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Fungal heavy metal adaptation through single nucleotide polymorphisms and copy‐number variation

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Abstract

Human‐altered environments can shape the evolution of organisms. Fungi are no exception, though little is known about how they withstand anthropogenic pollution. Here, we document adaptation in the mycorrhizal fungus Suillus luteus driven by soil heavy metal contamination. Genome scans across individuals from recently polluted and nearby unpolluted soils in Belgium revealed low divergence across isolates and no evidence of population structure based on soil type. However, we detected single nucleotide polymorphism divergence and gene copy number variation, with different genetic combinations potentially conferring ability to persist in contaminated soils. Variants were shared across the population but found to be under selection in isolates exposed to pollution and located across the genome, including in genes involved in metal exclusion, storage, immobilization, and reactive oxygen species detoxification. Together, our results point to S. luteus undergoing the initial steps of adaptive divergence and contribute to understanding the processes underlying local adaptation under strong environmental selection.

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... These include studies of allopatric isolation [3] and responses to environmental factors such as temperature [4][5][6], salinity [7], and domestication [8][9][10]. However, studies on adaptive evolution of mushroom-forming fungi using population genomics methods are still in their infancy, and are exemplified by reports focused on the mycorrhizal species Suillus brevipes and S. luteus [4,7,11]. Saline environments might have driven divergence of two S. brevipes populations in California, in which a gene enhancing salt tolerance was found to be under strong selection [7]. ...
... In S. brevipes populations across North America, genes under positive selection and significantly associated with environmental variables are mainly related to transmembrane transport and helicase activity, which are potentially involved in cold stress response [4]. Besides, a S. luteus population in Belgium was inferred to have undergone adaptive divergence driven by soil heavy metal contamination, as genes involved in heavy metal metabolism were detected to be under selection [11]. ...
... Increasing evidence from fungal population genomics studies has suggested how environmental adaptation could drive population differentiation [4,5,7,11,87]. Among the environmental factors, temperature has a strong effect on many important fungal traits, including growth, development and reproduction [88], and has already shown to be vital in fungal adaptation [89]. ...
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Introduction Mushroom-forming fungi comprise diverse species that develop complex multicellular structures. In cultivated species, both ecological adaptation and artificial selection have driven genome evolution. However, little is known about the connections among genotype, phenotype and adaptation in mushroom-forming fungi. Objectives This study aimed to (1) uncover the population structure and demographic history of Lentinula edodes, (2) dissect the genetic basis of adaptive evolution in L. edodes, and (3) determine if genes related to fruiting body development are involved in adaptive evolution. Methods we analyzed genomes and fruiting body-related traits (FBRTs) in 133 L. edodes strains and conducted RNA-seq analysis of fruiting body development in the YS69 strain. Combined methods of genomic scan for divergence, genome-wide association studies (GWAS), and RNA-seq were used to dissect the genetic basis of adaptive evolution. Results We detected three distinct subgroups of L. edodes via single nucleotide polymorphisms, which showed robust phenotypic and temperature response differentiation and correlation with geographical distribution. Demographic history inference suggests that the subgroups diverged 36,871 generations ago. Moreover, L. edodes cultivars in China may have originated from the vicinity of Northeast China. A total of 942 genes were found to be related to genetic divergence by genomic scan, and 719 genes were identified to be candidates underlying FBRTs by GWAS. Integrating results of genomic scan and GWAS, 80 genes were detected to be related to phenotypic differentiation. A total of 364 genes related to fruiting body development were involved in genetic divergence and phenotypic differentiation. Conclusion Adaptation to the local environment, especially temperature, triggered genetic divergence and phenotypic differentiation of L. edodes. A general model for genetic divergence and phenotypic differentiation during adaptive evolution in L. edodes, which involves in signal perception and transduction, transcriptional regulation, and fruiting body morphogenesis, was also integrated here.
... Metal defense in fungi includes components that are often redundant in number, and hence, tolerance has been considered as a polygenetic trait. 77 For example, a genome-wide comparison of Suillus luteus fruiting bodies from sites with differing levels of metal contamination found correlations with single nucleotide polymorphisms or copy numbers of genes, rather than single major differences. 77 A polygenetic mechanism is also consistent with genome changes in response to directed evolution for copper tolerance in S. cerevisiae. ...
