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Dynamics of Arbuscular Mycorrhizal Symbiosis and Its Role in Nutrient Acquisition: An Overview

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Mycorrhiza - Nutrient Uptake, Biocontrol, Ecorestoration

Abstract

Arbuscular mycorrhiza constitute a heterogeneous group of diverse fungal taxa that have been reported to form mutualistic interaction with the roots of more than 90% of all plant species. Accomplishment of this symbiotic interaction requires a high degree of synchronization between the two partners and is based on a finely regulated molecular dialogue. Where plant roots exude strigolactones that stimulate fungal metabolism and branching, fungus releases signaling molecules—myc factors that trigger symbiotic responses in the host plant. Among the various benefits bestowed by this symbiotic association, transport of limiting soil nutrients including phosphorus (P), nitrogen (N), sulphur (S) in exchange for fixed carbon is considered as the key feature which occurs in arbuscule containing host cortical cells. In the last few years, novel transporters involved in this mutualistic interaction have been unravelled. This chapter briefly summarizes the signaling pathways and nutrient exchange involved in the establishment of an effective symbiosis between the host plant and fungus that could provide better insight into the role of mycorrhizal fungi in sustainable agriculture.

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References

  • Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot (Lond) 97:925–931

    CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    CAS  PubMed  Google Scholar 

  • Allen JW, Shachar-Hill Y (2009) Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol 149:549–560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Antolın-Llovera M, Ried MK, Binder A, Parniske M (2012) Receptor kinase signaling pathways in plant-microbe interactions. Annu Rev Phytopathol 50:451–473

    PubMed  Google Scholar 

  • Aono T, Maldonado-Mendoza IE, Dewbre GR, Harrison MJ, Saito M (2004) Expression of alkaline phosphatase genes in arbuscular mycorrhizas. New Phytol 162:525–534

    CAS  Google Scholar 

  • Aroca R, Ruiz-Lozano JM, Zamarreňo AM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170:47–55

    CAS  PubMed  Google Scholar 

  • Azcón R, Barea JM (2010) Mycorrhizosphere interactions for legume improvement. In: Khan MS, Zaidi A, Musarrat J (eds) Microbes for legume improvement. Springer, Vienna, pp 237–271

    Google Scholar 

  • Bago B, Vierheilig H, Piché Y, Azcón-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

    CAS  PubMed  Google Scholar 

  • Bago B, Pfeffer P, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bago B, Pfeffer PE, Abubaker J, Allen JW, Brouillette J, Douds DD, Lammers PL, Shacher-Hill Y (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Am Soc Plant Biol 131:1496–1507

    CAS  Google Scholar 

  • Bakshi M, Sherameti I, Meichsner D, Thürich J, Varma A, Johri AK, Yeh K-W, Oelmüller R (2017) Piriformospora indica reprograms gene expression in Arabidopsis phosphate metabolism mutants but does not compensate for phosphate limitation. Front Microbiol 8:1262. https://doi.org/10.3389/fmicb.2017.01262

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Barea JM (2010) Mycorrhizas and agricultural fertility. In: González-Fontes A, Gárate A, Bonilla I (eds) Agricultural Sciences: topics in modern agriculture. Studium, Houston, TX, pp 257–274

    Google Scholar 

  • Barea JM, Azcón R, Azcón-Aguilar C (2005) 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, Berlin, pp 195–212

    Google Scholar 

  • Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2013) Microbial interactions in the rhizosphere. In: de Bruijn F (ed) Molecular microbial ecology of the rhizosphere. Wiley-Blackwell, Hoboken, NJ, pp 29–44

    Google Scholar 

  • Barea JM, Pozo MJ, López-Ráez JA, Aroca R, Ruíz-Lozano JM, Ferrol N, Azcón R, Azcón-Aguilar C (2014) Arbuscular mycorrhizas and their significance in promoting soil-plant system sustainability against environmental stresses. In: Rodelas MB, González-López J (eds) Beneficial plant-microbial interactions ecology and applications. CRC, Taylor & Francis, Boca Raton, FL, pp 353–387

    Google Scholar 

  • Behie SW, Bidochka MJ (2014) Nutrient transfer in plant—fungal symbioses. Trends Plant Sci 19:734–740

