Biology subjects

Nordborg, M.

Publications and source records attributed to Nordborg, M..

12 recordsLinked to original sources

bioRxiv2018

Stage-specific transcriptomes and DNA methylomes indicate an early and transient loss of transposon control in Arabidopsis shoot stem cells

In contrast to animals, postembryonic development in plants is modular, and aerial organs originate from stem cells in the center of the shoot apical meristem (SAM) throughout life. Descendants of SAM stem cells in the subepidermal layer (L2) give also rise to male and female gametes (reviewed in 1) and are therefore considered primordial germ cells. In these cells, transmission of somatic mutations including virus and TE insertions must be avoided. Despite their essential role for plant development and intergenerational continuity, no comprehensive molecular analysis of SAM stem cells exists, due to their low number, deep embedding among non-stem cells, and difficult isolation. Here we present a comprehensive analysis of stage-specific gene expression and DNA methylation dynamics in Arabidopsis SAM stem cells. Stem cell expression signatures are mostly defined by development, but we also identified a core set of differentially expressed stemness genes. Surprisingly, vegetative SAM stem cells showed increased expression of transposable elements (TEs) relative to surrounding cells, despite high expression of genes connected to epigenetic silencing. We also find increasing methylation at CHG and a drop in CHH methylation at TEs before stem cells enter the reproductive lineage, indicating an onset of epigenetic reprogramming at an early stage. Transiently elevated TE expression is reminiscent of that in animal primordial germ cells (PGCs) 2 and demonstrates commonality of transposon biology. Our results connect SAM stem cells with germline development and transposon evolution and will allow future experiments to determine the degree of epigenetic heritability between generations.

developmental biology↗

bioRxiv2018

Genome duplication and reorganization in Aquilegia

BackgroundWhole-genome duplications (WGD) have dominated the evolutionary history of plants. One consequence of WGD is a dramatic restructuring of the genome as it undergoes diploidization, a process under which deletions and rearrangements of various sizes scramble the genetic material, leading to a repacking of the genome and eventual return to diploidy. Here, we investigate the history of WGD in the columbine genus Aquilegia, a basal eudicot, and use it to illuminate the origins of the core eudicots.\n\nResultsWithin-genome synteny confirms that columbines are ancient tetraploids, and comparison with the grape genome reveals that this tetraploidy appears to be shared with the core eudicots. Thus, the ancient gamma hexaploidy found in all core eudicots must have involved a two-step process: first tetraploidy in the ancestry of all eudicots, then hexaploidy in the ancestry of core eudicots. Furthermore, the precise pattern of synteny sharing suggests that the latter involved allopolyploidization, and that core eudicots thus have a hybrid origin.\n\nConclusionsNovel analyses of synteny sharing together with the well-preserved structure of the columbine genome reveal that the gamma hexaploidy at the root of core eudicots is likely a result of hybridization between a tetraploid and a diploid species.

genomics↗

bioRxiv2018

Adaptive Reduction of Male Gamete Number in a Selfing Species

The number of male gametes produced is critical for reproductive success and varies greatly between and within species1-3. Evolutionary reduction of male gamete production has been widely reported in plants as a hallmark of the selfing syndrome, as well as in humans. Such a reduction may simply represent deleterious decay4-7, but evolutionary theory predicts that breeding systems could act as a major selective force on male gamete number: while large numbers of sperm should be produced in highly promiscuous species because of male-male gamete competition1, reduced sperm numbers may be advantageous at lower outcrossing rates because of the cost of gamete production. Here we used genome-wide association study (GWAS) to show a signature of polygenic selection on pollen number in the predominantly selfing plant Arabidopsis thaliana. The top associations with pollen number were significantly more strongly enriched for signatures of selection than those for ovule number and 107 phenotypes analyzed previously, indicating polygenic selection8. Underlying the strongest association, responsible for 20% of total pollen number variation, we identified the gene REDUCED POLLEN NUMBER 1 affecting cell proliferation in the male germ line. We validated its subtle but causal allelic effects using a quantitative complementation test with CRISPR-Cas9-generated null mutants in a nonstandard wild accession. Our results support polygenic adaptation underlying reduced male gamete numbers.

