Advertisement

Mycorrhizosphere Interactions to Improve a Sustainable Production of Legumes

  • José-Miguel BareaEmail author
  • Rosario Azcón
  • Concepción Azcón-Aguilar
Chapter

Abstract

The sustainability and productivity of agroecosystems depends exquisitely on the functionality of a framework of plant–soil interactions where microbial populations, including both mutualistic symbionts and saprophytic microorganisms, living at the root–soil interfaces, the rhizosphere, are involved. Among various beneficial and consumable plant species, legumes form useful symbiotic relationships with two types of soil microbiota: N2-fixing bacteria, often called rhizobia, and arbuscular mycorrhizal (AM) fungi. Also, the legume rhizosphere inhabits other valuable microbes such as plant growth-promoting rhizobacteria (PGPR). These microorganisms interact intensely among themselves, and with legume roots, to develop the multifunctional legume mycorrhizosphere, a microcosm environment of variable activities, appropriate for legume productivity. This chapter highlights (1) the types of microorganisms and processes involved in the establishment and functioning of the mycorrhizosphere, (2) the impact of the mycorrhizosphere activities on legume production, and (3) the possibilities to tailor an efficient mycorrhizosphere as a biotechnological tool to improve legume performance in different production systems following efficient rhizobial, PGPR, and AM fungal inoculants.

Keywords

Legume productivity Rhizosphere microorganisms Mycorrhizosphere services Microbial inoculants Mycorrhizosphere tailoring 

Notes

Acknowledgments

This research was supported by the Andalusian Research Programme (Project CVI-7640) and the Spanish National Research Programme (R & D)-European Union (Feder) (Project CGL2015-69118-C2-2-P).

References

  1. Achouak W, Haichar FZ (2013) Shaping of microbial community structure and function in the rhizosphere by four diverse plant species. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, NJ, pp 161–167CrossRefGoogle Scholar
  2. Ahmad MH (1995) Compatibility and coselection of vesicular-arbuscular mycorrhizal fungi and rhizobia for tropical legumes. Crit Rev Biotechnol 15:229–239CrossRefGoogle Scholar
  3. 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 41:59–68CrossRefGoogle Scholar
  4. Alguacil MM, Torres MP, Torrecillas E, Díaz G, Roldán A (2011) Plant type differently promote the arbuscular mycorrhizal fungi biodiversity in the rhizosphere after revegetation of a degraded, semiarid land. Soil Biol Biochem 43:167–173CrossRefGoogle Scholar
  5. Altieri MA (2004) Linking ecologists and traditional farmers in the search for sustainable agriculture. Front Ecol Environ 2:35–42CrossRefGoogle Scholar
  6. Antoun H (2012) Beneficial microorganisms for the sustainable use of phosphates in agriculture. Proc Eng 46:62–67CrossRefGoogle Scholar
  7. Arrese-Igor C (2010) Biological nitrogen fixation. In: González-Fontes A, Gárate A, Bonilla I (eds) Agricultural sciences: topics in modern agriculture. Stadium Press, Houston, TX, pp 233–255Google Scholar
  8. Azcón R, Barea JM (2010) Mycorrhizosphere interactions for legume improvement. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement, 1st edn. Springer, New York, pp 237–271CrossRefGoogle Scholar
  9. Azcón R, Barea JM, Hayman DS (1976) Utilization of rock phosphate in alkaline soils by plant inoculated with mycorrhizal fungi and phosphate-solubilizing bacteria. Soil Biol Biochem 8:135–138CrossRefGoogle Scholar
  10. 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 117:399–404CrossRefGoogle Scholar
  11. Azcón R, Medina A, Aroca R, Ruíz-Lozano JM (2013) Abiotic stress remediation by the arbuscular mycorrhizal symbiosis and rhizosphere bacteria/yeast interactions. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Wiley, Hoboken, NJ, pp 991–1002CrossRefGoogle Scholar
