Advertisement

Biogeochemistry

, Volume 108, Issue 1–3, pp 279–295 | Cite as

Litter decay rates are determined by lignin chemistry

  • Jennifer M. TalbotEmail author
  • Daniel J. Yelle
  • James Nowick
  • Kathleen K. Treseder
Article

Abstract

Litter decay rates are often correlated with the initial lignin:N or lignin:cellulose content of litter, suggesting that interactions between lignin and more labile compounds are important controls over litter decomposition. The chemical composition of lignin may influence these interactions, if lignin physically or chemically protects labile components from microbial attack. We tested the effect of lignin chemical composition on litter decay in the field during a year-long litterbag study using the model system Arabidopsis thaliana. Three Arabidopsis plant types were used, including one with high amounts of guaiacyl-type lignin, one with high aldehyde- and p-hydroxyphenyl-type lignin, and a wild type control with high syringyl-type lignin. The high aldehyde litter lost significantly more mass than the other plant types, due to greater losses of cellulose, hemicellulose, and N. Aldehyde-rich lignins and p-hydroxyphenyl-type lignins have low levels of cross-linking between lignins and polysaccharides, supporting the hypothesis that chemical protection of labile polysaccharides and N is a mechanism by which lignin controls total litter decay rates. 2D NMR of litters showed that lignin losses were associated with the ratio of guaiacyl-to-p-hydroxyphenyl units in lignin, because these units polymerize to form different amounts of labile- and recalcitrant-linkages within the lignin polymer. Different controls over lignin decay and polysaccharide and N decay may explain why lignin:N and lignin:cellulose ratios can be better predictors of decay rates than lignin content alone.

Keywords

Lignin Decomposition Cellulose Nitrogen 

Notes

Acknowledgements

We thank Steven Allison, Donovan German, Stephanie Kivlin, Matthew Whiteside, Sandra Dooley, Heather McGray, Marko Spasojevic, and Rebecca Aicher for their critical review and support of this work. We also thank Dr. Philip Dennison and the UCI NMR Facility for instrument and software support for this research. Dr. Lise Jouanin and Dr. Clint Chapple generously supplied seeds of Arabidopsis plants used in this experiment. NSF-EAR-044548, a UCI Environment Institute Research Grant, and a Graduate Research Fellowship from NSF supported this project.