... 77 For example, a genome-wide comparison of Suillus luteus fruiting bodies from sites with differing levels of metal contamination found correlations with single nucleotide polymorphisms or copy numbers of genes, rather than single major differences. 77 A polygenetic mechanism is also consistent with genome changes in response to directed evolution for copper tolerance in S. cerevisiae. 78 How HEPHAESTUS might interact with genes within the core genome should also be explored. ...
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... Fungi with the function of remediation of soil polluted by heavy metals are generally adaptive to the polluted environment. They may have evolved mechanisms to escape the damage that heavy metals do to them (figure 2)[10]. ...
... Model of heavy metal tolerance in Suillus luteus, including metal exclusion, storage, immobilization and reactiveoxygen species (ROS) detoxification.[10] ...
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... Metal defense in fungi includes components that are often redundant in number, and hence, tolerance has been considered as a polygenetic trait. 77 For example, a genome-wide comparison of Suillus luteus fruiting bodies from sites with differing levels of metal contamination found correlations with single nucleotide polymorphisms or copy numbers of genes, rather than single major differences. 77 A polygenetic mechanism is also consistent with genome changes in response to directed evolution for copper tolerance in S. cerevisiae. ...
... 77 For example, a genome-wide comparison of Suillus luteus fruiting bodies from sites with differing levels of metal contamination found correlations with single nucleotide polymorphisms or copy numbers of genes, rather than single major differences. 77 A polygenetic mechanism is also consistent with genome changes in response to directed evolution for copper tolerance in S. cerevisiae. 78 How HEPHAESTUS might interact with genes within the core genome should also be explored. ...
Preprint
The horizontal transfer of large gene clusters by mobile elements is a key driver of prokaryotic adaptation in response to environmental stresses. Eukaryotic microbes face similar environmental stresses yet a parallel role for mobile elements has not yet been established. A stress faced by all microorganisms is the prevalence of toxic metals in their environment. In fungi, identified mechanisms for protection against metals generally rely on genes that are dispersed within an organism's genome. Here we have discovered a large (~85 kb) region that confers resistance to several metals in the genomes of some, but not all, strains of a fungus, Paecilomyces variotii. We name this region HEPHAESTUS and present evidence that this region is mobile within the P. variotii genome with features highly characteristic of a transposable element. While large gene clusters including those for the synthesis of secondary metabolites have been widely reported in fungi, these are not mobile within fungal genomes. HEPHAESTUS contains the greatest complement of host-beneficial genes carried by a transposable element in eukaryotes. This suggests that eukaryotic transposable elements might play a role analogous to their bacterial counterparts in the horizontal transfer of large regions of host-beneficial DNA. Genes within HEPHAESTUS responsible for individual metal resistances include those encoding a P-type ATPase transporter, PcaA, required for cadmium and lead resistance, a transporter, ZrcA, providing resistance to zinc, and a multicopper oxidase, McoA, conferring resistance to copper. Additionally, a subregion of HEPHAESTUS; conferring resistance to arsenate was identified. The presence of a strikingly similar cluster in the genome of another fungus, Penicillium fuscoglaucum, suggests that HEPHAESTUS arrived in P. variotii via horizontal gene transfer.
... These studies also revealed high intraspecific variability and demonstrated that melanin content is one of the key functional traits conferring an advantage under water stress. In nature, C. geophilum isolates have shown patterns of local adaptation to serpentine soils with a significant effect of nickel concentrations on fitness-related traits (Gonçalves et al., 2009;Bazzicalupo et al., 2020). ...
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... Transcriptomics relies on RNA sequencing to survey gene expression through fold-changes in transcripts and proteomics assess foldchange in subsequent proteins. In fungi, omics is already incorporated into the identification of characteristics of multi-drug resistance, analysis of genomic divergence based on species origination, some analysis of metal tolerance due to short term exposure, and the analysis of the effects of exposure to non-metal selective pressures [210,301,[304][305][306]. ...
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... Furthermore, the ability of micro-organisms to persist or grow in the presence of elevated metal concentrations (i.e. the metal tolerance) is mediated by a wide variety of detoxification mechanisms, some of which are physiological changes induced by environmental conditions (e.g. metallothionein production, generation of antioxidant enzymes), and some that are genetically mediated, for example, mutations (Gadd and Griffiths 1978;Azevedo et al. 2007;Bazzicalupo et al. 2020). ...
