Changes in root architecture under elevated concentrations of CO 2 and nitrogen reflect alternate soil exploration strategies
Abstract
Summary Predicting the response of fine roots to increased atmospheric CO 2 concentration has important implications for carbon (C) and nutrient cycling in forest ecosystems. Root architecture is known to play an important role in how trees acquire soil resources in changing environments. However, the effects of elevated CO 2 on the fine‐root architecture of trees remain unclear. We investigated the architectural response of fine roots exposed to 14 yr of CO 2 enrichment and 6 yr of nitrogen (N) fertilization in a Pinus taeda (loblolly pine) forest. Root traits reflecting geometry, topology and uptake function were measured on intact fine‐root branches removed from soil monoliths and the litter layer. CO 2 enrichment resulted in the development of a fine‐root pool that was less dichotomous and more exploratory under N‐limited conditions. The per cent mycorrhizal colonization did not differ among treatments, suggesting that root growth and acclimation to elevated CO 2 were quantitatively more important than increased mycorrhizal associations. Our findings emphasize the importance of architectural plasticity in response to environmental change and suggest that changes in root architecture may allow trees to effectively exploit larger volumes of soil, thereby pre‐empting progressive nutrient limitations.
- Authors:
-
- Department of Biology College of Charleston 58 Coming St Charleston SC 29424 USA
- Ecology, Evolution, and Environmental Biology Columbia University 10th Floor Schermerhorn Ext. 1200 Amsterdam Ave New York NY 10027 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1778393
- Grant/Contract Number:
- DE‐FC03‐90ER61010
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 205 Journal Issue: 3; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Beidler, Katilyn V., Taylor, Benton N., Strand, Allan E., Cooper, Emily R., Schönholz, Marcos, and Pritchard, Seth G. Changes in root architecture under elevated concentrations of CO 2 and nitrogen reflect alternate soil exploration strategies. United Kingdom: N. p., 2014.
Web. doi:10.1111/nph.13123.
Beidler, Katilyn V., Taylor, Benton N., Strand, Allan E., Cooper, Emily R., Schönholz, Marcos, & Pritchard, Seth G. Changes in root architecture under elevated concentrations of CO 2 and nitrogen reflect alternate soil exploration strategies. United Kingdom. https://doi.org/10.1111/nph.13123
Beidler, Katilyn V., Taylor, Benton N., Strand, Allan E., Cooper, Emily R., Schönholz, Marcos, and Pritchard, Seth G. Tue .
"Changes in root architecture under elevated concentrations of CO 2 and nitrogen reflect alternate soil exploration strategies". United Kingdom. https://doi.org/10.1111/nph.13123.
@article{osti_1778393,
title = {Changes in root architecture under elevated concentrations of CO 2 and nitrogen reflect alternate soil exploration strategies},
author = {Beidler, Katilyn V. and Taylor, Benton N. and Strand, Allan E. and Cooper, Emily R. and Schönholz, Marcos and Pritchard, Seth G.},
abstractNote = {Summary Predicting the response of fine roots to increased atmospheric CO 2 concentration has important implications for carbon (C) and nutrient cycling in forest ecosystems. Root architecture is known to play an important role in how trees acquire soil resources in changing environments. However, the effects of elevated CO 2 on the fine‐root architecture of trees remain unclear. We investigated the architectural response of fine roots exposed to 14 yr of CO 2 enrichment and 6 yr of nitrogen (N) fertilization in a Pinus taeda (loblolly pine) forest. Root traits reflecting geometry, topology and uptake function were measured on intact fine‐root branches removed from soil monoliths and the litter layer. CO 2 enrichment resulted in the development of a fine‐root pool that was less dichotomous and more exploratory under N‐limited conditions. The per cent mycorrhizal colonization did not differ among treatments, suggesting that root growth and acclimation to elevated CO 2 were quantitatively more important than increased mycorrhizal associations. Our findings emphasize the importance of architectural plasticity in response to environmental change and suggest that changes in root architecture may allow trees to effectively exploit larger volumes of soil, thereby pre‐empting progressive nutrient limitations.},
doi = {10.1111/nph.13123},
journal = {New Phytologist},
number = 3,
volume = 205,
place = {United Kingdom},
year = {Tue Oct 28 00:00:00 EDT 2014},
month = {Tue Oct 28 00:00:00 EDT 2014}
}
https://doi.org/10.1111/nph.13123
Works referenced in this record:
Response and potential of agroforestry crops under global change
journal, April 2010
- Calfapietra, C.; Gielen, B.; Karnosky, D.
