Plant and Soil

, Volume 308, Issue 1–2, pp 239–253 | Cite as

The influence of soil type and altered lignin biosynthesis on the growth and above and belowground biomass allocation of Populus tremuloides

  • Jessica E. Hancock
  • Kate L. Bradley
  • Christian P. GiardinaEmail author
  • Kurt S. Pregitzer
Regular Article


Plants influence soil carbon (C) formation through the quality and quantity of C released to soil. Soil type, in turn can modify a plant’s influence on soil through effects on plant production, tissue quality and regulation of soil C decomposition and stabilization. Wild-type aspen and three transgenic aspen lines expressing reduced stem lignin concentrations and/or increased syringyl (S) to guaiacyl (G) ratio lignin were grown in greenhouse mesocosms containing a sandy loam, a silt loam, or a clay loam soil for 6 months in order to examine the effects of altered lignin biosynthesis and soil type on biomass partitioning (above vs. belowground) and soil C processes. Results indicated that soil type significantly affected plant performance. Aspen grown in soils with high sand/low clay content accumulated the most total biomass, while aspen grown in soils with high clay content accumulated the least total biomass. These reductions in growth combined with specific soil characteristics led to differences among soil types in soil C formation. Transformed aspen expressing high syringyl/guaiacyl (S/G) lignin accumulated less total plant C and subsequently accumulated less aspen derived C in soil. Reduced lignin content alone in aspen did not affect plant growth or soil C formation. There were significant soil type × genetic line interactions indicating that growth and soil C formation for transgenic and wild type aspen lines varied among the different soil types. Given these interactions, future investigation needs to include long-term field studies across a range of soil types before transgenic aspen are widely planted.


Biomass allocation Growth physiology Plant productivity Soil carbon formation Soil texture syringyl to guaiacyl ratio 



The authors would like to thank Cassie Miller and Noah Karberg for their assistance in the greenhouse and the lab and Drs. Chung-Jui and Scott Harding for invaluable advice on plant maintenance. Additionally we would like to thank Dr. John Adler and the Department of Biological Sciences at Michigan Technological University for use of greenhouse facilities. We also thank the Pawnee National Grassland, Konza Prairie Biological Station, and the Blackland Research and Extension Center in Temple Texas, for access to soils used in this experiment. Finally, we greatly appreciate funding and support from the US Department of Energy, the Northern and Pacific Southwest Research Stations of the USDA Forest Service, and the graduate school of Michigan Technological University.