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Gene flow is a fundamental evolutionary force in adaptation that is especially important to understand as humans are rapidly changing both the natural environment and natural levels of gene flow. Theory proposes a multifaceted role for gene flow in adaptation, but it focuses mainly on the disruptive effect that gene flow has on adaptation when selection is not strong enough to prevent the loss of locally adapted alleles. The role of gene flow in adaptation is now better understood due to the recent development of both genomic models of adaptive evolution and genomic techniques, which both point to the importance of genetic architecture in the origin and maintenance of adaptation with gene flow. In this review we discuss three main topics on the genomics of adaptation with gene flow. First, we investigate selection on migration and gene flow. Second, we discuss the three potential sources of adaptive variation in relation to the role of gene flow in the origin of adaptation. Third, we explain how local adaptation is maintained despite gene flow: we provide a synthesis of recent genomic models of adaptation, discuss the genomic mechanisms, and review empirical studies on the genomics of adaptation with gene flow. Despite predictions on the disruptive effect of gene flow in adaptation, an increasing number of studies show that gene flow can promote adaptation, that local adaptations can be maintained despite high gene flow, and that genetic architecture plays a fundamental role in the origin and maintenance of local adaptation with gene flow. This article is protected by copyright. All rights reserved.
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Measuring the effects of selection on the genome imposed by human-altered environment is currently a major goal in ecological genomics. Given the polygenic basis of most phenotypic traits, quantitative genetic theory predicts that selection is expected to cause subtle allelic changes among covarying loci rather than pronounced changes at few loci of large effects. The goal of this study was to test for the occurrence of polygenic selection in both North Atlantic eels (European Eel, Anguilla anguilla and American Eel, A. rostrata), using a method that searches for covariation among loci that would discriminate eels from "control" vs. "polluted" environments and be associated with specific contaminants acting as putative selective agents. RAD-seq libraries resulted in 23,659 and 14,755 filtered loci for the European and American Eels respectively. A total of 142 and 141 covarying markers discriminating European and American Eels from "control" vs. "polluted" sampling localities were obtained using the Random Forest algorithm. Distance-based redundancy analyses (db-RDAs) were used to assess the relationships between these covarying markers and concentration of 34 contaminants measured for each individual eel. PCB153, 4'4'DDE and selenium were associated with covarying markers for both species, thus pointing to these contaminants as major selective agents in contaminated sites . Gene enrichment analyses suggested that sterol regulation plays an important role in the differential survival of eels in "polluted" environment. This study illustrates the power of combining methods for detecting signals of polygenic selection and for associating variation of markers with putative selective agents in studies aiming at documenting the dynamics of selection at the genomic level, and particularly so in human altered environments. This article is protected by copyright. All rights reserved.
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Soils are subject to varying degrees of direct or indirect human disturbance, constituting a major global change driver. Factoring out natural from direct and indirect human influence is not always straightforward, but some human activities have clear impacts. These include land use change, land management, and land degradation (erosion, compaction, sealing and salinization). The intensity of land use also exerts a great impact on soils, and soils are also subject to indirect impacts arising from human activity, such as acid deposition (sulphur and nitrogen) and heavy metal pollution. In this critical review, we report the state-of-the-art understanding of these global change pressures on soils, identify knowledge gaps and research challenges, and highlight actions and policies to minimise adverse environmental impacts arising from these global change drivers. Soils are central to considerations of what constitutes sustainable intensification. Therefore, ensuring that vulnerable and high environmental value soils are considered when protecting important habitats and ecosystems, will help to reduce the pressure on land from global change drivers. To ensure that soils are protected as part of wider environmental efforts, a global soil resilience programme should be considered, to monitor, recover or sustain soil fertility and function, and to enhance the ecosystem services provided by soils. Soils cannot, and should not, be considered in isolation of the ecosystems that they underpin and vice versa. The role of soils in supporting ecosystems and natural capital needs greater recognition. The lasting legacy of the International Year of Soils in 2015 should be to put soils at the centre of policy supporting environmental protection and sustainable development. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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Understanding the interaction between phenotypic plasticity and evolutionary processes is important for predicting a species' response to changing environment. Strong recurrent selection each generation may be an important process in highly fecund species with broad dispersal and extensive early mortality. We tested whether selection was associated with spatial divergence in gene expression plasticity for osmoregulation in the eastern oyster (Crassostrea virginica). We collected adult oysters from high and low salinity reefs within a single estuary and after 9 weeks of acclimation at 10 and 30 salinity, measured gene expression in 24 oysters using next-generation RNA sequencing technology. The oysters had significantly different expression (DE) in response to salinity treatments for 7936 (18.9%) transcripts overall, with planned contrasts showing 8× more DE in oysters from the high-salinity reef and 15× more DE between reefs when tested at 10 salinity. The reef-by-treatment interaction was also genomically pervasive (5858 DE transcripts, 13.9%). Inter-reef F ST for transcript SNPs averaged 0.0025 with the top 1% between 0.29 and 0.73. Transcripts containing "outlier" SNPs were significantly enriched for osmoregulatory genes and showed patterns of variation consistent with selection on the low-salinity reef. Both phenotypic plasticity and recurrent selection seem to be important factors determining the realized niche of oysters within estuaries. © The American Genetic Association 2015. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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To elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell wall–degrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7–38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a ‘symbiosis toolkit’, with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.
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When plants are subjected to high metal exposure, different plant species take different strategies in response to metal-induced stress. Largely, plants can be distinguished in four groups: metal-sensitive species, metal-resistant excluder species, metal-tolerant non-hyperaccumulator species, and metal-hypertolerant hyperaccumulator species, each having different molecular mechanisms to accomplish their resistance/tolerance to metal stress or reduce the negative consequences of metal toxicity. Plant responses to heavy metals are molecularly regulated in a process called metal homeostasis, which also includes regulation of the metal-induced reactive oxygen species (ROS) signaling pathway. ROS generation and signaling plays an important duel role in heavy metal detoxification and tolerance. In this review, we will compare the different molecular mechanisms of nutritional (Zn) and non-nutritional (Cd) metal homeostasis between metal-sensitive and metal-adapted species. We will also include the role of metal-induced ROS signal transduction in this comparison, with the aim to provide a comprehensive overview on how plants cope with Zn/Cd stress at the molecular level.
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Closely related species often show substantial differences in ecological traits that allow them to occupy different environmental niches. For few of these systems is it clear what the genomic basis of adaptation is and whether a few loci of major effect or many genome-wide differences drive species divergence. Four cryptic species of the tabletop coral Acropora hyacinthus are broadly sympatric in American Samoa; here we show that two common species have differences in key environmental traits such as microhabitat distributions and thermal stress tolerance. We compared gene expression patterns and genetic polymorphism between these two species using RNA-Seq. The vast majority of polymorphisms are shared between species, but the two species show widespread differences in allele frequencies and gene expression, and tend to host different symbiont types. We find that changes in gene expression are related to changes in the frequencies of many gene regulatory variants, but that many of these differences are consistent with the action of genetic drift. However, we observe greater genetic divergence between species in amino acid replacement polymorphisms compared to synonymous variants. These findings suggest that polygenic evolution plays a major role in driving species differences in ecology and resilience to climate change. This article is protected by copyright. All rights reserved
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By 4000 years ago, people had introduced maize to the southwestern United States; full agriculture was established quickly in the lowland deserts but delayed in the temperate highlands for 2000 years. We test if the earliest upland maize was adapted for early flowering, a characteristic of modern temperate maize. We sequenced fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the temperate Southwest. Indirectly validated genomic models predicted that Turkey Pen maize was marginally adapted with respect to flowering, as well as short, tillering, and segregating for yellow kernel color. Temperate adaptation drove modern population differentiation and was selected in situ from ancient standing variation. Validated prediction of polygenic traits improves our understanding of ancient phenotypes and the dynamics of environmental adaptation.
