The evolution of metabolism: How to test evolutionary hypotheses at the genomic level

Abstract

The origin of primordial metabolism and its expansion to form the metabolic networks extant today represent excellent systems to study the impact of natural selection and the potential adaptive role of novel compounds. Here we present the current hypotheses made on the origin of life and ancestral metabolism and present the theories and mechanisms by which the large chemical diversity of plants might have emerged along evolution. In particular, we provide a survey of statistical methods that can be used to detect signatures of selection at the gene and population level, and discuss potential and limits of these methods for investigating patterns of molecular adaptation in plant metabolism.

Keywords: Adaptation; E&R, Evolve and Resequence; Evolution; GWAS, genome wide association study; Genomics; Metabolism; Plants; QTL, quantitative trait locus; Selection.

Graphical abstract

Fig. 1

Schematic diagrams representing the main hypotheses for the evolution of metabolic pathways. In the retrograde hypothesis (a), metabolic pathways are supposed to originate with sequential gene duplications starting from gene catalyzing the last step of current pathways. Depletion of the compounds present in the primordial soup may have originated a selection pressure leading to the survival and reproduction of the primordial cells able to produce the depleted compounds; this process could have then been repeated sequentially, in a backward direction, until the establishment of contemporary pathways. In Granick's hypothesis (b), pathways would have been assembled in a forward direction, from simple precursors to more complex products. Under this model, the older genes across evolutionary timescale would be represented by those catalyzing the earlier steps in contemporary pathways. In our diagram, the decoration and alkylating steps are examples of reactions adding complexity to the initial precursor and to the pathway intermediates. In the patchwork hypothesis (c), ancestral genes encoding promiscuous enzymes could have expanded the metabolic capabilities of primordial cells through gene duplication and subsequent divergence. A possible fate for an event of gene duplication is subfunctionalization (c), in which the catalytic activities of the ancestral gene are divided among the paralogs. In our example, following divergence of the duplicated genes, one of the ancestral reactions is taken on by one of the paralogs. In the shell hypothesis (d), evolution of metabolism can be traced back to the consecutive additions of distinct metabolic pathways. The core central pathway (reductive TCA, fatty acids biosynthesis), i.e., shell A, predated the addition of nitrogen metabolism in shell B; sulphur and cofactor metabolism were later added as shell C. As more pathways are added, the inner shells remain nested in the network as remnants of the earliest metabolisms. Abbreviations: E1, enzyme 1; E2, enzyme 2.