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Street, N. R.

Publications and source records attributed to Street, N. R..

17 recordsLinked to original sources

Comparative co-expression reveals a regulatory core shared by angiosperm and conifer roots under cold

* Climate change is reducing the boreal snowpack that insulates soils, exposing tree roots to more frequent freezing. The molecular cold response of roots is poorly characterised, and its conservation across the angiosperm-gymnosperm divide is unknown. We asked how much of the root cold response is shared among divergent boreal trees. * We profiled fine-root transcriptomes of four boreal trees (Picea abies, Pinus sylvestris, Betula pendula and Populus tremula) and two Arabidopsis thaliana ecotypes during a ten-day 5 {degrees}C treatment by RNA sequencing, and used comparative co-expression to detect conserved regulation independently of response timing. * Expressed genes were largely shared, but the genes differentially expressed, and the timing of their response, diverged between species. Despite this, a core of orthologues retained conserved co-expression neighbourhoods across more than 300 million years, enriched for growth regulation, metabolism and stress signalling, including a gibberellin-related metabolic component of the growth response. * The root cold response is therefore species specific in identity and timing, yet underlain by a conserved co-expression core.

plant biology↗

Comparative genomics of abiotic stress response in Norway spruce and Scots pine

Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) are dominant boreal forest species with globally important contributions to carbon capture and storage and sustain an extensive forestry industry. Both species have adapted to cold and episodic drought, yet each occupies a distinct ecological niche. How conserved their stress responses are, which features are lineage-specific, and how far mechanisms known from herbaceous angiosperms apply, remain open questions of importance in the face of ongoing climate change. We profiled roots and needles of both species under drought and cold, combining differential expression with an orthology-aware comparative co-expression framework that places each gene on a conservation-divergence gradient. Differential expression was largely organ- and stress-specific, yet cross-species overlap at the orthogroup level was extensive and increased with stress intensity. Comparative co-expression recovered a further conserved regulatory backbone that per-timepoint differential expression did not resolve, enriched for abscisic-acid-centred signalling, oxidative and osmotic-stress responses and growth suppression, and containing canonical stress response transcription-factor families including NAC, WRKY and bZIP/ABF. The breadth of co-expression conservation for a gene was coupled to purifying selection on its coding sequence and to network connectivity. Additionally, segmental duplicates shared between the species were enriched among conserved drought circuits, whereas lineage-specific duplicates were enriched among genes lacking conserved co-expression. Regulatory conservation and genome architecture thus describe a single conservation-divergence axis, providing an evolution-anchored criterion that helps separate candidate core regulators (which are conserved, network-central and constrained) from reactive change that differential expression alone cannot resolve. Significance statementCold and drought are recurring threats to boreal forests, yet how conifers coordinate their responses, and how much of that response is evolutionarily conserved, has been difficult to establish. Comparing Norway spruce and Scots pine, two species separated by a deep evolutionary divergence, we show that the genes whose co-expression is most broadly conserved between the species are also those under the strongest purifying selection on their protein-coding sequences. As these two species diverged so long ago, this conserved regulatory core stands out as an evolutionary signal that simple comparisons of differentially expressed genes fail to capture. The approach provides an evolution-anchored way to distinguish genes central to the stress response from lineage-specific or reactive change.

plant biology↗

A drought stress-induced MYB transcription factor regulates pavement cell shape in leaves of European aspen (Populus tremula)

The leaf pavement cells of many plant species develop fascinating jigsaw puzzle-like shapes in which neighboring cells interdigitate with each other, providing an ideal model for the study of cell shape acquisition. We analyzed pavement cell shape complexity in a natural population of European aspen (Populus tremula) genotypes and then used a genome-wide association study (GWAS) approach to identify a new candidate gene in cell shape regulation, Potra2n8c18226, encoding the transcription factor MYB305a. We subsequently validated a role for MYB305a in regulating aspen leaf pavement cell shape. We then demonstrated that drought conditions strongly induced MYB305a promoter expression in these cells and provided evidence implying that MYB305a plays a role in simplification of the cell shape in response to drought stress. Finally, we demonstrated negative correlations of pavement cell shape complexity with water-use efficiency, as well as with average precipitation, latitude and longitude of the genotypes original sampling sites in the natural European aspen population. Taken together, our results suggest that climatic variables affect the shape complexity of pavement cells in aspen leaf and provide a first step towards unravelling the molecular mechanisms controlling pavement cell shape acquisition in this species in response to environmental conditions, by implicating the involvement of the transcription factor MY305a.

