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Closely related species often use the same genes to adapt to similar environments. However, we know little about why such genes possess increased adaptive potential and whether this is conserved across deeper evolutionary lineages. Adaptation to climate presents a natural laboratory to test these ideas, as even distantly related species must contend with similar stresses. Here, we re-analyse genomic data from thousands of individuals from 25 plant species as diverged as lodgepole pine and Arabidopsis (~300 Myr). We test for genetic repeatability based on within-species associations between allele frequencies in genes and variation in 21 climate variables. Our results demonstrate significant statistical evidence for genetic repeatability across deep time that is not expected under randomness, identifying a suite of 108 gene families (orthogroups) and gene functions that repeatedly drive local adaptation to climate. This set includes many orthogroups with well-known functions in abiotic stress response. Using gene co-expression networks to quantify pleiotropy, we find that orthogroups with stronger evidence for repeatability exhibit greater network centrality and broader expression across tissues (higher pleiotropy), contrary to the 'cost of complexity' theory. These gene families may be important in helping wild and crop species cope with future climate change, representing important candidates for future study.
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BACKGROUND: Drought adaptation is critical to many tree species persisting under climate change, however our knowledge of the genetic basis for trees to adapt to drought is limited. This knowledge gap impedes our fundamental understanding of drought response and application to forest production and conservation. To improve our understanding of the genomic determinants, architecture, and trait constraints, we assembled a reference genome and detected ~ 6.5 M variants in 432 phenotyped individuals for the foundational tree Corymbia calophylla. RESULTS: We found 273 genomic variants determining traits with moderate heritability (h2SNP = 0.26-0.64). Significant variants were predominantly in gene regulatory elements distributed among several haplotype blocks across all chromosomes. Furthermore, traits were constrained by frequent epistatic and pleiotropic interactions. CONCLUSIONS: Our results on the genetic basis for drought traits in Corymbia calophylla have several implications for the ability to adapt to climate change: (1) drought related traits are controlled by complex genomic architectures with large haplotypes, epistatic, and pleiotropic interactions; (2) the most significant variants determining drought related traits occurred in regulatory regions; and (3) models incorporating epistatic interactions increase trait predictions. Our findings indicate that despite moderate heritability drought traits are likely constrained by complex genomic architecture potentially limiting trees response to climate change.
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Secas , Epistasia Genética , Genômica , Genoma de Planta , Haplótipos , Locos de Características Quantitativas , Fenótipo , Polimorfismo de Nucleotídeo ÚnicoRESUMO
Grasses are hyper-accumulators of silicon (Si), which is known to alleviate diverse environmental stresses, prompting speculation that Si accumulation evolved in response to unfavourable climatic conditions, including seasonally arid environments. We conducted a common garden experiment using 57 accessions of the model grass Brachypodium distachyon, sourced from different Mediterranean locations, to test relationships between Si accumulation and 19 bioclimatic variables. Plants were grown in soil with either low or high (Si supplemented) levels of bioavailable Si. Si accumulation was negatively correlated with temperature variables (annual mean diurnal temperature range, temperature seasonality, annual temperature range) and precipitation seasonality. Si accumulation was positively correlated with precipitation variables (annual precipitation, precipitation of the driest month and quarter, and precipitation of the warmest quarter). These relationships, however, were only observed in low-Si soils and not in Si-supplemented soils. Our hypothesis that accessions of B. distachyon from seasonally arid conditions have higher Si accumulation was not supported. On the contrary, higher temperatures and lower precipitation regimes were associated with lower Si accumulation. These relationships were decoupled in high-Si soils. These exploratory results suggest that geographical origin and prevailing climatic conditions may play a role in predicting patterns of Si accumulation in grasses.
