Cheaters divide and conquer

Three ‘killer genes’ in one species of fission yeast act selfishly and keep it reproductively isolated from a closely related species

Genetics of adaptation

The rediscovery of Mendel’s work showing that the heredity of phenotypes is controlled by discrete genes was followed by the reconciliation of Mendelian genetics with evolution by natural selection in the middle of the last century with the Modern Synthesis. In the past two decades, dramatic advances in genomic methods have facilitated the identification of the loci, genes, and even individual mutations that underlie phenotypic variants that are the putative targets of natural selection. Moreover, these methods have also changed how we can study adaptation by flipping the problem around, allowing us to first examine what loci show evidence of having been under selection, and then connecting these genetic variants to phenotypic variation. As a result, we now have an expanding list of actual genetic changes that underlie potentially adaptive phenotypic variation. Here, we synthesize how considering the effects of these adaptive loci in the context of cellular environments, genomes, organisms, and populations has provided new insights to the genetic architecture of adaptation

Redundant Enhancers Mediate Transcriptional Repression of AGAMOUS by APETALA2

AbstractThe floral homeotic gene AGAMOUS specifies stamen and carpel fate in the central whorls of Arabidopsis flowers. Transcription of AGAMOUS RNA is restricted to the center of developing flowers by several, partially redundant negative regulators, one of which is the homeotic gene APETALA2. We have identified regulatory elements that mediate transcriptional repression of AGAMOUS by APETALA2 and found that several redundant elements respond independently to loss of APETALA2 activity. Thus, redundancy at the level of cis-regulatory sequences is independent of redundancy at the level of trans-regulators. We have also found that only the early, but not the late, effects of APETALA2 on AGAMOUS require the meristem-identity protein LEAFY, a positive regulator of AGAMOUS

Extending Coalescent Theory to Autotetraploids

We develop coalescent models for autotetraploid species with tetrasomic inheritance. We show that the ancestral genetic process in a large population without recombination may be approximated using Kingman’s standard coalescent, with a coalescent effective population size 4N. Numerical results suggest that this approximation is accurate for population sizes on the order of hundreds of individuals. Therefore, existing coalescent simulation programs can be adapted to study population history in autotetraploids simply by interpreting the timescale in units of 4N generations. We also consider the possibility of double reduction, a phenomenon unique to polysomic inheritance, and show that its effects on gene genealogies are similar to partial self-fertilization.Organismic and Evolutionary Biolog

Complex Evolutionary Events at a Tandem Cluster of Arabidopsis thaliana Genes Resulting in a Single-Locus Genetic Incompatibility

Non-additive interactions between genomes have important implications, not only for practical applications such as breeding, but also for understanding evolution. In extreme cases, genes from different genomic backgrounds may be incompatible and compromise normal development or physiology. Of particular interest are non-additive interactions of alleles at the same locus. For example, overdominant behavior of alleles, with respect to plant fitness, has been proposed as an important component of hybrid vigor, while underdominance may lead to reproductive isolation. Despite their importance, only a few cases of genetic over- or underdominance affecting plant growth or fitness are understood at the level of individual genes. Moreover, the relationship between biochemical and fitness effects may be complex: genetic overdominance, that is, increased or novel activity of a gene may lead to evolutionary underdominance expressed as hybrid weakness. Here, we describe a non-additive interaction between alleles at the Arabidopsis thaliana OAK (OUTGROWTH-ASSOCIATED PROTEIN KINASE) gene. OAK alleles from two different accessions interact in F1 hybrids to cause a variety of aberrant growth phenotypes that depend on a recently acquired promoter with a novel expression pattern. The OAK gene, which is located in a highly variable tandem array encoding closely related receptor-like kinases, is found in one third of A. thaliana accessions, but not in the reference accession Col-0. Besides recruitment of exons from nearby genes as promoter sequences, key events in OAK evolution include gene duplication and divergence of a potential ligand-binding domain. OAK kinase activity is required for the aberrant phenotypes, indicating it is not recognition of an aberrant protein, but rather a true gain of function, or overdominance for gene activity, that leads to this underdominance for fitness. Our work provides insights into how tandem arrays, which are particularly prone to frequent, complex rearrangements, can produce genetic novelty

Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana

As Arabidopsis thaliana is increasingly employed in evolutionary and ecological studies, it is essential to understand patterns of natural genetic variation and the forces that shape them. Previous work focusing mostly on global and regional scales has demonstrated the importance of historical events such as long-distance migration and colonization. Far less is known about the role of contemporary factors or environmental heterogeneity in generating diversity patterns at local scales. We sampled 1,005 individuals from 77 closely spaced stands in diverse settings around Tübingen, Germany. A set of 436 SNP markers was used to characterize genome-wide patterns of relatedness and recombination. Neighboring genotypes often shared mosaic blocks of alternating marker identity and divergence. We detected recent outcrossing as well as stretches of residual heterozygosity in largely homozygous recombinants. As has been observed for several other selfing species, there was considerable heterogeneity among sites in diversity and outcrossing, with rural stands exhibiting greater diversity and heterozygosity than urban stands. Fine-scale spatial structure was evident as well. Within stands, spatial structure correlated negatively with observed heterozygosity, suggesting that the high homozygosity of natural A. thaliana may be partially attributable to nearest-neighbor mating of related individuals. The large number of markers and extensive local sampling employed here afforded unusual power to characterize local genetic patterns. Contemporary processes such as ongoing outcrossing play an important role in determining distribution of genetic diversity at this scale. Local "outcrossing hotspots" appear to reshuffle genetic information at surprising rates, while other stands contribute comparatively little. Our findings have important implications for sampling and interpreting diversity among A. thaliana accessions.Financial support came from an NIH Ruth Kirschstein NRSA Postdoctoral Fellowship (KB), a Human Frontiers Science Program Postdoctoral Fellowship (RAL), grants DFG ERA-PG ARelatives and FP6 IP AGRON-OMICS (contract LSHG-CT-2006-037704), from a Gottfried Wilhelm Leibniz Award of the DFG, and the Max Planck Society (DW)

Borrowed alleles and convergence in serpentine adaptation

ACKNOWLEDGMENTS. We thank members of the L.Y. and K.B. laboratories for helpful discussions. This work was supported through the European Research Council Grant StG CA629F04E (to L.Y.); a Harvard University Milton Fund Award (to K.B.); Ruth L. Kirschstein National Research Service Award 1 F32 GM096699 from the NIH (to L.Y.); National Science Foundation Grant IOS-1146465 (to K.B.); NIH National Institute of General Medical Sciences Grant 2R01GM078536 (to D.E.S.); and Biotechnology and Biological Sciences Research Council Grant BB/L000113/1 (to D.E.S.)Peer reviewedPublisher PD

Diffusion-mediated HEI10 coarsening can explain meiotic crossover positioning in Arabidopsis.

In most organisms, the number and distribution of crossovers that occur during meiosis are tightly controlled. All chromosomes must receive at least one 'obligatory crossover' and crossovers are prevented from occurring near one another by 'crossover interference'. However, the mechanistic basis of this phenomenon of crossover interference has remained mostly mysterious. Using quantitative super-resolution cytogenetics and mathematical modelling, we investigate crossover positioning in the Arabidopsis thaliana wild-type, an over-expressor of the conserved E3 ligase HEI10, and a hei10 heterozygous line. We show that crossover positions can be explained by a predictive, diffusion-mediated coarsening model, in which large, approximately evenly-spaced HEI10 foci grow at the expense of smaller, closely-spaced clusters. We propose this coarsening process explains many aspects of Arabidopsis crossover positioning, including crossover interference. Consistent with this model, we also demonstrate that crossover positioning can be predictably modified in vivo simply by altering HEI10 dosage, with higher and lower dosage leading to weaker and stronger crossover interference, respectively. As HEI10 is a conserved member of the RING finger protein family that functions in the interference-sensitive pathway for crossover formation, we anticipate that similar mechanisms may regulate crossover positioning in diverse eukaryotes

Genetic Adaptation Associated with Genome-Doubling in Autotetraploid Arabidopsis arenosa

Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.Organismic and Evolutionary Biolog