Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?
Abstract
Understanding the consequences of elevated CO2 (eCO2; 800 ppm) on terrestrial ecosystems is a central theme in global change biology, but relatively little is known about how altered plant C and N metabolism influences higher levels of biological organization. Here, we investigate the consequences of C and N interactions by genetically modifying the N-assimilation pathway in Arabidopsis and initiating growth chamber and mesocosm competition studies at current CO2 (cCO2; 400 ppm) and eCO2 over multiple generations. Using a suite of ecological, physiological, and molecular genomic tools, we show that a single-gene mutant of a key enzyme (nia2) elicited a highly orchestrated buffering response starting with a fivefold increase in the expression of a gene paralog (nia1) and a 63% increase in the expression of gene network module enriched for N-assimilation genes. The genetic perturbation reduced amino acids, protein, and TCA-cycle intermediate concentrations in the nia2 mutant compared to the wild-type, while eCO2 mainly increased carbohydrate concentrations. The mutant had reduced net photosynthetic rates due to a 27% decrease in carboxylation capacity and an 18% decrease in electron transport rates. The expression of these buffering mechanisms resulted in a penalty that negatively correlated with fitness and population dynamics yet showed onlymore »
- Authors:
-
- Biosciences Division Oak Ridge National Laboratory Oak Ridge Tennessee 37831‐6407
- Biological, Environmental &, Climate Sciences Department Brookhaven National Laboratory Upton New York 11973‐5000
- Environmental Sciences Division Oak Ridge National Laboratory Oak Ridge Tennessee 37831‐6301
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1345675
- Alternate Identifier(s):
- OSTI ID: 1195797; OSTI ID: 1228835; OSTI ID: 1786468
- Report Number(s):
- BNL-108472-2015-JA
Journal ID: ISSN 2045-7758
- Grant/Contract Number:
- AC05-00OR22725; AC02-98CHI0886; SC00112704
- Resource Type:
- Published Article
- Journal Name:
- Ecology and Evolution
- Additional Journal Information:
- Journal Name: Ecology and Evolution Journal Volume: 5 Journal Issue: 14; Journal ID: ISSN 2045-7758
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; buffering; carbon; ecological genomics; networks; nitrogen; robustness; scaling
Citation Formats
Weston, David J., Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E., Jawdy, Sara A., Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., and Wullschleger, Stan D. Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?. United Kingdom: N. p., 2015.
Web. doi:10.1002/ece3.1565.
Weston, David J., Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E., Jawdy, Sara A., Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., & Wullschleger, Stan D. Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?. United Kingdom. https://doi.org/10.1002/ece3.1565
Weston, David J., Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E., Jawdy, Sara A., Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., and Wullschleger, Stan D. Thu .
"Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?". United Kingdom. https://doi.org/10.1002/ece3.1565.
@article{osti_1345675,
title = {Scaling nitrogen and carbon interactions: what are the consequences of biological buffering?},
author = {Weston, David J. and Rogers, Alistair and Tschaplinski, Timothy J. and Gunter, Lee E. and Jawdy, Sara A. and Engle, Nancy L. and Heady, Lindsey E. and Tuskan, Gerald A. and Wullschleger, Stan D.},
abstractNote = {Understanding the consequences of elevated CO2 (eCO2; 800 ppm) on terrestrial ecosystems is a central theme in global change biology, but relatively little is known about how altered plant C and N metabolism influences higher levels of biological organization. Here, we investigate the consequences of C and N interactions by genetically modifying the N-assimilation pathway in Arabidopsis and initiating growth chamber and mesocosm competition studies at current CO2 (cCO2; 400 ppm) and eCO2 over multiple generations. Using a suite of ecological, physiological, and molecular genomic tools, we show that a single-gene mutant of a key enzyme (nia2) elicited a highly orchestrated buffering response starting with a fivefold increase in the expression of a gene paralog (nia1) and a 63% increase in the expression of gene network module enriched for N-assimilation genes. The genetic perturbation reduced amino acids, protein, and TCA-cycle intermediate concentrations in the nia2 mutant compared to the wild-type, while eCO2 mainly increased carbohydrate concentrations. The mutant had reduced net photosynthetic rates due to a 27% decrease in carboxylation capacity and an 18% decrease in electron transport rates. The expression of these buffering mechanisms resulted in a penalty that negatively correlated with fitness and population dynamics yet showed only minor alterations in our estimates of population function, including total per unit area biomass, ground cover, and leaf area index. This study provides insight into the consequences of buffering mechanisms that occur post-genetic perturbations in the N pathway and the associated outcomes these buffering systems have on plant populations relative to eCO2.},
doi = {10.1002/ece3.1565},
journal = {Ecology and Evolution},
number = 14,
volume = 5,
place = {United Kingdom},
year = {Thu Jun 25 00:00:00 EDT 2015},
month = {Thu Jun 25 00:00:00 EDT 2015}
}
https://doi.org/10.1002/ece3.1565
Web of Science
Works referenced in this record:
Robustness against mutations in genetic networks of yeast
journal, April 2000
- Wagner, Andreas
- Nature Genetics, Vol. 24, Issue 4
The effect of scale-free topology on the robustness and evolvability of genetic regulatory networks
journal, November 2010
- Greenbury, Sam F.; Johnston, Iain G.; Smith, Matthew A.