- Environmental Pollution, Vol. 158, Issue 4
Roots and fungi accelerate carbon and nitrogen cycling in forests exposed to elevated CO 2
journal, July 2012
- Phillips, Richard P.; Meier, Ina C.; Bernhardt, Emily S.
- Ecology Letters, Vol. 15, Issue 9
Effects of Root Restriction, Root Pruning and 6-Benzylaminopurine on the Growth of Peach Seedlings
journal, July 1977
- Richards, D.; Rowe, R. N.
- Annals of Botany, Vol. 41, Issue 4
Functional Diversity of Culturable Bacterial Communities in the Rhizosphere in Relation to Fine-root and Soil Parameters in Alder Stands on Forest, Abandoned Agricultural, and Oil-shale Mining Areas
journal, May 2006
- Lõhmus, K.; Truu, M.; Truu, J.
- Plant and Soil, Vol. 283, Issue 1-2
Root architecture and biomass allocation of three range grasses in response to nonuniform supply of nutrients and shoot defoliation
journal, August 1999
- Arredondo, J. T.; Johnson, D. A.
- New Phytologist, Vol. 143, Issue 2
Root response to CO2 enrichment and nitrogen supply in loblolly pine
journal, March 1994
- Larigauderie, A.; Reynolds, J. F.; Strain, B. R.
- Plant and Soil, Vol. 165, Issue 1
Production, turnover and mycorrhizal colonization of root systems of three Populus species grown under elevated CO2 (POPFACE)
journal, June 2003
- Lukac, Martin; Calfapietra, Carlo; Godbold, Douglas L.
- Global Change Biology, Vol. 9, Issue 6
Root Architecture and Plant Productivity
journal, September 1995
- Lynch, J.
- Plant Physiology, Vol. 109, Issue 1
The Root System Architecture and Development of Senecio vulgaris in Elevated CO 2 and Drought
journal, January 1992
- Berntson, G. M.; Woodward, F. I.
- Functional Ecology, Vol. 6, Issue 3
Architectural analysis of plant root systems 2. Influence of nutrient supply on architecture in contrasting plant species
journal, July 1991
- Fitter, A. H.; Stickland, T. R.
- New Phytologist, Vol. 118, Issue 3
The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO 2
journal, October 2014
- Meier, Ina C.; Pritchard, Seth G.; Brzostek, Edward R.
- New Phytologist, Vol. 205, Issue 3
Forest response to elevated CO2 is conserved across a broad range of productivity
journal, December 2005
- Norby, R. J.; DeLucia, E. H.; Gielen, B.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 50
An empirical assessment of tree branching networks and implications for plant allometric scaling models
journal, June 2013
- Bentley, Lisa Patrick; Stegen, James C.; Savage, Van M.
- Ecology Letters, Vol. 16, Issue 8
Forest soil carbon cycle under elevated CO2 - a case of increased throughput?
journal, January 2009
- Lukac, M.; Lagomarsino, A.; Moscatelli, M. C.
- Forestry, Vol. 82, Issue 1
Spatial and temporal deployment of crop roots in CO2-enriched environments: REVIEW Crop root growth in CO2-enriched environments
journal, July 2000
- Pritchard, Seth G.; Rogers, Hugo H.
- New Phytologist, Vol. 147, Issue 1
Ecological Lessons from Free-Air CO 2 Enrichment (FACE) Experiments
journal, December 2011
- Norby, Richard J.; Zak, Donald R.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 42, Issue 1
Soil conditions and cereal root system architecture: review and considerations for linking Darwin and Weaver
journal, February 2013
- Rich, Sarah M.; Watt, Michelle
- Journal of Experimental Botany, Vol. 64, Issue 5
Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2
journal, May 2001
- Schlesinger, William H.; Lichter, John
- Nature, Vol. 411, Issue 6836
Elevated CO2 alters deployment of roots in “small” growth containers
journal, July 1993
- Berntson, G. M.; McConnaughay, K. D. M.; Bazzaz, F. A.
- Oecologia, Vol. 94, Issue 4
Sources of increased N uptake in forest trees growing under elevated CO2: results of a large-scale 15N study
journal, July 2011
- Hofmockel, Kirsten S.; Gallet-Budynek, Anne; McCarthy, Heather R.
- Global Change Biology, Vol. 17, Issue 11
Modelling root architecture: are there tradeoffs between efficiency and potential of resource acquisition?
journal, June 1994
- Berntson, G. M.