    CAS  PubMed  Google Scholar 

  • Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577

    CAS  PubMed  Google Scholar 

  • Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627

    CAS  PubMed  Google Scholar 

  • Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559. https://doi.org/10.3389/fmicb.2015.01559

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • 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. Springer, Cham, pp 235–245

    Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Comm 1:48. https://doi.org/10.1038/ncomms1046

    Article  CAS  Google Scholar 

  • Bonfante P, Balestrini R, Mendgen K (1994) Storage and secretion processes in the spore of Gigaspora margarita Becker & Hall as revealed by high-pressure freezing and freeze substitution. New Phytol 128:93–101

    PubMed  Google Scholar 

  • Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter 4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 27:352–1366

    Google Scholar 

  • Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26

    CAS  PubMed  Google Scholar 

  • Bücking H, Kafle A (2015) Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: current knowledge and research gaps. Agronomy 5:587–612

    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

    PubMed  Google Scholar 

  • Bücking H, Liepold E, Ambilwade P (2012) The role of the mycorrhizal symbiosis in nutrient uptake of plants and the regulatory mechanisms underlying these transport processes. In: Dhal NK, Sahu SC (eds) Plant science. Intech, Rijeka, pp 107–539

    Google Scholar 

  • Cameron DD (2010) Arbuscular mycorrhizal fungi as (agro) ecosystem engineers. Plant Soil 333:1–5

    CAS  Google Scholar 

  • Carbonnel S, Gutjahr C (2014) Control of arbuscular mycorrhiza development by nutrient signals. Front Plant Sci 5(462). https://doi.org/10.3389/fpls.2014.00462

  • Casieri L, Gallardo K, Wipf D (2012) Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235:1431–1447

    CAS  PubMed  Google Scholar 

  • Cimen I, Pirinc V, Doran I, Turgay B (2010) Effect of soil solarization and arbuscular mycorrhizal fungus (Glomus intraradices) on yield and blossom-end rot of tomato. Int J Agric Biol 12:551–555

    Google Scholar 

  • Corrêa A, Cruz C, Ferrol N (2015) Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza 25:499–515

    PubMed  Google Scholar 

  • Drew EA, Murray RS, Smith SE, Jakobsen I (2003) Beyond the rhizosphere: growth and function of arbuscular mycorrhizal external hyphae in sands of varying pore sizes. Plant Soil 251:105–114

    CAS  Google Scholar 

  • Eriksen J, Askegaard M (2000) Sulphate leaching in an organic crop rotation on sandy soil in Denmark. Agric Ecosyst Environ 78:107–114

    CAS  Google Scholar 

  • Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, Bucking H (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656

    CAS  PubMed  Google Scholar 

  • Ferrol N, Barea JM, Azcón-Aguilar C (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37:112–118

    CAS  PubMed  Google Scholar 

  • Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol 124:221–230

    PubMed  Google Scholar 

  • Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599

    CAS  Google Scholar 

  • Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69:510–528

    CAS  PubMed  Google Scholar 

  • Genre A (2012) Signalling and the re-structuring of plant cell architecture in am symbiosis. In: Perotto S, Baluška F (eds) Signaling and communication in plant symbiosis, Signaling and communication in plants, vol 11. Springer, Berlin, pp 51–71

    Google Scholar 

  • 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 57–71

    Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard 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 198:190–202

    PubMed  Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Strani P (2004) Patterns of below-ground plant interconnections established by means of arbuscular mycorrhizal networks. New Phytol 164:175–181

    PubMed  Google Scholar 

  • Giovannetti M, Tolosano M, Volpe V, Kopriva S, Bonfante P (2014) Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol 204:609–619

    CAS  PubMed  Google Scholar 

  • Goltapeh EM, Danesh YR, Prasad R, Varma A (2008) Mycorrhizal fungi: what we know and what should we know? In: Varma A (ed) Mycorrhiza. Springer, Berlin, pp 3–27

    Google Scholar 

  • Gómez-Roldán V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    PubMed  Google Scholar 

  • Grønlund M, Albrechtsen M, Johansen IE, Hammer E, Nielsen TH, Jakobsen I (2013) The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant 149:234–248

