Plant and Soil

, Volume 367, Issue 1–2, pp 313–326 | Cite as

Insights into root growth, function, and mycorrhizal abundance from chemical and isotopic data across root orders

Regular Article
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Abstract

Background and aims

Detailed analyses of root chemistry by branching order may provide insights into root function, root lifespan and the abundance of root-associated mycorrhizal fungi in forest ecosystems.

Methods

We examined the nitrogen and carbon stable isotopes (δ15N and δ13C) and concentration (%N and %C) in the fine roots of an arbuscular mycorrhizal tree, Fraxinus mandshurica, and an ectomycorrhizal tree, Larix gmelinii, over depth, time, and across five root branching orders.

Results and conclusions

Larix δ15N increased by 2.3 ‰ from 4th order to 1st order roots, reflecting the increased presence of 15N-enriched ECM fungi on the lower root orders. In contrast, arbuscular mycorrhizal Fraxinus only increased by 0.7 ‰ from 4th order to 1st order roots, reflecting the smaller 15N enrichment and lower fungal mass on arbuscular mycorrhizal fine roots. Isotopic and anatomical mass balance calculations indicate that first, second, and third order roots in ectomycorrhizal Larix averaged 36 %, 23 %, and 8 % fungal tissue by mass, respectively. Using literature values of root production by root branching order, we estimate that about 25 % of fine root production in ECM species like Larix is actually of fungal sheaths. In contrast to %N, %C, and δ15N, δ13C changed minimally across depth, time, and branching order. The homogeneity of δ13C suggests root tissues are constructed from a large well-mixed reservoir of carbon, although compound specific δ13C data is needed to fully interpret these patterns. The measurements developed here are an important step towards explicitly including mycorrhizal production in forest ecosystem carbon budgets.

Keywords

Carbon Isotope Mycorrhizal fungi Nitrogen Root order 

Abbreviations

ECM

Ectomycorrhizal

AM

Arbuscular mycorrhizal

Larix

Larix gmelinii

Fraxinus

Fraxinus mandshurica

N

Nitrogen

C

Carbon

‰

Per mil

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Notes

Acknowledgments

Support for this project came from a grant awarded by the US Department of Energy (DOE). The manuscript was improved by critical reviews from Luke McCormack and Lucie Lepine.

Supplementary material

11104_2012_1464_MOESM1_ESM.doc (109 kb)
ESM 1 (DOC 109 kb)