- Journal of Theoretical Biology, Vol. 267, Issue 1
Robustness: mechanisms and consequences
journal, September 2009
- Masel, Joanna; Siegal, Mark L.
- Trends in Genetics, Vol. 25, Issue 9
Photosynthesis, carboxylation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert
journal, December 2004
- Ellsworth, David S.; Reich, Peter B.; Naumburg, Elke S.
- Global Change Biology, Vol. 10, Issue 12
limma: Linear Models for Microarray Data
book, January 2005
- Smyth, G. K.
- Bioinformatics and Computational Biology Solutions Using R and Bioconductor
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error
journal, September 2003
- Long, S. P.
- Journal of Experimental Botany, Vol. 54, Issue 392
Toward a Mechanistic Modeling of Nitrogen Limitation on Vegetation Dynamics
journal, May 2012
- Xu, Chonggang; Fisher, Rosie; Wullschleger, Stan D.
- PLoS ONE, Vol. 7, Issue 5
Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves?
journal, December 2006
- Ainsworth, E. A.; Rogers, A.; Leakey, A. D. B.
- Journal of Experimental Botany, Vol. 58, Issue 3
Complex networks: two ways to be robust?: Complex networks: two ways to be robust?
journal, November 2002
- Melián, Carlos J.; Bascompte, Jordi
- Ecology Letters, Vol. 5, Issue 6
A General Framework for Weighted Gene Co-Expression Network Analysis
journal, January 2005
- Zhang, Bin; Horvath, Steve
- Statistical Applications in Genetics and Molecular Biology, Vol. 4, Issue 1
Molecular ecology of global change: MOLECULAR ECOLOGY OF GLOBAL CHANGE
journal, August 2007
- Reusch, Thorsten B. H.; Wood, Troy E.
- Molecular Ecology, Vol. 16, Issue 19
A Comparison of Fluorescamine and Naphthalene-2,3-dicarboxaldehyde Fluorogenic Reagents for Microplate-Based Detection of Amino Acids
journal, October 2001
- Bantan-Polak, Tjaša; Kassai, Miki; Grant, Kathryn B.
- Analytical Biochemistry, Vol. 297, Issue 2
WGCNA: an R package for weighted correlation network analysis
journal, December 2008
- Langfelder, Peter; Horvath, Steve
- BMC Bioinformatics, Vol. 9, Issue 1
Comparative physiology and transcriptional networks underlying the heat shock response in Populus trichocarpa, Arabidopsis thaliana and Glycine max: Comparative analysis of the heat shock response
journal, June 2011
- Weston, David J.; Karve, Abhijit A.; Gunter, Lee E.
- Plant, Cell & Environment, Vol. 34, Issue 9
Leaf traits in relation to crown development, light interception and growth of elite families of loblolly and slash pine
journal, May 2008
- Chmura, D. J.; Tjoelker, M. G.
- Tree Physiology, Vol. 28, Issue 5
Gene Expression of the NO 3 – Transporter NRT1.1 and the Nitrate Reductase NIA1 Is Repressed in Arabidopsis Roots by NO 2 – , the Product of NO 3 – Reduction
journal, June 2003
- Loqué, Dominique; Tillard, Pascal; Gojon, Alain
- Plant Physiology, Vol. 132, Issue 2
Network Hubs Buffer Environmental Variation in Saccharomyces cerevisiae
journal, November 2008
- Levy, Sasha F.; Siegal, Mark L.