evolutionary biology↗

bioRxiv2018

The Aquilegia genome: adaptive radiation and an extraordinarily polymorphic chromosome with a unique history

The columbine genus Aquilegia is a classic example of an adaptive radiation, involving a wide variety of pollinators and habitats. Here we present the genome assembly of A. coerulea Goldsmith, complemented by high-coverage sequencing data from 10 wild species covering the world-wide distribution. Our analyses reveal extensive allele sharing among species and demonstrate that introgression and selection played a role in the Aquilegia radiation. We also present the remarkable discovery that the evolutionary history of an entire chromosome differs from that of the rest of the genome - a phenomenon which we do not fully understand, but which highlights the need to consider chromosomes in an evolutionary context.

evolutionary biology↗

bioRxiv2017

Plant genes influence microbial hubs that shape beneficial leaf communities

Although complex interactions between hosts and microbial associates are increasingly well documented, we still know little about how and why hosts shape microbial communities in nature. In addition, host genetic effects on microbial communities vary widely depending on the environment, obscuring conclusions about which microbes are impacted and which plant functions are important. We characterized the leaf microbiota of 200 A. thaliana genotypes in eight field experiments and detected consistent host effects on specific, broadly distributed microbial OTUs. Host genetics disproportionately influenced hubs within the microbial communities, with their impact then percolating through the community, as evidenced by a decline in the heritability of particular OTUs with their distance to the nearest hub. By simultaneously measuring host performance, we found that host genetics associated with microbial hubs explained over 10% of the variation in lifetime seed production among host genotypes across sites and years. We successfully cultured one of these microbial hubs and demonstrated its growth-promoting effects on plants grown in sterile conditions. Finally, genome-wide association mapping identified many putatively causal genes with small effects on the relative abundance of microbial hubs across sites and years, and these genes were enriched for those involved in the synthesis of specialized metabolites, auxins and the immune system. Using untargeted metabolomics, we corroborate the consistent association of variation in specialized metabolites and microbial hubs across field sites. Together, our results reveal that host natural variation impacts the microbial communities in consistent ways across environments and that these effects contribute to fitness variation among host genotypes.

microbiology↗

bioRxiv2017

The genetic architecture of the network underlying flowering time variation in Arabidopsis thaliana

Flowering time is a key adaptive trait in plants and is tightly controlled by a complex regulatory network that responds to seasonal signals. In a rapidly changing climate, understanding the genetic basis of flowering time variation is important for both agriculture and ecology. Genetic mapping has revealed many genetic variants affecting flowering time, but the effects on the gene regulatory networks in population-scale are still largely unknown. We dissected flowering time networks using multi-layered Swedish population data from Arabidopsis thaliana, consisting of flowering time and transcriptome collected under constant 10{degrees}C growth temperature in addition to full genome sequence data. Our analysis identified multiple alleles of the key flowering time gene FLOWERING LOCUS C (FLC) as the primary determinant of the network underlying flowering time variation under our condition. Genetic variation of FLC affects multiple-pathways through known flowering-time genes including FLOWERING LOCUS T (FT), and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1). We demonstrated that an extremely simple single-locus model of FLC involving allelic variation and expression explains almost a half of flowering time variation, with 60% of the effect being mediated through FLC expression. Furthermore, the accuracy of the model fitted at 10{degrees}C is almost unchanged at 16{degrees}C.

genetics↗

bioRxiv2017

The Maternal Environment Interacts With Genetic Variation In Regulating Seed Dormancy In Arabidopsis thaliana