  12. Azcón-Aguilar C, Barea JM (2015) Nutrient cycling in the mycorrhizosphere. (In: Gianfreda, L. (Guest Editor) Biogeochemical processes in the rhizosphere and their influence on plant nutrition. Special issue). J Soil Sci Plant Nutr 15:372–396Google Scholar
  13. Azcón-Aguilar C, Azcón R, Barea JM (1979) Endomycorrhizal fungi and Rhizobium as biological fertilizers for Medicago sativa in normal cultivation. Nature 279:325–327CrossRefGoogle Scholar
  14. Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13CrossRefGoogle Scholar
  15. Barea JM (1991) Vesicular-arbuscular mycorrhizae as modifiers of soil fertility. In: Stewart BA (ed) Advances in soil science, vol 7. Springer, New York, pp 1–40Google Scholar
  16. Barea JM (2010) Mycorrhizas and agricultural fertility. In: González-Fontes A, Gárate A, Bonilla I (eds) Agricultural sciences: topics in modern agriculture. Stadium Press, Houston, TX, pp 257–274Google Scholar
  17. Barea JM (2015) Future challenges and perspectives for applying microbial biotechnology in sustainable agriculture based on a better understanding of plant-microbiome interactions. (In: Gianfreda, L. (Guest Editor) Biogeochemical processes in the rhizosphere and their influence on plant nutrition. Special issue). J Soil Sci Plant Nutr 15:261–282Google Scholar
  18. 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 1–54Google Scholar
  19. Barea JM, Azcón-Aguilar C (2013) Evolution, biology and ecological effects of arbuscular mycorrhiza. In: Camisao AF, Pedroso CC (eds) Symbiosis: evolution biology and ecological effects. Nova Science, New York, pp 1–34Google Scholar
  20. Barea JM, Richardson AE (2015) Phosphate mobilisation by soil microorganisms. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 225–234Google Scholar
  21. 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 106:717–725CrossRefGoogle Scholar
  22. Barea JM, Azcón R, Azcón-Aguilar C (1989a) 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 112:399–404CrossRefGoogle Scholar
  23. Barea JM, El-Atrach F, Azcón R (1989b) Mycorrhiza and phosphate interactions as affecting plant development, N2 fixation, N-transfer and N-uptake from soil in legume grass mixtures by using a N15 dilution technique. Soil Biol Biochem 21:581–589CrossRefGoogle Scholar
  24. Barea JM, Toro M, Orozco MO, Campos E, Azcón R (2002) 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 63:35–42CrossRefGoogle Scholar
  25. 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, Developments in plant and soil sciences. Springer, Dordrecht, pp 223–227CrossRefGoogle Scholar
  26. Barea JM, Palenzuela J, Cornejo P, Sánchez-Castro I, Navarro-Fernández C, Lopéz-García A, Estrada B, Azcón R, Ferrol N, Azcón-Aguilar C (2011) Ecological and functional roles of mycorrhizas in semi-arid ecosystems of Southeast Spain. J Arid Environ 75:1292–1301CrossRefGoogle Scholar
  27. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2013a) Microbial interactions in the rhizosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley, Hoboken, NJ, pp 29–44CrossRefGoogle Scholar
  28. Barret M, Tan H, Egan F, Morrissey JP, Reen J, O'Gara F (2013) Exploiting new systems-based strategies to elucidate plant–bacterial interactions in the rhizosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, NJ, pp 57–68CrossRefGoogle Scholar
  29. Bashan Y, Trejo A, de Bashan LE (2011) Development of two culture media for mass cultivation of Azospirillum spp. and for production of inoculants to enhance plant growth. Biol Fertil Soils 47:963–969CrossRefGoogle Scholar
  30. Bashan Y, de Bashan LE, Prabhu SR, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant Soil 378:1–33CrossRefGoogle Scholar
  31. Bonfante P, Desirò A (2015) Arbuscular mycorrhizas: the lives of beneficial fungi and their plant host. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 235–245Google Scholar
  32. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48PubMedCrossRefGoogle Scholar
  33. Borriss R (2015) Towards a new generation of commercial microbial disease control and plant growth promotion products. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 329–337Google Scholar
