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

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Legume Nitrogen Fixation in Soils with Low Phosphorus Availability

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.

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References

  • 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 8:695–709

    Article  Google Scholar 

  • 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 122:85–94

    Article  Google Scholar 

  • Alizadeh O (2011) Mycorrhizal symbiosis. Adv Stud Biol 3:273–281

    Google Scholar 

  • 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 51:1289–1297

    CAS  PubMed  Google Scholar 

  • Al-Niemi TS, Kahn ML, McDermott TR (1998) Phosphorus uptake by bean nodules. Plant Soil 198:71–78

    Article  CAS  Google Scholar 

  • Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, rhizobia, and legume plants: a review. Agronomy 48:199

    CAS  Google Scholar 

  • 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 38:1234–1242

    Article  CAS  Google Scholar 

  • 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 4:266–277

    Article  Google Scholar 

  • 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 133:273–280

    Article  Google Scholar 

  • 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 121:263–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 128:108–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Bates T, Lynch J (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538

    Article  CAS  Google Scholar 

  • Bieleski R (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252

    Article  CAS  Google Scholar 

  • 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 26:4680–4701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bücking H (2004) Phosphate absorption and efflux of three ectomycorrhizal fungi as affected by external phosphate, cation and carbohydrate concentrations. Mycol Res 108:599–609

    Article  PubMed  Google Scholar 

  • 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 165:899–912

    Article  PubMed  Google Scholar 

  • 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 13:693–698

    Article  CAS  PubMed  Google Scholar 

  • 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 12:1647–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chalot M, Brun A, Finlay RD, Söderström B (1994) Metabolism of [14C] glutamate and [14C] glutamine by the ectomycorrhizal fungus Paxillus involutus. Microbiology 140:1641–1649

    Article  CAS  Google Scholar 

  • 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 24:823–838

    Google Scholar 

  • 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 385–414

    Google Scholar 

  • 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 66:137–146

    Article  PubMed  Google Scholar 

  • Denarie J, Debelle F, Prome J-C (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    Article  CAS  PubMed  Google Scholar 

  • Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489

    Article  CAS  PubMed  Google Scholar 

  • 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 60:215–222

    Article  Google Scholar 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • 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 6:76–87

    Article  CAS  PubMed  Google Scholar 

  • Frey B, Schüepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrinum L.) to maize via vesicular—arbuscular mycorrhizal hyphae. New Phytol 122:447–454

    Article  CAS  Google Scholar 

  • 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 316:1307–1312

    Article  PubMed  Google Scholar 

  • Goss M, De Varennes A (2002) Soil disturbance reduces the efficacy of mycorrhizal associations for early soybean growth and N2 fixation. Soil Biol Biochem 34:1167–1173

    Article  CAS  Google Scholar 

  • Gunawardena S, Danso S, Zapata F (1992) Phosphorus requirements and nitrogen accumulation by three mungbean (Vigna radiata (L) Welzek) cultivars. Plant Soil 147:267–274

    Article  CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  CAS  PubMed  Google Scholar 

  • Jakobsen I, Abbott L, Robson A (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380

    Article  CAS  Google Scholar 

  • 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 94:251–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712

    Article  CAS  Google Scholar 

  • 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 333:880–882

    Article  CAS  PubMed  Google Scholar 

  • 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 105:9823–9828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 64:1967–1981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:408–419

    Article  PubMed  Google Scholar 

  • Long SR (1996) Rhizobium symbiosis: nod factors in perspective. Plant Cell 8:1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:655–662

    Article  Google Scholar 

  • 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 469:58–63

    Article  CAS  PubMed  Google Scholar 

  • Martin F (1985) 15N-NMR studies of nitrogen assimilation and amino acid biosynthesis in the ectomycorrhizal fungus Cenococcum graniforme. FEBS Lett 182:350–354

    Article  CAS  Google Scholar 

  • 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 19:914–923

    Article  CAS  PubMed  Google Scholar 

  • 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 17:1282–1289

    Article  PubMed  Google Scholar 

  • Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11:252–263

    Article  CAS  PubMed  Google Scholar 

  • Oldroyd GE, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  CAS  PubMed  Google Scholar 

