Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes

New Phytologist

Volumn 207, Issue 3, 2015, Pages 505-518

  McCormack, M Luke ^a   Dickie, Ian A ^b   Eissenstat, David M ^c   Fahey, Timothy J ^d   Fernandez, Christopher W ^e   Guo, Dali ^a   Helmisaari, Heljä Sisko ^f   Hobbie, Erik A ^g   Iversen, Colleen M ^h   Jackson, Robert B ⁱ   Leppälammi Kujansuu, Jaana ^f   Norby, Richard J ^h   Phillips, Richard P ^j   Pregitzer, Kurt S ^k   Pritchard, Seth G ^l   Rewald, Boris ^m   Zadworny, Marcin ⁿ  

^a INSTITUTE OF GEOGRAPHIC SCIENCES AND NATURAL RESOURCES RESEARCH   (China)

^b LINCOLN UNIVERSITY   (New Zealand)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d Department of Obstetrics Gynecology   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f UNIVERSITY OF HELSINKI   (Finland)

^g UNIVERSITY OF NEW HAMPSHIRE   (United States)

^h OAK RIDGE NATIONAL LABORATORY   (United States)

ⁱ STANFORD UNIVERSITY   (United States)

^j INDIANA UNIVERSITY   (United States)

^k UNIVERSITY OF IDAHO   (United States)

^l School of Business   (United States)

^m UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

ⁿ INSTITUTE OF DENDROLOGY   (Poland)

more..

Author keywords

Below ground; Ecosystem; Ecosystem modeling; Fine root order; Mycorrhizal fungi; Net primary productivity (NPP); Plant allocation; Plant traits

Indexed keywords

ABSORPTION; BELOWGROUND BIOMASS; BIOGEOCHEMICAL CYCLE; BIOMASS ALLOCATION; BIOSPHERE; ECOSYSTEM MODELING; ESSENTIAL OIL; FINE ROOT; FUNGUS; MYCORRHIZA; NET PRIMARY PRODUCTION; PERENNIAL PLANT; TERRESTRIAL ECOSYSTEM;

FUNGI;

BIOMASS; ECOSYSTEM; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; QUANTITATIVE TRAIT;

BIOMASS; ECOSYSTEM; MYCORRHIZAE; PLANT ROOTS; QUANTITATIVE TRAIT, HERITABLE;

EID: 84936171362     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13363     Document Type: Review

References (111)