  34. Brearley FQ, Elliott DR, Iribar A, Sen R (2016) Arbuscular mycorrhizal community structure on co-existing tropical legume trees in French Guiana. Plant Soil 403:253–265CrossRefGoogle Scholar
  35. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  36. Chalk PM, Souza RD, Urquiaga S, Alves BJR, Boddey RM (2006) The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biol Biochem 38:2944–2951CrossRefGoogle Scholar
  37. Courty PE, Smith P, Koegel S, Redecker D, Wipf D (2015) Inorganic nitrogen uptake and transport in beneficial plant root-microbe interactions. Crit Rev Plant Sci 34:4–16CrossRefGoogle Scholar
  38. Danso SKA (1986) Review, estimation of N2 fixation by isotope dilution: an appraisal of techniques involving 15N enrichment and their application. Soil Biol Biochem 18:243–244CrossRefGoogle Scholar
  39. de Bruijn FJ (2015) Biological nitrogen fixation. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 215–224Google Scholar
  40. Delaux P-M, Sejalon-Delmas N, Becard G, Ane J-M (2013) Evolution of the plant-microbe symbiotic ‘toolkit’. Trends Plant Sci 18:298–304PubMedCrossRefGoogle Scholar
  41. Delaux P-M, Radhakrishnan GV, Jayaraman D et al (2015) Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci U S A 112:13390–13395PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-González C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879Google Scholar
  43. Drumbell AJ (2013) Arbuscular mycorrhizal fungi throughout the year: using massively parallel pyrosequencing to quantify spatiotemporal seasonal dynamics. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Wiley, Hoboken, NJ, pp 1113–1122Google Scholar
  44. Fernández-Bidondo L, Silvani V, Colombo R, Pérgola M, Bompadre J, Godeas A (2011) Pre-symbiotic and symbiotic interactions between Glomus intraradices and two Paenibacillus species isolated from AM propagules. In vitro and in vivo assays with soybean (AG043RG) as plant host. Soil Biol Biochem 43:1866–1872CrossRefGoogle Scholar
  45. Field KJ, Pressel S, Duckett JG, Rimington WR, Bidartondo MI (2015) Symbiotic options for the conquest of land. Trends Ecol Evol 30:477–486PubMedCrossRefGoogle Scholar
  46. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36PubMedCrossRefGoogle Scholar
  47. Genre A, Bonfante P (2010) The making of symbiotic cells in arbuscular mycorrhizal roots. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer, Dordrecht, pp 57–71CrossRefGoogle Scholar
  48. Genre A, Chabaud M, Balzergue C, Puech-Pages V, Novero M, Rey T, Fournier J, Rochange S, Becard G, Bonfante P, Barker DG (2013) Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:179–189PubMedCrossRefGoogle Scholar
  49. George TS, Hinsinger P, Turner BL (2016) Phosphorus in soils and plants—facing phosphorus scarcity. Plant Soil 401:1–6CrossRefGoogle Scholar
  50. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefGoogle Scholar
  51. Gianinazzi-Pearson V, van Tuinen D, Wipf D, Dumas-Gaudot E, Recorbet G, Lyu Y, Doidy J, Redecker D, Ferrol N (2012) Exploring the genome of Glomeromycotan fungi. In: Hock B (ed) The Mycota, a comprehensive treatise on fungi as experimental systems for basic and applied research. Springer, Berlin, pp 1–21Google Scholar
  52. Gutiérrez-Mañero J, Ramos-Solano B (2010) Bacteria and agriculture. In: González-Fontes A, Gárate A, Bonilla I (eds) Agricultural sciences: topics in modern agriculture. Stadium Press, Houston, TX, pp 275–289Google Scholar
  53. Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. In: Schekman R (ed) Annual review of cell and developmental biology, vol 29, pp 593–617Google Scholar
  54. Ha Y, Gray VM (2008) Growth yield of Vicia faba L in response to microbial symbiotic associations. S Afr J Bot 74:25–32CrossRefGoogle Scholar
  55. Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25PubMedCrossRefGoogle Scholar
  56. 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 59:129–133PubMedPubMedCentralGoogle Scholar
