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Carbon Fluxes in Mycorrhizal Plants

  • Veronika Řezáčová
  • Tereza Konvalinková
  • Jan JansaEmail author
Chapter

Abstract

Although declared as a research priority more than 40 years ago, the knowledge about the magnitude and mechanisms of carbon (C) fluxes between plants and their mycorrhizal fungal symbionts remains fragmentary. In spite of a number of experiments with isotopically labeled C documented rapid and directed C transfer from the host plant to its mycobionts, the molecular mechanisms and their regulation involved in such a transport remain largely unknown. It seems that in many arbuscular mycorrhizal (AM) symbioses, the C costs remains well below 10% of the C fixed photosynthetically by the host plants. Higher values were detected in the past only under specific situations such as in young plants, under low light intensities, and/or for particular partner combinations, involving very costly (in terms of C demand) and little nutritionally beneficial AM fungi such as Gigaspora sp. Ecological context of the common mycorrhizal networks in terms of redistribution of symbiotic C costs and nutritional benefits on one hand and C movement through soil food webs beyond mycorrhizal hyphae on the other are briefly discussed in this chapter, and further research challenges and open knowledge gaps with respect to C fluxes in mycorrhizal plants are outlined.

Notes

Acknowledgment

Research funding was provided by the Czech Science Foundation (project 14-19191S) and the Czech Ministry of Education, Youth and Sports (project No. LK11224). The authors also gratefully acknowledge further support from the Czech Academy of Sciences (J. E. Purkyně Fellowship to JJ) and the long-term research program RVO 61388971.