- New Phytologist, Vol. 127, Issue 3
Changes in the Morphology of Roots and Leaves of Carob Seedlings Induced by Nitrogen Source and Atmospheric Carbon Dioxide
journal, December 1997
- Cruz, C.
- Annals of Botany, Vol. 80, Issue 6
An Architectural Approach to the Comparative Ecology of Plant root Systems
journal, May 1987
- Fitter, A. H.
- New Phytologist, Vol. 106
Theories of Optimization, Form and Function in Branching Architecture in Plants
journal, June 1995
- Farnsworth, K. D.; Niklas, K. J.
- Functional Ecology, Vol. 9, Issue 3
Soil organisms and global climate change: Soil organisms and global climate change
journal, January 2011
- Pritchard, S. G.
- Plant Pathology, Vol. 60, Issue 1
Persistence of soil organic matter as an ecosystem property
journal, October 2011
- Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel
- Nature, Vol. 478, Issue 7367
A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2
journal, March 1999
- Hendrey, George R.; Ellsworth, David S.; Lewin, Keith F.
- Global Change Biology, Vol. 5, Issue 3
Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems
journal, December 2009
- Iversen, Colleen M.
- New Phytologist, Vol. 186, Issue 2
Effects of elevated carbon dioxide and sucrose concentrations on Arabidopsis thaliana root architecture and anatomy
journal, March 2007
- Lee-Ho, Elaine; Walton, Linda J.; Reid, David M.
- Canadian Journal of Botany, Vol. 85, Issue 3
Regenerating temperate forest mesocosms in elevated CO 2 : belowground growth and nitrogen cycling
journal, December 1997
- Berntson, G. M.; Bazzaz, F. A.
- Oecologia, Vol. 113, Issue 1
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests
journal, April 2013
- Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G.
- New Phytologist, Vol. 199, Issue 1
Elevated CO2 and plant structure: a review
journal, October 1999
- Pritchard, SetH. G.; Rogers, HugO. H.; Prior, Stephen A.
- Global Change Biology, Vol. 5, Issue 7
Is there an optimal root architecture for nitrate capture in leaching environments?: Root architecture and nitrate capture
journal, May 2003
- Dunbabin, V.; Diggle, A.; Rengel, Z.
- Plant, Cell & Environment, Vol. 26, Issue 6
The Topology and Geometry of Plant Root Systems: Influence of Watering Rate on Root System Topology in Trifolium pratense
journal, July 1986
- Fitter, A. H.
- Annals of Botany, Vol. 58, Issue 1
Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2: C fluxes belowground and long-term FACE productivity
journal, February 2011
- Drake, John E.; Gallet-Budynek, Anne; Hofmockel, Kirsten S.
- Ecology Letters, Vol. 14, Issue 4
Optimum experimental design for Free-Air Carbon dioxide Enrichment (FACE) studies
journal, October 2000
- Filion, Mathieu; Dutilleul, Pierre; Potvin, Catherine
- Global Change Biology, Vol. 6, Issue 7
Root length, biomass, tissue chemistry and mycorrhizal colonization following 14 years of CO2 enrichment and 6 years of N fertilization in a warm temperate forest
journal, July 2014
- Taylor, B. N.; Strand, A. E.; Cooper, E. R.
- Tree Physiology, Vol. 34, Issue 9
Mechanisms of Phosphorus Acquisition for Ponderosa Pine Seedlings under High CO2and Temperature,
journal, February 1997
- Delucia, E.
- Annals of Botany, Vol. 79, Issue 2
Architecture and Biomass Allocation as Components of the Plastic Response of Root Systems to Soil Heterogeneity
book, January 1994
- Fitter, A. H.
- Exploitation of Environmental Heterogeneity by Plants
Leading dimensions in absorptive root trait variation across 96 subtropical forest species
journal, May 2014
- Kong, Deliang; Ma, Chengen; Zhang, Qian
- New Phytologist, Vol. 203, Issue 3
Carbon cost of root systems: an architectural approach
journal, March 1994
- Nielsen, Kai L.; Lynch, Jonathan P.; Jablokow, Andrei G.
- Plant and Soil, Vol. 165, Issue 1
Conventional detection methodology is limiting our ability to understand the roles and functions of fine roots
journal, March 2005
- Pierret, Alain; Moran, Christopher J.; Doussan, Claude
- New Phytologist, Vol. 166, Issue 3
Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency
journal, July 1991
- Fitter, A. H.; Stickland, T. R.; Harvey, M. L.