  57. Hidri R, Barea JM, Metoui-Ben Mahmoud O, Abdellya C, Azcón R (2016) Impact of microbial inoculations on biomass accumulation by Sulla carnosa provenances, and in regulating nutrition, physiological and antioxidant activities of this species under non-saline and saline conditions. J Plant Physiol 201:28–41PubMedCrossRefGoogle Scholar
  58. Hirsch PR, Mauchline TH, Clark IM (2013a) Culture-independent molecular approaches to microbial ecology in soil and the rhizosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, NJ, pp 45–55CrossRefGoogle Scholar
  59. Hirsch PR, Miller AJ, Dennis PG (2013b) Do root exudates exert more influence on rhizosphere bacterial community structure than other rhizodeposits? In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, NJ, pp 229–242CrossRefGoogle Scholar
  60. Honrubia M (2009) The Mycorrhizae: a plant-fungus relation that has existed for more than 400 million years. Anal Jardin Bot Madrid 66:133–144CrossRefGoogle Scholar
  61. Ijdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16PubMedCrossRefGoogle Scholar
  62. Kamilova F, Okon Y, de Weert S, Hora K (2015) Commercialization of microbes: manufacturing, inoculation, best practice for objective field testing, and registration. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 319–327Google Scholar
  63. Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW (2010) Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biol Biochem 42:125–127CrossRefGoogle Scholar
  64. Khan M, Zaidi A, Ahemad M, Oves M, Wani P (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56:73–98CrossRefGoogle Scholar
  65. Kloepper JW (1994) Plant growth-promoting rhizobacteria (other systems). In: Okon Y (ed) Azospirillum/plant associations. CRC, Boca Raton, FL, pp 111–118Google Scholar
  66. 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, Dordrecht, pp 315–326Google Scholar
  67. König S, Wubet T, Dormann CF, Hempel S, Renker C, Buscot F (2010) Taqman real-time PCR assays to assess arbuscular mycorrhizal responses to field manipulation of grassland biodiversity: effects of soil characteristics, plant species richness, and functional traits. Appl Environ Microbiol 76:3765–3775PubMedPubMedCentralCrossRefGoogle Scholar
  68. Krüger M, Walker C, Schüßer A (2011) Acaulospora brasiliensis comb. Nov. and Acaulospora alpina (Glomeromycota) from upland Scotland: morphology, molecular phylogeny and DNA-based detection in roots. Mycorrhiza 21:577–587PubMedCrossRefGoogle Scholar
  69. Lagunas B, Schaefer P, Gifford ML (2015) Housing helpful invaders: the evolutionary and molecular architecture underlying plant root-mutualist microbe interactions. J Exp Bot 66:2177–2186PubMedPubMedCentralCrossRefGoogle Scholar
  70. Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95:1045–1054PubMedCrossRefGoogle Scholar
  71. 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. Agric Syst 73:37–45CrossRefGoogle Scholar
  72. Lin K, Limpens E, Zhang Z et al (2014) Single nucleous genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10:e1004078PubMedPubMedCentralCrossRefGoogle Scholar
  73. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora. The mycorrhizosphere effects. Phytopathology 78:366–371Google Scholar
  74. López-Ráez JA, Pozo MJ, García-Garrido JM (2011) Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522CrossRefGoogle Scholar
  75. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25PubMedCrossRefGoogle Scholar
  76. Lugtenberg B (2015) Life of microbes in the rhizosphere. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 7–15Google Scholar
  77. Lugtenberg BJJ, Malfanova N, Kamilova F, Berg G (2013a) Microbial control of plant root diseases. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2. Wiley Blackwell, Hoboken, NJ, pp 575–586CrossRefGoogle Scholar
  78. Lugtenberg BJJ, Malfanova N, Kamilova F, Berg G (2013b) Plant growth promotion by microbes. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2. Wiley Blackwell, Hoboken, NJ, pp 561–573Google Scholar