References

  1. Badeck FW, Tcherkez G, Nogues S, Piel C, Ghashghaie J (2005) Post-photo synthetic fractionation of stable carbon isotopes between plant organs—a widespread phenomenon. Rapid Commun Mass Spectrom 19(11):1381–1391. doi: 10.1002/rcm.1912 PubMedCrossRefGoogle Scholar
  2. Bauer GA, Gebauer G, Harrison AF, Hogberg P, Hogbom L, Schinkel H, Taylor ASF, Novak M, Buzek F, Harkness D, Persson T, Schulze ED (2000) Biotic and abiotic controls over ecosystem cycling of stable natural nitrogen, carbon and sulphur isotopes. In: Schulze ED (ed) Carbon and nitrogen cycling in European forest ecosystems. Springer, New York, pp 189–216CrossRefGoogle Scholar
  3. Boström B, Comstedt D, Ekblad A (2007) Isotope fractionation and C-13 enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153(1):89–98. doi: 10.1007/s00442-007-0700-8 PubMedCrossRefGoogle Scholar
  4. Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Viewpoint: why are non-photosynthetic tissues generally (13)C enriched compared with leaves in C(3) plants? Review and synthesis of current hypotheses. Funct Plant Biol 36(3):199–213. doi: 10.1071/fp08216 CrossRefGoogle Scholar
  5. 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(2):952–961. doi: 10.1104/pp. 111.177618 PubMedCrossRefGoogle Scholar
  6. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Penuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183(4):980–992. doi: 10.1111/j.1469-8137.2009.02917.x PubMedCrossRefGoogle Scholar
  7. Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147(1):33–42. doi: 10.1046/j.1469-8137.2000.00686.x CrossRefGoogle Scholar
  8. Fan P, Jiang Y (2010) Nitrogen dynamics differed among the first six root branch orders of Fraxinus mandshurica and Larix gmelinii during short-term decomposition. J Plant Res 123(4):433–438. doi: 10.1007/s10265-009-0303-z PubMedCrossRefGoogle Scholar
  9. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol 40:503–537CrossRefGoogle Scholar
  10. Gaudinski JB, Trumbore SE, Davidson EA, Cook AC, Markewitz D, Richter DD (2001) The age of fine-root carbon in three forests of the eastern United States measured by radiocarbon. Oecologia 129(3):420–429Google Scholar
  11. Gaudinski JB, Torn MS, Riley WJ, Swanston C, Trumbore SE, Joslin JD, Majdi H, Dawson TE, Hanson PJ (2009) Use of stored carbon reserves in growth of temperate tree roots and leaf buds: analyses using radiocarbon measurements and modeling. Glob Chang Biol 15(4):992–1014. doi: 10.1111/j.1365-2486.2008.01736.x CrossRefGoogle Scholar
  12. Gebauer G, Schulze ED (1991) Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia 87(2):198–207. doi: 10.1007/bf00325257 CrossRefGoogle Scholar
  13. Goebel M, Hobbie SE, Bulaj B, Zadworny M, Archibald DD, Oleksyn J, Reich PB, Eissenstat DM (2011) Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure. Ecol Monogr 81(1):89–102. doi: 10.1890/09-2390.1 CrossRefGoogle Scholar
  14. Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140(3):450–457. doi: 10.1007/s00442-004-1596-1 PubMedCrossRefGoogle Scholar
  15. Guo DL, Li H, Mitchell RJ, Han W, Hendricks JJ, Fahey TJ, Hendrick RL (2008a) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177(2):443–456. doi: 10.1111/j.1469-8137.2007.02242.x PubMedGoogle Scholar
  16. Guo DL, Mitchell RJ, Withington JM, Fan P-P, Hendricks JJ (2008b) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96(4):737–745. doi: 10.1111/j.1365-2745.2008.01385.x CrossRefGoogle Scholar
  17. Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ (2008c) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180(3):673–683. doi: 10.1111/j.1469-8137.2008.02573.x PubMedCrossRefGoogle Scholar
  18. Helle G, Schleser GH (2004) Beyond CO(2)-fixation by Rubisco—an interpretation of (13)C/(12)C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27(3):367–380. doi: 10.1111/j.0016-8025.2003.01159.x CrossRefGoogle Scholar
  19. Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87(3):563–569. doi: 10.1890/05-0755 PubMedCrossRefGoogle Scholar
  20. Hobbie EA, Colpaert JV (2003) Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phytol 157(1):115–126. doi: 10.1046/j.1469-8137.2003.00657.x CrossRefGoogle Scholar
  21. Hobbie EA, Colpaert JV (2004) Nitrogen availability and mycorrhizal colonization influence water use efficiency and carbon isotope patterns in Pinus sylvestris. New Phytol 164(3):515–525. doi: 10.1111/j.1469-8137.2004.01187.x CrossRefGoogle Scholar
  22. Hobbie JE, Hobbie EA (2006) N-15 in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87(4):816–822. doi: 10.1890/0012-9658(2006)87[816:nisfap]2.0.co;2 PubMedCrossRefGoogle Scholar
  23. Hobbie EA, Hobbie JE (2008) Natural abundance of N-15 in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11(5):815–830. doi: 10.1007/s10021-008-9159-7 CrossRefGoogle Scholar
