Adaptive Genomic Regions Research Articles

Implications of the three-dimensional chromatin organization for genome evolution in a fungal plant pathogen

The spatial organization of eukaryotic genomes is linked to their biological functions, although it is not clear how this impacts the overall evolution of a genome. Here, we uncover the three-dimensional (3D) genome organization of the phytopathogen Verticillium dahliae, known to possess distinct genomic regions, designated adaptive genomic regions (AGRs), enriched in transposable elements and genes that mediate host infection. Short-range DNA interactions form clear topologically associating domains (TADs) with gene-rich boundaries that show reduced levels of gene expression and reduced genomic variation. Intriguingly, TADs are less clearly insulated in AGRs than in the core genome. At a global scale, the genome contains bipartite long-range interactions, particularly enriched for AGRs and more generally containing segmental duplications. Notably, the patterns observed for V. dahliae are also present in other Verticillium species. Thus, our analysis links 3D genome organization to evolutionary features conserved throughout the Verticillium genus.

Natural hybridization reduces vulnerability to climate change

Under climate change, species unable to track their niche via range shifts are largely reliant on genetic variation to adapt and persist. Genomic vulnerability predictions are used to identify populations that lack the necessary variation, particularly at climate-relevant genes. However, hybridization as a source of novel adaptive variation is typically ignored in genomic vulnerability studies. We estimated environmental niche models and genomic vulnerability for closely related species of rainbowfish (Melanotaenia spp.) across an elevational gradient in the Australian Wet Tropics. Hybrid populations between a widespread generalist and several narrow range endemic species exhibited reduced vulnerability to projected climates compared to pure narrow endemics. Overlaps between introgressed and adaptive genomic regions were consistent with a signal of adaptive introgression. Our findings highlight the often-underappreciated conservation value of hybrid populations and indicate that adaptive introgression may contribute to evolutionary rescue of species with narrow environmental ranges.

Genomic-environmental associations in wild cranberry (Vaccinium macrocarpon Ait.).

Understanding the genetic basis of local adaptation in natural plant populations, particularly crop wild relatives, may be highly useful for plant breeding. By characterizing genetic variation for adaptation to potentially stressful environmental conditions, breeders can make targeted use of crop wild relatives to develop cultivars for novel or changing environments. This is especially appealing for improving long-lived woody perennial crops such as the American cranberry (Vaccinium macrocarpon Ait.), the cultivation of which is challenged by biotic and abiotic stresses. In this study, we used environmental association analyses in a collection of 111 wild cranberry accessions to identify potentially adaptive genomic regions for a range of bioclimatic and soil conditions. We detected 126 significant associations between SNP marker loci and environmental variables describing temperature, precipitation, and soil attributes. Many of these markers tagged genes with functional annotations strongly suggesting a role in adaptation to biotic or abiotic conditions. Despite relatively low genetic variation in cranberry, our results suggest that local adaptation to divergent environments is indeed present, and the identification of potentially adaptive genetic variation may enable a selective use of this germplasm for breeding more stress-tolerant cultivars.

Transposable Elements Contribute to Genome Dynamics and Gene Expression Variation in the Fungal Plant Pathogen Verticillium dahliae.

Transposable elements (TEs) are a major source of genetic and regulatory variation in their host genome and are consequently thought to play important roles in evolution. Many fungal and oomycete plant pathogens have evolved dynamic and TE-rich genomic regions containing genes that are implicated in host colonization and adaptation. TEs embedded in these regions have typically been thought to accelerate the evolution of these genomic compartments, but little is known about their dynamics in strains that harbor them. Here, we used whole-genome sequencing data of 42 strains of the fungal plant pathogen Verticillium dahliae to systematically identify polymorphic TEs that may be implicated in genomic as well as in gene expression variation. We identified 2,523 TE polymorphisms and characterize a subset of 8% of the TEs as polymorphic elements that are evolutionary younger, less methylated, and more highly expressed when compared with the remaining 92% of the total TE complement. As expected, the polyrmorphic TEs are enriched in the adaptive genomic regions. Besides, we observed an association of polymorphic TEs with pathogenicity-related genes that localize nearby and that display high expression levels. Collectively, our analyses demonstrate that TE dynamics in V. dahliae contributes to genomic variation, correlates with expression of pathogenicity-related genes, and potentially impacts the evolution of adaptive genomic regions.