  79. Lumini E, Orgiazzi A, Borriello R, Bonfante P, Bianciotto V (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179PubMedGoogle Scholar
  80. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martínez EA, Driguez H, Bécard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–64PubMedCrossRefGoogle Scholar
  81. Martínez-García LB, Armas C, Padilla FM, Miranda JD, Pugnaire FI (2011) Shrubs influence arbuscular mycorrhizal fungi communities in a semiarid environment. Soil Biol Biochem 43:682–689CrossRefGoogle Scholar
  82. Martinez-Viveros O, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319CrossRefGoogle Scholar
  83. 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 Yarrowia lipolytica. Chemosphere 56:449–456PubMedCrossRefGoogle Scholar
  84. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100PubMedCrossRefGoogle Scholar
  85. Mercado-Blanco J (2015) Life of microbes inside the plant. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Springer International, Heidelberg, pp 25–32Google Scholar
  86. 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 40:1019–1027CrossRefGoogle Scholar
  87. Muleta D (2010) Legume responses to arbuscular mycorrhizal fungi inoculation in sustainable agriculture. In: Khan MS, Musarrat J, Zaidi A (eds) Microbes for legume improvement, 1st edn. Springer, Vienna, pp 293–323CrossRefGoogle Scholar
  88. Oehl F, Sieverding E, Palenzuela J, Ineichen K, da Silva GA (2011a) Advances in Glomeromycota taxonomy and classification. IMA Fungus 2:191–199PubMedPubMedCentralCrossRefGoogle Scholar
  89. Oehl F, da Silva GA, Sánchez-Castro I, Goto BT, Maia LC, Evangelista Vieira HE, Barea JM, Sieverding E, Palenzuela J (2011b) Revision of Glomeromycetes with entrophosporoid and glomoid spore formation with three new genera. Mycotaxon 117:297–316CrossRefGoogle Scholar
  90. Olivares J, Bedmar EJ, Sanjuan J (2013) Biological nitrogen fixation in the context of global change. Mol Plant Microb Interact 26:486–494CrossRefGoogle Scholar
  91. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME, Liira J, Metsis M, Neshataeva V, Paal J, Phosri C, Polme S, Reier U, Saks U, Schimann H, Thiery O, Vasar M, Moora M (2013) Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23:411–430PubMedCrossRefGoogle Scholar
  92. Ordoñez YM, Fernández BR, Lara LS, Rodríguez A, Uribe-Vélez D, Sanders IR (2016) Bacteria with phosphate solubilizing capacity alter mycorrhizal fungal growth both inside and outside the root and in the presence of native microbial communities. PLoS One 11:e0154438PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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. Agric Syst 74:231–242CrossRefGoogle Scholar
  94. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefGoogle Scholar
  95. Patil CR, Alagawady AR (2010) Microbial inoculants for sustainable legume production. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement, 1st edn. Springer, New York, pp 515–535CrossRefGoogle Scholar
  96. Pellegrino E, Turrini A, Gamper HA, Cafa G, Bonari E, Young JPW, Giovannetti M (2012) Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:810–822PubMedCrossRefGoogle Scholar
  97. Pérez-Tienda J, Correa A, Azcón-Aguilar C, Ferrol N (2014) Transcriptional regulation of host NH4 + transporters and GS/GOGAT pathway in arbuscular mycorrhizal rice roots. Plant Physiol Biochem 75:1–8PubMedCrossRefGoogle Scholar
  98. Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375PubMedCrossRefGoogle Scholar
  99. Pozo MJ, Jung SC, Martínez-Medina A, López-Ráez JA, Azcón-Aguilar C, Barea JM (2013) Root allies: arbuscular mycorrhizal fungi help plants to cope with biotic stresses. In: Aroca R (ed) Symbiotic endophytes. Springer, Berlin, pp 289–307CrossRefGoogle Scholar
  100. Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436PubMedCrossRefGoogle Scholar