plant biology↗

Comparative regulomics provides novel insight into the evolution of wood formation across dicot and conifer trees

Understanding the regulatory program underlying wood formation is key to improving biomass production and carbon sequestration in trees. However, how wood formation evolved and how these programs have been rewired across lineages remains unclear. Here, we present the first high-spatial-resolution evo-devo resource spanning the wood transcriptomes of six tree species - three dicots and three conifers - capturing 250 million years of evolutionary divergence. Using orthology-aware co-expression network analysis, we identified genes with conserved and lineage-specific expression patterns. By integrating chromatin accessibility data and transcription factor motif analysis, we further inferred regulatory networks for xylem differentiation and secondary cell wall formation. We demonstrate how this dataset can be used to answer long standing questions in wood biology related to differences in acetylation of cell wall polymers and master regulators of xylem specification across dicot and conifer tree species. The data offer a foundational resource for the tree biology and evo-devo communities, and are publicly available at PlantGenIE.org.

genomics↗

A transcriptome atlas of zygotic and somatic embryogenesis in Norway spruce

Somatic embryogenesis (SE) is a powerful model system for studying embryo development and an important method for scaling up availability of elite and climate-adapted genetic material of Norway spruce (Picea abies L. Karst). However, there are several steps during the development of the somatic embryo (Sem) that are suboptimal compared to zygotic embryo (Zem) development. These differences are poorly understood and result in substantial yield losses during plant production, which limits cost-effective large-scale production of SE plants. This study presents a comprehensive data resource profiling gene expression during zygotic and somatic embryo development to support studies aiming to advance understanding of gene regulatory programmes controlling embryo development. Transcriptome expression patterns were analysed during zygotic embryogenesis (ZE) in Norway spruce, including separated samples of the female gametophytes and Zem and at multiple stages during SE. Expression data from eight developmental stages of SE, starting with pro-embryogenic masses (PEMs) up until germination, revealed extensive modulation of the transcriptome between the early and mid-stage maturing embryos and at the transition of desiccated embryos to germination. Comparative analysis of ZE and SE identified differences in timing relative to SE development and functional enrichment of these provided insight into the associated biological processes. Orthologs of transcription factors known to regulate embryo development in angiosperms were differentially expressed during Zem and Sem development and in the different zygotic embryo tissues, providing clues to the differences in development observed between Zem and Sem. This resource represents the most comprehensive dataset available for exploring embryo development in conifers. Significance StatementSomatic embryogenesis is used as a model system to study embryo development, however detailed information to verify similarities and explain differences between somatic and zygotic embryogenesis is largely missing for conifers. This data resource provides sequential mRNA transcriptome data from nine stages of conifer zygotic embryo and female gametophyte development, and eight stages of somatic embryo development, to enable exploration of biological questions and comparisons of the two developmental processes.

plant biology↗

Identification of new leaf intrinsic yield genes using cross-species network analysis in plants

With the need to increase plant productivity, one of the challenges plant scientists are facing is to identify genes playing a role in beneficial plant traits. Moreover, even when such genes are found, it is generally not trivial to transfer this knowledge about gene function across species to identify functional orthologs. Here, we focused on the leaf to study plant growth. First, we built leaf growth transcriptional networks in Arabidopsis thaliana, maize (Zea mays), and aspen (Populus tremula). Next, known growth regulators, here defined as genes that when mutated or ectopically expressed alter plant growth, together with cross-species conserved networks, were used as guides to predict novel Arabidopsis growth regulators. Using an in-depth literature screening, 34 out of 100 top predicted growth regulators were confirmed to affect leaf phenotype when mutated or overexpressed and thus represent novel potential growth regulators. Globally, these new growth regulators were involved in cell cycle, plant defense responses, gibberellin, auxin, and brassinosteroid signaling. Phenotypic characterization of loss-of-function lines confirmed two newly predicted growth regulators to be involved in leaf growth (NPF6.4 and LATE MERISTEM IDENTITY2). In conclusion, the presented network approach offers an integrative cross-species strategy to identify new genes involved in plant growth and development. One-sentence summaryCross-species network analysis results in the identification and validation of new growth regulators in Arabidopsis.

