Sian Bray

Small gene effects involved in complex/omnigenic traits remain costly to analyse using current genome-wide association methods (GWAS) because of the number of individuals required to return meaningful association(s), a.k.a. study power. Inspired by field theory in physics, we provide a different method called Genomic Informational Field Theory (GIFT). In contrast to GWAS, GIFT assumes that the phenotype is measured precisely enough and/or the number of individuals in the population is too small to permit the creation of categories. To extract information, GIFT uses the information contained in the cumulative sums difference of gene microstates between two configurations: (i) when the individuals are taken at random without information on phenotype values, and (ii) when individuals are ranked as a function of their phenotypic value. The difference in the cumulative sum is then attributed to the emergence of phenotypic fields. We demonstrate that GIFT recovers GWAS, that is, Fisher’s theory, when the phenotypic fields are linear (first order). However, unlike GWAS, GIFT demonstrates how the variance of microstate distribution density functions can also be involved in genotype-phenotype associations when the phenotypic fields are quadratic (second order). Using genotype-phenotype simulations based on Fisher’s theory as a toy model, we illustrate the application of the method with a small sample size of 1000 individuals.

Proteasomal control of division in Archaea: In eukaryotes, proteasome-mediated degradation of cell cycle factors triggers mitotic exit, DNA segregation, and cytokinesis, a process that culminates in abscission dependent on the protein ESCRT-III. By studying cell division in an archaeal relative of eukaryotes, Tarrason Risa et al. identified a role for the proteasome in triggering cytokinesis by an archaeal ESCRT-III homolog. Cell division in this archaeon was driven by stepwise remodeling of a composite ESCRT-III–based division ring, where rapid proteasome-mediated degradation of one ESCRT-III subunit triggered the constriction of the remaining ESCRT-III–based copolymer. These data strengthen the case for the eukaryotic cell division machinery having its origins in Archaea. Science , this issue p. eaaz2532

Convergent evolution is observed broadly across the web of life, but the degree of evolutionary constraint during adaptation of core intracellular processes is not known. High constraint has been assumed for conserved processes, such as cell division and DNA repair, but reports of nimble evolutionary shifts in these processes have confounded this expectation. Whole genome duplication (WGD) necessitates the concerted adjustment of a wide range of fundamental intracellular functions but nevertheless has been repeatedly survived in all kingdoms. Given this repeated adaptation to WGD despite obvious intracellular challenges to core processes such as meiosis, we asked: how do lineages not only survive WGD, but sometimes ultimately thrive? Are the solutions employed constrained or diverse? Here we detect genes and processes under selection following WGD in the Cochlearia species complex by performing a scan for selective sweeps following WGD in a large-scale survey of 73 resequenced individuals from 23 populations across Europe. We then contrast our results from two independent WGDs in Arabidopsis arenosa and Cardamine amara. We find that while WGD does require the adaptation of particular functional processes in all three cases, the specific genes recruited to respond are highly flexible. We also observe evidence of varying degrees of convergence between different cases. Our results point to a polygenic basis for the distributed adaptive systems that control meiotic crossover number, ionomic rewiring, cell cycle control, and nuclear regulation. Given the sheer number of loci under selection post-WGD, we surmise that this polygenicity may explain the general lack of convergence between these species that are ~30 million years diverged. Based on our results, we speculate that adaptive processes themselves – such as the rate of generation of structural genomic variants—may be altered by WGD in nascent autopolyploids, contributing to the occasionally spectacular adaptability of autopolyploids observed across kingdoms.

It is a plausible hypothesis that parallel adaptation events to the same environmental challenge should result in genetic changes of similar or identical effects, depending on the underlying fitness landscapes. However, systematic testing of this is scarce. Here we examine this hypothesis in two closely related plant species, Arabidopsis halleri and Arabidopsis arenosa , which co-occur at two calamine metalliferous (M) sites harbouring toxic levels of the heavy metals zinc and cadmium. We conduct individual genome resequencing alongside soil elemental analysis for 64 plants from eight populations on M and non-metalliferous (NM) soils, and identify genomic footprints of selection and local adaptation. Selective sweep and environmental association analyses indicate a modest degree of gene as well as functional network convergence, whereby the proximal molecular factors mediating this convergence mostly differ between site pairs and species. Notably, we observe repeated selection on identical single nucleotide polymorphisms in several A. halleri genes at two independently colonized M sites. Our data suggest that species-specific metal handling and other biological features could explain a low degree of convergence between species. The parallel establishment of plant populations on calamine M soils involves convergent evolution, which will probably be more pervasive across sites purposely chosen for maximal similarity in soil composition. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.