  101. Raaijmakers JM, Lugtenberg BJJ (2013) Perspectives for rhizosphere research. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2. Wiley Blackwell, Hoboken, NJ, pp 1227–1232CrossRefGoogle Scholar
  102. Ramos-Solano B, Barriuso Maicas J, Pereyra de la Iglesia MT, Domenech J, Gutiérrez Mañero FJ (2008) Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors. Phytopathology 98:451–457PubMedCrossRefGoogle Scholar
  103. Ramos-Solano B, Barriuso J, Gutiérrez Mañero J (2009) Biotechnology of the rhizosphere. In: Kirakosyan A, Kaufman P (eds) Recent advances in plant biotechnology. Springer, New York, pp 137–162CrossRefGoogle Scholar
  104. Ravensberg WJ (2015) Commercialisation of microbes: present situation and future prospects. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 309–317Google Scholar
  105. Redecker D, Schuessler A, Stockinger H, Stuermer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23:515–531PubMedCrossRefGoogle Scholar
  106. 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 67:495–498PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 321:305–339CrossRefGoogle Scholar
  108. Robinson-Boyer L, Grzyb I, Jeffries P (2009) Shifting the balance from qualitative to quantitative analysis of arbuscular mycorrhizal communities in field soils. Fungal Ecol 2:1–9CrossRefGoogle Scholar
  109. Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, De Pascale S, Bonini P, Colla G (2015) Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Sci Hortic 196:91–108CrossRefGoogle Scholar
  110. Sánchez-Romera B, Ruiz-Lozano JM, Zamarreno AM, Garcia-Mina JM, Aroca R (2016) Arbuscular mycorrhizal symbiosis and methyl jasmonate avoid the inhibition of root hydraulic conductivity caused by drought. Mycorrhiza 26:111–122PubMedCrossRefGoogle Scholar
  111. Savka MA, Dessaux Y, McSpadden Gardener BB, Mondy S, Kohler PRA, de Bruijn FJ, Rossbach S (2013) The “biased rhizosphere” concept and advances in the omics era to study bacterial competitiveness and persistence in the phytosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2. Wiley Blackwell, Hoboken, NJ, pp 1147–1161Google Scholar
  112. Schreiter S, Eltlbany N, Smalla K (2015) Microbial communities in the rhizosphere analyzed by cultivation-independent DNA-based methods. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Microbes for sustainable agriculture. Springer International, Heidelberg, pp 289–298Google Scholar
  113. Schüßler A, Walker C (2011) Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In: Pöggeler S, Wöstemeyer J (eds) Evolution of fungi and fungal-like organisms. Springer, Berlin, pp 163–185CrossRefGoogle Scholar
  114. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota, phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  115. Selosse M-A, Strullu-Derrien C, Martin FM, Kamoun S, Kenrick P (2015) Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere. New Phytol 206:501–506PubMedCrossRefGoogle Scholar
  116. Shtark O, Provorov N, Mikić A, Borisov A, Ćupina B, Tikhonovich I (2011) Legume root symbioses: natural history and prospects for improvement. Field Veg Crop Res 48:291–304Google Scholar
  117. Shtark OY, Borisov AY, Zhukov VA, Tikhonovich IA (2012) Mutually beneficial legume symbioses with soil microbes and their potential for plant production. Symbiosis 58:51–62CrossRefGoogle Scholar
  118. Shtark O, Kumari S, Singh R, Sulima A, Akhtemova G, Zhukov V, Shcherbakov A, Shcherbakova E, Adholeya A, Borisov A (2015a) Advances and prospects for development of multi-component microbial inoculant for legumes. Legum Perspect 8:40–44Google Scholar
  119. Shtark O, Zhukov V, Sulima A, Singh R, Naumkina T, Akhtemova G, AY B (2015b) Prospects for the use of multi-component symbiotic systems of the legumes. Ecol Genet 13:33–46CrossRefGoogle Scholar
  120. Singh S, Srivastava K, Sharma S, Sharma AK (2014) Mycorrhizal inoculum production. In: Solaiman ZM, Abbott LK, Varma A (eds) Mycorrhizal fungi: use in sustainable agriculture and land restoration, Soil biology, vol 41. Springer, Berlin, pp 67–80Google Scholar