References

  1. Aber JD, Melillo JM, McClaugherty CA (1990) Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can J Bot 68:2201–2208CrossRefGoogle Scholar
  2. Adler E (1977) Lignin chemistry—past, present and future. Wood Sci Technol 11:169–218CrossRefGoogle Scholar
  3. Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449CrossRefGoogle Scholar
  4. Alexander M (1977) Soil microbiology. John Wiley and Sons, New YorkGoogle Scholar
  5. Allison SD, Treseder KK (2008) Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Glob Change Biol 14:2898–2909CrossRefGoogle Scholar
  6. Bahri H, Dignac M, Rumpel C, Rasse D, Chenu C, Mariotti A (2006) Lignin turnover kinetics in an agricultural soil is monomer specific. Soil Biol Biochem 38:1977–1988CrossRefGoogle Scholar
  7. Baucher M, Bernard-vailhé MA, Chabbert B, Besle J-M, Opsomer C, Van Montagu M, Botterman J (1999) Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility. Plant Mol Biol 39:437–447CrossRefGoogle Scholar
  8. Berg B, McClaugherty C (2003) Plant litter: decomposition, humus formation, carbon sequestration. Springer, BerlinGoogle Scholar
  9. Berg B, McClaugherty C, Johansson MB (1993) Litter mass-loss rates in late stages of decomposition at some climatically and nutritionally different pine sites. Long-term decomposition in a Scots pine forest. VIII. Can J Bot 71:680–692CrossRefGoogle Scholar
  10. Bernard Vailhé MA, Besle JM, Maillot MP, Cornu A, Halpin C, Knight M (1998) Effect of down-regulation of cinnamyl alcohol dehydrogenase on cell wall composition and on degradability of tobacco stems. J Sci Food Agric 76:505–514CrossRefGoogle Scholar
  11. Bertrand I, Chabbert B, Kurek B, Recous S (2006) Can the biochemical features and histology of wheat residues explain their decomposition in soil? Plant Soil 281:291–307CrossRefGoogle Scholar
  12. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546CrossRefGoogle Scholar
  13. Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629CrossRefGoogle Scholar
  14. Campbell MM, Sederoff RR (1996) Variation in lignin content and composition—mechanism of control and implications for the genetic improvement of plants. Plant Physiol 110:3–13Google Scholar
  15. Chefetz B, Chen Y, Clapp CE, Hatcher PG (2000) Characterization of organic matter in soils by thermochemolysis using tetramethylammonium hydroxide (TMAH). Soil Sci Soc Am J 64:583–589CrossRefGoogle Scholar
  16. Cherney J, Anliker K, Albrecht K, Wood K (1989) Soluble phenolic monomers in forage crops. J Sci Food Agric 37:345–350CrossRefGoogle Scholar
  17. Christman RF, Oglesby RT (1971) Microbial degradation and the formation of humus. In: Sarkanen SV, Ludwig CH (eds) Lignins. Wiley, New York, pp 769–795Google Scholar
  18. Cortez J, Demard J, Bottner P, Jocteur Monrozier L (1996) Decomposition of Mediterranean leaf litters: a microcosm experiment investigating relationships between decomposition rates and litter quality. Soil Biol Biochem 28:443–452CrossRefGoogle Scholar
  19. Croci C, Arguello J, Orioli G (1994) Biochemical changes in garlic (Allium sativum L.) during storage following gamma-irradiation. Int J Radiat Biol 65:263–266CrossRefGoogle Scholar
  20. Dignac M, Rumpel C (2006) Relative distributions of phenol dimers and hydroxy acids in a cultivated soil and above ground maize tissue. Org Geochem 37:1634–1638CrossRefGoogle Scholar
  21. Dümig A, Knicker H, Schad P, Rumpel C, Dignac M, Kögel Knabner I (2009) Changes in soil organic matter composition are associated with forest encroachment into grassland with long term fire history. Eur J Soil Sci 60:578–589CrossRefGoogle Scholar
  22. Goni M, Hedges J (1992) Lignin dimers: structures, distribution, and potential geochemical applications. Geochim Cosmochim Ac 56:4025–4043CrossRefGoogle Scholar
  23. Goni M, Nelson B, Blanchette R, Hedges J (1993) Fungal degradation of wood lignins: geochemical perspectives from CuO-derived phenolic dimers and monomers. Geochim Cosmochim Ac 57:3985–4002CrossRefGoogle Scholar