1. Adams TS, Eissenstat DM. 2014. The continuous incorporation of carbon into existing Sassafras albidum fine roots and its implications for estimating root turnover. PLoS ONE 9: e95321.
2. Agerer R. 2001. Exploration types of ectomycorrhizae. Mycorrhiza 11: 107-114.
3. Ahrens B, Hansson K, Solly EF, Schrumpf M. 2014. Reconcilable differences: a joint calibration of fine-root turnover times with radiocarbon and minirhizotrons. New Phytologist 204: 932-942.
4. Allen MF, Kitajima K. 2013. In situ high-frequency observations of mycorrhizas. New Phytologist 200: 222-228.
5. Averill C, Turner BL, Finzi AC. 2014. Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505: 543-545.
6. Bagniewska-Zadworna A, Byczyk J, Eissenstat DM, Oleksyn J, Zadworny M. 2012. Avoiding transport bottlenecks in an expanding root system: xylem vessel development in fibrous and pioneer roots under field conditions. American Journal of Botany 99: 1417-1426.
7. Beerling DJ. 2005. Leaf evolution: gases, genes and geochemistry. Annals of Botany 96: 345-352.
8. Böhm W. 1979. Methods of studying root systems. Berlin, Germany: Springer-Verlag.
9. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N. 1996. Working with mycorrhizas in forestry and agriculture. Canberra, ACT, Australia: Australian Centre for International Agricultural Research Canberra.
10. Brzostek ER, Fisher JB, Phillips RP. 2014. Modeling the carbon cost of plant nitrogen acquisition: mycorrhizal trade-offs and multipath resistance uptake improve predictions of retranslocation. Journal of Geophysical Research: Biogeosciences 119: 1684-1697.
11. Burton AJ, Jarvey JC, Jarvi MP, Zak DR, Pregitzer KS. 2012. Chronic N deposition alters root respiration-tissue N relationship in northern hardwood forests. Global Change Biology 18: 258-266.
12. Cannon WA. 1949. A tentative classification of root systems. Ecology 30: 542-548.
13. Chagnon P-L, Bradley RL, Maherali H, Klironomos JN. 2013. A trait-based framework to understand life history of mycorrhizal fungi. Trends in Plant Science 18: 484-491.
14. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. 2009. Towards a worldwide wood economics spectrum. Ecology Letters 12: 351-366.
15. Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD. 2013. Roots and associated fungi drive long-term carbon sequestration in foreal forest. Science 339: 1615-1618.
16. Comas LH, Bouma TJ, Eissenstat DM. 2002. Linking root traits to potential growth rate in six temperate tree species. Oecologia 132: 34-43.
17. Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J. 2005. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytologist 167: 309-319.
18. Dickie IA, Holdaway RJ, eds. 2011. Podocarp roots, mycorrhizas, and nodules. Tropical podocarps. Washington, DC, USA: Smithsonian Institution Scholarly Press.
19. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R. 2014. Nonstructural carbon in woody plants. Annual Review of Plant Biology 65: 667-687.
20. Dybzinski R, Farrior C, Wolf A, Reich PB, Pacala SW. 2011. Evolutionarily stable strategy carbon allocation to foliage, wood, and fine roots in trees competing for light and nitrogen: an analytically tractable, individual-based model and quantitative comparisons to data. American Naturalist 177: 153-166.
21. Espeleta JF, West JB, Donovan LA. 2009. Tree species fine-root demography parallels habitat specialization across a sandhill soil resource gradient. Ecology 90: 1773-1787.
22. Fan P, Guo D. 2010. Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil. Oecologia 163: 509-515.
23. Fernandez CW, Koide RT. 2012. The role of chitin in the decomposition of ectomycorrhizal fungal litter. Ecology 93: 24-28.
24. Fernandez CW, Koide RT. 2013. The function of melanin in the ectomycorrhizal fungus Cenococcum geophilum under water stress. Fungal Ecology 6: 479-486.
25. Fitter A. 1982. Morphometric analysis of root systems: application of the technique and influence of soil fertility on root system development in two herbaceous species. Plant, Cell & Environment 5: 313-322.
26. Freschet GT, Cornelissen JH, van Logtestijn RS, Aerts R. 2010. Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytologist 186: 879-889.
27. Gambetta GA, Fei J, Rost TL, Knipfer T, Matthews MA, Shackel KA, Walker MA, McElrone AJ. 2013. Water uptake along the length of grapevine fine roots: developmental anatomy, tissue-specific aquaporin expression, and pathways of water transport. Plant Physiology 163: 1254-1265.
