The evolution of gene duplicates in angiosperms and the impact of protein-protein interactions and the mechanism of duplication

Gene duplicates, generated through either whole genome duplication (WGD) or small-scale duplication (SSD), are prominent in angiosperms and are believed to play an important role in adaptation and in generating evolutionary novelty. Previous studies reported contrasting evolutionary and functional dynamics of duplicate genes depending on the mechanism of origin, a behavior that is hypothesized to stem from constraints to maintain the relative dosage balance between the genes concerned and their interaction context. However, the mechanism ultimately influencing loss and retention of gene duplicates over evolutionary time are not yet fully elucidated. Here, by using a robust classification of gene duplicates in Arabidopsis thaliana, Solanumlycopersicum, and Zea mays, large RNAseq expression compendia and an extensive protein-protein interaction (PPI) network from Arabidopsis, we investigated the impact of PPIs on the differential evolutionary and functional fate ofWGD and SSD duplicates. In all three species, retained WGD duplicates show stronger constraints to diverge at the sequence and expression level than SSD ones, a pattern that is also observed for shared PPI partners between Arabidopsis duplicates. PPIs are preferentially distributed among WGD duplicates and specific functional categories. Furthermore, duplicates with PPIs tend to be under stronger constraints to evolve than their counterparts without PPIs regardless of their mechanism of origin. Our results support dosage balance constraint as a specific property of genes involved in biological interactions, including physical PPIs, and suggest that additional factors may be differently influencing the evolution of genes following duplication, depending on the species, time, and mechanism of origin

Polyploidy : an evolutionary and ecological force in stressful times

Polyploidy has been hypothesized to be both an evolutionary dead-end and a source for evolutionary innovation and species diversification. Although polyploid organisms, especially plants, abound, the apparent non-random long-term establishment of genome duplications suggests a link with environmental conditions. Whole-genome duplications seem to correlate with periods of extinction or global change, while polyploids often thrive in harsh or disturbed environments. Evidence is also accumulating that biotic interactions, for instance, with pathogens or mutualists, affect polyploids differently than non-polyploids. Here, we review recent findings and insights on the effect of both abiotic and biotic stress on polyploids versus non-polyploids and propose that stress response in general is an important and even determining factor in the establishment and success of polyploidy

Genomics of Evolutionary Novelty in Hybrids and Polyploids

It has long been recognized that hybridization and polyploidy are prominent processes in plant evolution. Although classically recognized as significant in speciation and adaptation, recognition of the importance of interspecific gene flow has dramatically increased during the genomics era, concomitant with an unending flood of empirical examples, with or without genome doubling. Interspecific gene flow is thus increasingly thought to lead to evolutionary innovation and diversification, via adaptive introgression, homoploid hybrid speciation and allopolyploid speciation. Less well understood, however, are the suite of genetic and genomic mechanisms set in motion by the merger of differentiated genomes, and the temporal scale over which recombinational complexity mediated by gene flow might be expressed and exposed to natural selection. We focus on these issues here, considering the types of molecular genetic and genomic processes that might be set in motion by the saltational event of genome merger between two diverged species, either with or without genome doubling, and how these various processes can contribute to novel phenotypes. Genetic mechanisms include the infusion of new alleles and the genesis of novel structural variation including translocations and inversions, homoeologous exchanges, transposable element mobilization and novel insertional effects, presence-absence variation and copy number variation. Polyploidy generates massive transcriptomic and regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory factors, small RNAs and other genome interactions that cascade from single-gene expression change up through entire networks of transformed regulatory modules. We highlight both these novel combinatorial possibilities and the range of temporal scales over which such complexity might be generated, and thus exposed to natural selection and drift

Robustness and the generalist niche of polyploid species: Genome shock or gradual evolution?