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Two genes, SlZnT1 and SlZnT2, encoding Cation Diffusion Facilitator (CDF) family transporters were isolated from Suillus luteus mycelium by genome walking. Both gene models are very similar and phylogenetic analysis indicates that they are most likely the result of a recent gene duplication event. Comparative sequence analysis of the deduced proteins predicts them to be Zn transporters. This function was confirmed by functional analysis in yeast for SlZnT1. SlZnT1 was able to restore growth of the highly Zn sensitive yeast mutant Δzrc1 and localized to the vacuolar membrane. Transformation of Δzrc1 yeast cells with SlZnT1 resulted in an increased accumulation of Zn compared to empty vector transformed Δzrc1 yeast cells and equals Zn accumulation in wild type yeast cells. We were not able to express functional SlZnT2 in yeast. In S. luteus, both SlZnT genes are constitutively expressed whatever the external Zn concentrations. A labile Zn pool was detected in the vacuoles of S. luteus free-living mycelium. Therefore we conclude that SlZnT1 is indispensable for maintenance of Zn homeostasis by transporting excess Zn into the vacuole. This article is protected by copyright. All rights reserved.
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Ectomycorrhizal (ECM) fungi largely determine the element offer at the fungusroot interface, although they do not take over the plant nutrient uptake system. In complex forest soils, trees undoubtedly benefit from the well-adapted nutrient acquisition strategies evolved in the huge diversity of ECM fungi that occupy the numerous niches in the different soil types. As with all organisms, mycorrhizal fungi feature genes encoding proteins involved in trace element acquisition, storage and remobilization to assure cellular homeostasis regardless of natural external fluctuations. A constant cellular concentration of essential trace elements is required to secure growth and reproduction and to overcome toxicity. Transcriptome analysis is the most prominently used approach to identify genes and gene products involved in trace element homeostasis. Imbalances in the cellular homeostasis of trace elements, even brief ones, produces reactive oxygen species (ROS). ROS can be generated directly by redox-active elements or indirectly by redox-inactive elements.
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Microgeographic adaptation provides a particularly interesting context for understanding the genetic basis of phenotypic divergence, and may also present unique empirical challenges. In particular, plant adaptation to extreme soil mosaics may generate barriers to gene flow or shifts in mating system that confound simple genomic scans for adaptive loci. Here, we combine three approaches - QTL mapping of candidate intervals in controlled crosses, population resequencing (PoolSeq), and analyses of wild recombinant individuals - to investigate one trait associated with Mimulus guttatus (yellow monkeyflower) adaptation to geothermal soils in Yellowstone National Park. We mapped a major QTL causing dense leaf trichomes in thermally-adapted plants to a < 50kb region of Linkage Group 14 (Tr14) previously implicated in trichome divergence between independent M. guttatus populations. A PoolSeq scan of Tr14 region revealed a cluster of six genes, co-incident with the inferred QTL peak, with high allele frequency differences sufficient to explain observed phenotypic differentiation. One of these, the R2R3 MYB transcription factor Migut.N02661, is a plausible functional candidate, and was also strongly-associated (r(2) = 0.27) with trichome phenotype in analyses of wild-collected admixed individuals. Although functional analyses will be necessary to definitively link molecular variants in Tr14 with trichome divergence, our analyses are a major step in that direction. They point to a simple, and parallel, genetic basis for one axis of Mimulus guttatus adaptation to an extreme habitat, suggest a broadly conserved genetic basis for trichome variation across flowering plants, and pave the way for further investigations of this challenging case of microgeographic incipient speciation. This article is protected by copyright. All rights reserved.
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Population genetic models predict that alleles with small selection coefficients may be swamped by migration and will not contribute to local adaptation. But if most alleles contributing to standing variation are of small effect, how does local adaptation proceed? Here I review predictions of population and quantitative genetic models and use individual-based simulations to illustrate how the architecture of local adaptation depends on the genetic redundancy of the trait, the maintenance of standing genetic variation (VG), and the susceptibility of alleles to swamping. Even when population genetic models predict swamping for individual alleles, considerable local adaptation can evolve at the phenotypic level if there is sufficient VG. However, in such cases the underlying architecture of divergence is transient: FST is low across all loci, and no locus makes an important contribution for very long. Because this kind of local adaptation is mainly due to transient frequency changes and allelic covariances, these architectures will be difficult-if not impossible-to detect using current approaches to studying the genomic basis of adaptation. Even when alleles are large and resistant to swamping, architectures can be highly transient if genetic redundancy and mutation rates are high. These results suggest that drift can play a critical role in shaping the architecture of local adaptation, both through eroding VG and affecting the rate of turnover of polymorphisms with redundant phenotypic effects.