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Synteny, the ordering of sequences within homologous chromosomes, must be maintained within the genomes of sexually reproducing species for the sharing of alleles and production of viable, reproducing offspring. However, when the genomes of closely related species are compared, a loss of synteny is often observed. Unequal homologous recombination is the primary mechanism behind synteny loss, occurring more often in transposon rich regions, and resulting in the formation of chromosomal rearrangements. To examine patterns of synteny among three closely related, interbreeding, and wild Eucalyptus species, we assembled their genomes using long-read DNA sequencing and de novo assembly. We identify syntenic and rearranged regions between these genomes and estimate that ~48% of our genomes remain syntenic while ~36% is rearranged. We observed that rearrangements highly fragment microsynteny. Our results suggest that synteny between these species is primarily lost through small-scale rearrangements, not through sequence loss, gain, or sequence divergence. Further examination of identified rearrangements suggests that rearrangements may be altering the phenotypes of Eucalyptus species. Our study also underscores that the use of single reference genomes in genomic variation studies could lead to reference bias, especially given the scale at which we show potentially adaptive loci have highly diverged, deleted, duplicated and/or rearranged. This study provides an unbiased framework to look at potential speciation and adaptive loci among a rapidly radiating foundation species of woodland trees that are free from selective breeding seen in most crop species.
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Eucalyptus , Eucalyptus/genética , Genoma , Sintenia/genética , Cromossomos , Análise de Sequência de DNA/métodosRESUMO
Oryza australiensis is a wild rice native to monsoonal northern Australia. The International Oryza Map Alignment Project emphasises its significance as the sole representative of the EE genome clade. Assembly of the O. australiensis genome has previously been challenging due to its high Long Terminal Repeat (LTR) retrotransposon (RT) content. Oxford Nanopore long reads were combined with Illumina short reads to generate a high-quality ~ 858 Mbp genome assembly within 850 contigs with 46× long read coverage. Reference-guided scaffolding increased genome contiguity, placing 88.2% of contigs into 12 pseudomolecules. After alignment to the Oryza sativa cv. Nipponbare genome, we observed several structural variations. PacBio Iso-Seq data were generated for five distinct tissues to improve the functional annotation of 34,587 protein-coding genes and 42,329 transcripts. We also report SNV numbers for three additional O. australiensis genotypes based on Illumina re-sequencing. Although genetic similarity reflected geographical separation, the density of SNVs also correlated with our previous report on variations in salinity tolerance. This genome re-confirms the genetic remoteness of the O. australiensis lineage within the O. officinalis genome complex. Assembly of a high-quality genome for O. australiensis provides an important resource for the discovery of critical genes involved in development and stress tolerance.
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Oryza , Genoma , Sequenciamento de Nucleotídeos em Larga Escala , Oryza/genética , Retroelementos/genética , Análise de Sequência de DNARESUMO
From its origins in Australia, Eucalyptus grandis has spread to every continent, except Antarctica, as a wood crop. It has been cultivated and bred for over 100 yr in places such as South Africa. Unlike most annual crops and fruit trees, domestication of E. grandis is still in its infancy, representing a unique opportunity to interrogate the genomic consequences of artificial selection early in the domestication process. To determine how a century of artificial selection has changed the genome of E. grandis, we generated single nucleotide polymorphism genotypes for 1080 individuals from three advanced South African breeding programmes using the EUChip60K chip, and investigated population structure and genome-wide differentiation patterns relative to wild progenitors. Breeding and wild populations appeared genetically distinct. We found genomic evidence of evolutionary processes known to have occurred in other plant domesticates, including interspecific introgression and intraspecific infusion from wild material. Furthermore, we found genomic regions with increased linkage disequilibrium and genetic differentiation, putatively representing early soft sweeps of selection. This is, to our knowledge, the first study of genomic signatures of domestication in a timber species looking beyond the first few generations of cultivation. Our findings highlight the importance of intra- and interspecific hybridization during early domestication.
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Domesticação , Genoma de Planta , Genômica , Melhoramento Vegetal , Polimorfismo de Nucleotídeo Único/genética , Seleção Genética , Madeira/genéticaRESUMO
The genetic consequences of adaptation to changing environments can be deciphered using population genomics, which may help predict species' responses to global climate change. Towards this, we used genome-wide SNP marker analysis to determine population structure and patterns of genetic differentiation in terms of neutral and adaptive genetic variation in the natural range of Eucalyptus grandis, a widely cultivated subtropical and temperate species, serving as genomic reference for the genus. We analysed introgression patterns at subchromosomal resolution using a modified ancestry mapping approach and identified provenances with extensive interspecific introgression in response to increased aridity. Furthermore, we describe potentially adaptive genetic variation as explained by environment-associated SNP markers, which also led to the discovery of what is likely a large structural variant. Finally, we show that genes linked to these markers are enriched for biotic and abiotic stress responses.