  24. Goulden ML, Wofsy SC, Harden JW, Trumbore SE, Crill PM, Gower ST, Fries T, Daube BC, Fan SM, Sutton DJ, Bazzaz A, Munger JW (1998) Sensitivity of boreal forest carbon balance to soil thaw. Science 279:214–217CrossRefGoogle Scholar
  25. Grabber J (2005) How do lignin composition, structure, and cross-linking affect degradability? A review of cell wall model studies. Crop Sci 45:820CrossRefGoogle Scholar
  26. Grabber JH, Ralph J, Hatfield RD, Quideau S (1997) p-hydroxyphenyl, guaiacyl, and syringyl lignins have similar inhibitory effects on wall degradability. J Agr Food Chem 45:2530–2532CrossRefGoogle Scholar
  27. Grabber J, Ralph J, Hatfield R (1998a) Ferulate cross-links limit the enzymatic degradation of synthetically lignified primary walls of maize. J Agric Food Chem 46:2609–2614CrossRefGoogle Scholar
  28. Grabber JH, Hatfield RD, Ralph J (1998b) Diferulate cross-links impede the enzymatic degradation of non-lignified maize walls. J Sci Food Agric 77:193–200CrossRefGoogle Scholar
  29. Grabber JH, Ralph J, Hatfield RD (1998c) Severe inhibition of maize wall degradation by synthetic lignins formed with coniferaldehyde. J Sci Food Agric 78:81–87CrossRefGoogle Scholar
  30. Grabber JH, Mertens DR, Kim H, Funk C, Lu FC, Ralph J (2009) Cell wall fermentation kinetics are impacted more by lignin content and ferulate cross-linking than by lignin composition. J Sci Food Agric 89:122–129CrossRefGoogle Scholar
  31. Haider K, Lim S, Flaig W (1964) Experimente und Theorien über den Ligninabbau bei der Weißfäule des Holzes und bei der Verrottung pflanzlicher Substanz im Boden. Holzforschung 18:81–88CrossRefGoogle Scholar
  32. Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier MT, Schuch W (1994) Manipulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J 6:339–350CrossRefGoogle Scholar
  33. Hammel KE (1997) Fungal degradation of lignin. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, pp 33–46Google Scholar
  34. Hansen J, Møller I (1975) Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal Biochem 68:87–94CrossRefGoogle Scholar
  35. Hatfield RD, Grabber J, Ralph J, Brei K (1999) Using the acetyl bromide assay to determine lignin concentrations in herbaceous plants: some cautionary notes. J Sci Food Agric 47:628–632CrossRefGoogle Scholar
  36. Hedges J, Mann D (1979) The characterization of plant tissues by their lignin oxidation products. Geochim Cosmochim Ac 43:1803–1807CrossRefGoogle Scholar
  37. Hedges JI, Cowie GL, Ertel JR, James Barbour R, Hatcher PG (1985) Degradation of carbohydrates and lignins in buried woods. Geochim Cosmochim Ac 49:701–711CrossRefGoogle Scholar
  38. Hedges J, Blanchette R, Weliky K, Devol A (1988) Effects of fungal degradation on the CuO oxidation products of lignin: a controlled laboratory study. Geochim Cosmochim Ac 52:2717–2726CrossRefGoogle Scholar
  39. Hemm MR, Ruegger MO, Chapple C (2003) The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glucosinolate phenotypes. Plant Cell 15:179–194CrossRefGoogle Scholar
  40. Hénault C, English L, Halpin C, Andreux F, Hopkins D (2006) Microbial community structure in soils with decomposing residues from plants with genetic modifications to lignin biosynthesis. FEMS Microbiol Let 263:68–75CrossRefGoogle Scholar
  41. Hobbie SE (2005) Contrasting effects of substrate and fertilizer nitrogen on the early stages of litter decomposition. Ecosystems 8:644–656CrossRefGoogle Scholar
  42. Howard P, Frankland J (1974) Effects of certain full and partial sterilization treatments on leaf litter. Soil Biol Biochem 6:117–123CrossRefGoogle Scholar
  43. Huang Y, Stankiewicz B, Eglinton G, Snape C, Evans B, Latter P, Ineson P (1998) Monitoring biomacromolecular degradation of Calluna vulgaris in a 23 year field experiment using solid state 13C-NMR and pyrolysis-GC/MS. Soil Biol Biochem 30:1517–1528CrossRefGoogle Scholar