The prevalence of polyploidy in wild and crop species has stimulated debate over its evolutionary advantages and disadvantages. Previous studies have focused on changes occurring at the polyploidization events, including genome-wide changes termed “genome shock,” as well as ancient polyploidy. Recent bioinformatics advances and empirical studies of Arabidopsis and wheat relatives are filling a research gap: the functional evolutionary study of polyploid species using RNA-seq, DNA polymorphism, and epigenomics. Polyploid species can become generalists in natura through environmental robustness by inheriting and merging parental stress responses. Their evolvability is enhanced by mutational robustness working on inherited standing variation. The identification of key genes responsible for gradual adaptive evolution will encourage synthetic biological approaches to transfer polyploid advantages to other species

Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae

[EN] Biological systems remain robust against certain genetic and environmental challenges. Robustness allows the exploration of ecological adaptations. It is unclear what factors contribute to increasing robustness. Gene duplication has been considered to increase genetic robustness through functional redundancy, accelerating the evolution of novel functions. However, recent findings have questioned the link between duplication and robustness. In particular, it remains elusive whether ancient duplicates still bear potential for innovation through preserved redundancy and robustness. Here we have investigated this question by evolving the yeast Saccharomyces cerevisiae for 2200 generations under conditions allowing the accumulation of deleterious mutations, and we put mechanisms of mutational robustness to a test. S. cerevisiae declined in fitness along the evolution experiment, but this decline decelerated in later passages, suggesting functional compensation of mutated genes. We resequenced 28 genomes from experimentally evolved S. cerevisiae lines and found more mutations in duplicates-mainly small-scale duplicates-than in singletons. Genetically interacting duplicates evolved similarly and fixed more amino acid replacing mutations than expected. Regulatory robustness of the duplicates was supported by a larger enrichment for mutations at the promoters of duplicates than at those of singletons. Analyses of yeast gene expression conditions showed a larger variation in the duplicates' expression than that of singletons under a range of stress conditions, sparking the idea that regulatory robustness allowed a wider range of phenotypic responses to environmental stresses, hence faster adaptations. Our data support the persistence of genetic and regulatory robustness in ancient duplicates and its role in adaptations to stresses.We thank Dr. Pablo Labrador for very valuable discussions on the manuscript. This study has been supported by a grant from the Spanish Ministerio de Economia y Competitividad (BFU2009-12022) and another grant from the Science Foundation Ireland (12/IP/1673) to M.A.F. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. C.T. was funded by an EMBO long-term postdoctoral fellowship (reference: ALTF730-2011). We also thank the anonymous reviewers who contributed to improving this manuscript.Keane, O.; Toft, C.; Carretero Paulet, L.; Jones, G.; Fares Riaño, MA. (2014). Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae. Genome Research. 24(11):1830-1841. https://doi.org/10.1101/gr.176792.114S18301841241

Adaptive evolvability through direct selection instead of indirect, second‐order selection

Can evolvability itself be the product of adaptive evolution? To answer this question is challenging, because any DNA mutation that alters only evolvability is subject to indirect, “second order” selection on the future effects of this mutation. Such indirect selection is weaker than “first-order” selection on mutations that alter fitness, in the sense that it can operate only under restrictive conditions. Here I discuss a route to adaptive evolvability that overcomes this challenge. Specifically, a recent evolution experiment showed that some mutations can enhance both fitness and evolvability through a combination of direct and indirect selection. Unrelated evidence from gene duplication and the evolution of gene regulation suggests that mutations with such dual effects may not be rare. Through such mutations, evolvability may increase at least in part because it provides an adaptive advantage. These observations suggest a research program on the adaptive evolution of evolvability, which aims to identify such mutations and to disentangle their direct fitness effects from their indirect effects on evolvability. If evolvability is itself adaptive, Darwinian evolution may have created more than life's diversity. It may also have helped create the very conditions that made the success of Darwinian evolution possible

Occurrence and implicatons of biological network evolution following polyploidy

The mapping and comparison of biological networks allows for analysis to understand forces of evolution. Here, we synthesize information about polyploidy, or whole genome duplication, and its effects on network rewiring. Network changes may have lead to the diversity and survival of some lineages of life, and by understanding network evolution, we may discover patterns that explain how organisms evolve. Specifically, we focus on the consequences of polyploidy on flowering time. Our work aids those studying different aspects of polyploidy to see a bigger picture of how it contributes to evolutionary change and important features that may be involved in cancer. Future studies of biological networks will help improve models of disease and biological processes to make better crops for food, fuel, fiber, and pharmaceuticals