Stressors such as soil salinity and dehydration are major constraints on plant growth, causing worldwide crop losses. Compounding these insults, increasing climate volatility requires adaptation to fluctuating conditions. Salinity stress responses are relatively well understood in Arabidopsis thaliana , making this system suited for the rapid molecular dissection of evolutionary mechanisms. In a large-scale genomic analysis of Catalonian A. thaliana , we resequenced 77 individuals from multiple salinity gradients along the coast and integrated these data with 1,135 worldwide A. thaliana genomes for a detailed understanding of the demographic and evolutionary dynamics of naturally evolved salinity tolerance. This revealed that Catalonian varieties adapted to highly fluctuating soil salinity are not Iberian relicts but instead have immigrated to this region more recently. De novo genome assembly of three allelic variants of the high-affinity K ⁺ transporter ( HKT1;1 ) locus resolved structural variation between functionally distinct alleles undergoing fluctuating selection in response to seasonal changes in soil salinity. Plants harboring alleles responsible for low root expression of HKT1;1 and consequently high leaf sodium ( HKT1;1 ^HLS ) were migrants that have moved specifically into areas where soil sodium levels fluctuate widely due to geography and rainfall variation. We demonstrate that the proportion of plants harboring HKT1;1 ^HLS alleles correlates with soil sodium level over time, HKT1;1 ^HLS -harboring plants are better adapted to intermediate levels of salinity, and the HKT1;1 ^HLS allele clusters with high-sodium accumulator accessions worldwide. Together, our evidence suggests that HKT1;1 is under fluctuating selection in response to climate volatility and is a worldwide determinant in adaptation to saline conditions.

The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short- and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as “sponges” accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew.

Evolution has devised countless remarkable solutions to diverse challenges. Understanding the mechanistic basis of these solutions provides insights into how biological systems can be subtly tweaked without maladaptive consequences. The knowledge gained from illuminating these mechanisms is equally important to our understanding of fundamental evolutionary mechanisms as it is to our hopes of developing truly rational plant breeding and synthetic biology. In particular, modern population genomic approaches are proving very powerful in the detection of candidate alleles for mediating consequential adaptations that can be tested functionally. Especially striking are signals gained from contexts involving genetic transfers between populations, closely related species, or indeed between kingdoms. Here we discuss two major classes of these scenarios, adaptive introgression and horizontal gene flow, illustrating discoveries made across kingdoms.

In eukaryotes, the covalent attachment of ubiquitin chains directs substrates to the proteasome for degradation. Recently, ubiquitin-like modifications have also been described in the archaeal domain of life. It has subsequently been hypothesized that ubiquitin-like proteasomal degradation might also operate in these microbes, since all archaeal species utilize homologues of the eukaryotic proteasome. Here we perform a structural and biochemical analysis of a ubiquitin-like modification pathway in the archaeon Sulfolobus acidocaldarius. We reveal that this modifier is homologous to the eukaryotic ubiquitin-related modifier Urm1, considered to be a close evolutionary relative of the progenitor of all ubiquitin-like proteins. Furthermore we demonstrate that urmylated substrates are recognized and processed by the archaeal proteasome, by virtue of a direct interaction with the modifier. Thus, the regulation of protein stability by Urm1 and the proteasome in archaea is likely representative of an ancient pathway from which eukaryotic ubiquitin-mediated proteolysis has evolved.

The HerA ATPase cooperates with the NurA nuclease and the Mre11–Rad50 complex for the repair of double-strand DNA breaks in thermophilic archaea. Here we extend our structural knowledge of this minimal end-resection apparatus by presenting the first crystal structure of hexameric HerA. The full-length structure visualizes at atomic resolution the N-terminal HerA-ATP synthase domain and a conserved C-terminal extension, which acts as a physical brace between adjacent protomers. The brace also interacts in trans with nucleotide-binding residues of the neighbouring subunit. Our observations support a model in which the coaxial interaction of the HerA ring with the toroidal NurA dimer generates a continuous channel traversing the complex. HerA-driven translocation would propel the DNA towards the narrow annulus of NurA, leading to duplex melting and nucleolytic digestion. This system differs substantially from the bacterial end-resection paradigms. Our findings suggest a novel mode of DNA-end processing by this integrated archaeal helicase–nuclease machine.

During DNA repair by HR (homologous recombination), the ends of a DNA DSB (double-strand break) must be resected to generate single-stranded tails, which are required for strand invasion and exchange with homologous chromosomes. This 5′–3′ end-resection of the DNA duplex is an essential process, conserved across all three domains of life: the bacteria, eukaryota and archaea. In the present review, we examine the numerous and redundant helicase and nuclease systems that function as the enzymatic analogues for this crucial process in the three major phylogenetic divisions.