Abstract
Proximate analysis (PA) is widely used to assess foliar, litter, and wood quality. The acid-unhydrolyzable residue (AUR) of PA, originally known as Klason lignin from wood analysis, is often assumed to be entirely lignin-derived, but the AUR of much plant material also includes contributions from condensed tannins (CT) and cutin or suberin. To improve understanding of chemical changes throughout the PA procedure, we characterized seven foliar litters and their sequential PA fractions (nonpolar and hot-water extracted, AUR). Changes in total C and N, extractable and insoluble CT (as detected by butanol/HCl hydrolysis), δ13C values and solid-state 13C NMR spectra were consistent with loss of carbohydrates and protein after acid hydrolysis, and support previous studies that the AUR residue includes lignin, cutin and CT, all of which are depleted in δ13C. Hot-water extraction removed the bulk of extractable plus insoluble CT. Only trace levels were detected in the AUR, although 13C NMR shows that these are likely underestimates. The assumption of lignin-AUR equivalence still causes misinterpretation of PA results for many sample categories. It is time for the scientific community to limit use of “lignin” to chemically meaningful contexts?
Similar content being viewed by others
Abbreviations
- AUR:
-
Acid unhydrolyzable residue
- CP:
-
Cross polarization
- CT:
-
Condensed tannin
- DD:
-
Dipolar dephasing
- MAS:
-
Magic-angle spinning
- NMR:
-
Nuclear magnetic resonance
- NPR:
-
Residue after nonpolar (dichloromethane) extraction
- PA:
-
Proximate analysis
- TP:
-
Total phenolics
- SSB:
-
Spinning sidebands
- TOSS:
-
Total suppression of sidebands
- WSR:
-
Residue after dichloromethane and hot water extraction
- %REM:
-
Percent remaining
References
Almendros G, Dorado J, González-Vila FJ, Blanco MJ, Lankes U (2000) 13C NMR assessment of decomposition patterns during composting of forest and shrub biomass. Soil Biol Biochem 32:793–804
Baldock JA, Masiello CA, Gélinas Y, Hedges JI (2004) Cycling and composition of organic matter in terrestrial and marine ecosystems. Mar Chem 92:39–64
Benner R, Fogel ML, Sprague EK, Hodson RE (1987) Depletion of 13C in lignin and its implications for stable isotope studies. Nature 329:708–710
Bowling DR, Pataki DE, Randerson JT (2008) Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol 178:24–40
Bradley R (2002) Dynamics of nitrogen associated to acid insoluble substances derived from plant litter. Commun Soil Sci Plant Anal 33:1277–1290
Bunzel M, Schüssler A, Saha GT (2011) Chemical characterization of Klason lignin preparations from plant-based foods. J Agric Food Chem 59:12506–12513
Chabbi A, Rumpel C, Kögel-Knabner I (2007) Stable carbon isotope signature and chemical composition of organic matter in lignite-containing mine soils and sediments are closely linked. Org Geochem 38:835–844
Effland MJ (1977) Modified procedure to determine acid-insoluble lignin in wood and pulp. Tappi 60:143–144
Ferrer J-L, Austin MB, Stewart C Jr, Noel JP (2008) Structure and function of enzymes involved in the biosynthesis of phenypropanoids. Plant Physiol Biochem 46:356–370
Gea A, Stringano E, Brown RH, Mueller-Harvey I (2011) In situ analysis and structural elucidation of sainfoin (Onobrychis viciifolia) tannins for high-throughput germplasm screening. J Agric Food Chem 59:495–503
Goñi MA, Hedges JI (1990) Potential applications of cutin-derived CuO reaction products for discriminating vascular plant sources in natural environments. Geochim Cosmochim Acta 54:3073–3081
Gonzales GB, Smagghe G, Raes K, Van Camp J (2014) Combined alkaline hydrolysis and ultrasound-assisted extraction for the release of nonextractable phenolics from cauliflower (Brassica oleracea var. botrytis) waste. J Agric Food Chem 62:3371–3376
Grabber JH, Zeller WE, Mueller-Harvey I (2013) Acetone enhances the direct analysis of procyanidin- and prodelphinidin-based condensed tannins in Lotus species by the butanol-HCl-iron assay. J Agric Food Chem 61:2669–2678
Harun J, Labosky P Jr (1985) Chemical constituents of five northeastern barks. Wood Fiber Sci 17:274–280
Haw JF, Maciel GE, Schroeder HA (1984) Carbon-13 nuclear magnetic resonance spectrometric study of wood and wood pulping with cross polarization and magic-angle spinning. Anal Chem 56:1323–1329