    PubMed  Google Scholar 

  • Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 150:73–83

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutjahr C (2014) Phytohormone signaling in arbuscular mycorrhiza development. Curr Opin Plant Biol 20:26–34

    CAS  PubMed  Google Scholar 

  • Gutjahr C, Parniske M (2013) Cell and developmental biology of the arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 29:593–617

    CAS  PubMed  Google Scholar 

  • Gutjahr C, Casieri L, Paszkowski U (2009) Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol 182:829–837

    PubMed  Google Scholar 

  • Hamel C (2004) Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Can J Soil Sci 84:383–395

    CAS  Google Scholar 

  • Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for Tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76:236–244

    CAS  PubMed  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    CAS  PubMed  Google Scholar 

  • Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    CAS  PubMed  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110

    CAS  PubMed  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    CAS  Google Scholar 

  • He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

    Google Scholar 

  • Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Jakobsen I, Hammer EC (2015) Nutrient dynamics in arbuscular mycorrhizal networks. In: Horton TR (ed) Mycorrhizal networks, ecological studies, vol 224. Springer, Dordrecht, pp 91–131

    Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007a) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725

    CAS  PubMed  PubMed Central  Google Scholar 

  • Javot H, Pumplin N, Harrison M (2007b) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    CAS  PubMed  Google Scholar 

  • Javot H, Penmetsa RV, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965

    CAS  PubMed  Google Scholar 

  • Jeffries P, Barea JM (2012) Arbuscular mycorrhiza—a key component of sustainable plant-soil ecosystems. In: Hock B (ed) The mycota. Springer, Berlin, pp 51–75

    Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1993) Hyphal transport by vesicular-arbuscular mycorrhizal fungus on N applied to the soil as ammonium or nitrate. Biol Fert Soils 16:66–70

    CAS  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    CAS  PubMed  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    CAS  PubMed  Google Scholar 

  • Koegel S, Ait Lahmidi N, Arnould C, Chatagnier O, Walder F, Ineichen K, Boller T, Wipf D, Wiemken A, Courty PE (2013) The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol 198:853–865

    CAS  PubMed  Google Scholar 

  • Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P, Haider I, Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ, López-Ráez JA (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE 8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547

    CAS  PubMed  Google Scholar 

  • Koltai H, Kapulnik Y (2009) Effect of arbuscular mycorrhizal symbiosis on enhancement of tolerance to abiotic stresses. In: White JF, Torres MS (eds) Defensive mutualism in microbial symbiosis. CRC, Taylor & Francis, Boca Raton, FL, pp 217–234

    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 USA 105:9823–9828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kranabetter JM (2014) Ectomycorrhizal fungi and the nitrogen economy of conifers—implications for genecology and climate change mitigation. Botany 92:417–423

    Google Scholar 

  • Kumar A, Dames JF, Gupta A, Sharma S, Gilbert JA, Ahmad P (2015) Current developments in arbuscular mycorrhizal fungi research and its role in salinity stress alleviation: a biotechnological perspective. Crit Crit Rev Biotechnol 35:461–474

    PubMed  Google Scholar 

  • Lammers PJ, Jun J, Abubaker J, Arreola R, Gopalan A, Bago B, Hernandez-Sebastia C, Allen JW, Douds DD, Pfeffer PE, Shachar-Hill Y (2001) The glyoxylate cycle in an arbuscular mycorrhizal fungus. Carbon flux and gene expression. Plant Physiol 127:1287–1298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lanfranco L, Vallino M, Bonfante P (1999) Expression of chitin synthase genes in the arbuscular mycorrhizal fungus Gigaspora margarita. New Phytol 142:347–354

    CAS  Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops—a meta-analysis. Soil Biol Biochem 81:147–158

    CAS  Google Scholar 

  • Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants—a meta-analysis. Soil Biol Biochem 69:123–131

    CAS  Google Scholar 

  • Leigh EG (2010) The evolution of mutualism. J Evol Biol 23:2507–2528

    PubMed  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

    CAS  PubMed  Google Scholar 

  • López-Pedrosa A, González-Guerrero M, Valderas A, Azcón-Aguilar C, Ferrol N (2006) GintAmt1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol 43:102–110