plant biology↗

Molecular basis of differential adventitious rooting competence in poplar genotypes

O_LIRecalcitrant adventitious root (AR) development is a major hurdle in propagating commercially important woody plants. Although significant progress has been made to identify genes involved in subsequent steps of AR development, the molecular basis of differences in apparent recalcitrance to form AR between easy-to-root and difficult-to-root genotypes remains unknown. C_LIO_LITo address this, we generated cambium tissue-specific transcriptomic data from stem cuttings of hybrid aspen, T89 (difficult-to-root) and hybrid poplar OP42 (easy-to-root) and used transgenic approaches to verify the role of several transcription factors (TF) in the control of adventitious rooting. C_LIO_LIIncreased peroxidase activity is positively correlated with better rooting. We found differentially expressed genes encoding Reactive Oxygen Species (ROS) scavenging proteins to be enriched in OP42 compared to T89. A higher number of differentially expressed TF in OP42 compared to T89 cambium cells was revealed by a more intense transcriptional reprograming in the former. PtMYC2, a potential negative regulator, was less expressed in OP42 compared to T89. Using transgenic approaches, we have demonstrated that PttARF17.1 and PttMYC2.1 negatively regulate adventitious rooting. C_LIO_LIOur results provide insights into the molecular basis of genotypic differences in AR and implicate differential expression of the master regulator MYC2 as a critical player in this process. C_LI

plant biology↗

Adaptive introgression and standing genetic variation, two facilitators of adaptation to high latitudes in European aspen (Populus tremula L.)

Understanding local adaptation in plants from a genomic perspective has become a key research area given the ongoing climate challenge and the concomitant requirement to conserve genetic resources. Perennial plants, such as forest trees, are good models to study local adaptation given their wide geographic distribution, largely outcrossing mating systems and demographic histories. We evaluated signatures of local adaptation in European aspen (Populus tremula) across Europe by means of whole genome re-sequencing of a collection of 411 individual trees. We dissected admixture patterns between aspen lineages and observed a strong genomic mosaicism in Scandinavian trees, evidencing different colonization trajectories into the peninsula from Russia, Central and Western Europe. As a consequence of the secondary contacts between populations after the last glacial maximum (LGM), we detected an adaptive introgression event in a genome region of [~]500kb in chromosome 10, harboring a large-effect locus that has previously been shown to contribute to adaptation to the short growing seasons characteristic of northern Scandinavia. Demographic simulations and ancestry inference suggest an Eastern origin - probably Russian - of the adaptive Nordic allele which nowadays is present in a homozygous state at the north of Scandinavia. The strength of introgression and positive selection signatures in this region is a unique feature in the genome. Furthermore, we detected signals of balancing selection, shared across regional populations, that highlight the importance of standing variation as a primary source of alleles that facilitate local adaptation. Our results therefore emphasize the importance of migration-selection balance underlying the genetic architecture of key adaptive quantitative traits.

evolutionary biology↗

Norway spruce deploys tissue specific canonical responses to acclimate to the cold

