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Title: 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 » 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.« less

Authors:
 [1];  [2];  [1];  [1];  [1];  [1];  [2];  [1];  [3]
  1. Biosciences Division Oak Ridge National Laboratory Oak Ridge Tennessee 37831‐6407
  2. Biological, Environmental &, Climate Sciences Department Brookhaven National Laboratory Upton New York 11973‐5000
  3. 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}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1002/ece3.1565

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