  1. Amthor JS (2003) Efficiency of lignin biosynthesis: a quantitative analysis. Ann Botony 9:673–695CrossRefGoogle Scholar
  2. Anderson TM, Dong Y, McNaughton SJ (2006) Nutrient acquisition and physiological responses of dominant Serengeti grasses to variation in soil texture and grazing. J Ecol 94:1164–1175CrossRefGoogle Scholar
  3. Atjay G, Ketner P, Duvigneaud D (1979) Terrestrial primary production and phytomass. In: Bolin B, Degens E, Kempe S, Ketner P (eds) The global C cycle. Wiley, Chichester, UK, pp 129–181Google Scholar
  4. Barnes BV, Wagner WH (2004) Michigan trees. University of Michigan Press, Ann Arbor, p 447Google Scholar
  5. Baucher M, Chabbert B, Pilate G, Van Doorsselaere J, Tollier M-T, Petit-Conil M, Cornu D, Monties B, Van Montagu M, Inzé D, Jouanin L, Boerjan W (1996) Red xylem and higher lignin extraction extractability by down regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479–1490PubMedGoogle Scholar
  6. Baucher M, Halpin C, Petit-Conil M, Boerjan W (2003) Lignin: Genetic engineering and impact on pulping. Crit Rev Biochem Mol Biol 38:305–350PubMedCrossRefGoogle Scholar
  7. Berg B, Lundmark J-E (1985) Decomposition of needles and root litter in lodgepole pine and Scots pine monocultural systems. Plant Soil 138:123–132Google Scholar
  8. Bonde T, Christensen BT, Cerri CC (1992) Dynamics of organic matter as reflected by natural 13C abundance in the particle size fractions of forested and cultivated oxisols. Soil Biol Biochem 24:275–277CrossRefGoogle Scholar
  9. Bouma TJ, Bryla DR (2000) On the assessment of root and soil respiration for soils of different textures: interactions with soil moisture contents and soil CO2 concentrations. Plant Soil 227:215–221CrossRefGoogle Scholar
  10. Bradley KL, Hancock JE, Giardina CP, Pregitzer KS (2007) Soil microbial community responses to altered lignin biosynthesis in Populus tremuloides vary among three distinct soils. Plant Soil 294:185–201CrossRefGoogle Scholar
  11. Bradshaw HD, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313CrossRefGoogle Scholar
  12. Brady NC, Weil RR (2002) The nature and properties of soils. Prentice Hall, Upper Saddle River, p 960Google Scholar
  13. Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56PubMedCrossRefGoogle Scholar
  14. Chen C, Baucher M, Christensen JH, Boerjan W (2001) Biotechnology in trees: towards improved paper pulping by lignin engineer. Euphytica 118:185–195CrossRefGoogle Scholar
  15. Christensen BT (1987) Decomposability of organic matter in particle size fractions from field soils with straw incorporation. Soil Biol Biochem 19:429–435CrossRefGoogle Scholar
  16. Cox MS, Gerard PD, Abshire MJ (2006) Selected soil properties’ variability and their relationships with yield in three Mississippi fields. Soil Sci 171:541–551CrossRefGoogle Scholar
  17. Desjardins T, Andreux F, Volkoff B, Cerri CC (1994) Organic carbon and 13C contents in soils and soil size fractions, and their changes due to deforestation and pasture installation in eastern Amazonia. Geoderma 61:103–108CrossRefGoogle Scholar
  18. Fisher RF, Binkley D (2000) Ecology and management of forest soils. Wiley, New York, p 489Google Scholar
  19. Frostegård Å, Tunlid A, Bååth E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14:151–163CrossRefGoogle Scholar
  20. Gale WJ, Cambardella CA, Bailey TB (2000) Root-derived C and the formation and stabilization of aggregates. Soil Sci Soc Am J 64:201–207Google Scholar
  21. Giardina CP, Ryan MG, Hubbard RM, Binkley D (2001) Tree species and soil textural controls on carbon and nitrogen mineralization rates. Soil Sci Soc Am J 65:1272–1279Google Scholar
  22. Graham SA, Harrison RP, Westell CE (1963) Aspens: Phoenix trees of the great lakes region. University of Michigan Press, Ann Arbor, p 272Google Scholar
  23. Gustafson EJ, Lietz SM, Wright JL (2003) Predicting the spatial distribution of aspen growth potential in the upper great lakes region. For Scie 49:499–508Google Scholar
  24. Halpin C, Thain SC, Tilston EL, Guiney E, Lapierre C, Hopkins DW (2007) Ecological impacts of trees with modified lignin. Tree Genet Genomes 3:101–110CrossRefGoogle Scholar
  25. Hancock JE, Loya WM, Giardina CP, Li L, Chiang VL, Pregitzer KS (2007) Plant growth, biomass partitioning and soil carbon formation in response to altered lignin biosynthesis in Populus tremuloides. New Phytol 173:732–742PubMedCrossRefGoogle Scholar
  26. Harding SA, Leshkevich J, Chiang VL, Tsai C-J (2002) Differential substrate inhibition couples kinetically distinct 4-coumarate:conenzyme A ligases with spatially distinct metabolic roles in quaking aspen. Plant Physiol 128:428–438PubMedCrossRefGoogle Scholar
  27. Hassink J (1997) The capacity of soils to preserve organic C and N by their association with clay and silt particles. Plant Soil 191:77–87CrossRefGoogle Scholar
  28. Herrera S (2005) Struggling to see the forest through the trees. Nature Biotechnol 23:165–167CrossRefGoogle Scholar