- PLoS Biology, Vol. 6, Issue 11
The use of mutants and transgenic plants to study nitrate assimilation
journal, May 1994
- Hoff, T.; Truong, H. -N.; Caboche, M.
- Plant, Cell and Environment, Vol. 17, Issue 5
Salicylate and catechol levels are maintained in nahG transgenic poplar
journal, August 2007
- Morse, Alison M.; Tschaplinski, Timothy J.; Dervinis, Christopher
- Phytochemistry, Vol. 68, Issue 15
Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide
journal, December 2006
- Reich, Peter B.; Hungate, Bruce A.; Luo, Yiqi
- Annual Review of Ecology, Evolution, and Systematics, Vol. 37, Issue 1
Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants
journal, February 2008
- Weston, David J.; Gunter, Lee E.; Rogers, Alistair
- BMC Systems Biology, Vol. 2, Issue 1
Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions
journal, November 2010
- Nunes-Nesi, Adriano; Fernie, Alisdair R.; Stitt, Mark
- Molecular Plant, Vol. 3, Issue 6
Reproductive allocation of an annual, Xanthium canadense , at an elevated carbon dioxide concentration
journal, September 2003
- Kinugasa, Toshihiko; Hikosaka, Kouki; Hirose, Tadaki
- Oecologia, Vol. 137, Issue 1
Network structure and the biology of populations
journal, July 2006
- May, Robert M.
- Trends in Ecology & Evolution, Vol. 21, Issue 7
Network structure and biodiversity loss in food webs: robustness increases with connectance
journal, July 2002
- Dunne, Jennifer A.; Williams, Richard J.; Martinez, Neo D.
- Ecology Letters, Vol. 5, Issue 4
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
NIH Image to ImageJ: 25 years of image analysis
journal, June 2012
- Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
- Nature Methods, Vol. 9, Issue 7
The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development
journal, July 2013
- May, Patrick; Liao, Will; Wu, Yijin
- Nature Communications, Vol. 4, Issue 1
The Ecology and Economics of Storage in Plants
journal, November 1990
- Chapin, F. S.; Schulze, E.; Mooney, H. A.
- Annual Review of Ecology and Systematics, Vol. 21, Issue 1
Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco
journal, September 2000
- Migge, Andrea; Bork, Christiane; Hell, Rüdiger
- Planta, Vol. 211, Issue 4
Understanding ecosystem robustness
journal, October 2007
- Wilmers, Christopher C.
- Trends in Ecology & Evolution, Vol. 22, Issue 10
Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO 2 and ozone concentrations for 3 years under fully open-air field conditions
journal, November 2006
- Bernacchi, Carl J.; Leakey, Andrew D. B.; Heady, Lindsey E.
- Plant, Cell and Environment, Vol. 29, Issue 11
Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen
journal, November 2014
- Bloom, Arnold J.
- Photosynthesis Research, Vol. 123, Issue 2
A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana
journal, July 2004
- Noren, Hanna; Svensson, Per; Andersson, Bertil
- Physiologia Plantarum, Vol. 121, Issue 3
A Robot-Based Platform to Measure Multiple Enzyme Activities in Arabidopsis Using a Set of Cycling Assays: Comparison of Changes of Enzyme Activities and Transcript Levels during Diurnal Cycles and in Prolonged Darkness
journal, November 2004
- Gibon, Yves; Blaesing, Oliver E.; Hannemann, Jan
- The Plant Cell, Vol. 16, Issue 12
Differential Expression of the Two Arabidopsis Nitrate Reductase Genes
journal, May 1991
- Cheng, Chi-Lien; Acedo, Gregoria N.; Dewdney, Julia
- Plant Physiology, Vol. 96, Issue 1
The evolutionary context of robust and redundant cell biological mechanisms
journal, May 2009
- Delattre, Marie; Félix, Marie-Anne
- BioEssays, Vol. 31, Issue 5
Genes encoding hub and bottleneck enzymes of the Arabidopsis metabolic network preferentially retain homeologs through whole genome duplication
journal, January 2010
- Wu, Xudong; Qi, Xiaoquan
- BMC Evolutionary Biology, Vol. 10, Issue 1
Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain
journal, August 2001
- Evans, J. R.; Poorter, H.
