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Title: Scaling carbon and nitrogen interactions. What are the consequences of biological buffering?

Abstract

Understanding the consequences of elevated CO 2 (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 CO 2 (cCO 2; 400 ppm) and eCO 2 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 eCO 2 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 andmore » 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 eCO 2.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1195797
Alternate Identifier(s):
OSTI ID: 1228835
Report Number(s):
BNL-108472-2015-JA
Journal ID: ISSN 2045-7758; KP1702010; ERKP788
Grant/Contract Number:  
AC05-00OR22725; SC00112704
Resource Type:
Accepted Manuscript
Journal Name:
Ecology and Evolution
Additional Journal Information:
Journal Volume: 5; Journal Issue: 14; Journal ID: ISSN 2045-7758
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; buffering; carbon; ecological genomics; networks; nitrogen; robustness; scaling

Citation Formats

Weston, David, Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E, Jawdy, Sara, Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., and Wullschleger, Stan D. Scaling carbon and nitrogen interactions. What are the consequences of biological buffering?. United States: N. p., 2015. Web. doi:10.1002/ece3.1565.
Weston, David, Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E, Jawdy, Sara, Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., & Wullschleger, Stan D. Scaling carbon and nitrogen interactions. What are the consequences of biological buffering?. United States. doi:10.1002/ece3.1565.
Weston, David, Rogers, Alistair, Tschaplinski, Timothy J., Gunter, Lee E, Jawdy, Sara, Engle, Nancy L., Heady, Lindsey E., Tuskan, Gerald A., and Wullschleger, Stan D. Thu . "Scaling carbon and nitrogen interactions. What are the consequences of biological buffering?". United States. doi:10.1002/ece3.1565. https://www.osti.gov/servlets/purl/1195797.
@article{osti_1195797,
title = {Scaling carbon and nitrogen interactions. What are the consequences of biological buffering?},
author = {Weston, David and Rogers, Alistair and Tschaplinski, Timothy J. and Gunter, Lee E and Jawdy, Sara 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 States},
year = {2015},
month = {6}
}

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Works referenced in this record:

Robustness against mutations in genetic networks of yeast
journal, April 2000

  • Wagner, Andreas
  • Nature Genetics, Vol. 24, Issue 4
  • DOI: 10.1038/74174

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
  • DOI: 10.1016/j.jtbi.2010.08.006

Robustness: mechanisms and consequences
journal, September 2009


Toward a Mechanistic Modeling of Nitrogen Limitation on Vegetation Dynamics
journal, May 2012


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
  • DOI: 10.1093/jxb/erl233

Complex networks: two ways to be robust?: Complex networks: two ways to be robust?
journal, November 2002


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
  • DOI: 10.2202/1544-6115.1128

Molecular ecology of global change: MOLECULAR ECOLOGY OF GLOBAL CHANGE
journal, August 2007


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
  • DOI: 10.1006/abio.2001.5338

WGCNA: an R package for weighted correlation network analysis
journal, December 2008


Network Hubs Buffer Environmental Variation in Saccharomyces cerevisiae
journal, November 2008


The use of mutants and transgenic plants to study nitrate assimilation
journal, May 1994


Salicylate and catechol levels are maintained in nahG transgenic poplar
journal, August 2007


Carbon-Nitrogen Interactions in Terrestrial Ecosystems in Response to Rising Atmospheric Carbon Dioxide
journal, December 2006


Identification of the Arabidopsis CHL3 gene as the nitrate reductase structural gene NIA2.
journal, May 1991


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
  • DOI: 10.1186/1752-0509-2-16

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
  • DOI: 10.1093/mp/ssq049

Reproductive allocation of an annual, Xanthium canadense , at an elevated carbon dioxide concentration
journal, September 2003


Network structure and the biology of populations
journal, July 2006


Network structure and biodiversity loss in food webs: robustness increases with connectance
journal, July 2002


Elevated CO2 and plant structure: a review
journal, October 1999


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
  • DOI: 10.1038/nmeth.2089

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
  • DOI: 10.1038/ncomms3145

The Ecology and Economics of Storage in Plants
journal, November 1990


Negative regulation of nitrate reductase gene expression by glutamine or asparagine accumulating in leaves of sulfur-deprived tobacco
journal, September 2000


Understanding ecosystem robustness
journal, October 2007


Photorespiration and nitrate assimilation: a major intersection between plant carbon and nitrogen
journal, November 2014


A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana
journal, July 2004


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
  • DOI: 10.1104/pp.96.1.275

The evolutionary context of robust and redundant cell biological mechanisms
journal, May 2009


Adjustment of growth and central metabolism to a mild but sustained nitrogen-limitation in Arabidopsis
journal, March 2009


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
  • DOI: 10.1104/pp.116.3.1091

Tree responses to rising CO 2 in field experiments: implications for the future forest
journal, June 1999


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
  • DOI: 10.1038/nature04486

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
  • DOI: 10.1093/jxb/erq435

Molecular and functional regulation of two NO3- uptake systems by N- and C-status of Arabidopsis plants
journal, June 1999


Principles for the Buffering of Genetic Variation
journal, February 2001


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
  • DOI: 10.1007/BF03031134

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
  • DOI: 10.1093/gbe/evp043

RISING ATMOSPHERIC CARBON DIOXIDE: Plants FACE the Future
journal, June 2004


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
  • DOI: 10.1098/rspb.2003.2560

The growth of soybean under free air [CO2] enrichment (FACE) stimulates photosynthesis while decreasing in vivo Rubisco capacity
journal, July 2004


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
  • DOI: 10.1093/molbev/msq204

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
  • DOI: 10.1890/ES11-00283.1

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
  • DOI: 10.1104/pp.85.2.355

Acclimation of Arabidopsis thaliana to long-term CO 2 enrichment and nitrogen supply is basically a matter of growth rate adjustment
journal, December 2006


Maladaptation and the Paradox of Robustness in Evolution
journal, October 2007