Molecular Communication and Nutrient Transfer of Arbuscular Mycorrhizal Fungi, Symbiotic Nitrogen-Fixing Bacteria, and Host Plant in Tripartite Symbiosis

  • Chunling Chang
  • Fahad Nasir
  • Lina Ma
  • Chunjie Tian
Chapter

Abstract

Plants colonized by Arbuscular mycorrhizal fungi (AMF) greatly enhance Phosphorus (P) and Nitrogen (N) acquisition, especially by extra radical mycelium. On the other hand, soil bacteria referred to as rhizobia establish a symbiotic relationship with legume plants by making novel root organ known as nodules, which fix atmospheric dinitrogen (N2) and transfer it to the host plant. The symbiotic relationship of both AMF and rhizobia with the same host leguminous plants is termed a “tripartite symbiosis”. This tripartite interaction allows legume plants to grow well in nutrient-deficient soils. Sophisticated and complex molecular communication exists between the AMF, rhizobia and host plant during tripartite symbiosis. In this chapter, we focus on some common features of the molecular dialogue shared during tripartite symbiosis. AMF and the nodulation process of rhizobia requires molecular recognition, regulation and specialized complex signaling molecules. For instance, plants secrets strigolactone (SL), which activates and up-regulates the mycorrhizal factor (myc factor) genes of AMF, which make an association with plant root hairs. SL exudates of plant roots also play a crucial role in rhizobial symbiosis, with SL-biosynthesis mutants of Pisum sativum and Lotus japonicus plants showing reduced nodule number. On the other hand, specific flavonoids molecules secreted by legume plants not only trigger the rhizobial nodulation factor (nod factor) genes responsible for nodule formation, but are also vital for hyphal growth of AMF. Moreover, the small polysaccharides, glycoproteins, and proteins (e.g., chitin-related compounds) responsible for stimulating transcription for enzymes involved in the synthesis of flavonoids are considered to be of fungal origin. Thus, establishment of tripartite symbiosis likely requires coordinated gene regulation synchronized by mutual exchange of diffusible signal molecules to induce the expression of genes involved in activation of a common symbiotic pathway and in colonization by microbial symbionts. Another common feature between AMF and rhizobia is that both benefit from carbohydrates provided by the host plant, which uses these symbionts as a source of energy. Finally, after the exchange of common signaling and the establishment of tripartite symbiotic interactions, the genes responsible for P and N metabolism and translocation are up-regulated, which increases the P and N supply to the host plant, especially in nutrient-scarce conditions, and ultimately increases agricultural productivity. However, to date, our knowledge of the synergistic or antagonism effects of the tripartite symbiosis on different beneficial microbes remains sparse, and requires further investigation in future studies.

Keywords

Tripartite symbiosis Phosphorus Nitrogen Signaling Flavonoids Strigolactone Arbuscular mycorrhizal fungi Rhizobia Legume 