- Plant, Cell and Environment, Vol. 24, Issue 8
Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis
journal, March 2009
- Tschoep, Hendrik; Gibon, Yves; Carillo, Petronia
- Plant, Cell & Environment, Vol. 32, Issue 3
Differential Expression of the Arabidopsis Nia1 and Nia2 Genes : Cytokinin-Induced Nitrate Reductase Activity Is Correlated With Increased
journal, March 1998
- Yu, Xiaodan; Sukumaran, Sujatha; Márton, László
- Plant Physiology, Vol. 116, Issue 3
Tree responses to rising CO 2 in field experiments: implications for the future forest
journal, June 1999
- Norby, R. J.; Wullschleger, S. D.; Gunderson, C. A.
- Plant, Cell and Environment, Vol. 22, Issue 6
Nitrogen limitation constrains sustainability of ecosystem response to CO2
journal, April 2006
- Reich, Peter B.; Hobbie, Sarah E.; Lee, Tali
- Nature, Vol. 440, Issue 7086
Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max)
journal, January 2011
- Gillespie, K. M.; Rogers, A.; Ainsworth, E. A.
- Journal of Experimental Botany, Vol. 62, Issue 8
Molecular and functional regulation of two NO3- uptake systems by N- and C-status of Arabidopsis plants
journal, June 1999
- Lejay, Laurence; Tillard, Pascal; Lepetit, Marc
- The Plant Journal, Vol. 18, Issue 5
Principles for the Buffering of Genetic Variation
journal, February 2001
- Hartman IV, J. L.
- Science, Vol. 291, Issue 5506
Effect of sulfur on nitrate reductase and ATP sulfurylase Activities in groundnut (Arachis hypogea L.)
journal, December 2006
- Jamal, Arshad; Fazli, Inayat Saleem; Ahmad, Saif
- Journal of Plant Biology, Vol. 49, Issue 6
Evolutionary Persistence of Functional Compensation by Duplicate Genes in Arabidopsis
journal, January 2009
- Hanada, Kousuke; Kuromori, Takashi; Myouga, Fumiyoshi
- Genome Biology and Evolution, Vol. 1
Microarray Analysis of the Nitrate Response in Arabidopsis Roots and Shoots Reveals over 1,000 Rapidly Responding Genes and New Linkages to Glucose, Trehalose-6-Phosphate, Iron, and Sulfate Metabolism
journal, June 2003
- Wang, Rongchen; Okamoto, Mamoru; Xing, Xiujuan
- Plant Physiology, Vol. 132, Issue 2
RISING ATMOSPHERIC CARBON DIOXIDE: Plants FACE the Future
journal, June 2004
- Long, Stephen P.; Ainsworth, Elizabeth A.; Rogers, Alistair
- Annual Review of Plant Biology, Vol. 55, Issue 1
Duplicate genes and robustness to transient gene knock-downs in Caenorhabditis elegans
journal, January 2004
- Conant, Gavin C.; Wagner, Andreas
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1534
The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity
journal, July 2004
- Bernacchi, Carl J.; Morgan, Patrick B.; Ort, Donald R.
- Planta, Vol. 220, Issue 3
Functional Compensation of Primary and Secondary Metabolites by Duplicate Genes in Arabidopsis thaliana
journal, August 2010
- Hanada, K.; Sawada, Y.; Kuromori, T.
- Molecular Biology and Evolution, Vol. 28, Issue 1
Intraspecific variation in response to warming across levels of organization: a test with Solidago altissima
journal, December 2011
- Souza, Lara; Weston, Dave J.; Sanders, Nathan J.
- Ecosphere, Vol. 2, Issue 12
The Nitrogen Use Efficiency of C 3 and C 4 Plants : III. Leaf Nitrogen Effects on the Activity of Carboxylating Enzymes in
journal, October 1987
- Sage, Rowan F.; Pearcy, Robert W.; Seemann, Jeffrey R.
- Plant Physiology, Vol. 85, Issue 2
Acclimation of Arabidopsis thaliana to long-term CO 2 enrichment and nitrogen supply is basically a matter of growth rate adjustment
journal, December 2006
- Tocquin, Pierre; Ormenese, Sandra; Pieltain, Alexandra
- Physiologia Plantarum, Vol. 128, Issue 4
Maladaptation and the Paradox of Robustness in Evolution
journal, October 2007
- Frank, Steven A.
- PLoS ONE, Vol. 2, Issue 10