Hilli S, Stark S, Willför S, Smeds A, Reunanen M, Hautajärvi R (2012) What is the composition of AIR? Pyrolysis-GC-MS characterization of acid-insoluble residue from fresh litter and organic horizons under boreal forests in southern Finland. Geoderma 179–180:63–72
Jin Z, Akiyama A, Chung BY, Matsumoto Y, Iiyama K, Watanabe S (2003) Changes in lignin content of leaf litters during mulching. Phytochemistry 64:1023–1031
Joanisse GD, Bradley RL, Preston CM, Munson AD (2007) Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. New Phytol 175:535–546
Klotzbücher T, Filley TR, Kaiser K, Kalbitz K (2011) A study of lignin degradation in leaf and needle litter using 13C-labelled tetramethylammonium hydroxide (TMAH) and thermochemolysis: comparison with CuO oxidation and van Soest methods. Org Geochem 42:1271–1278
Kosonen M, Keski-Saari S, Ruuhola T, Constabel PC, Julkunen-Tiitto R (2012) Effects of overproduction of condensed tannins and elevated temperature on chemical and ecological traits of genetically modified hybrid aspens (Populus tremula × P. tremuloides). J Chem Ecol 38:1235–1246
Leary GJ, Newman RH, Morgan KR (1986) A carbon-13 nuclear magnetic resonance study of chemical processes involved in the isolation of Klason lignin. Holzforschung 40:267–272
Lorenz K, Preston CM (2002) Characterization of high-tannin fractions from humus by carbon-13 cross-polarization and magic-angle spinning nuclear magnetic resonance. J Environ Qual 31:431–436
Makkar HPS, Gamble G, Becker K (1999) Limitation of the butanol-hydrochloric acid-iron assay for bound condensed tannins. Food Chem 66:129–133
Marín-Spiotta E, Gruley KE, Crawford J, Atkinson EE, Miesel JR, Greene S, Cardona-Correa C, Spencer RGM (2014) Paradigm shifts in soil organic matter research affect interpretations of aquatic carbon cycling: transcending disciplinary and ecosystem boundaries. Biogeochemistry 117:279–297
Marles MAS, Coulman BE, Bett KE (2008) Interference of condensed tannin in lignin analyses of dry bean and forage crops. J Agric Food Chem 56:9797–9802
Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472
Melillo JM, Aber JD, Linkins AE, Ricca A, Fry B, Nadelhoffer KJ (1989) Carbon and nitrogen dynamics along the decay continuun: plant litter to soil organic matter. Plant Soil 115:189–198
Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941
Naczk M, Amarowicz R, Pink D, Shahidi F (2000) Insoluble condensed tannins of canola/rapeseed. J Agric Food Chem 48:1758–1762
Nierop KGJ, Preston CM, Kaal J (2005) Thermally assisted hydrolysis and methylation of purified tannins from plants. Anal Chem 77:5604–5614
Nierop KGJ, Speelman EN, de Leeuw JW, Reichart G-J (2011) The omnipresent water fern Azolla caroliniana does not contain lignin. Org Geochem 42:846–850
Norris CE, Preston CM, Hogg KE, Titus BD (2011) The influence of condensed tannin structure on rate of microbial mineralization and reactivity to chemical assays. J Chem Ecol 37:311–319
Pérez-Jiménez J, Torres JL (2011) Analysis of nonextractable phenolic compounds in foods: the current state of the art. J Agric Food Chem 59:12713–12724
Pan D-R , Tai D-S, Chen C-L (1990) Comparative studies on chemical composition of wood components in recent and ancient woods of Bischofia polycarpa. Holzforschung 44:7–16
Preston CM (1999) Condensed tannins of salal (Gaultheria shallon Pursh): a contributing factor to seedling “growth-check” on northern Vancouver Island? In: Gross GG, Hemingway RW, Yoshida T (eds) Plant polyphenols 2: chemistry, biology, pharmacology, ecology. Kluwer Academic/Plenum Publishers, New York, pp 825–841
Preston CM (2014) Environmental NMR: solid-state methods. eMagRes 3:29–42. doi:10.1002/9780470034590.emrstm1338
Preston CM (2015) Environmental NMR—the early years. Magn Reson Chem 53:635–647
Preston CM, Sollins P, Sayer BG (1990) Changes in organic components for fallen logs in old-growth Douglas-fir forests monitored by 13C nuclear magnetic resonance spectroscopy. Can J For Res 20:1382–1391
Preston CM, Trofymow JA, Sayer BG, Niu J (1997) 13C nuclear magnetic resonance spectroscopy with cross-polarization and magic-angle spinning investigation of the proximate-analysis fractions used to assess litter quality in decomposition studies. Can J Bot 75:1601–1613