References

  1. Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OC, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Yoo Ra Hs, Zhu Xg (2002) A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield. Glob Chang Biol 8:695–709CrossRefGoogle Scholar
  2. Ainsworth EA, Rogers A, Nelson R, Long SP (2004) Testing the “source–sink” hypothesis of down-regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agric For Meteorol 122:85–94CrossRefGoogle Scholar
  3. Alizadeh O (2011) Mycorrhizal symbiosis. Adv Stud Biol 3:273–281Google Scholar
  4. Almeida JF, Hartwig UA, Frehner M, Nösberger J, Lüscher A (2000) Evidence that P deficiency induces N feedback regulation of symbiotic N2 fixation in white clover (Trifolium repens L.) J Exp Bot 51:1289–1297PubMedGoogle Scholar
  5. Al-Niemi TS, Kahn ML, McDermott TR (1998) Phosphorus uptake by bean nodules. Plant Soil 198:71–78CrossRefGoogle Scholar
  6. Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, rhizobia, and legume plants: a review. Agronomy 48:199Google Scholar
  7. Antunes PM, De Varennes A, Rajcan I, Goss MJ (2006) Accumulation of specific flavonoids in soybean (Glycine max (L.) Merr.) as a function of the early tripartite symbiosis with arbuscular mycorrhizal fungi and Bradyrhizobium japonicum (Kirchner) Jordan. Soil Biol Biochem 38:1234–1242CrossRefGoogle Scholar
  8. Ardakani MR, Pietsch G, Moghaddam A, Raza A, Friedel JK (2009) Response of root properties to tripartite symbiosis between lucerne (Medicago sativa L.), rhizobia and mycorrhiza under dry organic farming conditions. Am J Agric Biol Sci 4:266–277CrossRefGoogle Scholar
  9. Bago B, Vierheilig H, Piché Y, Azcon-Aguilar C (1996) Nitrate depletion and pH changes induced by the extraradical mycelium of the arbuscular mycorrhizal fungus Glomus intraradices grown in monoxenic culture. New Phytol 133:273–280CrossRefGoogle Scholar
  10. Bago B, Pfeffer PE, Douds DD, Brouillette J, Bécard G, Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121:263–272CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124CrossRefPubMedPubMedCentralGoogle Scholar
  12. Barea JM, Azcon R, Azcón-Aguilar C (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-fixing systems. Methods Microbiol 24:391–416CrossRefGoogle Scholar
  13. Bates T, Lynch J (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  14. Bieleski R (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252CrossRefGoogle Scholar
  15. Breakspear A, Liu C, Roy S, Stacey N, Rogers C, Trick M, Morieri G, Mysore KS, Wen J, Oldroyd GE (2014) The root hair “infectome” of Medicago truncatula uncovers changes in cell cycle genes and reveals a requirement for auxin signaling in rhizobial infection. Plant Cell 26:4680–4701CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bücking H (2004) Phosphate absorption and efflux of three ectomycorrhizal fungi as affected by external phosphate, cation and carbohydrate concentrations. Mycol Res 108:599–609CrossRefPubMedGoogle Scholar
  17. Bücking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165:899–912CrossRefPubMedGoogle Scholar
  18. Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant-Microbe Interact 13:693–698CrossRefPubMedGoogle Scholar
  19. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet E-P, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1665CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chalot M, Brun A, Finlay RD, Söderström B (1994) Metabolism of [14C] glutamate and [14C] glutamine by the ectomycorrhizal fungus Paxillus involutus. Microbiology 140:1641–1649CrossRefGoogle Scholar
  21. Chen T, Zhu H, Ke D, Cai K, Wang C, Gou H, Hong Z, Zhang Z (2012) A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus Japonicus. Plant Cell 24:823–838Google Scholar
  22. Day R, Loh J, Cohn J, Stacey G, Triplett E (2000) Signal exchange involved in the establishment of the Bradyrhizobium-legume symbiosis. In: Triplett E (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Norfolk, pp 385–414Google Scholar
  23. De Cuyper C, Fromentin J, Yocgo RE, De Keyser A, Guillotin B, Kunert K, Boyer F-D, Goormachtig S (2015) From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J Exp Bot 66:137–146CrossRefPubMedGoogle Scholar
  24. Denarie J, Debelle F, Prome J-C (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535CrossRefPubMedGoogle Scholar
  25. Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489CrossRefPubMedGoogle Scholar
  26. Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (Myc−) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.) Plant Sci 60:215–222CrossRefGoogle Scholar
  27. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966CrossRefPubMedGoogle Scholar
  28. Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234:1073–1081CrossRefPubMedGoogle Scholar
  29. Foo E, Yoneyama K, Hugill CJ, Quittenden LJ, Reid JB (2013) Strigolactones and the regulation of pea symbioses in response to nitrate and phosphate deficiency. Mol Plant 6:76–87CrossRefPubMedGoogle Scholar
  30. Frey B, Schüepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrinum L.) to maize via vesicular—arbuscular mycorrhizal hyphae. New Phytol 122:447–454CrossRefGoogle Scholar
  31. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre J-C, Jaubert M, Simon D, Cartieaux F, Prin Y (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:1307–1312CrossRefPubMedGoogle Scholar
  32. Goss M, De Varennes A (2002) Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol Biochem 34:1167–1173CrossRefGoogle Scholar
  33. Gunawardena S, Danso S, Zapata F (1992) Phosphorus requirements and nitrogen accumulation by three mungbean (Vigna radiata (L) Welzek) cultivars. Plant Soil 147:267–274CrossRefGoogle Scholar
  34. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299CrossRefPubMedGoogle Scholar
  35. Jakobsen I, Abbott L, Robson A (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380CrossRefGoogle Scholar
  36. Jia Y, Gray VM, Straker CJ (2004) The influence of rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann Bot 94:251–258CrossRefPubMedPubMedCentralGoogle Scholar
  37. Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712CrossRefGoogle Scholar
  38. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882CrossRefPubMedGoogle Scholar