    PubMed  Google Scholar 

  • López-Ráez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243:1375–1385

    PubMed  Google Scholar 

  • López-Ráez JA, Pozo MJ (2013) Chemical signalling in the arbuscular mycorrhizal symbiosis: biotechnological applications. In: Aroca R (ed) Symbiotic endophytes, Soil biology, vol 37. Springer, Berlin, pp 215–232

    Google Scholar 

  • López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601

    PubMed  PubMed Central  Google Scholar 

  • López-Ráez JA, Bouwmeester H, Pozo MJ (2012) Communication in the rhizosphere, a target for pest management. In: Lichtfouse E (ed) Agroecology and strategies for climate change, Sustainable agriculture reviews, vol 8. Springer, Dordrecht, pp 109–133

    Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    CAS  PubMed  Google Scholar 

  • Malbreil M, Tisserant E, Martin F, Roux C (2014) Genomics of arbuscular mycorrhizal fungi. Out of the shadows. Adv Bot Res 70:259–290

    Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake and mycorrhizal symbiosis. Plant Soil 159:89–102

    CAS  Google Scholar 

  • Marzluf GA (1996) Regulation of nitrogen metabolism in mycelial fungi. In: Brambl R, Marzluf GA (eds) Biochemistry and molecular biology, The mycota, vol 3. Springer, Berlin, pp 357–368

    Google Scholar 

  • Matsumura A, Taniguchi S, Yamawaki K, Hattori R, Tarui A (2013) Nitrogen uptake from amino acids in maize through arbuscular mycorrhizal symbiosis. Am J Plant Sci 4:2290–2294

    Google Scholar 

  • McFarland JW, Ruess RW, Kielland K, Pregitzer K, Hendrick R, Allen M (2010) Cross-ecosystem comparisons of in situ plant uptake of amino acid-N and NH4. Ecosystems 13:177–193

    CAS  Google Scholar 

  • Miransari M (2013) Arbuscular mycorrhizal fungi and uptake of nutrients. In: Aroca R (ed) Symbiotic endophytes, Soil biology, vol 37. Springer, Berlin, pp 253–270

    Google Scholar 

  • Mohanta TK, Bae H (2015) Functional genomics and signaling events in mycorrhizal symbiosis. J Plant Interact 10(1):21–40

    CAS  Google Scholar 

  • Nagy R, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250

    CAS  PubMed  Google Scholar 

  • Nasim G (2013) Host allelopathy and arbuscular mycorrhizal fungi. In: Cheema ZA, Farooq M, Wahid A (eds) Allelopathy. Springer, Berlin, pp 429–450

    Google Scholar 

  • Nygren CMR, Edqvist J, Elfstrand M, Heller G, Taylor AF (2007) Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi. Mycorrhiza 17:241–248

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Nat Acad Sci USA 99:13324–13329

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Tienda J, Testillano PS, Balestrini R, Fiorilli V, Azcón-Aguilar C, Ferrol N (2011) GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet Biol 48:1044–1055

    PubMed  Google Scholar 

  • Pfeffer P, Douds DD, Becard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–598

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pozo MJ, López-Raéez JA, Azcón C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436

    CAS  PubMed  Google Scholar 

  • Prasad R, Bhola D, Akdi K, Cruz C, Sairam KVSS, Tuteja N, Varma A (2017) Introduction to mycorrhiza: historical development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza. Springer, Cham, pp 1–7

    Google Scholar 

  • Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494

    CAS  PubMed  Google Scholar 

  • Purin S, Rillig MC (2007) The arbuscular mycorrhizal fungal protein glomalin: limitations, progress and a new hypothesis for its function. Pedobiologia 51:123–130

    CAS  Google Scholar 

  • Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129:611–618

    Google Scholar 

  • Ravnskov S, Wu Y, Graham JH (2003) Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytol 157:539–545

    CAS  PubMed  Google Scholar 

  • Read D (1998) Biodiversity—plants on the web. Nature 396:22–23

    CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B Biol Sci 355:815–831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy S, Schorderet M, Feller U, Reinhardt D (2007) A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J 51:739–750

    Google Scholar 

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

    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

    CAS  Google Scholar 

  • 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 196:91–108

    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

    CAS  PubMed  Google Scholar 

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

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shah MA (2014) Mycorrhizas: novel dimensions in the changing world. Springer, New Delhi, p 5

    Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazzo G, DeWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sieh D, Watanabe M, Devers EA, Brueckner F, Hoefgen R, Krajinski F (2013) The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytol 197:606–616

    CAS  PubMed  Google Scholar 

  • Singh S, Katzer K, Lambert J, Cerri M, Parniske M (2014) CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:139–152

    CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York, p 800

    Google Scholar 

  • 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 62:227–250

    CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13

    PubMed  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solaiman MZ, Saito M (1997) Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol 136:533–538

    CAS  Google Scholar 

  • Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG (2010) Inter plant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5(10):e13324

    PubMed  PubMed Central  Google Scholar 

  • St. John TV, Coleman DC, Reid CPP (1983) Association of vesicular–arbuscular mycorrhizal hyphae with soil organic particles. Ecology 64:957–959

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97:245–250

    CAS  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JP, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769

    CAS  PubMed  Google Scholar 

  • Tisserant E, Malbreil M, Kuoc A, Kohlera A, Symeonidid A, Balestrini R, Charron P, Duensing N, dit Frey NF, Gianinazzi-Pearsoni V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, Clemente HS, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill Y, Tuskans GA, Young JPW, Sanders IR, Henrissat B, Rensing SA, Grigorievc IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci USA 110:20117–20122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trépanier M, Bécard G, Moutoglis P, Willemot C, Gagné S, Avis TJ, Rioux JA (2005) Dependence of arbuscular-mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl Environ Microbiol 71:5341–5347

    PubMed  PubMed Central  Google Scholar 

  • Valentine AJ, Mortimer PE, Kleinert A, Kang Y, Benedito VA (2013) Carbon metabolism and costs of arbuscular mycorrhizal associations to host roots. In: Aroca R (ed) Symbiotic endophytes, Soil biology, vol 37. Springer, Berlin, pp 233–252

    Google Scholar 

  • Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311

    CAS  PubMed  Google Scholar 

  • Volpe V, Giovannetti M, Sun X-G, Fiorilli V, Bonfante P (2016) The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non-mycorrhizal roots. Plant Cell Environ 39:660–671

    CAS  PubMed  Google Scholar 

  • Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty P-E (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol 205:1632–1645

    CAS  PubMed  Google Scholar 

  • Walker C (1995) AM or VAM: what’s in a word? In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 25–26

    Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891

    Google Scholar 

  • Xie X, Huang W, Liu F, Tang N, Liu Y, Lin H, Zhao B (2013) Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytol 198:836–852

    CAS  PubMed  Google Scholar 

  • Yang Q, Chen ZZ, Zhou XF, Yin HB, Li X, Xin XF, Hong XH, Zhu JK, Gong Z (2009) Overexpression of SOS (salt overly sensitive) genes increases salt tolerance in transgenic Arabidopsis. Mol Plant 2:22–31

    CAS  PubMed  Google Scholar 

  • Yang S-Y, Grønlund M, Jakobsen I, Suter Grotemeyer M, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U (2012) Non redundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24:4236–4251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kim H, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235:1197–1207

    CAS  PubMed  Google Scholar 

  • Zaefarian F, Rezvani M, Rejali F, Ardakani MR, Noormohammadi G (2011) Effect of heavy metals and arbuscular mycorrhizal fungal on growth and nutrients (N, P, K, Zn, Cu and Fe) accumulation of alfalfa (Medicago sativa L.) Am Eurasian J Agric Environ Sci 11:346–352

    CAS  Google Scholar 

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Acknowledgements

The authors are grateful to the Department of science and technology (DST—under PURSE GRANT) and Department of Biotechnology (DBT), Government of India for providing financial assistance for undertaking the research in the above context.

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Bhandari, P., Garg, N. (2017). Dynamics of Arbuscular Mycorrhizal Symbiosis and Its Role in Nutrient Acquisition: An Overview. In: Varma, A., Prasad, R., Tuteja, N. (eds) Mycorrhiza - Nutrient Uptake, Biocontrol, Ecorestoration. Springer, Cham. https://doi.org/10.1007/978-3-319-68867-1_2

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