28. Gaudinski JB, Torn MS, Riley WJ, Dawson TE, Joslin JD, Majdi H. 2010. Measuring and modeling the spectrum of fine-root turnover times in three forests using isotopes, minirhizotrons, and the Radix model. Global Biogeochemical Cycles 24: GB3029.
29. Gill RA, Jackson RB. 2000. Global patterns of root turnover for terrestrial ecosystems. New Phytologist 147: 13-31.
30. 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. Ecological Monographs 81: 89-102.
31. Guo D, Li H, Mitchell RJ, Han W, Hendricks JJ, Fahey TJ, Hendrick RL. 2008b. Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytologist 177: 443-456.
32. Guo D, Mitchell RJ, Withington JM, Fan P-P, Hendricks JJ. 2008a. Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. Journal of Ecology 96: 737-745.
33. Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z. 2008c. Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytologist 180: 673-683.
34. 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: 450-457.
35. Guo Y-Y, Wang J-J, Kong D-L, Wang W, Guo D-L, Wang Y-B, Xie Q-L, Liu Y-S, Zeng H. 2013. Fine root branch orders contribute differentially to uptake, allocation, and return of potentially toxic metals. Environmental Science & Technology 47: 11465-11472.
36. Helmisaari H-S, Derome J, Nöjd P, Kukkola M. 2007. Fine root biomass in relation to site and stand characteristics in Norway spruce and Scots pine stands. Tree Physiology 27: 1493-1504.
37. Helmisaari H-S, Ostonen I, Lõhmus K, Derome J, Lindroos A-J, Merilä P, Nöjd P. 2009. Ectomycorrhizal root tips in relation to site and stand characteristics in Norway spruce and Scots pine stands in boreal forests. Tree Physiology 29: 445-456.
38. Hishi T. 2007. Heterogeneity of individual roots within the fine root architecture: causal links between physiological and ecosystem functions. Journal of Forest Research 12: 126-133.
39. Hobbie EA. 2006. Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87: 563-569.
40. Hobbie EA, Agerer R. 2010. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant and Soil 327: 71-83.
41. Hodge A, Storer K. 2015. Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil 386: 1-19.
42. Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA. 2011. Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. Journal of Ecology 99: 954-963.
43. Iversen CM. 2014. Using root form to improve our understanding of root function. New Phytologist 203: 707-709.
44. Jackson RB, Mooney HA, Schulze ED. 1997. A global budget for fine root biomass, surface area, and nutrient contents. Proceedings of the National Academy of Sciences, USA 94: 7362-7366.
45. Jackson RB, Schenk HJ, Jobbagy EG, Canadell J, Colello GD, Dickinson RE, Field CB, Friedlingstein P, Heimann M, Hibbard K et al. 2000. Belowground consequences of vegetation change and their treatment in models. Ecological Applications 10: 470-483.
46. Jia S, Wang Z, Li X, Zhang X, 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 Physiology 31: 718-726.
47. Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ. 2011. TRY - a global database of plant traits. Global Change Biology 17: 2905-2935.
48. Koide RT, Malcolm GM. 2009. N concentration controls decomposition rates of different strains of ectomycorrhizal fungi. Fungal Ecology 2: 197-202.
49. Kong D, Li L, Ma C, Zeng H, Guo D. 2014. Leading dimensions of root trait variation in subtropical forests. New Phytologist 203: 863-872.
50. Kong D, Ma C. 2014. Acquisition of ephemeral module in roots: a new view and test. Scientific Reports 4: 1-4.
51. Leakey ADB, Ainsworth EA, Bernard SM, Markelz RJC, Ort DR, Placella SA, Rogers A, Smith MD, Sudderth EA, Weston DJ. 2009. Gene expression profiling: opening the black box of plant ecosystem responses to global change. Global Change Biology 15: 1201-1213.
52. Leppälammi-Kujansuu J, Salemaa M, Kleja DB, Linder S, Helmisaari H-S. 2014. Fine root turnover and litter production of Norway spruce in a long-term temperature and nutrient manipulation experiment. Plant and Soil 374: 73-88.
53. Liao Y, McCormack ML, Fan H, Wang H, Wu J, Tu J, Liu W, Guo D. 2014. Relation of fine root distribution to soil C in a Cunninghamia lanceolata plantation in subtropical China. Plant and Soil 381: 225-234.
54. Litton CM, Raich JW, Ryan MG. 2007. Carbon allocation in forest ecosystems. Global Change Biology 13: 2089-2109.
55. Long Y, Kong D, Chen Z, Zeng H. 2013. Variation of the linkage of root function with root branch order. PLoS ONE 8: e57153.
56. Lyford WH. 1980. Development of the root system of northern red oak (Quercus rubra L.). Cambridge, MA, USA: Harvard University, Harvard Forest.