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Eucalyptus , Aclimatação , Adaptação Fisiológica/genética , Eucalyptus/genética , Genômica , Árvores/genéticaRESUMO
Global climate change poses a significant threat to natural communities around the world, with many plant species showing signs of climate stress. Grassland ecosystems are not an exception, with climate change compounding contemporary pressures such as habitat loss and fragmentation. In this study, we assess the climate resilience of Themeda triandra, a foundational species and the most widespread plant in Australia, by assessing the relative contributions of spatial, environmental and ploidy factors to contemporary genomic variation. Reduced-representation genome sequencing on 472 samples from 52 locations was used to test how the distribution of genomic variation, including ploidy polymorphism, supports adaptation to hotter and drier climates. We explicitly quantified isolation by distance (IBD) and isolation by environment (IBE) and predicted genomic vulnerability of populations to future climates based on expected deviation from current genomic composition. We found that a majority (54%) of genomic variation could be attributed to IBD, while an additional 22% (27% when including ploidy information) could be explained by two temperature and two precipitation climate variables demonstrating IBE. Ploidy polymorphisms were common within populations (31/52 populations), indicating that ploidy mixing is characteristic of T. triandra populations. Genomic vulnerabilities were found to be heterogeneously distributed throughout the landscape, and our analysis suggested that ploidy polymorphism, along with other factors linked to polyploidy, reduced vulnerability to future climates by 60% (0.25-0.10). Our data suggests that polyploidy may facilitate adaptation to hotter climates and highlight the importance of incorporating ploidy in adaptive management strategies to promote the resilience of this and other foundation species.
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Ecossistema , Poaceae , Austrália , Mudança Climática , Genômica , Ploidias , Poaceae/genéticaRESUMO
Epigenomic changes have been considered a potential missing link underlying phenotypic variation in quantitative traits but is potentially confounded with the underlying DNA sequence variation. Although the concept of epigenetic inheritance has been discussed in depth, there have been few studies attempting to directly dissect the amount of epigenomic variation within inbred natural populations while also accounting for genetic diversity. By using known genetic relationships between Brachypodium lines, multiple sets of nearly identical accession families were selected for phenotypic studies and DNA methylome profiling to investigate the dual role of (epi)genetics under simulated natural seasonal climate conditions. Despite reduced genetic diversity, appreciable phenotypic variation was still observable in the measured traits (height, leaf width and length, tiller count, flowering time, ear count) between as well as within the inbred accessions. However, with reduced genetic diversity there was diminished variation in DNA methylation within families. Mixed-effects linear modeling revealed large genetic differences between families and a minor contribution of DNA methylation variation on phenotypic variation in select traits. Taken together, this analysis suggests a limited but significant contribution of DNA methylation toward heritable phenotypic variation relative to genetic differences.
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Brachypodium , Brachypodium/genética , Metilação de DNA , Epigênese Genética , Epigenômica , Variação Genética , Genótipo , Humanos , FenótipoRESUMO
Spatial genetic patterns are influenced by numerous factors, and they can vary even among coexisting, closely related species due to differences in dispersal and selection. Eucalyptus (L'Héritier 1789; the "eucalypts") are foundation tree species that provide essential habitat and modulate ecosystem services throughout Australia. Here we present a study of landscape genomic variation in two woodland eucalypt species, using whole-genome sequencing of 388 individuals of Eucalyptus albens and Eucalyptus sideroxylon. We found exceptionally high genetic diversity (π ≈ 0.05) and low genome-wide, interspecific differentiation (FST = 0.15) and intraspecific differentiation between localities (FST ≈ 0.01-0.02). We found no support for strong, discrete population structure, but found substantial support for isolation by geographic distance (IBD) in both species. Using generalized dissimilarity modelling, we identified additional isolation by environment (IBE). Eucalyptus albens showed moderate IBD, and environmental variables have a small but significant amount of additional predictive power (i.e. IBE). Eucalyptus sideroxylon showed much stronger IBD and moderate IBE. These results highlight the vast adaptive potential of these species and set the stage for testing evolutionary hypotheses of interspecific adaptive differentiation across environments.
