogen-fixation and translocation in field grown fababean. Agron J 79:505–509

    Article  Google Scholar 

  • Zarei M, Saleh-Rastin N, Alikhani HA, Aliasgharzadeh N (2006) Responses of lentil to co-inoculation with phosphate-solubilizing rhizobial strains and arbuscular mycorrhizal fungi. J Plant Nutr 29:1509–1522

    Article  CAS  Google Scholar 

  • Zhukov VA, Shtark OY, Borisov AY, Tikhonovich IA (2009) Molecular genetic mechanisms used by legumes to control early stages of mutually beneficial (mutualistic) symbiosis. Russ J Genet 45:1279–1288

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study is included in the framework of the following Research Projects from the Spanish National Research Programme (R & D)-European Union (Feder): AGL 2006-09453-CO2-02/FOR, (2006–2009) and CGL-2006-02584/BOS (2006–2009).

Author information

Authors and Affiliations

  1. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Prof. Albareda 1, 18008, Granada, Spain

    Rosario Azcón & José-Miguel Barea

Authors
  1. Rosario Azcón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. José-Miguel Barea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosario Azcón .

Editor information

Editors and Affiliations

  1. Fac. Agricultural Sciences Dept. Agricultural Microbiology, Aligarh Muslim University, 202002, Aligarh, India

    Mohammad Saghir Khan , Javed Musarrat  & Almas Zaidi ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag/Wien

About this chapter

Cite this chapter

Azcón, R., Barea, JM. (2010). Mycorrhizosphere Interactions for Legume Improvement. In: Khan, M.S., Musarrat, J., Zaidi, A. (eds) Microbes for Legume Improvement. Springer, Vienna. https://doi.org/10.1007/978-3-211-99753-6_10

Download citation

Publish with us

Policies and ethics

Search

Navigation