Cold acclimation in plants is a complex phenomenon involving numerous stress-responsive transcriptional and metabolic pathways. Existing gene expression studies have primarily addressed short-term cold acclimation responses in herbaceous plants, while few have focused on perennial evergreens, such as conifers, that survive extremely low temperatures during winter. To characterize the transcriptome changes during cold acclimation in Picea abies (L.) H. Karst (Norway spruce), we performed RNA-Sequencing analysis of needles and roots subjected to a chilling progression (5 {degrees}C) followed by 10 days at freezing temperature (-5 {degrees}C). Comparing gene expression responses of needles against Arabidopsis thaliana L. (Arabidopsis) leaves, our results showed that early transient inductions were observed in both species but the transcriptional response of Norway spruce was delayed. Our results indicate that, similar to herbaceous species, Norway spruce principally utilizes early response transcription factors (TFs) that belong to the APETALA 2/ethylene-responsive element binding factor (AP2/ERF) superfamily and NACs. However, unique to the Norway spruce response was a large group of TFs that mounted a late transcriptional response to low temperature. A predicted regulatory network analysis identified key conserved TFs, including a root-specific bHLH101 homolog and other members of the same family with a pervasive role in cold regulation, such as homologs of ICE1 and AKS3 and also homologs of the NAC (anac47 and anac28) and AP2/ERF superfamilies (DREB2 and ERF3), providing new functional insights into cold stress response strategies in Norway spruce. One sentence summaryNorway spruce shares elements of the cold regulon described in herbaceous species but has undescribed components that contribute to the cold tolerance of this evergreen coniferous species.

plant biology↗

The mitogenome of Norway spruce and a reappraisal of mitochondrial recombination in plants

Plant mitogenomes can be difficult to assemble because they are structurally dynamic and prone to intergenomic DNA transfers, leading to the unusual situation where an organelle genome is far outnumbered by its nuclear counterparts. As a result, comparative mitogenome studies are in their infancy and some key aspects of genome evolution are still known mainly from pre-genome, qualitative methods. To help address these limitations, we combined machine learning and in silico enrichment of mitochondrial-like long reads to assemble the bacterial-sized mitogenome of Norway spruce (Pinaceae: Picea abies). We conducted comparative analyses of repeat abundance, intergenomic transfers, substitution and rearrangement rates, and estimated repeat-by-repeat homologous recombination rates. Prompted by our discovery of highly recombinogenic small repeats in P. abies, we assessed the genomic support for the prevailing hypothesis that intramolecular recombination is predominantly driven by repeat length, with larger repeats facilitating DNA exchange more readily. Overall, we found mixed support for this view: recombination dynamics were heterogeneous across vascular plants and highly active small repeats (ca. 200 bp) were present in about a third of studied mitogenomes. As in previous studies, we did not observe any robust relationships among commonly-studied genome attributes, but we identify variation in recombination rates as a underinvestigated source of plant mitogenome diversity.

genomics↗

Constructing a high-density linkage map to infer the genomic landscape of recombination rate variation in European Aspen (Populus tremula)

The rate of meiotic recombination is one of the central factors determining levels of linkage disequilibrium and the efficiency of natural selection, and many organisms show a positive correlation between local rates of recombination and levels of nucleotide diversity indicating that linked selection is an important factor determining genome-wide levels of nucleotide diversity. Several methods for estimating recombination rates from segregating polymorphisms in natural populations have recently been developed. These methods have been extensively used in part because they are relatively simple to implement even in many non-model organisms, but also because they potentially offer higher resolution than traditional map-based methods. However, thorough comparisons of LD and map-based estimates of recombination are not readily available in plants. Here we present a new, high-resolution linkage map for Populus tremula and use this to estimate variation in recombination rates across the P. tremula genome. We compare these results to recombination rates estimated based on linkage disequilibrium in a large number of unrelated individuals. We also assess how variation in recombination rates is associated with genomic features, such as gene density, repeat density and methylation levels. We find that recombination rates obtained from the two methods largely agree, although the LD-based method identify a number of genomic regions with very high recombination rates that the map-based method fail to detect. Linkage map and LD-based estimates of recombination rates are positively correlated and show similar correlations with other genomic features, showing that both methods can accurately infer recombination rate variation across the genome.

evolutionary biology↗

Candidate regulators and target genes of drought stress in needles and roots of Norway spruce