  44. Iiyama K, Wallis AFA (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:145–161CrossRefGoogle Scholar
  45. Jung HJG, Buxton DR (1994) Forage quality variation among maize inbreds—relationships of cell-wall composition and in vitro degradability for stem internodes. J Sci Food Agric 66:313–322CrossRefGoogle Scholar
  46. Jung HG, Casler MD (1991) Relationship of lignin and esterified phenolics to fermentation of smooth bromegrass fiber. Anim Feed Sci Tech 32:63–68CrossRefGoogle Scholar
  47. Jung HJG, Vogel KP (1992) Lignification of switchgrass (Panicum virgatum) and big bluestem (Andropogon Gerardii) plant-parts during maturation and its effect on fiber degradability. J Sci Food Agric 59:169–176CrossRefGoogle Scholar
  48. Jung HG, Smith RR, Endres CS (1994) Cell-wall composition and degradability of stem tissue from lucerne divergently selected for lignin and in vitro dry-matter disappearance. Grass Forage Sci 49:295–304CrossRefGoogle Scholar
  49. Jung HJG, Ni WT, Chapple CCS, Meyer K (1999) Impact of lignin composition on cell-wall degradability in an Arabidopsis mutant. J Sci Food Agric 79:922–928CrossRefGoogle Scholar
  50. Kato Y, Nevins D (1985) Isolation and identification of O-(5-O-feruloyl-[alpha]-l-arabinofuranosyl)-1(-→3)-O-[beta]-d-xylopyranosyl-(1→)-d-xylopyranose as a component of Zea shoot cell-walls. Carbohyd Res 137:139–150CrossRefGoogle Scholar
  51. Kim H, Ralph J, Akiyama T (2008) Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d(6). BioEnergy Res 1:56–66CrossRefGoogle Scholar
  52. King S, Harden J, Manies KL, Munster J, White LD (2002) Fate of carbon in Alaskan landscape project—database for soils from eddy covariance tower sites. U. S. Geological Survey, Delta Junction, Menlo ParkGoogle Scholar
  53. Kirk TK, Farrell RL (1987) Enzymatic combustion—the microbial-degradation of lignin. Annu Rev Microbiol 41:465–505CrossRefGoogle Scholar
  54. Kirk TK, Chang H-m, Lorenz LF (1975) Topochemistry of the fungal degradation of lignin in birch wood as related to the distribution of guaiacyl and syringyl lignins. Wood Sci Technol 9:81–86CrossRefGoogle Scholar
  55. Kögel I (1986) Estimation and decomposition pattern of the lignin component in forest humus layers. Soil Biol Biochem 18:589–594CrossRefGoogle Scholar
  56. Li X, Ximenes E, Kim Y, Slininger M, Meilan R, Ladisch M, Chapple C (2010) Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment. Biotechnology for Biofuels 3:27–33CrossRefGoogle Scholar
  57. Machinet GE, Bertrand I, Chabbert B, Recous S (2009) Decomposition in soil and chemical changes of maize roots with genetic variations affecting cell wall quality. Eur J Soil Sci 60:176–185CrossRefGoogle Scholar
  58. Mack MC, Treseder KK, Manies KL, Harden JW, Schuur EAG, Vogel JG, Randerson JT, Chapin FS (2008) Recovery of aboveground plant biomass and productivity after fire in mesic and dry black spruce forests of interior Alaska. Ecosystems 11:209–225CrossRefGoogle Scholar
  59. Marita JM, Ralph J, Hatfield RD, Chapple C (1999) NMR characterization of lignins in Arabidopsis altered in the activity of ferulate 5-hydroxylase. P Natl Acad Sci USA 96:12328–12332CrossRefGoogle Scholar
  60. Marschner B, Brodowski S, Dreves A, Gleixner G, Gude A, Grootes P, Hamer U, Heim A, Jandl G, Ji R (2008) How relevant is recalcitrance for the stabilization of organic matter in soils? J Plant Nutr Soil Sci 171:91–110CrossRefGoogle Scholar
  61. Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472CrossRefGoogle Scholar
  62. Melillo JM, Aber JD, Muratore JM (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  63. Moore T, Trofymow J, Taylor B, Prescott C, Camire C, Duschene L, Fyles J, Kozak L, Kranabetter M, Morrison I (1999) Litter decomposition rates in Canadian forests. Glob Change Biol 5:75–82CrossRefGoogle Scholar
