Advertisement

Plant and Soil

, Volume 396, Issue 1–2, pp 369–380 | Cite as

Plant carbon limitation does not reduce nitrogen transfer from arbuscular mycorrhizal fungi to Plantago lanceolata

  • Haiyang ZhangEmail author
  • Waldemar Ziegler
  • Xingguo Han
  • Susan Trumbore
  • Henrik Hartmann
Regular Article

Abstract

Aims

The stress-gradient-hypothesis predicts that interactions among organisms shift from competition to facilitation as environmental stress increases. Whether the strength of mutualism will increase among symbiotically associated organisms when partners are forced into resource limitation remains unknown. Plants exchange photosynthetic carbohydrates (plant C) for nutrients in mycorrhizal symbiosis but how this exchange varies with plant C limitation is not fully understood.

Methods

We investigated the influence of plant C availability and of arbuscular mycorrhizal fungi (AMF) on plant nitrogen (N) uptake and resource allocation using 13C and 15N labeling. We grew Plantago lanceolata with and without AMF Rhizophagus irregularis under ambient (400 ppm, AC) and low (100 ppm, LC) atmospheric [CO2] and physically restricted plant root but not mycorrhizal access to soil N.

Results

We found that plants grown under LC used AMF to obtain the same amount of N as those grown under AC, but the amount of newly fixed C correlated with the acquisition of N only under LC. The LC plants allocated more of their C to aboveground tissues.

Conclusions

Overall our results suggest a more beneficial role of symbiosis under C limitation. The tight reciprocal control on N transfer and C allocation under C limited conditions supports the stress-gradient hypothesis of mutualistic symbiotic functioning.

Keywords

Symbiosis Resource allocation Plant carbon limitation Stable isotopes 13C and 15Stress-gradient hypothesis 

Notes

Acknowledgments

We appreciate the comments from Xiaotao Lv on an early version of the manuscipt. We thank Katrin Krause for supplying AMF inoculum, Iris Kuhlmann and Agnes Fastnacht for their help with lab analysis and in the greenhouse, Gabriela Pereyra, Lenka Forkelova, Saadat Malghani and Savoyane Lambert for their help during the project, and Willy Brand and Heike Geilmann for isotopes analysis. This research was supported by a DFG grant to HH (HA 6400/1-1) and the Chinese Academy of Science - Max Planck Society Joint Programme.