Three putative DNA methyltransferases of Verticillium dahliae differentially contribute to DNA methylation that is dispensable for growth, development and virulence

BackgroundDNA methylation is an important epigenetic control mechanism that in many fungi is restricted to genomic regions containing transposable elements (TEs). Two DNA methyltransferases, Dim2 and Dnmt5, are known to perform methylation at cytosines in fungi. While most ascomycete fungi encode both Dim2 and Dnmt5, only few functional studies have been performed in species containing both.MethodsIn this study, we report functional analysis of both Dim2 and Dnmt5 in the plant pathogenic fungus Verticillium dahliae.ResultsOur results show that Dim2, but not Dnmt5 or the putative sexual-cycle-related DNA methyltransferase Rid, is responsible for the majority of DNA methylation under the tested conditions. Single or double DNA methyltransferase mutants did not show altered development, virulence, or transcription of genes or TEs. In contrast, Hp1 and Dim5 mutants that are impacted in chromatin-associated processes upstream of DNA methylation are severely affected in development and virulence and display transcriptional reprogramming in specific hypervariable genomic regions (so-called adaptive genomic regions) that contain genes associated with host colonization. As these adaptive genomic regions are largely devoid of DNA methylation and of Hp1- and Dim5-associated heterochromatin, the differential transcription is likely caused by pleiotropic effects rather than by differential DNA methylation.ConclusionOverall, our study suggests that Dim2 is the main DNA methyltransferase in V. dahliae and, in conjunction with work on other fungi, is likely the main active DNMT in ascomycetes, irrespective of Dnmt5 presence. We speculate that Dnmt5 and Rid act under specific, presently enigmatic, conditions or, alternatively, act in DNA-associated processes other than DNA methylation.

A unique chromatin profile defines adaptive genomic regions in a fungal plant pathogen.

Genomes store information at scales beyond the linear nucleotide sequence, which impacts genome function at the level of an individual, while influences on populations and long-term genome function remains unclear. Here, we addressed how physical and chemical DNA characteristics influence genome evolution in the plant pathogenic fungus Verticillium dahliae. We identified incomplete DNA methylation of repetitive elements, associated with specific genomic compartments originally defined as Lineage-Specific (LS) regions that contain genes involved in host adaptation. Further chromatin characterization revealed associations with features such as H3 Lys-27 methylated histones (H3K27me3) and accessible DNA. Machine learning trained on chromatin data identified twice as much LS DNA as previously recognized, which was validated through orthogonal analysis, and we propose to refer to this DNA as adaptive genomic regions. Our results provide evidence that specific chromatin profiles define adaptive genomic regions, and highlight how different epigenetic factors contribute to the organization of these regions.

Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks.

Regulation of gene expression is thought to play a major role in adaptation, but the relative importance of cis- and trans- regulatory mechanisms in the early stages of adaptive divergence is unclear. Using RNAseq of threespine stickleback fish gill tissue from four independent marine-freshwater ecotype pairs and their F1 hybrids, we show that cis-acting (allele-specific) regulation consistently predominates gene expression divergence. Genes showing parallel marine-freshwater expression divergence are found near to adaptive genomic regions, show signatures of natural selection around their transcription start sites and are enriched for cis-regulatory control. For genes with parallel increased expression among freshwater fish, the quantitative degree of cis- and trans-regulation is also highly correlated across populations, suggesting a shared genetic basis. Compared to other forms of regulation, cis-regulation tends to show greater additivity and stability across different genetic and environmental contexts, making it a fertile substrate for the early stages of adaptive evolution.

Adaptation to Plant Communities across the Genome of Arabidopsis thaliana.

Despite the importance of plant-plant interactions on plant community dynamics and crop yield, our understanding of the adaptive genetics underlying these interactions is still limited and deserves to be investigated in the context of complex and diffuse interactions occurring in plant assemblages. Here, based on 145 natural populations of Arabidopsis thaliana located in south-west of France and characterized for plant communities, we conducted a Genome-Environment Association analysis to finely map adaptive genomic regions of A. thaliana associated with plant community descriptors. To control for correlated abiotic environment effects, we also characterized the populations for a set of biologically meaningful climate and soil variables. A nonnegligible fraction of top single nucleotide polymorphisms was associated with both plant community descriptors and abiotic variables, highlighting the importance of considering the actual abiotic drivers of plant communities to disentangle genetic variants for biotic adaptation from genetic variants for abiotic adaptation. The adaptive loci associated with species abundance were highly dependent on the identity of the neighboring species suggesting a high degree of biotic specialization of A. thaliana to members of its plant interaction network. Moreover, the identification of adaptive loci associated with α-diversity and composition of plant communities supports the ability of A. thaliana to interact simultaneously with multiple plant neighbors, which in turn can help to understand the role of community-wide selection. Altogether, our study highlights that dissecting the genetic basis underlying plant-plant interactions at a regional scale while controlling for abiotic confounding factors can help understanding the adaptive mechanisms modulating natural plant assemblages.

Adaptive genetic changes related to haemoglobin concentration in native high-altitude Tibetans.