Preston CM, Trofymow JA, Niu J, Fyfe CA (1998) CPMAS 13C NMR spectroscopy and chemical analysis of coarse woody debris in coastal forests of Vancouver Island. For Ecol Manag 111:51–68
Preston CM, Trofymow JA, Canadian Intersite Decomposition Experiment Working Group (2000) Variability in litter quality and its relationship to litter decay in Canadian forests. Can J Bot 78:1269–1287
Preston CM, Trofymow JA, Flanagan LB (2006) Decomposition, δ13C, and the ‘lignin paradox’. Can J Soil Sci 86:235–245
Preston CM, Nault JR, Trofymow JA, Smyth C, CIDET Working Group (2009a) Chemical changes during 6 years of decomposition of 11 litters in some Canadian forest sites. Part 1. Elemental composition, tannins, phenolics, and proximate fractions. Ecosystems 12:1053–1077
Preston CM, Nault JR, Trofymow JA (2009b) Chemical changes during 6 years of decomposition of 11 litters in some Canadian forest sites. Part 2. 13C abundance, solid-state 13C NMR spectroscopy and the meaning of “lignin”. Ecosystems 12:1078–1102
Preston CM, Norris CE, Bernard GM, Beilman DW, Quideau SA, Wasylishen RE (2014) Carbon and nitrogen in the silt-size fraction and its HCl-hydroysis residues from coarse-textured Canadian boreal forest soils. Can J Soil Sci 94:157–168
Reeves JB III, Schmidt WF (1994) Solid-state 13C NMR analysis of forage and byproduct-derived fiber and lignin residues. Resolution of some discrepancies among chemical, infrared, and pyrolysis-gas chromatography-mass spectroscopic analyses. J Agric Food Chem 42:1462–1468
Ryan MG, Mellilo JM, Ricca A (1990) A comparison of methods for determining proximate carbon fractions of forest litter. Can J For Res 20:166–171
Sluitter JB, Ruiz RO, Scarlata CJ, Sluiter AD, Templeton DW (2010) Compositional analysis of lignocellulosic feedstocks. 1. Review and description of methods. J Agric Food Chem 58:9043–9053
Stewart CE, Moturi P, Follett RF, Halvorson AD (2015) Lignin biochemistry and soil N determine crop residue decomposition and soil priming. Biogeochemistry 124:335–351
Thevenot M, Dignac M-F, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42:1200–1211
Trofymow JA, Preston CM, Prescott CE (1995) Litter quality and its potential effect on decay rates of materials from Canadian forests. Water Air Soil Pollut 82:215–226
van Groenigen J-W, van Kessel C (2002) Salinity-induced patterns of natural abundance carbon-13 and nitrogen-15 in plant and soil. Soil Sci Soc Am J 66:489–498
Walia A, Guy RD, White B (2010) Carbon isotope discrimination in western hemlock and its relationship to mineral nutrition and growth. Tree Physiol 30:728–740
White BL, Howard LR, Prior RL (2010) Release of bound proanthocyanidins from cranberry pomace by alkaline hydrolysis. J Agric Food Chem 58:7572–7579
Williams CJ, Yavitt JB, Wieder RK, Cleavitt NL (1998) Cupric oxide oxidation products of northern peat and peat-forming plants. Can J Bot 76:51–62
Wilson MA, Sawyer J, Hatcher PG, Lerch HE III (1989) 1,3,5-Hydroxybenzene structures in mosses. Phytochemistry 28:1395–1400
Xie L, Roto AV, Bolling BW (2012) Characterization of ellagitannins, gallotannins, and bound proanthocyanidins from California almond (Prunus dulcis) varieties. J Agric Food Chem 60:12151–12156
Yu Z, Dahlgren RA (2000) Evaluation of methods for measuring polyphenols in conifer foliage. J Chem Ecol 26:2119–2140
Zech W, Johansson M-J, Haumaier L, Malcolm RL (1987) CPMAS 13C NMR and IR spectra of spruce and pine litter and of the Klason lignin fraction at different stages of decomposition. Z Pflanzenernähr Bodenk 150:262–265
Acknowledgments
Litter C and N analyses were completed by the PFC Chemical Service Lab. We thank Peter Constabel (University of Victoria) for the poplar tannin. Litter samples were originally collected for the CIDET study by members of the CIDET Working Group (http://cfs-scf.nrcan-rncan.gc.ca/projects/76/1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jonathan Sanderman
An erratum to this article can be found at http://dx.doi.org/10.1007/s10533-016-0242-4.
Rights and permissions
About this article
Cite this article
Preston, C.M., Trofymow, J.A. The chemistry of some foliar litters and their sequential proximate analysis fractions. Biogeochemistry 126, 197–209 (2015). https://doi.org/10.1007/s10533-015-0152-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-015-0152-x