References

  1. Abuzinadah RA, Read DJ (1989) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. 5. Nitrogen transfer in birch (Betula pendula) grown in association with mycorrhizal and non-mycorrhizal fungi. New Phytol 112:61–68CrossRefGoogle Scholar
  2. Baas R, Lambers H (1988) Effects of vesicular-arbuscular mycorrhizal infection and phosphate on Plantago major ssp. pleiosperma in relation to the internal phosphate concentration. Physiol Plant 74:701–707CrossRefGoogle Scholar
  3. Bahn M, Schmitt M, Siegwolf R, Richter A, Bruggemann N (2009) Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale? New Phytol 182:451–460PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barrett CF, Freudenstein JV, Taylor DL, Koljalg U (2010) Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. Am J Bot 97:628–643PubMedCrossRefGoogle Scholar
  5. Bever JD (2015) Preferential allocation, physio-evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytol 205:1503–1514PubMedCrossRefGoogle Scholar
  6. Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392PubMedCrossRefGoogle Scholar
  7. Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725CrossRefGoogle Scholar
  8. Brown MS, Bethlenfalvay GJ (1987) Glycine-Glomus-Rhizobium symbiosis. 6. Photosynthesis in nodulated, mycorrhizal, or N-fertilized and P-fertilized soybean plants. Plant Physiol 85:120–123PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bryla DR, Eissenstat DM (2005) Respiratory costs of mycorrhiza associations. In: Lambers H, Ribas-Carbo M (eds) Plant respiration. Springer, Dordrecht, pp 207–224CrossRefGoogle Scholar
  10. Brzostek ER, Fisher JB, Phillips RP (2014) Modeling the carbon cost of plant nitrogen acquisition: Mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation. J Geophys Res Biogeosci 119:1684–1697CrossRefGoogle Scholar
  11. Cairney JWG (2000) Evolution of mycorrhiza systems. Naturwissenschaften 87:467–475PubMedCrossRefGoogle Scholar
  12. Calderón FJ, Schultz DJ, Paul EA (2012) Carbon allocation, belowground transfers, and lipid turnover in a plant-microbial association. Soil Sci Soc Am J 76:1614–1623CrossRefGoogle Scholar
  13. Cameron DD, Johnson I, Read DJ, Leake JR (2008) Giving and receiving: measuring the carbon cost of mycorrhizas in the green orchid, Goodyera repens. New Phytol 180:176–184PubMedCrossRefGoogle Scholar
  14. Casieri L, Lahmidi NA, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Courty PE, Garcia K, Charbonnier M, Delteil A et al (2013) Biotrophic transportome in mutualistic plant-fungal interactions. Mycorrhiza 23:597–625PubMedCrossRefGoogle Scholar
  15. Cavagnaro TR, Smith FA, Smith SE, Jakobsen I (2005) Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant Cell Environ 28:642–650CrossRefGoogle Scholar
  16. Cheng L, Booker FL, Tu C, Burkey KO, Zhou LS, Shew HD, Rufty TW, Hu SJ (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087PubMedCrossRefGoogle Scholar
  17. Correa A, Hampp R, Magel E, Martins-Loucao MA (2011) Carbon allocation in ectomycorrhizal plants at limited and optimal N supply: an attempt at unraveling conflicting theories. Mycorrhiza 21:35–51PubMedCrossRefGoogle Scholar
  18. Courty PE, Walder F, Boller T, Ineichen K, Wiemken A, Rousteau A, Selosse MA (2011) Carbon and nitrogen metabolism in mycorrhizal networks and mycoheterotrophic plants of tropical forests: a stable isotope analysis. Plant Physiol 156:952–961PubMedPubMedCentralCrossRefGoogle Scholar
  19. Crowther TW, Boddy L, Jones TH (2012) Functional and ecological consequences of saprotrophic fungus-grazer interactions. ISME J 6:1992–2001PubMedPubMedCentralCrossRefGoogle Scholar
  20. Deslippe JR, Simard SW (2011) Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytol 192:689–698PubMedCrossRefGoogle Scholar
  21. Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiol 134:706–715PubMedPubMedCentralCrossRefGoogle Scholar
  22. Doidy J, Grace E, Kuhn C, Simon-Plas F, Casieri L, Wipf D (2012) Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci 17:413–422PubMedCrossRefGoogle Scholar
  23. Douds DD, Johnson CR, Koch KE (1988) Carbon cost of the fungal symbiont relative to net leaf-P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol 86:491–496PubMedPubMedCentralCrossRefGoogle Scholar
  24. Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 107–129CrossRefGoogle Scholar
  25. Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA et al (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc Natl Acad Sci USA 107:10938–10942PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ferrol N, Barea JM, Azcón-Aguilar C (2002) Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas. Plant Soil 244:231–237CrossRefGoogle Scholar
  27. Field KJ, Leake JR, Tille S, Allinson KE, Rimington WR, Bidartondo MI, Beerling DJ, Cameron DD (2015) From mycoheterotrophy to mutualism: mycorrhizal specificity and functioning in Ophioglossum vulgatum sporophytes. New Phytol 205:1492–1502PubMedCrossRefGoogle Scholar