What is the topic of this review? Tibetans have genetic adaptations that are hypothesized to underlie the distinct set of traits they exhibit at altitude. What advances does it highlight? Several adaptive signatures in the same genomic regions have been identified among Tibetan populations resident throughout the Qinghai-Tibetan Plateau. Many highland Tibetans exhibit a haemoglobin concentration within the range expected at sea level, and this trait is associated with putatively adaptive regions harbouring the hypoxia-inducible factor pathway genes EGLN1, EPAS1 and PPARA. Precise functional variants at adaptive loci and relationships to physiological traits, beyond haemoglobin concentration, are currently being examined in this population. Some native Tibetan, Andean and Ethiopian populations have lived at altitudes ranging from 3000 to >4000m above sea level for hundreds of generations and exhibit distinct combinations of traits at altitude. It was long hypothesized that genetic factors contribute to adaptive differences in these populations, and recent advances in genomics provide evidence that some of the strongest signatures of positive selection in humans are those identified in Tibetans. Many of the top adaptive genomic regions highlighted thus far harbour genes related to hypoxia sensing and response. Putatively adaptive copies of three hypoxia-inducible factor pathway genes, EPAS1, EGLN1 and PPARA, are associated with sea-level range, rather than elevated, haemoglobin concentration observed in many Tibetans at high altitude, and recent studies provide insight into some of the precise adaptive variants, timing of adaptive events and functional roles. While several studies in highland Tibetans have converged on a few hypoxia-inducible factor pathway genes, additional candidates have been reported in independent studies of Tibetans located throughout the Qinghai-Tibetan Plateau. Various aspects of adaptive significance have yet to be identified, integrated, and fully explored. Given the rapid technological advances and interdisciplinary efforts in genomics, physiology and molecular biology, careful examination of Tibetans and comparisons with other distinctively adapted highland populations will provide valuable insight into evolutionary processes and models for both basic and clinical research.

Genetic perspectives on northern population cycles: bridging the gap between theory and empirical studies.

Many key species in northern ecosystems are characterised by high-amplitude cyclic population demography. In 1924, Charles Elton described the ecology and evolution of cyclic populations in a classic paper and, since then, a major focus has been the underlying causes of population cycles. Elton hypothesised that fluctuations reduced population genetic variation and influenced the direction of selection pressures. In concordance with Elton, present theories concern the direct consequences of population cycles for genetic structure due to the processes of genetic drift and selection, but also include feedback models of genetic composition on population dynamics. Most of these theories gained mathematical support during the 1970s and onwards, but due to methodological drawbacks, difficulties in long-term sampling and a complex interplay between microevolutionary processes, clear empirical data allowing the testing of these predictions are still scarce. Current genetic tools allow for estimates of genetic variation and identification of adaptive genomic regions, making this an ideal time to revisit this subject. Herein, we attempt to contribute towards a consensus regarding the enigma described by Elton almost 90 years ago. We present nine predictions covering the direct and genetic feedback consequences of population cycles on genetic variation and population structure, and review the empirical evidence. Generally, empirical support for the predictions was low and scattered, with obvious gaps in the understanding of basic population processes. We conclude that genetic variation in northern cyclic populations generally is high and that the geographic distribution and amount of diversity are usually suggested to be determined by various forms of context- and density-dependent dispersal exceeding the impact of genetic drift. Furthermore, we found few clear signatures of selection determining genetic composition in cyclic populations. Dispersal is assumed to have a strong impact on genetic structuring and we suggest that the signatures of other microevolutionary processes such as genetic drift and selection are weaker and have been over-shadowed by density-dependent dispersal. We emphasise that basic biological and demographical questions still need to be answered and stress the importance of extensive sampling, appropriate choice of tools and the value of standardised protocols.

Phylogeography and adaptation genetics of stickleback from theHaidaGwaii archipelago revealed using genome‐wide single nucleotide polymorphism genotyping

Threespine stickleback populations are model systems for studying adaptive evolution and the underlying genetics. In lakes on the Haida Gwaii archipelago (off western Canada), stickleback have undergone a remarkable local radiation and show phenotypic diversity matching that seen throughout the species distribution. To provide a historical context for this radiation, we surveyed genetic variation at >1000 single nucleotide polymorphism (SNP) loci in stickleback from over 100 populations. SNPs included markers evenly distributed throughout genome and candidate SNPs tagging adaptive genomic regions. Based on evenly distributed SNPs, the phylogeographic pattern differs substantially from the disjunct pattern previously observed between two highly divergent mtDNA lineages. The SNP tree instead shows extensive within watershed population clustering and different watersheds separated by short branches deep in the tree. These data are consistent with separate colonizations of most watersheds, despite underlying genetic connections between some independent drainages. This supports previous suppositions that morphological diversity observed between watersheds has been shaped independently, with populations exhibiting complete loss of lateral plates and giant size each occurring in several distinct clades. Throughout the archipelago, we see repeated selection of SNPs tagging candidate freshwater adaptive variants at several genomic regions differentiated between marine–freshwater populations on a global scale (e.g. EDA, Na/K ATPase). In estuarine sites, both marine and freshwater allelic variants were commonly detected. We also found typically marine alleles present in a few freshwater lakes, especially those with completely plated morphology. These results provide a general model for postglacial colonization of freshwater habitat by sticklebacks and illustrate the tremendous potential of genome-wide SNP data sets hold for resolving patterns and processes underlying recent adaptive divergences.