Drought stress impacts on seedling establishment, survival and whole-plant productivity. Drought stress responses have been extensively studied at the physiological and molecular level in angiosperms, particularly in agricultural species and the model Arabidopsis thaliana, with the vast majority of work performed on aboveground tissues. Boreal forests are dominated by coniferous tree species and cover vast areas of the terrestrial surface. These areas are predicted to be particularly influenced by ongoing climate change and will be exposed to more frequent and acute drought. The associated impact at all stages of the forest tree life cycle is expected to have large-scale ecological and economic impacts. To provide a comprehensive understanding of the drought response mechanisms of Picea abies seedlings, we assayed the physiological response of needles and transcriptional responses of roots and needles after exposure to mild and severe drought. Shoots and needles showed extensive reversible plasticity for physiological measures indicative of drought response mechanisms, including stomatal conductance (gs) and shoot water potential. Root and needle transcriptional responses contrasted, with an extensive root-specific down-regulation of growth. When we compared the responses of P. abies with previously-characterised A. thaliana drought response genes, we found that the majority of the genes were conserved across lineages. However, in P. abies, transcription factors (TFs) previously identified as belonging to the ABA-dependent pathway had a more limited role and most differentially expressed genes were specific to the stress response of P. abies. These results highlight the importance of profiling both above- and below-ground tissues and provide a comprehensive framework to advance understanding of the drought response mechanism of P. abies.\n\nOne sentence summaryAnalysis of the drought transcriptome of Norway spruce reveals divergent molecular response pathways in conifers.

plant biology↗

An ultra-dense haploid genetic map for evaluating the highly fragmented genome assembly of Norway spruce (Picea abies)

Norway spruce (Picea abies (L.) Karst.) is a conifer species of substanital economic and ecological importance. In common with most conifers, the P. abies genome is very large ([~]20 Gbp) and contains a high fraction of repetitive DNA. The current P. abies genome assembly (v1.0) covers approximately 60% of the total genome size but is highly fragmented, consisting of >10 million scaffolds. The genome annotation contains 66,632 gene models that are at least partially validated (www.congenie.org), however, the fragmented nature of the assembly means that there is currently little information available on how these genes are physically distributed over the 12 P. abies chromosomes. By creating an ultra-dense genetic linkage map, we anchored and ordered scaffolds into linkage groups, which complements the fine-scale information available in assembly contigs. Our ultra-dense haploid consensus genetic map consists of 21,056 markers derived from 14,336 scaffolds that contain 17,079 gene models (25.6% of the validated gene models) that we have anchored to the 12 linkage groups. We used data from three independent component maps, as well as comparisons with previously published Picea maps to evaluate the accuracy and marker ordering of the linkage groups. We demonstrate that approximately 3.8% of the anchored scaffolds and 1.6% of the gene models covered by the consensus map have likely assembly errors as they contain genetic markers that map to different regions within or between linkage groups. We further evaluate the utility of the genetic map for the conifer research community by using an independent data set of unrelated individuals to assess genome-wide variation in genetic diversity using the genomic regions anchored to linkage groups. The results show that our map is sufficiently dense to enable detailed evolutionary analyses across the P. abies genome.

genetics↗

Seidr: A toolkit for calculation of crowd networks

Gene regulatory and gene co-expression networks are powerful research tools for identifying biological signal within high-dimensional gene expression data. In recent years, research has focused on addressing shortcomings of these techniques with regard to the low signal-to-noise ratio, non-linear interactions and dataset dependent biases of published methods. Furthermore, it has been shown that aggregating networks from multiple methods provides improved results. Despite this, few usable and scalable software tools have been implemented to perform such best-practice analyses. Here, we present Seidr (stylized Seithr), a software toolkit designed to assist scientists in gene regulatory and gene co-expression network inference. Seidr creates community networks to reduce algorithmic bias and utilizes noise corrected network backboning to prune noisy edges in the networks. Using benchmarks in real-world conditions across three eukaryotic model organisms, Saccharomyces cerevisiae, Drosophila melanogaster, and Arabidopsis thaliana, we show that individual algorithms are biased toward functional evidence for certain gene-gene interactions. We further demonstrate that the community network is less biased, providing robust performance across different standards and comparisons for the model organisms. Finally, we apply Seidr to a network of drought stress in Norway spruce (Picea abies (L.) H. Krast) as an example application in a non-model species. We demonstrate the use of a network inferred using Seidr for identifying key components, communities and suggesting gene function for non-annotated genes.