  29. Ho CK, Chang S-H, Tsay J-Y, Tsai C-J, Chiang VL, Chen Z-Z (1998) Agrobacterium tumefaciens-mediated transformation in Eucalyptus camaldulensis and production of transgenic plants. Plant Cell Rep 17:675–680CrossRefGoogle Scholar
  30. Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R, Hale C, Karolewski P (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297PubMedCrossRefGoogle Scholar
  31. Hu W-J, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai C-J, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol 17:808–812CrossRefGoogle Scholar
  32. Jenkinson DS (1988) Soil organic matter and its dynamics. In: Wild A (ed) Russel’s soil conditions and plant growth. Longman, New York, pp 564–607Google Scholar
  33. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  34. Kuzyakov Y, Domanski G (2000) Carbon inputs by plants into the soil. Rev J Plant Nutr Soil Sci 163:421–431CrossRefGoogle Scholar
  35. Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100:4939–4944PubMedCrossRefGoogle Scholar
  36. Lorenz K, Lal R (2005) The depth distribution of soil organic carbon in relation to land use and management and the potential of carbon sequestration in subsoil horizons. Adv Agron 88:35–66CrossRefGoogle Scholar
  37. Meentemeyer V (1978) Macroclimate and lignin control of litter decomposition rates. Ecology 59:465–472CrossRefGoogle Scholar
  38. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  39. Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long term decomposition. Science 315:361–364PubMedCrossRefGoogle Scholar
  40. Pastor J, Post WM (1986) Influence of climate, soil moisture, and succession on forest carbon and nitrogen cycles. Biogeochemistry 2:3–27CrossRefGoogle Scholar
  41. Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–612PubMedCrossRefGoogle Scholar
  42. Russell AE, Raich JW, Valverde-Barrantes OJ, Fisher RF (2007) Tree species effects on soil properties in experimental plantations in tropical moist forest. Soil Sci Soc Amer J 71:1389–1397CrossRefGoogle Scholar
  43. Schimel DS, Braswell BH, Holland EA, Mckeown R, Ojima DS, Painter TH, Parton WJ, Townsend AR (1994) Climatic, edaphic, and biotic controls over storage and turnover of C in soils. Glob Biogeochem Cycles 8:279–293CrossRefGoogle Scholar
  44. Silver WL, Neff J, McGroddy M, Veldkamp E, Keller M, Cosme R (2000) Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian forest ecosystem. Ecosystems 3:193–209CrossRefGoogle Scholar
  45. Six J, Conant RT, Paul A, Paustian K (2002) Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils. Plant Soil 241:155–176CrossRefGoogle Scholar
  46. Sorensen LH (1972) Stabilization of newly formed amino acid metabolites in soil by clay minerals. Soil Sci 114:5–11CrossRefGoogle Scholar
  47. Stevenson FJ (1994) Humus Chemistry: genesis, composition, reactions. Wiley, New York, p 512Google Scholar
  48. Strauss SH, DiFazio SP, Meilan R (2001) Genetically modified poplars in context. For Chron 77:271–279Google Scholar
  49. Thornton B, Paterson E, Midwood A, Sim A, Pratt SM (2004) Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labeling. Physiol Plant 120:434–441PubMedCrossRefGoogle Scholar
  50. Tilston EL, Halpin C, Hopkins DW (2004) Genetic modifications to lignin biosynthesis in field-grown poplar trees have inconsistent effects on the rate of woody trunk decomposition. Soil Biol Biochem 36:1903–1906CrossRefGoogle Scholar
  51. Torn MS, Trumbore SE, Vitousek PM (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173CrossRefGoogle Scholar
  52. Tsai C-J, Podila GK, Chiang VL (1994) Agrobacterium-mediated transformation of quaking aspen (Populus tremuloides) and regeneration of transgenic plants. Plant Cell Rep 14:64–97CrossRefGoogle Scholar
  53. Tsai C-J, Popko JL, Miclke MR, Hu W-J, Podila GK, Chiang VL (1998) Suppression of O-methyltransferase gene by homologous sense transgene in quaking aspen causes red-brown wood pheonotypes. Plant Physiol 117:101–112PubMedCrossRefGoogle Scholar
  54. Van Veen JA, Kuikman PJ (1990) Soil Structural aspects of decomposition of organic matter by microorganisms. Biogeochem 11:213–233CrossRefGoogle Scholar
  55. Zak DR, Tilman D, Parmenter RR, Rice CW, Fisher FM, Vose J, Michunas D, Martin CW (1994) Plant production and soil microorganisms in late successional ecosystems: a continental-scale study. Ecology 75:2333–2347CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Jessica E. Hancock
    • 1
  • Kate L. Bradley
    • 1
  • Christian P. Giardina
    • 2
    Email author
  • Kurt S. Pregitzer
    • 3
  1. 1.Ecosystem Science Center, School of Forest Resources and Environmental ScienceMichigan Technological UniversityHoughtonUSA
  2. 2.PSW Research StationInstitute of Pacific Islands Forestry-USDA Forest ServiceHiloUSA
  3. 3.Department of Natural ResourcesUniversity of NevadaRenoUSA

Personalised recommendations