- New Phytologist, Vol. 118, Issue 3
A global budget for fine root biomass, surface area, and nutrient contents
journal, July 1997
- Jackson, R. B.; Mooney, H. A.; Schulze, E. - D.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 14
Independent and contrasting effects of elevated CO2 and N-fertilization on root architecture in Pinus ponderosa
journal, September 2004
- Tingey, David T.; Johnson, Mark G.; Phillips, Donald L.
- Trees, Vol. 19, Issue 1
Costs and benefits of constructing roots of small diameter
journal, June 1992
- Eissenstat, David M.
- Journal of Plant Nutrition, Vol. 15, Issue 6-7
Phosphate Availability Regulates Root System Architecture in Arabidopsis
journal, June 2001
- Williamson, Lisa C.; Ribrioux, Sebastien P. C. P.; Fitter, Alastair H.
- Plant Physiology, Vol. 126, Issue 2
Plant root growth, architecture and function
journal, March 2009
- Hodge, Angela; Berta, Graziella; Doussan, Claude
- Plant and Soil, Vol. 321, Issue 1-2
Re-assessment of plant carbon dynamics at the Duke free-air CO2 enrichment site: interactions of atmospheric [CO2] with nitrogen and water availability over stand development
journal, November 2009
- McCarthy, Heather R.; Oren, Ram; Johnsen, Kurt H.
- New Phytologist, Vol. 185, Issue 2
Morphological responses of plant roots to heterogeneity of soil resources
journal, June 2002
- Šmilauerová, Marie; Šmilauer, Petr
- New Phytologist, Vol. 154, Issue 3
The Characterization of Topology: A Comparison of Four topological Indices for Rooted Binary Trees
journal, December 1995
- Berntson, G. M.
- Journal of Theoretical Biology, Vol. 177, Issue 3
Species control variation in litter decomposition in a pine forest exposed to elevated CO 2: SPECIES and CO 2 CONTROLS ON DECOMPOSITION
journal, October 2002
- Finzi, Adrien C.; Schlesinger, William H.
- Global Change Biology, Vol. 8, Issue 12
Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests
journal, June 2008
- Bonan, G. B.
- Science, Vol. 320, Issue 5882
Fine root foraging strategies in Norway spruce forests across a European climate gradient
journal, September 2011
- Ostonen, Ivika; Helmisaari, Heljä-Sisko; Borken, Werner
- Global Change Biology, Vol. 17, Issue 12
Fine root Architecture of nine North American Trees
journal, May 2002
- Pregitzer, Kurt S.; DeForest, Jared L.; Burton, Andrew J.
- Ecological Monographs, Vol. 72, Issue 2
Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2
journal, February 2001
- BassiriRad, Hormoz; Gutschick, Vincent Peter; Lussenhop, John
- Oecologia, Vol. 126, Issue 3
Progressive Nitrogen Limitation of Ecosystem Responses to Rising Atmospheric Carbon Dioxide
journal, January 2004
- Luo, Yiqi; Su, Bo; Currie, William S.
- BioScience, Vol. 54, Issue 8
Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2
journal, August 2007
- Finzi, A. C.; Norby, R. J.; Calfapietra, C.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 35
Root System Topology of Plants from Habitats Differing in Soil Resource Availability
journal, April 1996
- Taub, D. R.; Goldberg, D.
- Functional Ecology, Vol. 10, Issue 2
Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species
journal, November 2008
- Guo, Dali; Xia, Mengxue; Wei, Xing
- New Phytologist, Vol. 180, Issue 3
CO 2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest
journal, August 2008
- Iversen, Colleen M.; Ledford, Joanne; Norby, Richard J.
- New Phytologist, Vol. 179, Issue 3
The role of nutrient availability in regulating root architecture
journal, June 2003
- López-Bucio, José; Cruz-Ramı́rez, Alfredo; Herrera-Estrella, Luis
- Current Opinion in Plant Biology, Vol. 6, Issue 3, p. 280-287
Long-term dynamics of mycorrhizal root tips in a loblolly pine forest grown with free-air CO 2 enrichment and soil N fertilization for 6 years
journal, February 2014
- Pritchard, Seth G.; Taylor, Benton N.; Cooper, Emily R.
- Global Change Biology, Vol. 20, Issue 4
Identification de descripteurs morphométriques sensibles aux conditions générales de croissance des semis de chêne rouge [ Quercus rubra ) en milieu naturel
journal, January 1995
- Trencia, J.
- Canadian Journal of Forest Research, Vol. 25, Issue 1