bioinformatics↗

Natural variation at FLOWERING LOCUS T2 mediates local adaptation in a key life history trait in European aspen

BackgroundThe initiation of growth cessation and dormancy represent critical life-history tradeoffs between survival and growth, and have important fitness effects in perennial plants. Such adaptive life history traits often show strong local adaptation along environmental gradients but despite their importance, the genetic architecture of these traits remains poorly understood.\n\nResultsWe integrate whole genome re-sequencing with environmental and phenotypic data from common garden experiments to investigate the genomic basis of local adaptation across a latitudinal gradient in European aspen (Populus tremula). We discover a single genomic region containing the PtFT2 gene that mediates local adaptation in the timing of bud set and that explains 65% of the observed genetic variation in bud set. This locus is the likely target of a recent selective sweep that originated right before or during colonization of northern Scandinavia following the last glaciation. Field and greenhouse experiments confirm that variation in PtFT2 gene expression affect the phenotypic variation in bud set that we observe in wild natural populations.\n\nConclusionsOur results reveal a major effect locus that determine the timing of bud set and that have facilitated rapid adaptation to shorter growing seasons and colder climates in European aspen. The discovery of a single locus explaining a substantial fraction of the variation in a key life history trait is remarkable given that such traits are generally considered to be highly polygenic. These findings provide a dramatic illustration of how loci of large-effect for adaptive traits can arise and be maintained over large geographical scales in natural populations.

evolutionary biology↗

Interspecific plastome recombination reveals ancient reticulate evolution in Picea (Pinaceae)

Plastid sequences are a cornerstone in plant systematic studies and key aspects of their evolution, such as uniparental inheritance and absent recombination, are often treated as axioms. While exceptions to these assumptions can profoundly influence evolutionary inference, detecting them can require extensive sampling, abundant sequence data, and detailed testing. Using advancements in high-throughput sequencing, we analyzed the whole plastomes of 65 accessions of Picea, a genus of ~35 coniferous forest tree species, to test for deviations from canonical plastome evolution. Using complementary hypothesis and data-driven tests, we found evidence for chimeric plastomes generated by interspecific hybridization and recombination in the clade comprising Norway spruce (P. abies) and ten other species. Support for interspecific recombination remained after controlling for sequence saturation, positive selection, and potential alignment artifacts. These results reconcile previous conflicting plastid-based phylogenies and strengthen the mounting evidence of reticulate evolution in Picea. Given the relatively high frequency of hybridization and biparental plastid inheritance in plants, we suggest interspecific plastome recombination may be more widespread than currently appreciated and could underlie reported cases of discordant plastid phylogenies.

genomics↗

High-spatial-resolution transcriptome profiling reveals uncharacterized regulatory complexity underlying cambial growth and wood formation in Populus tremula

Trees represent the largest terrestrial carbon sink and a renewable source of ligno-cellulose. There is significant scope for yield and quality improvement in these largely undomesticated species, and efforts to engineer new, elite varieties will benefit from an improved understanding of the transcriptional network underlying cambial growth and wood formation. We generated high-spatial-resolution RNA Sequencing data spanning the secondary phloem, vascular cambium and wood forming tissues. The transcriptome comprised 28,294 expressed, previously annotated genes, 78 novel protein-coding genes and 567 long intergenic non-coding RNAs. Most paralogs originating from the Salicaceae whole genome duplication were found to have diverged expression, with the notable exception of those with high expression during secondary cell wall deposition. Co-expression network analysis revealed that the regulation of the transcriptome underlying cambial growth and wood formation comprises numerous modules forming a continuum of active processes across the tissues. The high spatial resolution enabled identification of novel roles for characterised genes involved in xylan and cellulose biosynthesis, regulators of xylem vessel and fiber differentiation and lignification. The associated web resource (AspWood, http://aspwood.popgenie.org) integrates the data within a set of interactive tools for exploring the expression profiles and co-expression network.

plant biology↗