57. Lynch DJ, Matamala R, Iversen CM, Norby RJ, Gonzalez-Meler MA. 2013. Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots. New Phytologist 199: 420-430.
58. Makita N, Hirano Y, Dannoura M, Kominami Y, Mizoguchi T, Ishii H, Kanazawa Y. 2009. Fine root morphological traits determine variation in root respiration of Quercus serrata. Tree Physiology 29: 579-585.
59. Malhi Y, Doughty C, Galbraith D. 2011. The allocation of ecosystem net primary productivity in tropical forests. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 3225-3245.
60. McCormack ML, Adams TS, Smithwick EA, Eissenstat DM. 2012. Predicting fine root lifespan from plant functional traits in temperate trees. New Phytologist 195: 823-831.
61. McCormack ML, Crisfield E, Raczka BM, Schnekenburger F, Eissensat DM, Smithwick EAH. 2015. Sensitivity of four ecological models to adjustments in fine root turnover in temperate forests: does fine root turnover matter? Ecological Modelling 297: 107-117.
62. 2 in a model regenerating longleaf pine-wiregrass ecosystem. Ecosystems 13: 901-916.
63. McMurtrie RE, Iversen CM, Dewar RC, Medlyn BE, Näsholm T, Pepper DA, Norby RJ. 2012. Plant root distributions and nitrogen uptake predicted by a hypothesis of optimal root foraging. Ecology and Evolution 2: 1235-1250.
64. Miller RM, Jastrow JD, Reinhardt DR. 1995. External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103: 17-23.
65. Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, Pitman A, Hemmings FA, Leishman MR. 2009. Global patterns in plant height. Journal of Ecology 97: 923-932.
66. Orwin KH, Kirschbaum MU, St John MG, Dickie IA. 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecology Letters 14: 493-502.
67. Ostle NJ, Smith P, Fisher R, Woodward IF, Fisher JB, Smith JU, Galbraith D, Levy P, Meir P, McNamara NP et al. 2009. Integrating plant-soil interactions into global carbon cycle models. Journal of Ecology 97: 851-863.
68. Ostonen I, Helmisaari HS, Borken W, Tedersoo L, Kukumägi M, Bahram M, Lindroos AJ, Nöjd P, Uri V, Merilä P. 2011. Fine root foraging strategies in Norway spruce forests across a European climate gradient. Global Change Biology 17: 3620-3632.
69. Ostonen I, Lõhmus K. 2003. Proportion of fungal mantle, cortex and stele of ectomycorrhizas in Picea abies (L.) Karst. in different soils and site conditions. Plant and Soil 257: 435-442.
70. Ostonen I, Lõhmus K, Pajuste K. 2005. Fine root biomass, production and its proportion of NPP in a fertile middle-aged Norway spruce forest: comparison of soil core and ingrowth core methods. Forest Ecology and Management 212: 264-277.
71. Ouimette A, Guo D, Hobbie E, Gu J. 2013. Insights into root growth, function, and mycorrhizal abundance from chemical and isotopic data across root orders. Plant and Soil 367: 313-326.
72. Pagés L, Kervella J. 1990. Growth and development of root systems: geometrical and structural aspects. Acta Biotheoretica 38: 289-302.
73. Parton WJ, Hanson PJ, Swanston C, Torn M, Trumbore SE, Riley W, Kelly R. 2010. ForCent model development and testing using the enriched background isotope study experiment. Journal of Geophysical Research-Biogeosciences 115: G04001.
74. Peay KG, Kennedy PG, Bruns TD. 2011. Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecology 4: 233-240.
75. Phillips RP, Brzostek E, Midgley MG. 2013. The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytologist 199: 41-51.
76. 2. Ecology Letters 15: 1042-1049.
77. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL. 2002. Fine root architecture of nine North American trees. Ecological Monographs 72: 293-309.
78. Rasse DP, Rumpel C, Dignac MF. 2005. Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant and Soil 269: 341-356.
79. Rewald B, Raveh E, Gendler T, Ephrath JE, Rachmilevitch S. 2012. Phenotypic plasticity and water flux rates of Citrus root orders under salinity. Journal of Experimental Botany 63: 2717-2727.
80. Rewald B, Rechenmacher A, Godbold DL. 2014. It's complicated - intra-root system variability of respiration and morphological traits in four deciduous tree species. Plant Physiology 166: 736-745.
81. Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami P, Schaberg PG, Xu X. 2013. Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytologist 197: 850-861.
82. 2 enrichment in two California annual grasslands. Oecologia 119: 572-577.
83. Salguero-Gómez R, Casper BB. 2011. Introducing short roots in a desert perennial: anatomy and spatiotemporal foraging responses to increased precipitation. New Phytologist 191: 173-183.
84. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478: 49-56.
85. Silver WL, Miya RK. 2001. Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129: 407-419.
86. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. London, UK: Academic Press.
87. Smithwick EAH, Lucash MS, McCormack ML, Sivandran G. 2014. Improving the representation of roots in terrestrial models. Ecological Modelling 291: 193-204.
88. Steudle E, Peterson CA. 1998. How does water get through roots? Journal of Experimental Botany 49: 775-788.
89. Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R. 2008. Irreconcilable differences: fine-root life spans and soil carbon persistence. Science 319: 456-458.
90. Sun T, Mao Z. 2011. Functional relationships between morphology and respiration of fine roots in two Chinese temperate tree species. Plant and Soil 346: 375-384.
91. Sutton RF, Tinus RW. 1983. Root and root system terminology. Forest Science 29(Suppl 24): 1-138.
92. Taylor BN, Beidler KV, Cooper ER, Strand AE, Pritchard SG. 2013. Sampling volume in root studies: the pitfalls of under-sampling exposed using accumulation curves. Ecology Letters 16: 862-869.
93. Taylor AFS, Martin F, Read DJ. 2000. Fungal diversity in ectomycorrhizal communities of Norway spruce [Picea abies (L.) Karst.] and beech (Fagus sylvatica L.) along north-south transects in Europe. In: Schulze E-D, ed. Carbon and nitrogen cycling in European forest ecosystems. Heidelberg, Germany: Springer, 343-365.
94. 14C content. Forest Ecology and Management 263: 131-137.
95. Thomas RQ, Williams M. 2014. A model using marginal efficiency of investment to analyze carbon and nitrogen interactions in terrestrial ecosystems (ACONITE Version 1). Geoscientific Model Development 7: 2015-2137.
96. Tierney GL, Fahey TJ. 2002. Fine root turnover in a northern hardwood forest: a direct comparison of the radiocarbon and minirhizotron methods. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 32: 1692-1697.
97. Trappe JM. 1965. Tuberculate mycorrhizae of Douglas-fir. Forest Science 11: 27-32.
98. Valenzuela-Estrada LR, Vera-Caraballo V, Ruth LE, Eissenstat DM. 2008. Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). American Journal of Botany 95: 1506-1514.
99. Wallander H, Ekblad A, Godbold DL, Johnson D, Bahr A, Baldrian P, Björk RG, Kieliszewska-Rokicka B, Kjøller R, Kraigher H. 2013. Evaluation of methods to estimate production, biomass and turnover of ectomycorrhizal mycelium in forests soils - a review. Soil Biology and Biochemistry 57: 1034-1047.
100. 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 and Soil 288: 155-171.
101. Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD. 2015. Root structural and functional dynamics in terrestrial biosphere models - evaluation and recommendations. New Phytologist 205: 59-78.
102. Wells CE, Eissenstat DM. 2001. Marked differences in survivorship among apple roots of different diameters. Ecology 82: 882-892.
103. Weston DJ, Gunter LE, Rogers A, Wullschleger SD. 2008. Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants. BMC Systems Biology 2: 16.
104. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428: 821-827.
105. Xia M, Guo D, Pregitzer KS. 2010. Ephemeral root modules in Fraxinus mandshurica. New Phytologist 188: 1065-1074.
106. Xiong Y, Fan P, Fu S, Zeng H, Guo D. 2013. Slow decomposition and limited nitrogen release by lower order roots in eight Chinese temperate and subtropical trees. Plant and Soil 363: 19-31.
107. Yanai RD, McFarlane KJ, Lucash MS, Kulpa SE, Wood DM. 2009. Similarity of nutrient uptake and root dimensions of Engelmann spruce and subalpine fir at two contrasting sites in Colorado. Forest Ecology and Management 258: 2233-2241.
108. Yuan ZY, Chen HYH. 2012. Indirect methods produce higher estimates of fine root production and turnover rates than direct methods. PLoS ONE 7: e48989.
109. Zadworny M, Eissenstat DM. 2011. Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots. New Phytologist 190: 213-221.
110. Zadworny M, McCormack ML, Wiczyska K, Jagodzinski AM. In press. Seasonal variation in root chemistry, but not root morphology, in roots of Quercus robur growing in different soil types. Tree Physiology.
111. Zaehle S, Friend AD. 2010. Carbon and nitrogen cycle dynamics in the O-CN land surface model: 1. Model description, site-scale evaluation, and sensitivity to parameter estimates. Global Biogeochemical Cycles 24: 1-13.