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 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.
Highlights
Hierarchical theory states that functional importance is observed at higher levels of biological organization, while lower levels explain mechanism (Bartholomew 1964)
A number of studies have shown that single-gene mutant do not always result in a noticeable phenotype as a result of multiple biological buffering mechanisms ranging from partial redundancy in gene paralogs and phenotypic capacitors to network architecture
We show that a single-gene mutation in the gateway enzyme to the N-assimilation pathway is followed by effects that became increasing less evident through levels of biological organization via buffering from gene paralogs, changes in network architecture, and mechanisms yet to be discovered
Summary
Hierarchical theory states that functional importance is observed at higher levels of biological organization, while lower levels explain mechanism (Bartholomew 1964). In regard to carbon (C) and nitrogen (N) interactions, metabolic processes at lower levels of organization [e.g., at the DNA level] elicit complex regulatory networks that scale through organelles, cells, and tissues to influence organismal physiology, developmental ontogeny, and fitness (Reich et al 2006a,b). Complicating this hierarchical view is that each level of biological organization is inherently robust against perturbation (Dunne et al 2002; Melian and Bascompte 2002; Delattre and Felix 2009; Greenbury et al 2010).
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