  28. Fitter AH (1991) Costs and benefits of mycorrhizas – implications for functioning under natural conditions. Experientia 47:350–355CrossRefGoogle Scholar
  29. Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132CrossRefGoogle Scholar
  30. Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12:406–412CrossRefGoogle Scholar
  31. Fokom R, Mofor CT, Wakam LN, Megapche ELN, Tchameni S, Nwaga D, Rillig CM, Amvam PHA (2013) Glomalin, carbon, nitrogen and soil aggregate stability as affected by land use changes in the humid forest zone in South Cameroon. Appl Ecol Environ Res 11:581–592CrossRefGoogle Scholar
  32. Gadkar V, Rillig MC (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263:93–101PubMedCrossRefGoogle Scholar
  33. Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty PE (2016) Take a trip through the plant and fungal transportome of mycorrhiza. Trends Plant Sci 21:937–950PubMedCrossRefGoogle Scholar
  34. Graham JH, Drouillard DL, Hodge NC (1996) Carbon economy of sour orange in response to different Glomus spp. Tree Physiol 16:1023–1029PubMedCrossRefGoogle Scholar
  35. Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366PubMedCrossRefGoogle Scholar
  36. Grimoldi AA, Kavanová M, Lattanzi FA, Schaufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by 13CO2/12CO2 steady-state labelling and gas exchange. New Phytol 172:544–553PubMedCrossRefGoogle Scholar
  37. Hammer EC, Rillig MC (2011) The influence of different stresses on glomalin levels in an arbuscular mycorrhizal fungus—salinity increases glomalin content. PLoS ONE 6(12):e28426. doi: 10.1371/journal.pone.0028426 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Harley J (1975) Problems of mycotrophy. In: Sanders FE, Mosse B, Tinker PB (eds) Endomycorrhizas. Academic Press, London, pp 1–24Google Scholar
  39. Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean-Rhizobium-Glomus associations. New Phytol 101:427–440CrossRefGoogle Scholar
  40. Heinemeyer A, Ineson P, Ostle N, Fitter AH (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytol 171:159–170PubMedCrossRefGoogle Scholar
  41. 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 23:3812–3823PubMedPubMedCentralCrossRefGoogle Scholar
  42. Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384CrossRefGoogle Scholar
  43. Hobbie EA, Hofmockel KS, Van Diepen LTA, Lilleskov EA, Ouimette AP, Finzi AC (2014) Fungal carbon sources in a pine forest: evidence from a 13C-labeled global change experiment. Fungal Ecol 10:91–100CrossRefGoogle Scholar
  44. Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273CrossRefGoogle Scholar
  45. Hughes E, Mitchell DT (1995) Utilization of sucrose by Hymenoscyphus ericae (an ericoid endomycorrhizal fungus) and ectomycorrhizal fungi. Mycol Res 99:1233–1238CrossRefGoogle Scholar
  46. Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83CrossRefGoogle Scholar
  47. Jansa J, Bukovská P, Gryndler M (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts – or just soil free-riders? Front Plant Sci 4:134PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jemo M, Souleymanou A, Frossard E, Jansa J (2014) Cropping enhances mycorrhizal benefits to maize in a tropical soil. Soil Biol Biochem 79:117–124CrossRefGoogle Scholar
  49. Johnson D (2008) Resolving uncertainty in the carbon economy of mycorrhizal fungi. New Phytol 180:3–5PubMedCrossRefGoogle Scholar
  50. Johnson D (2015) Priorities for research on priority effects. New Phytol 205:1375–1377PubMedCrossRefGoogle Scholar
  51. Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytol 205:1448–1453PubMedCrossRefGoogle Scholar
  52. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  53. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002a) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334CrossRefGoogle Scholar
  54. Johnson D, Leake JR, Read DJ (2002b) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14C. Soil Biol Biochem 34:1521–1524CrossRefGoogle Scholar
  55. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515CrossRefGoogle Scholar
  56. Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytol 205:1473–1484PubMedCrossRefGoogle Scholar
  57. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205:1537–1551PubMedCrossRefGoogle Scholar
  58. Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244CrossRefGoogle Scholar
  59. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882PubMedCrossRefGoogle Scholar
  60. Klein T, Siegwolf RTW, Korner C (2016) Belowground carbon trade among tall trees in a temperate forest. Science 352:342–344PubMedCrossRefGoogle Scholar
  61. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  62. Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fertil Soils 21:43–52CrossRefGoogle Scholar