  121. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier, Academic, New YorkGoogle Scholar
  122. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250PubMedCrossRefGoogle Scholar
  123. Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13PubMedCrossRefGoogle Scholar
  124. Spence C, Bais H (2013) Probiotics for plants: rhizospheric microbiome and plant fitness. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 2. Wiley Blackwell, Hoboken, NJ, pp 713–721CrossRefGoogle Scholar
  125. Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S, Morris RJ, Ane J-M, Denarie J, Oldroyd GED (2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27:823–838PubMedPubMedCentralCrossRefGoogle Scholar
  126. Tamayo E, Gómez-Gallego T, Azcón-Aguilar C, Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:547PubMedPubMedCentralCrossRefGoogle Scholar
  127. Tisserant E, Malbreil M, Kuo A, Kohler A et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110:20117–20122PubMedPubMedCentralCrossRefGoogle Scholar
  128. 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 138:265–273CrossRefGoogle Scholar
  129. 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 90:168–172Google Scholar
  130. van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423PubMedCrossRefGoogle Scholar
  131. Varela-Cervero S, Vasar M, Davison J, Barea JM, Opik M, Azcon-Aguilar C (2015) The composition of arbuscular mycorrhizal fungal communities differs among the roots, spores and extraradical mycelia associated with five Mediterranean plant species. Environ Microbiol 17:2882–2895PubMedCrossRefGoogle Scholar
  132. Varela-Cervero S, López-García A, Barea JM, Azcón-Aguilar C (2016) Spring to autumn changes in the arbuscular mycorrhizal fungal community composition in the different propagule types associated to a Mediterranean shrubland. Plant Soil 403:1–14CrossRefGoogle Scholar
  133. Verbruggen E, van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109PubMedCrossRefGoogle Scholar
  134. 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, Berlin, pp 419–438CrossRefGoogle Scholar
  135. Zaidi A, Khan MS (2007) Stimulatory effects of dual inoculation with phosphate solubilising microorganisms and arbuscular mycorrhizal fungus on chickpea. Aust J Exp Agric 47:1016–1022CrossRefGoogle Scholar
  136. Zaidi A, Khan MS, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Inmunol Hung 56:263–284CrossRefGoogle Scholar
  137. Zaidi A, Ahemad M, Oves M, Ahmad E, Khan MS (2010) Role of phosphate-solubilizing bacteria in legume improvement. In: Khan MS, Musarrat J, Zaidi A (eds) Microbes for legume improvement, 1st edn. Springer, Vienna, pp 273–292CrossRefGoogle Scholar
  138. Zancarini A, Lépinay C, Burstin J, Duc G, Lemanceau P, Moreau D, Munier-Jolain N, Pivato B, Rigaud T, Salon C, Mougel C (2013) Combining molecular microbial ecology with ecophysiology and plant genetics for a better understanding of plant-microbial communities’ interactions in the rhizosphere. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere, vol 1. Wiley Blackwell, Hoboken, NJ, pp 69–86CrossRefGoogle Scholar
  139. Zapata F (1990) Isotope techniques in soil fertility and plant nutrition studies. In: Hardarson G (ed) Use of nuclear techniques in studies of soil-plant relationships. IAEA, Vienna, pp 61–128Google Scholar
  140. Zapata F, Danso SKA, Hardanson G, Fried M (1987) Nitrogen-fixation and translocation in field grown fababean. Agron J 79:505–509CrossRefGoogle Scholar
  141. Zhukov VA, Shtark OY, Borisov AY, Tikhonovich IA (2013) Breeding to improve symbiotic effectiveness of legumes. In: Andersen SB (ed) Plant breeding from laboratories to fields. InTech, Rijeka, Croatia. doi: 10.5772/53003 Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • José-Miguel Barea
    • 1
    Email author
  • Rosario Azcón
    • 1
  • Concepción Azcón-Aguilar
    • 1
  1. 1.Departamento de Microbiología del Suelo y Sistemas SimbióticosEstación, Experimental del ZaidínGranadaSpain

Personalised recommendations