Seed dormancy is a complex adaptive trait that controls the timing of seed germination, one of the major fitness components in many plant species. Despite being highly heritable, seed dormancy is extremely plastic and influenced by a wide range of environmental cues. Here, using a set of 92 Arabidopsis thaliana lines from Sweden, we investigate the effect of seed maturation temperature on dormancy variation at the population level. The response to temperature differs dramatically between lines, demonstrating that genotype and the maternal environment interact in controlling the trait. By performing a genome-wide association study (GWAS), we identified several candidate genes that could account for this plasticity, two of which are involved in the photoinduction of germination. Altogether, our results provide insight into both the molecular mechanisms and the evolution of dormancy plasticity, and can serve to improve our understanding of environmentally dependent life-history transitions.\n\nHighlightThe effect of low seed-maturation temperatures on seed dormancy is highly variable in Arabidopsis thaliana accessions from Sweden, denoting strong genotype-environment interactions, and a genome-wide association study identified compelling candidates that could account for this plasticity.

plant biology↗

bioRxiv2017

Verification of Arabidopsis stock collections using SNPmatch - an algorithm for genotyping high-plexed samples

Large-scale studies such as the Arabidopsis thaliana 1001 Genomes Project aim to understand genetic variation in populations and link it to phenotypic variation. Such studies require routine genotyping of stocks to avoid sample contamination and mix-ups. To genotype samples efficiently and economically, sequencing must be inexpensive and data processing simple. Here we present SNPmatch, a tool which identifies the most likely strain (inbred line, or \"accession\") from a SNP database. We tested the tool by performing low-coverage sequencing of over 2000 strains. SNPmatch could readily genotype samples correctly from 1-fold coverage sequencing data, and could also identify the parents of F1 or F2 individuals. SNPmatch can be run either on the command line or through AraGeno (https://arageno.gmi.oeaw.ac.at), a web interface that permits sample genotyping from a user-uploaded VCF or BED file.\n\nAvailability and implementation: https://github.com/Gregor-Mendel-Institute/SNPmatch.git

genomics↗

bioRxiv2017

Patterns of polymorphism at the self-incompatibility locus in 1,083 Arabidopsis thaliana genomes

Although the transition to selfing in the model plant Arabidopsis thaliana involved the loss of the self-incompatibility (SI) system, it clearly did not occur due to the fixation of a single inactivating mutation at the locus determining the specificities of SI (the S-locus). At least three groups of divergent haplotypes (haplogroups), corresponding to ancient functional S-alleles, have been maintained at this locus, and extensive functional studies have shown that all three carry distinct inactivating mutations. However, the historical process of loss of SI is not well understood, in particular its relation with the last glaciation. Here, we took advantage of recently published genomic re-sequencing data in 1,083 Arabidopsis thaliana accessions that we combined with BAC sequencing to obtain polymorphism information for the whole S-locus region at a species-wide scale. The accessions differed by several major rearrangements including large deletions and inter-haplogroup recombinations, forming a set of haplogroups that are widely distributed throughout the native range and largely overlap geographically. Relict A. thaliana accessions that directly derive from glacial refugia are polymorphic at the S-locus, suggesting that the three haplogroups were already present when glacial refugia from the last Ice Age became isolated. Inter-haplogroup recombinant haplotypes were highly frequent, and detailed analysis of recombination breakpoints suggested multiple independent origins. These findings suggest that the complete loss of SI in A. thaliana involved independent self-compatible mutants that arose prior to the last Ice Age, and experienced further rearrangements during post-glacial colonization.

evolutionary biology↗

bioRxiv2016

Ancient hybridization and strong adaptation to viruses across African vervet monkey populations