  63. Koch KE, Johnson CR (1984) Photosynthate partitioning in split-root Citrus seedlings with mycorrhizal and nonmycorrhizal root systems. Plant Physiol 75:26–30PubMedPubMedCentralCrossRefGoogle Scholar
  64. Konvalinková T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci 7Google Scholar
  65. Krajinski F, Courty PE, Sieh D, Franken P, Zhang HQ, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M et al (2014) The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 26:1808–1817PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kucey RMN, Paul EA (1982) Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans (Vicia faba L.) Soil Biol Biochem 14:407–412CrossRefGoogle Scholar
  67. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371CrossRefGoogle Scholar
  68. Kytoviita MM, Vestberg M, Tuom J (2003) A test of mutual aid in common mycorrhizal networks: established vegetation negates benefit in seedlings. Ecology 84:898–906CrossRefGoogle Scholar
  69. Landis FC, Fraser LH (2008) A new model of carbon and phosphorus transfers in arbuscular mycorrhizas. New Phytol 177:466–479PubMedGoogle Scholar
  70. Leake JR (2005) Plants parasitic on fungi: unearthing the fungi in mycoheterotrophs and debunking the ‘Saprophytic’ plant myth. Mycologist 19:113–122Google Scholar
  71. Leake JR, Cameron DD (2010) Physiological ecology of mycoheterotrophy. New Phytol 185:601–605PubMedCrossRefGoogle Scholar
  72. Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, Jansa J (2011) Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21:689–702PubMedCrossRefGoogle Scholar
  73. Lerat S, Lapointe L, Gutjahr S, Piche Y, Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157:589–595CrossRefGoogle Scholar
  74. Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447PubMedCrossRefGoogle Scholar
  75. McGuire KL (2007) Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88:567–574PubMedCrossRefGoogle Scholar
  76. Mencuccini M, Hölttä T (2010) The significance of phloem transport for the speed with which canopy photosynthesis and belowground respiration are linked. New Phytol 185:189–203PubMedCrossRefGoogle Scholar
  77. Merrild MP, Ambus P, Rosendahl S, Jakobsen I (2013) Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol 200:229–240PubMedCrossRefGoogle Scholar
  78. Midgley DJ, Chambers SM, Cairney JWG (2004) Utilisation of carbon substrates by multiple genotypes of ericoid mycorrhizal fungal endophytes from eastern Australian Ericaceae. Mycorrhiza 14:245–251PubMedCrossRefGoogle Scholar
  79. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  80. Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59:1097–1108PubMedCrossRefGoogle Scholar
  81. Newbery DM, Alexander IJ, Rother JA (2000) Does proximity to conspecific adults influence the establishment of ectomycorrhizal trees in rain forest? New Phytol 147:401–409CrossRefGoogle Scholar
  82. Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000CrossRefGoogle Scholar
  83. Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248CrossRefGoogle Scholar
  84. Olsson PA, Johnson NC (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8:1264–1270CrossRefGoogle Scholar
  85. Pang PC, Paul EA (1980) Effects of vesicular-arbuscular mycorrhiza on 14C and 15N distribution in nodulated fababeans. Can J Soil Sci 60:241–250CrossRefGoogle Scholar
  86. Paul EA, Kucey RMN (1981) Carbon flow in plant microbial associations. Science 213:473–474PubMedCrossRefGoogle Scholar
  87. Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488CrossRefGoogle Scholar
  88. Peng SB, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal Citrus at high phosphorus supply – analysis of carbon costs. Plant Physiol 101:1063–1071PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 120:587–598PubMedPubMedCentralCrossRefGoogle Scholar
  90. Pfeffer PE, Douds DD, Bücking H, Schwartz DP, Shachar-Hill Y (2004) The fungus does not transfer carbon to or between roots in an arbuscular mycorrhizal symbiosis. New Phytol 163:617–627CrossRefGoogle Scholar
  91. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799PubMedCrossRefGoogle Scholar
  92. 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, Switzerland, pp 1–7Google Scholar
  93. Prieto I, Roldán A, Huygens D, Alguacil MD, Navarro-Cano JA, Querejeta JI (2016) Species-specific roles of ectomycorrhizal fungi in facilitating interplant transfer of hydraulically redistributed water between Pinus halepensis saplings and seedlings. Plant Soil 406:15–27CrossRefGoogle Scholar
  94. Rillig MC (2005) A connection between fungal hydrophobins and soil water repellency? Pedobiologia 49:395–399CrossRefGoogle Scholar
  95. Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205:1385–1388PubMedCrossRefGoogle Scholar
  96. Rousseau A, Benhamou N, Chet I, Piche Y (1996) Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86:434–443CrossRefGoogle Scholar