  24. Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95(2–3):355–371. doi: 10.1007/s10533-009-9328-6 CrossRefGoogle Scholar
  25. Hobbie EA, Werner RA (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C-3 and C-4 plants: a review and synthesis. New Phytol 161(2):371–385. doi: 10.1046/j.1469-8137.2004.00970.x CrossRefGoogle Scholar
  26. Hobbie EA, Colpaert JV, White MW, Ouimette AP, Macko SA (2008) Nitrogen form, availability, and mycorrhizal colonization affect biomass and nitrogen isotope patterns in Pinus sylvestris. Plant Soil 310(1–2):121–136. doi: 10.1007/s11104-008-9637-x CrossRefGoogle Scholar
  27. Hobbie EA, Sanchez FS, Rygiewicz PT (2012) Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi. Soil Biol Biochem 48:60–68CrossRefGoogle Scholar
  28. Högberg P (1997) Tansley review No 95 - N-15 natural abundance in soil-plant systems. New Phytol 137(2):179–203. doi: 10.1046/j.1469-8137.1997.00808.x CrossRefGoogle Scholar
  29. Högberg P, Hogbom L, Schinkel H, Högberg M, Johannisson C, Wallmark H (1996) N-15 abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108(2):207–214Google Scholar
  30. Högberg P, Högberg MN, Gottlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T, Linder S, Nasholm T (2008) High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytol 177(1):220–228. doi: 10.1111/j.1469-8137.2007.02238.x PubMedGoogle Scholar
  31. Hunt HW, Reuss DE, Elliott ET (1999) Correcting estimates of root chemical composition for soil contamination. Ecology 80(2):702–707. doi: 10.2307/176645 CrossRefGoogle Scholar
  32. Janzen HH, Entz T, Ellert BH (2002) Correcting mathematically for soil adhering to root samples. Soil Biol Biochem 34(12):1965–1968. doi: 10.1016/s0038-0717(02)00206-7 CrossRefGoogle Scholar
  33. Jia SX, Wang ZQ, Li XP, Zhang XP, McLaughlin NB (2011) Effect of nitrogen fertilizer, root branch order and temperature on respiration and tissue N concentration of fine roots in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 31(7):718–726. doi: 10.1093/treephys/tpr057 PubMedCrossRefGoogle Scholar
  34. Joslin JD, Gaudinski JB, Torn MS, Riley WJ, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a C-14-labeled hardwood forest. New Phytol 172(3):523–535. doi: 10.1111/j.1469-8137.2006.01847.x PubMedCrossRefGoogle Scholar
  35. Keel SG, Siegwolf RTW, Korner C (2006) Canopy CO(2) enrichment permits tracing the fate of recently assimilated carbon in a mature deciduous forest. New Phytol 172(2):319–329. doi: 10.1111/j.1469-8137.2006.01831.x PubMedCrossRefGoogle Scholar
  36. King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon in put to soil is control led by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154(2):389–398. doi: 10.1046/j.1469-8137.2002.00393.x CrossRefGoogle Scholar
  37. Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84(9):2302–2312. doi: 10.1890/02-0282 CrossRefGoogle Scholar
  38. Langley JA, Chapman SK, Hungate BA (2006) Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecol Lett 9(8):955–959. doi: 10.1111/j.1461-0248.2006.00948.x PubMedCrossRefGoogle Scholar
  39. Litton CM, Giardina CP (2008) Below-ground carbon flux and partitioning: global patterns and response to temperature. Funct Ecol 22(6):941–954. doi: 10.1111/j.1365-2435.2008.01479.x CrossRefGoogle Scholar
  40. Majdi H, Damm E, Nylund JE (2001) Longevity of mycorrhizal roots depends on branching order and nutrient availability. New Phytol 150(1):195–202. doi: 10.1046/j.1469-8137.2001.00065.x CrossRefGoogle Scholar
  41. Marron N, Plain C, Longdoz B, Epron D (2009) Seasonal and daily time course of the (13)C composition in soil CO(2) efflux recorded with a tunable diode laser spectrophotometer (TDLS). Plant Soil 318(1–2):137–151. doi: 10.1007/s11104-008-9824-9 CrossRefGoogle Scholar
  42. Mayor JR, Schuur EAG, Henkel TW (2009) Elucidating the nutritional dynamics of fungi using stable isotopes. Ecol Lett 12(2):171–183. doi: 10.1111/j.1461-0248.2008.01265.x PubMedCrossRefGoogle Scholar
  43. Mei L, Gu J, Zhang Z, Wang Z (2010) Responses of fine root mass, length, production and turnover to soil nitrogen fertilization in Larix gmelinii and Fraxinus mandshurica forests in Northeastern China. J For Res 15(3):194–201. doi: 10.1007/s10310-009-0176-y CrossRefGoogle Scholar
  44. Michelsen A, Quarmby C, Sleep D, Jonasson S (1998) Vascular plant N-15 natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115(3):406–418. doi: 10.1007/s004420050535 CrossRefGoogle Scholar
  45. Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14(5):493–502. doi: 10.1111/j.1461-0248.2011.01611.x PubMedCrossRefGoogle Scholar