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The metal tolerance of isolates of some common ectomycorrhizal fungi (Suillus, Amanita, Paxillus) of Pinus and Betula spp., collected on heavily metal-polluted sites was compared with that of strains of the same species from non-polluted areas. The strains isolated from carpophores on unpolluted soils were greatly inhibited by the metals, whereas most of the strains derived from polluted soils were strongly tolerant to heavy metals; some strains were still able to grow very well at concentrations of 1000 μg g-1 Zn. The mechanisms for Zn and Cu tolerance are completely different. -from Authors
This unit describes how to use BWA and the Genome Analysis Toolkit (GATK) to map genome sequencing data to a reference and produce high-quality variant calls that can be used in downstream analyses. The complete workflow includes the core NGS data processing steps that are necessary to make the raw data suitable for analysis by the GATK, as well as the key methods involved in variant discovery using the GATK.
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Ectomycorrhizal (EM) fungi form symbiotic associations with plant roots that regulate nutrient exchange between forest plants and soil. Environmental metagenomics approaches that employ next-generation sequencing show great promise for studying EM symbioses, however, metatranscriptomic studies have been constrained by the inherent difficulties associated with isolation and sequencing of RNA from mycorrhizae. Here we apply an optimized method for combined DNA/RNA extraction using field-collected EM fungal-pine root clusters, together with protocols for taxonomic identification of expressed ribosomal RNA, and inference of EM function based on plant and fungal metatranscriptomics. We used transcribed portions of ribosomal RNA genes to identify several transcriptionally dominant fungal taxa associated with loblolly pine including Amphinema, Russula, and Piloderma spp. One taxon, Piloderma croceum, has a publically available genome that allowed us to identify patterns of gene content and transcript abundance. Over 1500 abundantly expressed Piloderma genes were detected from mycorrhizal roots, including genes for protein metabolism, cell signaling, electron transport, terpene synthesis, and other extracellular activities. In contrast, Piloderma gene encoding an ammonia transporter showed highest transcript abundance in soil samples. Our methodology highlights the potential of metatranscriptomics to identify genes associated with symbiosis and ecosystem function using field-collected samples.
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We evaluated soil contamination research based on a bibliometric analysis of 14,090 articles published in journals in the Science Citation Index and Social Sciences Citation Index bibliographic databases from 1999 to 2012, which revealed scientific outputs, subject categories and major journals, international collaboration and geographic distribution of authors and countries, keywords, and hot issues. The results suggested that research on soil contamination developed well with increasing scientific production and research collaboration. Environmental science, engineering environment, soil science, and applied microbiology were the most frequently used subject categories in soil contamination studies. Chemosphere was the most active journal in this field. The clusters of authors were more in the USA, Western European countries, China, Japan, and India. Q. X. Zhou of Nankai University was the most productive author, and S. P. Mcgrath of Rothamsted Research England published the most influential articles. The USA exceeded all other countries with the most independent and collaborative papers in research on global soil contamination. Heavy metal pollution was the hottest issue, and bioremediation is the most promising research topic in combating against heavy metal pollution of soils. The status of publication on soil contamination research described here is significant for researchers on soil contamination in their future work.
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Tools for estimating population structure from genetic data are now used in a wide variety of applications in population genetics. However, inferring population structure in large modern data sets imposes severe computational challenges. Here, we develop efficient algorithms for approximate inference of the model underlying the STRUCTURE program using a variational Bayesian framework. Variational methods pose the problem of computing relevant posterior distributions as an optimization problem, allowing us to build on recent advances in optimization theory to develop fast inference tools. In addition, we propose useful heuristic scores to identify the number of populations represented in a dataset and a new hierarchical prior to detect weak population structure in the data. We test the variational algorithms on simulated data, and illustrate using genotype data from the CEPH-Human Genome Diversity Panel. The variational algorithms are almost two orders of magnitude faster than STRUCTURE and achieve accuracies comparable to those of ADMIXTURE. Furthermore, our results show that the heuristic scores for choosing model complexity provide a reasonable range of values for the number of populations represented in the data, with minimal bias towards detecting structure when it is very weak. Our algorithm, fastSTRUCTURE, is freely available online at http://pritchardlab.stanford.edu/structure.html.