  97. Sato T, Ezawa T, Cheng WG, Tawaraya K (2015) Release of acid phosphatase from extraradical hyphae of arbuscular mycorrhizal fungus Rhizophagus clarus. Soil Sci Plant Nutr 61:269–274CrossRefGoogle Scholar
  98. Schrey SD, Hartmann A, Hampp R. (2015) Rhizosphere interactions. In: Ecological biochemistry: environmental and interspecies interactions. Wiley, Weinheim, pp 293–310Google Scholar
  99. Schuur EAG, Carbone MS, Hicks Pries CE, Hopkins FM, Natali SM (2016) Radiocarbon in terrestrial ecosystems. In: EAG S, ERM D, Trumbore SE (eds) Radiocarbon and climate change. Mechanisms, applications and laboratory techniques. Springer, Cham, pp 167–220Google Scholar
  100. Schüβler A, Martin H, Cohen D, Fitz M, Wipf D (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444:933–936CrossRefGoogle Scholar
  101. Selosse MA, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70PubMedCrossRefGoogle Scholar
  102. Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165CrossRefGoogle Scholar
  103. Slavíková R, Püschel D, Janoušková M, Hujslová M, Konvalinková T, Gryndlerová H, Gryndler M, Weiser M, Jansa J (2017) Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. Mycorrhiza 27:35–51PubMedCrossRefGoogle Scholar
  104. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  105. Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13PubMedCrossRefGoogle Scholar
  106. Snellgrove RC, Splittstoesser WE, Stribley DP, Tinker PB (1982) The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular arbuscular mycorrhizas. New Phytol 92:75–87CrossRefGoogle Scholar
  107. Sochorová L, Jansa J, Verbruggen E, Hejcman M, Schellberg J, Kiers ET, Johnson NC (2016) Long-term agricultural management maximizing hay production can significantly reduce belowground C storage. Agric Ecosyst Environ 220:104–114CrossRefGoogle Scholar
  108. Taktek S, Trepanier M, Servin PM, St-Arnaud M, Piche Y, Fortin JA, Antoun H (2015) Trapping of phosphate solubilizing bacteria on hyphae of the arbuscular mycorrhizal fungus Rhizophagus irregularis DAOM 197198. Soil Biol Biochem 90:1–9CrossRefGoogle Scholar
  109. Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963CrossRefGoogle Scholar
  110. Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388CrossRefGoogle Scholar
  111. Tinker PB, Durall DM, Jones MD (1994) Carbon use efficiency in mycorrhizas – theory and sample calculations. New Phytol 128:115–122CrossRefGoogle Scholar
  112. Toju H, Sato H, Yamamoto S, Kadowaki K, Tanabe AS, Yazawa S, Nishimura O, Agata K (2013) How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants. Ecol Evol 3:3112–3124PubMedPubMedCentralCrossRefGoogle Scholar
  113. Tomé E, Tagliavini M, Scandellari F (2015) Recently fixed carbon allocation in strawberry plants and concurrent inorganic nitrogen uptake through arbuscular mycorrhizal fungi. J Plant Physiol 179:83–89PubMedCrossRefGoogle Scholar
  114. Treseder KK, Allen MF (2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytol 147:189–200CrossRefGoogle Scholar
  115. Valentine AJ, Mortimer PE, Kleinert A, Kang Y, Benedito VA (2013) Carbon metabolism and costs of arbuscular mycorrhizal associations to host roots. Symbiotic Endophytes 37:233–252CrossRefGoogle Scholar
  116. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  117. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095PubMedCrossRefGoogle Scholar
  118. Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1(11). doi: 10.1038/nplants.2015.159
  119. Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wang GM, Coleman DC, Freckman DW, Dyer MI, Mcnaughton SJ, Acra MA, Goeschl JD (1989) Carbon partitioning patterns of mycorrhizal versus non-mycorrhizal plants – real-time dynamic measurements using 11CO2. New Phytol 112:489–493CrossRefGoogle Scholar
  121. Weremijewicz J, Janos DP (2013) Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol 198:203–213PubMedCrossRefGoogle Scholar
  122. Weremijewicz J, da Silveira Lobo O’Reilly Sternberg L, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212:461–471PubMedCrossRefGoogle Scholar
  123. Workman RE, Cruzan MB (2016) Common mycelial networks impact competition in an invasive grass. Am J Bot 103:1041–1049PubMedCrossRefGoogle Scholar
  124. Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891CrossRefGoogle Scholar
  125. Wright SF, Nichols KA, Schmidt WF (2006) Comparison of efficacy of three extractants to solubilize glomalin on hyphae and in soil. Chemosphere 64:1219–1224PubMedCrossRefGoogle Scholar
  126. Zhang L, Xu MG, Liu Y, Zhang FS, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Veronika Řezáčová
    • 1
  • Tereza Konvalinková
    • 1
  • Jan Jansa
    • 1
    Email author
  1. 1.Laboratory of Fungal BiologyInstitute of Microbiology, Czech Academy of SciencesPragueCzech Republic

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