Models and molecular mechanisms for trade‐offs in the context of metabolism

Abstract

Accumulating evidence for trade‐offs involving metabolic traits has demonstrated their importance in the evolution of organisms. Metabolic models with different levels of complexity have already been considered when investigating mechanisms that explain various metabolic trade‐offs. Here we provide a systematic review of modelling approaches that have been used to study and explain trade‐offs between: (i) the kinetic properties of individual enzymes, (ii) rates of metabolic reactions, (iii) the rate and yield of metabolic pathways and networks, (iv) different metabolic objectives in single organisms and in metabolic communities, and (v) metabolic concentrations. In providing insights into the mechanisms underlying these five types of metabolic trade‐offs obtained from constraint‐based metabolic modelling, we emphasize the relationship of metabolic trade‐offs to the classical black box Y‐model that provides a conceptual explanation for resource acquisition–allocation trade‐offs. In addition, we identify several pressing concerns and offer a perspective for future research in the identification and manipulation of metabolic trade‐offs by relying on the toolbox provided by constraint‐based metabolic modelling for single organisms and microbial communities.

Comparative constraint‐based modelling of fruit development across species highlights nitrogen metabolism in the growth‐defence trade‐off

“…Interestingly, most of negative values of correlation coefficients were obtained between reactions of Growth cluster (green) and TCA&TPC cluster (red) supporting that constraint‐based metabolic modelling allowed to find trade‐offs as described in Hashemi et al. (2023).…”

“…The metabolic trade-off was confirmed by calculating the correlation coefficients between 119 fluxes and RGR values extracted at the fourth stage of development among 30 in the panel of the eight fruit species (Table S10; Figure S14). Interestingly, most of negative values of correlation coefficients were obtained between reactions of Growth cluster (green) and TCA&TPC cluster (red) supporting that constraint-based metabolic modelling allowed to find trade-offs as described in Hashemi et al (2023).…”

Rapid evolutionary adaptation: Potential and constraints

“…In their contribution, Hashemi et al (2023) The authors compare approaches to quantify trade-offs based on phenotypic data between individuals and the resulting genetic correlations. This framework is yet still limited to simple traits, and is not generalised to trade-offs between multiple traits, a feature that may be common due to the overlap of gene and metabolic pathways.…”

“…Conversely, in the second part, we focus on the theory and empirical evidence for rapid adaptation via quantitative (polygenic) traits and potential constraints. More precisely, three theoretical papers investigate the core assumptions underpinning and slowing down adaptation by polygenic traits: the existence of (metabolic) trade‐offs (Hashemi et al., 2023; Laitinen & Nikoloski, 2023) and the effects of epistatic interactions and recombination (Li et al., 2023). Three further genomic studies reveal how recombination and genetic architecture of traits determine the speed of adaptation in the invasive brown anole ( Anolis sagrei ) (Bock et al., 2023), in the Italian wall lizard ( Podarcis siculus ) (Sabolić et al., 2023) and during domestication of yeast ( Saccharomyces cerevisiae ) (Raas & Dutheil, 2023).…”

Strategies to identify and dissect trade‐offs in plants

“…From a biological perspective, three types of trade‐offs are considered fundamental depending on the processes that determine trade‐offs; namely, trade‐offs that result from allocation of resources, trade‐offs in mortality due to duration of resource acquisition, and trade‐offs due to specialization in a particular environment (Angilletta et al, 2003) (Figure 2d). Although several authors have stressed the need to develop models and theories to explain how these trade‐offs arise due to the inherent constraints on the limited resources in relation to the environment (Reznick, 1985; Roff & Fairbairn, 2007; Stearns, 1989), little effort has been made in this area of research, predominantly focused on black‐box models or specific cellular systems (e.g., metabolism, see Hashemi et al (2022)).…”