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Chemical toxins have been a persistent source of evolutionary challenges throughout the history of life, and deep within the genomic storehouse of evolutionary history lay ancient adaptations to diverse chemical poisons. However, the rate of change of contemporary environments mediated by human-introduced pollutants is rapidly screening this storehouse and severely testing the adaptive potential of many species. In this chapter, we briefly review the deep history of evolutionary adaptation to environmental toxins, and then proceed to describe the attributes of stressors and populations that may facilitate contemporary adaptation to pollutants introduced by humans. We highlight that phenotypes derived to enable persistence in polluted habitats may be multi-dimensional, requiring global genome-scale tools and approaches to uncover their mechanistic basis, and include examples of recent progress in the field. The modern tools of genomics offer promise for discovering how pollutants interact with genomes on physiological timescales, and also for discovering what genomic attributes of populations may enable resistance to pollutants over evolutionary timescales. Through integration of these sophisticated genomics tools and approaches with an understanding of the deep historical forces that shaped current populations, a more mature understanding of the mechanistic basis of contemporary ecological-evolutionary dynamics should emerge.
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A powerful metaphor for evolutionary diversification is a tree. A typical spreading tree has a single trunk, two or more major branches, several minor branches and many twigs. Its foundations--its roots and the remnants of the original seed--remain hidden from sight. The metaphor applies to the full set of living things on Earth--"the tree of life"--as well as to small groups of species, whether they are marsupial mammals or Hawaiian Drosophila. We can think of the typical crown of a tree as resembling the shape of an umbrella, with twig-bearing branches radiating in all directions (Figure 2, top). The ends of the twigs represent organisms adapted to separate microenvironments; the tree overall represents an adaptive radiation. Darwin's finches are a prime example of an adaptive radiation. Fourteen or perhaps 15 species, all derived from a common ancestor, occupy individual ecological niches to
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It is generally believed that isolation has played an important part in evolution. If an organism is to evolve so as to adapt itself to a special type of environment, e.g. a cave or a desert, it must not be swamped in each generation by migrants from the original habitat.(Received February 12 1930)(Accepted February 24 1930)
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Recent work has demonstrated that minerals in plants are circulated between root and shoot. This occurs during the whole life time and renders possible response to changing environmental conditions. This mineral circulation occurs through intensive solute exchange between xylem and phloem in roots, stems, and leaves. The transport form of heavy metals such as iron, manganes, zinc and copper in the phloem, whether ionic or chelated, is unclear in most cases. The unusual amino acid nicotianamine (NA) is ubiquitous throughout the plant kingdom. It is a chelator of several divalent transition metals. Its physiological role was investigated with the tomato mutant chloronerva, the only known NA-free multicellular plant. The mutant also exhibits disturbances of its iron metabolism and that of other heavy metals. This leads, among others, to a typical intercostal chlorosis and progressive iron accumulation in the leaves. From the heavy metal chelating properties of NA and from the phenotype of the mutant chloronerva it is concluded that NA is needed for normal distribution of heavy metals in young growing tissues fed via the phloem. This function could be fulfilled by mediating phloem loading or unloading of heavy metals as well as by preventing their precipitation in the alkaline phloem sap. An attempt is made to explain the chloronerva phenotype in the light of the phloem transport hypothesis of chelated iron.
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Summary • Zn tolerance was investigated in populations of four ectomycorrhizal fungi: Suillus luteus, Suillus bovinus, Rhizopogon luteolus and Paxillus involutus. The fungi were collected in pioneer pine forests at 14 different locations, situated along a Zn pollution gradient. Genetic adaptation to Zn toxicity was previously presumed in a population of S. luteus. • Mycelial biomass production was assessed for 235 isolates exposed to increasing Zn2+ stress. EC50 concentrations were determined. • Adaptive Zn tolerance was found in the three species from the Suilloid clade and not in P. involutus. The Suilloid fungi collected within 5 km from a Zn smelter were highly Zn-tolerant, in contrast to isolates collected at least 15 km away from a pollution source. Mixed populations with tolerant and sensitive S. luteus isolates were found in a transition zone, between 5 and 15 km from the Zn smelters. • The severe Zn pollution in the surroundings of the Zn smelters has clearly triggered the evolution of an increased Zn tolerance in the pioneer Suilloid fungi. With increasing distances from the Zn smelters, the frequency of Zn-tolerant genotypes decreases.