Vervet monkeys (genus Chlorocebus, also known as African green monkeys), are highly abundant in savannahs and riverine forests throughout sub-Saharan Africa. They are amongst the most widely distributed nonhuman primates, show considerable phenotypic diversity, and have long been an important biomedical model for a variety of human diseases1 and in vaccine research2-4. They are particularly interesting for HIV/AIDS research as they are the most abundant natural hosts of simian immunodeficiency virus (SIV), a close relative of HIV. Here we present the first genome-wide survey of polymorphism in vervets, using sequencing data from 163 individuals sampled from across Africa and the Caribbean islands where vervets were introduced during the colonial era. We find high diversity, within and between taxa, and clear evidence that taxonomic divergence was reticulate rather than following a simple branching pattern. A scan for diversifying selection across vervet taxa yields gene enrichments much stronger than in similar studies on humans5. In particular, we report strong and highly polygenic selection signals affecting viral processes -- in line with recent evidence that proposes a driving role for viruses in protein evolution in mammals6. Furthermore, selection scores are highly elevated in genes whose human orthologs interact with HIV, and in genes that show a response to experimental SIV infection in vervet monkeys but not in rhesus macaques, suggesting that part of the signal reflects taxon-specific adaptation to SIV. Intriguingly, rather than affecting genes with antiviral and inflammatory-related functions7, selection in vervets appears to have primarily targeted genes involved in the transcriptional regulation of viruses, and in particular those that are harmful only under immunodeficiency, suggesting adaptation to living with SIV rather than defense against infection.

evolutionary biology↗

bioRxiv2016

Unstable inheritance of 45S rRNA genes in Arabidopsis thaliana

The considerable genome size variation in Arabidopsis thaliana has been shown largely to be due to copy number variation (CNV) in 45S ribosomal RNA (rRNA) genes. Surprisingly, attempts to map this variation by means of genome-wide association studies (GWAS) failed to identify either of the two likely sources, namely the nucleolar organizer regions (NORs). Instead, GWAS implicated a trans-acting locus, as if rRNA CNV was a phenotype rather than a genotype. To explain these results, we investigated the inheritance and stability of rRNA gene copy number using the variety of genetic resources available in A. thaliana -- F2 crosses, recombinant inbred lines, the multiparent advanced generation inter-cross population, and mutation accumulation lines. Our results clearly show that rRNA gene CNV can be mapped to the NORs themselves, with both loci contributing equally to the variation. However, NOR size is unstably inherited, and dramatic copy number changes are visible already within tens of generations, which explains why it is not possible to map the NORs using GWAS. We did not find any evidence of trans-acting loci in crosses, which is also expected since changes due to such loci would take very many generations to manifest themselves. rRNA gene copy number is thus an interesting example of \"missing heritability\" -- a trait that is heritable in pedigrees, but not in the general population.

genetics↗

bioRxiv2016

Genomic Rearrangements Considered as Quantitative Traits

To understand the population genetics of structural variants (SVs), and their effects on phenotypes, we developed an approach to mapping SVs, particularly transpositions, segregating in a sequenced population, and which avoids calling SVs directly. The evidence for a potential SV at a locus is indicated by variation in the counts of short-reads that map anomalously to the locus. These SV traits are treated as quantitative traits and mapped genetically, analogously to a gene expression study. Association between an SV trait at one locus and genotypes at a distant locus indicate the origin and target of a transposition. Using ultra-low-coverage (0.3x) population sequence data from 488 recombinant inbred Arabidopsis genomes, we identified 6,502 segregating SVs. Remarkably, 25% of these were transpositions. Whilst many SVs cannot be delineated precisely, PCR validated 83% of 44 predicted transposition breakpoints. We show that specific SVs may be causative for quantitative trait loci for germination, fungal disease resistance and other phenotypes. Further we show that the phenotypic heritability attributable to sequence anomalies differs from, and in the case of time to germination and bolting, exceeds that due to standard genetic variation. Gene expression within SVs is also more likely to be silenced or dysregulated. This approach is generally applicable to large populations sequenced at low-coverage, and complements the prevalent strategy of SV discovery in fewer individuals sequenced at high coverage.

genetics↗