QTL mapping in three tropical maize populations reveals a set of constitutive and adaptive genomic regions for drought tolerance

Despite numerous published reports of quantitative trait loci (QTL) for drought-related traits, practical applications of such QTL in maize improvement are scarce. Identifying QTL of sizeable effects that express more or less uniformly in diverse genetic backgrounds across contrasting water regimes could significantly complement conventional breeding efforts to improve drought tolerance. We evaluated three tropical bi-parental populations under water-stress (WS) and well-watered (WW) regimes in Mexico, Kenya and Zimbabwe to identify genomic regions responsible for grain yield (GY) and anthesis-silking interval (ASI) across multiple environments and diverse genetic backgrounds. Across the three populations, on average, drought stress reduced GY by more than 50 % and increased ASI by 3.2 days. We identified a total of 83 and 62 QTL through individual environment analyses for GY and ASI, respectively. In each population, most QTL consistently showed up in each water regime. Across the three populations, the phenotypic variance explained by various individual QTL ranged from 2.6 to 17.8 % for GY and 1.7 to 17.8 % for ASI under WS environments and from 5 to 19.5 % for GY under WW environments. Meta-QTL (mQTL) analysis across the three populations and multiple environments identified seven genomic regions for GY and one for ASI, of which six mQTL on chr.1, 4, 5 and 10 for GY were constitutively expressed across WS and WW environments. One mQTL on chr.7 for GY and one on chr.3 for ASI were found to be ‘adaptive’ to WS conditions. High throughput assays were developed for SNPs that delimit the physical intervals of these mQTL. At most of the QTL, almost equal number of favorable alleles was donated by either of the parents within each cross, thereby demonstrating the potential of drought tolerant × drought tolerant crosses to identify QTL under contrasting water regimes.Electronic supplementary materialThe online version of this article (doi:10.1007/s00122-012-2003-7) contains supplementary material, which is available to authorized users.

Evidence for a residual postglacial founder effect in a highly dispersive freshwater invertebrate

In the northern hemisphere, glacial periods have had profound and lasting effects on the population genetics of numerous species, with founder effects often persisting for many generations in formerly glaciated regions. We found an unusual example of this in the freshwater bryozoan Cristatella mucedo, which showed regional differences in haplotype diversity with relatively low levels of haplotype diversity in northern Europe compared to central/southern Europe despite previous evidence for frequent dispersal between C. mucedo populations. Such contradictions between high dispersal and low gene flow have now been reported in several other freshwater taxa and may be attributed to persistent founder effects following colonization of sites by a few individuals whose efficient reproduction leads to rapid population growth. Alternatively, selection may determine which genotypes can thrive in northerly locations, or it may be that C. mucedo has undergone cryptic speciation. Future work on adaptive genomic regions is required before we can understand how gene flow, local adaptation, and speciation influence the current distribution patterns of bryozoans and other freshwater invertebrates.

A cyclophilin gene marker confirming geographical differentiation of Norway spruce populations and indicating viability response on excess soil‐born salinity

A newly identified cyclophilin-encoding cDNA clone was used to design a codominant inherited EST-PCR marker in Norway spruce. The study of the current minor polymorphism revealed a geographically structured differentiation pattern across 17 test populations, showing a slight clinal variation south-north through Europe. Based on the frequency of alleles, isolation-by-distance analysis and the Ewens-Watterson test, we conclude that a selectively neutral random-drift mutation recently occurred within the Alpine population group, thus being responsible for the genetic variation detected. Analysis of tolerant and susceptible subsets of two adjacent Bavarian spruce populations affected by soil-born NaCl pollution, revealed that the cyclophilin marker locus also confirms biased genotype frequencies. Considering an unlinked PCR marker of a ribosomal protein-encoding EST clone, deviations between pooled tolerant subsets and pooled sensitive subsets were proven to be more significant for two-locus homozygous genotypes than for each locus alone. We suggest that both loci are linked to adaptive genomic regions. Their potential to test the feasibility of marker-assisted selection of both NaCl-tolerant and drought resistant tree populations is discussed.