  64. Nierop KGJ, Filley TR (2007) Assessment of lignin and (poly-)phenol transformations in oak (Quercus robur) dominated soils by 13C-TMAH thermochemolysis. Org Geochem 38:551–565CrossRefGoogle Scholar
  65. Nierop KGJ, Van Lagen B, Buurman P (2001) Composition of plant tissues and soil organic matter in the first stages of a vegetation succession. Geoderma 100:1–24CrossRefGoogle Scholar
  66. Nilsson T, Daniel G (1989) Chemistry and microscopy of wood decay by some higher ascomycetes. Holzforschung 43:11–18CrossRefGoogle Scholar
  67. Opsahl S, Benner R (1995) Early diagenesis of vascular plant tissues: lignin and cutin decomposition and biogeochemical implications. Geochim Cosmochim Ac 59:4889–4904CrossRefGoogle Scholar
  68. Otto A, Simpson M (2006) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochem 80:121–142CrossRefGoogle Scholar
  69. Provan GJ, Scobbie L, Chesson A (1997) Characterisation of lignin from CAD and OMT deficient BM mutants of maize. J Sci Food Agric 73:133–142CrossRefGoogle Scholar
  70. Ralph J, Hatfield RD, Piquemal J, Yahiaoui N, Pean M, Lapierre C, Boudet AM (1998) NMR characterization of altered lignins extracted from tobacco plants down-regulated for lignification enzymes cinnamyl-alcohol dehydrogenase and cinnamoyl-CoA reductase. P Natl Acad Sci USA 95:12803–12808CrossRefGoogle Scholar
  71. Ralph J, Marita JM, Ralph S, Hatfield RD, Lu F, Ede RM, Peng J, Landucci LL (1999) Solution state NMR of lignins. In: Argyropoulos DS (ed) Advances in lignocellulosics characterization. TAPPI Press, Atlanta, pp 55–108Google Scholar
  72. Ralph J, Lapierre C, Marita J, Kim H, Lu F, Hatfield R, Ralph S, Chapple C, Franke R, Hemm M (2001) Elucidation of new structures in lignins of CAD-and COMT-deficient plants by NMR. Phytochem 57:993–1003CrossRefGoogle Scholar
  73. Ralph S, Landucci L, Ralph J (2005) NMR database of lignin and cell wall model compounds. http://ars.usda.gov/Services/docs.htm?docid=10429
  74. Ralph J, Akiyama T, Kim H, Lu F, Ralph S, Chapple C, Nair R, Wagner A, Chen F, Reddy M (2006a) Lignification in transgenics deficient in 4-coumarate 3-hydroxylase (C3H) or the associated hydroxycinnamoyl transferase (HCT). In: Polyphenols communications 2006, XXIII international conference on polyphenols, Winnipeg, Manitoba, CanadaGoogle Scholar
  75. Ralph J, Akiyama T, Kim H, Lu F, Schatz PF, Marita JM, Ralph SA, Reddy MSS, Chen F, Dixon RA (2006b) Effects of coumarate 3-hydroxylase down-regulation on lignin structure. J Biol Chem 281:8843–8853CrossRefGoogle Scholar
  76. Ramiah MV (1970) Thermogravimetric and differential thermal analysis of cellulose, hemicellulose, and lignin. J Appl Polym Sci 14:1323–1337CrossRefGoogle Scholar
  77. Rencoret J, Marques G, Gutierrez A, Nieto L, Jimenez-Barbero J, Martinez AT, del Rio JC (2009) Isolation and structural characterization of the milled-wood lignin from Paulownia fortunei wood. Ind Crop Prod 30:137–143CrossRefGoogle Scholar
  78. Schlesinger WH (1997) Biogeochemistry: an analysis of global change. Academic Press, San DiegoGoogle Scholar
  79. Sibout R, Eudes A, Pollet B, Goujon T, Mila I, Granier F, Seguin A, Lapierre C, Jouanin L (2003) Expression pattern of two paralogs encoding cinnamyl alcohol dehydrogenases in Arabidopsis. Isolation and characterization of the corresponding mutants. Plant Physiol 132:848–860CrossRefGoogle Scholar
  80. Soja AJ, Tchebakova NM, French NHF, Flannigan MD, Shugart HH, Stocks BJ, Sukhinin AI, Parfenova EI, Chapin Iii FS, Stackhouse JPW (2007) Climate-induced boreal forest change: predictions versus current observations. Global Planet Change 56:274–296CrossRefGoogle Scholar
  81. Tai D, Terasawa M, Chen C, Chang H, Kirk T (1983) Biodegradation of guaiacyl and guaiacyl-syringyl lignins in wood by Phanerochaete chrysosporium. In: Recent advances in lignin biodegradation research: fundamentals and biotechnology. Uni Publishers, Tokyo, pp 44–63Google Scholar