  39. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci 105:9823–9828CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liu J, Novero M, Charnikhova T, Ferrandino A, Schubert A, Ruyter-Spira C, Bonfante P, Lovisolo C, Bouwmeester HJ, Cardinale F (2013) CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus. J Exp Bot 64:1967–1981CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liu Z, Li Y, Ma L, Wei H, Zhang J, He X, Tian C (2015) Coordinated regulation of arbuscular mycorrhizal fungi and soybean mapk pathway genes improved mycorrhizal soybean drought tolerance. Mol Plant-Microbe Interact 28:408–419CrossRefPubMedGoogle Scholar
  42. Long SR (1996) Rhizobium symbiosis: nod factors in perspective. Plant Cell 8:1885CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lüscher A, Hartwig UA, Suter D, Nösberger J (2000) Direct evidence that symbiotic N2 fixation in fertile grassland is an important trait for a strong response of plants to elevated atmospheric CO2. Glob Chang Biol 6:655–662CrossRefGoogle Scholar
  44. Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63CrossRefPubMedGoogle Scholar
  45. Martin F (1985) 15N-NMR studies of nitrogen assimilation and amino acid biosynthesis in the ectomycorrhizal fungus Cenococcum graniforme. FEBS Lett 182:350–354CrossRefGoogle Scholar
  46. Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant-Microbe Interact 19:914–923CrossRefPubMedGoogle Scholar
  47. Nasto MK, Alvarez-Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC (2014) Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17:1282–1289CrossRefPubMedGoogle Scholar
  48. Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263CrossRefPubMedGoogle Scholar
  49. Oldroyd GE, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576CrossRefPubMedGoogle Scholar
  50. Olsson PA, van Aarle IM, Allaway WG, Ashford AE, Rouhier H (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130:1162–1171CrossRefPubMedPubMedCentralGoogle Scholar
  51. Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39CrossRefGoogle Scholar
  52. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980CrossRefPubMedGoogle Scholar
  53. Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–598CrossRefPubMedPubMedCentralGoogle Scholar
  54. Raghothama K (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693CrossRefGoogle Scholar
  55. Ribet J, Drevon JJ (1995) Increase in permeability to oxygen and in oxygen uptake of soybean nodules under limiting phosphorus nutrition. Physiol Plant 94:298–304CrossRefGoogle Scholar
  56. Rogers A, Gibon Y, Stitt M, Morgan PB, Bernacchi CJ, Ort DR, Long SP (2006) Increased C availability at elevated carbon dioxide concentration improves N assimilation in a legume. Plant Cell Environ 29:1651–1658CrossRefPubMedGoogle Scholar
  57. Rogers A, Ainsworth EA, Leakey AD (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sa T-M, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97:928–935CrossRefPubMedPubMedCentralGoogle Scholar
  59. Schaarschmidt S, Roitsch T, Hause B (2006) Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J Exp Bot 57:4015–4023CrossRefPubMedGoogle Scholar
  60. Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936CrossRefPubMedGoogle Scholar
  61. Science, O.A.C.D.o.L.R., Antunes PM (2004) Determination of nutritional and signalling factors involved ij tripartite symbiosis formed by arbuscular mycorrhizal fungi, Bradyrhizobium and soybean. University of Guelph, GuelphGoogle Scholar
  62. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiol 108:7–15CrossRefPubMedPubMedCentralGoogle Scholar
  63. Smith SE, Read DJ (1996) Mycorrhizal symbiosis. Academic Press, London/San DiegoGoogle Scholar
  64. Smith S, Read D (2008) Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. In: Mycorrhizal symbiosis, 3rd edn. Academic Press, London, pp 145–148Google Scholar
  65. Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385CrossRefGoogle Scholar
  66. Soussana J, Hartwig U (1995) The effects of elevated CO2 on symbiotic N2 fixation: a link between the carbon and nitrogen cycles in grassland ecosystems. Plant Soil 187:321–332CrossRefGoogle Scholar
  67. Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, LondonGoogle Scholar
  68. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962CrossRefPubMedGoogle Scholar
  69. Tian C, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y (2010) Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 153:1175–1187CrossRefPubMedPubMedCentralGoogle Scholar
  70. Tobar RM, Azcón-Aguilar C, Sanjuán 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 4:15–21CrossRefGoogle Scholar
  71. Trappe JM (1987) Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC Press, Boca RatonGoogle Scholar
  72. Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805CrossRefPubMedGoogle Scholar
  73. Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10:222–228Google Scholar
  74. Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  75. van der Heijden MG, de Bruin S, Luckerhoff L, van Logtestijn RS, Schlaeppi K (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399CrossRefPubMedGoogle Scholar
  76. van Zeijl A, Liu W, Xiao TT, Kohlen W, Yang W-C, Bisseling T, Geurts R (2015) The strigolactone biosynthesis gene DWARF27 is co-opted in rhizobium symbiosis. BMC Plant Biol 15:1Google Scholar
  77. Vance C, Heichel G (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390CrossRefGoogle Scholar
  78. Wegel E, Schauser L, Sandal N, Stougaard J, Parniske M (1998) Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol Plant-Microbe Interact 11:933–936Google Scholar
  79. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143–180PubMedGoogle Scholar
  80. Zanetti S, Hartwig UA, Luscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nosberger J (1996) Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiol 112:575–583CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zhang F, Smith DL (1995) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol 108:961–968CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Chunling Chang
    • 1
    • 2
  • Fahad Nasir
    • 1
    • 3
  • Lina Ma
    • 1
  • Chunjie Tian
    • 1
  1. 1.Northeast Institute of Geography and Agroecology, Chinese Academy of SciencesChangchunChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.School of Life SciencesNortheast Normal UniversityChangchunChina

Personalised recommendations