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Twenty-one isolates of the ectomycorrhizal fungus Suillus luteus were screened for their tolerance to the heavy metals Zn, Cd, Cu and Ni, measured as inhibition of radial growth and biomass production. Two populations from even-aged pine stands were investigated: 10 isolates were obtained from an area polluted with high levels of Zn, Cd and Cu, and 11 isolates were obtained from a control population located in a nearby unpolluted area. RFLP patterns of the internal transcribed spacer region of the isolates confirmed the morphological identification of the carpophores. All isolates were maintained on basic medium without elevated metals to avoid phenotypically acquired metal tolerance. The in vitro Zn and Cd tolerance of the S. luteus isolates from the polluted habitat were significantly higher than the tolerances measured in the isolates from the nonpolluted site. This observation suggests that the elevated soil metal concentrations might be responsible for the evolution of adaptive Zn and Cd tolerance. Tolerance was maintained in an isolate not exposed to elevated metals for 3 yr. The two S. luteus populations did not differ in tolerance to Cu and Ni. The mechanisms for the adaptive Zn and Cd tolerance are not identical as there was no correlation between response to the two metals; the most Zn-tolerant isolate was the most sensitive for Cd in the metal-tolerant population. Zinc did not accumulate in basidiocarp tissue, whereas Cd levels in basidiocarps were significantly higher in the population on the polluted site. Inter-simple sequence-repeat fingerprints showed that 90% of the isolates were from different individuals. The genetic variation in the population from the unpolluted site was considerably larger than that observed at the polluted site.
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Basidiospores from five randomly selected species of mycorrhiza-forming Hymenomycetes, viz. Laccaria laccata, Amanita muscaria, Lactarius helvus, Paxillus involutus, and Leccinum scabrum, did not germinate on any agar media tested (except for very few and irregular germinations in A. muscaria), nor did an addition of activated charcoal or a living Rhodotorula glutinis colony induce spore germination. However, with these two supplements together on the same agar plate slight germination occurred in all five species. In P. involutus percentage germination was further increased by a volatile factor produced by the mycelium of P. involutus. In L. scabrum a non-volatile substance exuded from its own mycelium strongly promoted germ vesicle and germ tube formation in the presence of activated charcoal. In both of these mycelial germination-inducing factors a certain specificity was indicated.
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The search for the alleles that matter, the quantitative trait nucleotides (QTNs) that underlie heritable variation within populations and divergence among them, is a popular pursuit. But what is the question to which QTNs are the answer? Although their pursuit is often invoked as a means of addressing the molecular basis of phenotypic evolution or of estimating the roles of evolutionary forces, the QTNs that are accessible to experimentalists, QTNs of relatively large effect, may be uninformative about these issues if large-effect variants are unrepresentative of the alleles that matter. Although 20th century evolutionary biology generally viewed large-effect variants as atypical, the field has recently undergone a quiet realignment toward a view of readily discoverable large-effect alleles as the primary molecular substrates for evolution. I argue that neither theory nor data justify this realignment. Models and experimental findings covering broad swaths of evolutionary phenomena suggest that evolution often acts via large numbers of small-effect polygenes, individually undetectable. Moreover, these small-effect variants are different in kind, at the molecular level, from the large-effect alleles accessible to experimentalists. Although discoverable QTNs address some fundamental evolutionary questions, they are essentially misleading about many others.
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There is a long tradition in population genetics of exploring the maintenance of variation under migration-selection balance using deterministic models that assume infinite population size. With finite population size, stochastic dynamics can greatly reduce the potential for the maintenance of polymorphism, but this has yet to be explored in detail. Here, classical two-patch models are extended to predict: (1) the probability of a locally beneficial mutation rising in frequency in the patch where it is favored and (2) the critical threshold migration rate above which the maintenance of polymorphism is much less likely. Individual-based simulations show that these approximations provide accurate predictions across a wide range of parameter space.