  82. Takacs L, McHenry JS (2006) Temperature of the milling balls in shaker and planetary mills. J Mater Sci 41:5246–5249CrossRefGoogle Scholar
  83. Theander O, Aman P, Westerlund E, Andersson R, Petersson D (1995) Total dietary fiber determined as neutral sugar residues, uronic acid residues, and klason lignin (The Uppsala method): collaborative study. Journal of Aoac International 78:1030–1044Google Scholar
  84. Thevenot M, Dignac M, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42:1200–1211CrossRefGoogle Scholar
  85. Thorstensson EMG, Buxton DR, Cherney JH (1992) Apparent inhibition to digestion by lignin in normal and brown midrib stems. J Sci Food Agric 59:183–188CrossRefGoogle Scholar
  86. Treseder KK, Turner KM, Mack MC (2007) Mycorrhizal responses to nitrogen fertilization in boreal ecosystems: potential consequences for soil carbon storage. Glob Change Biol 13:78–88CrossRefGoogle Scholar
  87. Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Meth 26:53–59CrossRefGoogle Scholar
  88. Trofymow J, Moore T, Titus B, Prescott C, Morrison I, Siltanen M, Smith S, Fyles J, Wein R, Camiré C (2002) Rates of litter decomposition over 6 years in Canadian forests: influence of litter quality and climate. Can J For Res 32:789–804CrossRefGoogle Scholar
  89. Updegraf D (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–425CrossRefGoogle Scholar
  90. Vailhe MAB, Migne C, Cornu A, Maillot MP, Grenet E, Besle JM, Atanassova R, Martz F, Legrand M (1996) Effect of modification of the O-methyltransferase activity on cell wall composition, ultrastructure and degradability of transgenic tobacco. J Sci Food Agric 72:385–391CrossRefGoogle Scholar
  91. Vailhé MAB, Besle JM, Maillot MP, Cornu A, Halpin C, Knight M (1998) Effect of down-regulation of cinnamyl alcohol dehydrogenase on cell wall composition and on degradability of tobacco stems. J Sci Food Agric 76:505–514CrossRefGoogle Scholar
  92. Webster EA, Halpin C, Chudek JA, Tilston EL, Hopkins DW (2005) Decomposition in soil of soluble, insoluble and lignin-rich fractions of plant material from tobacco with genetic modifications to lignin biosynthesis. Soil Biol Biochem 37:751–760CrossRefGoogle Scholar
  93. Wolf DC, Dao TH, Scott HD, Lavy TL (1989) Influence of sterlilization methods on selected soil microbiological, physical, and chemical-properties. Journal Environ Qual 18:39–44CrossRefGoogle Scholar
  94. Wu D, Ye Q, Wang Z, Xia Y (2004) Effect of gamma irradiation on nutritional components and Cry1Ab protein in the transgenic rice with a synthetic cry1Ab gene from Bacillus thuringiensis. Radiat Phys chem 69:79–83CrossRefGoogle Scholar
  95. Yarie J, Van Cleve K (1996) Effects of carbon, fertilizer, and drought on foliar chemistry of tree species in interior Alaska. Ecol Appl 6:815–827CrossRefGoogle Scholar
  96. Yelle DJ, Ralph J, Frihart CR (2008a) Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy. Magn Reson Chem 46:508CrossRefGoogle Scholar
  97. Yelle DJ, Ralph J, Lu F, Hammel KE (2008b) Evidence for cleavage of lignin by a brown rot basidiomycete. Environ Microbiol 10:1844–1849CrossRefGoogle Scholar
  98. Zech W, Senesi N, Guggenberger G, Kaiser K, Lehmann J, Miano T, Miltner A, Schroth G (1997) Factors controlling humification and mineralization of soil organic matter in the tropics. Geoderma 79:117–161CrossRefGoogle Scholar
  99. Zhang L, Gellerstedt G (2007) Quantitative 2D HSQC NMR determination of polymer structures by selecting suitable internal standard references. Magn Reson Chem 45:37–45CrossRefGoogle Scholar
  100. Zhang D, Hui D, Luo Y, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Jennifer M. Talbot
    • 1
    Email author
  • Daniel J. Yelle
    • 2
  • James Nowick
    • 3
  • Kathleen K. Treseder
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA
  2. 2.USDA Forest ServiceMadisonUSA
  3. 3.Department of ChemistryUniversity of CaliforniaIrvineUSA

Personalised recommendations