References

  1. Aghili F, Jansa J, Khoshgoftarmanesh AH, Afyuni M, Schulin R, Frossard E, Gamper HA (2014) Wheat plants invest more in mycorrhizae and receive more benefits from them under adverse than favorable soil conditions. Appl Soil Ecol 84:93–111CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B,  Walker S (2013) lme4: linear mixed-effects models using Eigen and S4 (R package version 1.0-4). http://cran.r-project.org/package=lme4/.
  3. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefPubMedGoogle Scholar
  4. Bethlenfalvay GJ, Pacovsky RS (1983) Light effects in mycorrhizal soybeans. Plant Physiol 73:969–972PubMedCentralCrossRefPubMedGoogle Scholar
  5. Blanke V, Wagner M, Renker C, Lippert H, Michulitz M, Kuhn AJ, Buscot F (2011) Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen. Plant Soil 343:379–392CrossRefGoogle Scholar
  6. Brooker RW, Maestre FT, Callaway RM et al (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34CrossRefGoogle Scholar
  7. Brundrett MC, Ashwath N, Jasper DA (1996) Mycorrhizas in the Kakadu region of tropical Australia.1. Propagules of mycorrhizal fungi and soil properties in natural habitats. Plant Soil 184:159–171CrossRefGoogle Scholar
  8. 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
  9. Cavagnaro T, Barrios-Masias F, Jackson L (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant Soil 353:181–194CrossRefGoogle Scholar
  10. Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087CrossRefPubMedGoogle Scholar
  11. Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bücking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 109:2666–2671PubMedCentralCrossRefPubMedGoogle Scholar
  12. Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, Bücking H (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656CrossRefPubMedGoogle Scholar
  13. Field KJ, Cameron DD, Leake JR, Tille S, Bidartondo MI, Beerling DJ (2012) Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated Palaeozoic CO2 decline. Nat Commun 3:1–8CrossRefGoogle Scholar
  14. Fitter AH, Helgason T, Hodge A (2011) Nutritional exchanges in the arbuscular mycorrhizal symbiosis: Implications for sustainable agriculture. Fungal Biol Rev 25:68–72CrossRefGoogle Scholar
  15. Gabriel-Neumann E, Neumann G, Leggewie G, George E (2011) Constitutive overexpression of the sucrose transporter SoSUT1 in potato plants increases arbuscular mycorrhiza fungal root colonization under high, but not under low, soil phosphorus availability. J Plant Physiol 168:911–919CrossRefPubMedGoogle Scholar
  16. Gamnitzer U, Schäufele R, Schnyder H (2009) Observing 13C labelling kinetics in CO2 respired by a temperate grassland ecosystem. New Phytol 84:376–386CrossRefGoogle Scholar
  17. Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823CrossRefPubMedGoogle Scholar
  18. Grman E (2012) Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711–718CrossRefPubMedGoogle Scholar
  19. Grman E, Robinson TMP (2013) Resource availability and imbalance affect plant–mycorrhizal interactions: a field test of three hypotheses. Ecology 94:62–71CrossRefPubMedGoogle Scholar
  20. 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 76:236–244CrossRefPubMedGoogle Scholar
  21. Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger–declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349CrossRefPubMedGoogle Scholar
  22. Heinemeyer A, Ineson P, Ostle N, Fitter A (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytol 171:159–170CrossRefPubMedGoogle Scholar
  23. Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci U S A 107:13754–13759PubMedCentralCrossRefPubMedGoogle Scholar
  24. 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
  25. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380CrossRefGoogle Scholar
  26. Jin H, Pfeffer P, Douds D, Piotrowski E, Lammers P, Shachar-Hill Y (2005) The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol 168:687–696CrossRefPubMedGoogle Scholar
  27. Johnson D, Leake J, Read D (2002) 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
  28. Johnson NC, Angelard C, Sanders IR, Kiers ET (2013) Predicting community and ecosystem outcomes of mycorrhizal responses to global change. Ecol Lett 16:140–153CrossRefPubMedGoogle Scholar
  29. 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
  30. Knegt B, Jansa J, Franken O, Engelmoer DJP, Werner GDA, Bücking H, Kiers ET (2014) Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol. doi: 10.1016/j.funeco.2014.09.011 Google Scholar
  31. Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytol 111:35–44CrossRefGoogle Scholar
  32. Kytöviita M-M, Le Thiec D, Dizengremel P (2001) Elevated CO2 and ozone reduce nitrogen acquisition by Pinus halepensis from its mycorrhizal symbiont. Physiol Plant 111:305–312CrossRefPubMedGoogle Scholar
  33. 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 181:199–207CrossRefPubMedGoogle Scholar
  34. Olsson PA, Johnson NC (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8:1264–1270CrossRefGoogle Scholar
  35. Olsson O, Olsson P, Hammer E (2014) Phosphorus and carbon availability regulate structural composition and complexity of AM fungal mycelium. Mycorrhiza 24:1–9CrossRefGoogle Scholar
  36. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161Google Scholar
  37. Pierik R, Keuskamp DH, Sasidharan R, Djakovic-Petrovic T, de Wit M, Voesenek L (2009) Light quality controls shoot elongation through regulation of multiple hormones. Plant Signal Behav 4:755–756PubMedCentralCrossRefPubMedGoogle Scholar
  38. Sage RF, Coleman JR (2001) Effects of low atmospheric CO2 on plants: more than a thing of the past. Trends Plant Sci 6:18–24CrossRefPubMedGoogle Scholar
  39. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. 3rd edn. Cambridge, UK: Academic PressGoogle Scholar
  40. 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 62:227–250CrossRefPubMedGoogle Scholar
  41. Son C, Smith S (1988) Mycorrhizal growth responses: interactions between photon irradiance and phosphorus nutrition. New Phytol 108:305–314CrossRefGoogle Scholar
  42. Stonor R, Smith S, Manjarrez M, Facelli E, Smith FA (2014) Mycorrhizal responses in wheat: shading decreases growth but does not lower the contribution of the fungal phosphate uptake pathway. Mycorrhiza 24:1–8CrossRefGoogle Scholar
  43. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254CrossRefGoogle Scholar
  44. Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001CrossRefGoogle Scholar
  45. Thornton B, Bausenwein U (2000) Seasonal protease activity in storage tissue of the deciduous grass Molinia caerulea. New Phytol 146:75–81CrossRefGoogle Scholar
  46. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  47. 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 159:789–797PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Haiyang Zhang
    • 1
    • 2
    • 3
    Email author
  • Waldemar Ziegler
    • 1
  • Xingguo Han
    • 2
  • Susan Trumbore
    • 1
  • Henrik Hartmann
    • 1
  1. 1.Max-Planck Institute for BiogeochemistryJenaGermany
  2. 2.State Key Laboratory of Forest and Soil Ecology, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  3. 3.University of Chinese Academy of SciencesBeijingChina

Personalised recommendations