  • Olsson PA, van Aarle IM, Allaway WG, Ashford AE, Rouhier H (2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol 130:1162–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peoples MB, Craswell ET (1992) Biological nitrogen fixation: investments, expectations and actual contributions to agriculture. Plant Soil 141:13–39

    Article  CAS  Google Scholar 

  • Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980

    Article  CAS  PubMed  Google Scholar 

  • 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 120:587–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghothama K (1999) Phosphate acquisition. Annu Rev Plant Biol 50:665–693

    Article  CAS  Google Scholar 

  • Ribet J, Drevon JJ (1995) Increase in permeability to oxygen and in oxygen uptake of soybean nodules under limiting phosphorus nutrition. Physiol Plant 94:298–304

    Article  CAS  Google Scholar 

  • 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 29:1651–1658

    Article  CAS  PubMed  Google Scholar 

  • Rogers A, Ainsworth EA, Leakey AD (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 151:1009–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sa T-M, Israel DW (1991) Energy status and functioning of phosphorus-deficient soybean nodules. Plant Physiol 97:928–935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 57:4015–4023

    Article  CAS  PubMed  Google Scholar 

  • Schüßler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936

    Article  PubMed  Google Scholar 

  • 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, Guelph

    Google Scholar 

  • 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 108:7–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (1996) Mycorrhizal symbiosis. Academic Press, London/San Diego

    Google Scholar 

  • 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 145–148

    Google Scholar 

  • 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 42:383–385

    Article  CAS  Google Scholar 

  • 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 187:321–332

    Article  Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, London

    Google Scholar 

  • 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 417:959–962

    Article  CAS  PubMed  Google Scholar 

  • 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 153:1175–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:15–21

    Article  Google Scholar 

  • 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 Raton

    Google Scholar 

  • Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64:781–805

    Article  CAS  PubMed  Google Scholar 

  • Udvardi MK, Tabata S, Parniske M, Stougaard J (2005) Lotus japonicus: legume research in the fast lane. Trends Plant Sci 10:222–228

    Google Scholar 

  • 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 11:296–310

    Article  PubMed  Google Scholar 

  • 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 10:389–399

    Article  PubMed  Google Scholar 

  • 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 15:1

    Google Scholar 

  • Vance C, Heichel G (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Biol 42:373–390

    Article  CAS  Google Scholar 

  • 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 11:933–936

    Google Scholar 

  • 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 79:143–180

    CAS  PubMed  Google Scholar 

  • 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 112:575–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang F, Smith DL (1995) Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol 108:961–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Dr. Lam-Son Phan Tran and Dr. Saad Sulieman for inviting us to write this chapter. This work was supported financially by the Science Foundation of Chinese Academy of Sciences (XDB15030103), the National Natural Science Foundation of China (31370144, 41571255), the National Basic Foundation (2016YFC0501202), the Natural Science Foundation of Jilin Province (20140101017JC) and the 13.5 project of IGA.

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  1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, Jilin Province, 130102, China

    Chunling Chang, Fahad Nasir, Lina Ma & Chunjie Tian

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Chunling Chang

  3. School of Life Sciences, Northeast Normal University, Changchun, Jilin Province, 130024, China

    Fahad Nasir

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  1. Chunling Chang
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  1. Department of Agronomy, Faculty of Agriculture, University of Khartoum, Shambat, Khartoum North, Sudan

    Saad Sulieman

  2. Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science (CSRS), Tsurumi, Yokohama, Japan

    Lam-Son Phan Tran

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Chang, C., Nasir, F., Ma, L., Tian, C. (2017). Molecular Communication and Nutrient Transfer of Arbuscular Mycorrhizal Fungi, Symbiotic Nitrogen-Fixing Bacteria, and Host Plant in Tripartite Symbiosis. In: Sulieman, S., Tran, LS. (eds) Legume Nitrogen Fixation in Soils with Low Phosphorus Availability. Springer, Cham. https://doi.org/10.1007/978-3-319-55729-8_9

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