  46. Pardo LH, Templer PH, Goodale CL, Duke S, Groffman PM, Adams MB, Boeckx P, Boggs J, Campbell J, Colman B, Compton J, Emmett B, Gundersen P, Kjonaas J, Lovett G, Mack M, Magill A, Mbila M, Mitchell MJ, McGee G, McNulty S, Nadelhoffer K, Ollinger S, Ross D, Rueth H, Rustad L, Schaberg P, Schiff S, Schleppi P, Spoelstra J, Wessel W (2006) Regional assessment of N saturation using foliar and root delta N-15. Biogeochemistry 80(2):143–171. doi: 10.1007/s10533-006-9015-9 CrossRefGoogle Scholar
  47. Pate J, Arthur D (1998) delta C-13 analysis of phloem sap carbon: novel means of evaluating seasonal water stress and interpreting carbon isotope signatures of foliage and trunk wood of Eucalyptus globulus. Oecologia 117(3):301–311. doi: 10.1007/s004420050663 CrossRefGoogle Scholar
  48. Polley HW, Johnson HB, Mayeux HS (1992) Determination of root biomasses of 3 species grown in a mixture using stable isotopes of carbon and nitrogen. Plant Soil 142(1):97–106Google Scholar
  49. Pregitzer KS (2002) Fine roots of trees—a new perspective. New Phytol 154(2):267–270. doi: 10.1046/j.1469-8137.2002.00413_1.x CrossRefGoogle Scholar
  50. Pregitzer KS (2008) Tree root architecture—form and function. New Phytol 180(3):562–564. doi: 10.1111/j.1469-8137.2008.02648.x PubMedCrossRefGoogle Scholar
  51. Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL (1997) Relationships among roof branch order, carbon, and nitrogen in four temperate species. Oecologia 111(3):302–308. doi: 10.1007/s004420050239 CrossRefGoogle Scholar
  52. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72(2):293–309. doi: 10.1890/0012-9615(2002)072[0293:fraonn]2.0.co;2 CrossRefGoogle Scholar
  53. Robinson D (2001) delta N-15 as an integrator of the nitrogen cycle. Trends Ecol Evol 16(3):153–162. doi: 10.1016/s0169-5347(00)02098-x PubMedCrossRefGoogle Scholar
  54. Sah SP, Jungner H, Oinonen M, Kukkola M, Helmisaari HS (2011) Does the age of fine root carbon indicate the age of fine roots in boreal forests? Biogeochemistry 104(1–3):91–102. doi: 10.1007/s10533-010-9485-7 CrossRefGoogle Scholar
  55. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, New YorkGoogle Scholar
  56. Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of C-14. Science 300(5622):1138–1140. doi: 10.1126/science.1084269 PubMedCrossRefGoogle Scholar
  57. Sun Y, Gu J-C, Zhuang H-F, Wang Z-Q (2010) Effects of ectomycorrhizal colonization and nitrogen fertilization on morphology of root tips in a Larix gmelinii plantation in northeastern China. Ecol Res 25(2):295–302. doi: 10.1007/s11284-009-0654-x CrossRefGoogle Scholar
  58. Taylor AFS, Fransson PM, Högberg P, Högberg MN, Plamboeck AH (2003) Species level patterns in C-13 and N-15 abundance of ectomycorrhizal and saprotrophic fungal sporocarps. New Phytol 159(3):757–774. doi: 10.1046/j.1469-8137.2003.00838.x CrossRefGoogle Scholar
  59. Templer PH, Arthur MA, Lovett GM, Weathers KC (2007) Plant and soil natural abundance delta(15)N: indicators of relative rates of nitrogen cycling in temperate forest ecosystems. Oecologia 153(2):399–406. doi: 10.1007/s00442-007-0746-7 PubMedCrossRefGoogle Scholar
  60. Trudell SA, Rygiewicz PT, Edmonds RL (2004) Patterns of nitrogen and carbon stable isotope ratios in macrofungi, plants and soils in two old-growth conifer forests. New Phytol 164(2):317–335. doi: 10.1111/j.1469-8137.2004.01162.x CrossRefGoogle Scholar
  61. Wallander H, Goransson H, Rosengren U (2004) Production, standing biomass and natural abundance of N-15 and C-13 in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139(1):89–97. doi: 10.1007/s00442-003-1477-z PubMedCrossRefGoogle Scholar
  62. Wang Z, Guo D, Wang X, Gu J, Mei L (2006) Fine root architecture, morphology, and biomass of different branch orders of two Chinese temperate tree species. Plant Soil 288(1–2):155–171. doi: 10.1007/s11104-006-9101-8 CrossRefGoogle Scholar
  63. Xia M, Guo D, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188(4):1065–1074. doi: 10.1111/j.1469-8137.2010.03423.x PubMedCrossRefGoogle Scholar
  64. Zadworny M, Eissenstat DM (2011) Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots. New Phytol 190:213–221CrossRefGoogle Scholar
  65. Zhou XF (1994) Long-term research on China’s forest ecosystems. Northeast Forestry University Press, Harbin, in ChineseGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Andrew Ouimette
    • 1
  • Dali Guo
    • 2
    • 3
  • Erik Hobbie
    • 1
  • Jiacun Gu
    • 4
  1. 1.Earth Systems Research CenterUniversity of New HampshireDurhamUSA
  2. 2.Department of Ecology, College of Urban and Environmental SciencesPeking UniversityBeijingChina
  3. 3.Key Laboratory of Science and Technology of Urban EnvironmentPeking University Shenzhen Graduate SchoolShenzhenChina
  4. 4.School of ForestryNortheast Forestry UniversityHarbinChina

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