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Ecossistema , Eucalyptus/genética , Variação Genética/genética , Seleção Genética , Austrália , Eucalyptus/crescimento & desenvolvimento , Florestas , Fluxo Gênico , Genética Populacional , Genoma de Planta/genética , Genômica , Árvores/genética , Árvores/crescimento & desenvolvimentoRESUMO
Field-grown plants have variable exposure to sunlight as a result of shifting cloud-cover, seasonal changes, canopy shading, and other environmental factors. As a result, they need to have developed a method for dissipating excess energy obtained from periodic excessive sunlight exposure. Non-photochemical quenching (NPQ) dissipates excess energy as heat, however, the physical and molecular genetic mechanics of NPQ variation are not understood. In this study, we investigated the genetic loci involved in NPQ by first growing different Arabidopsis thaliana accessions in local and seasonal climate conditions, then measured their NPQ kinetics through development by chlorophyll fluorescence. We used genome-wide association studies (GWAS) to identify 15 significant quantitative trait loci (QTL) for a range of photosynthetic traits, including a QTL co-located with known NPQ gene PSBS (AT1G44575). We found there were large alternative regulatory segments between the PSBS promoter regions of the functional haplotypes and a significant difference in PsbS protein concentration. These findings parallel studies in rice showing recurrent regulatory evolution of this gene. The variation in the PSBS promoter and the changes underlying other QTLs could give insight to allow manipulations of NPQ in crops to improve their photosynthetic efficiency and yield.
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BACKGROUND: The development of whole genome bisulfite sequencing has made it possible to identify methylation differences at single base resolution throughout an entire genome. However, a persistent challenge in DNA methylome analysis is the accurate identification of differentially methylated regions (DMRs) between samples. Sensitive and specific identification of DMRs among different conditions requires accurate and efficient algorithms, and while various tools have been developed to tackle this problem, they frequently suffer from inaccurate DMR boundary identification and high false positive rate. RESULTS: We present a novel Histogram Of MEthylation (HOME) based method that takes into account the inherent difference in the distribution of methylation levels between DMRs and non-DMRs to discriminate between the two using a Support Vector Machine. We show that generated features used by HOME are dataset-independent such that a classifier trained on, for example, a mouse methylome training set of regions of differentially accessible chromatin, can be applied to any other organism's dataset and identify accurate DMRs. We demonstrate that DMRs identified by HOME exhibit higher association with biologically relevant genes, processes, and regulatory events compared to the existing methods. Moreover, HOME provides additional functionalities lacking in most of the current DMR finders such as DMR identification in non-CG context and time series analysis. HOME is freely available at https://github.com/ListerLab/HOME . CONCLUSION: HOME produces more accurate DMRs than the current state-of-the-art methods on both simulated and biological datasets. The broad applicability of HOME to identify accurate DMRs in genomic data from any organism will have a significant impact upon expanding our knowledge of how DNA methylation dynamics affect cell development and differentiation.
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Algoritmos , Metilação de DNA/genética , Aprendizado de Máquina , Animais , Simulação por Computador , Bases de Dados Genéticas , Camundongos , Anotação de Sequência Molecular , Fatores de TempoRESUMO
The development of model systems requires a detailed assessment of standing genetic variation across natural populations. The Brachypodium species complex has been promoted as a plant model for grass genomics with translation to small grain and biomass crops. To capture the genetic diversity within this species complex, thousands of Brachypodium accessions from around the globe were collected and genotyped by sequencing. Overall, 1897 samples were classified into two diploid or allopolyploid species, and then further grouped into distinct inbred genotypes. A core set of diverse B. distachyon diploid lines was selected for whole genome sequencing and high resolution phenotyping. Genome-wide association studies across simulated seasonal environments was used to identify candidate genes and pathways tied to key life history and agronomic traits under current and future climatic conditions. A total of 8, 22, and 47 QTL were identified for flowering time, early vigor, and energy traits, respectively. The results highlight the genomic structure of the Brachypodium species complex, and the diploid lines provided a resource that allows complex trait dissection within this grass model species.
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Aclimatação , Brachypodium/genética , Estudo de Associação Genômica Ampla/métodos , Características de História de Vida , Melhoramento Vegetal/métodos , Polimorfismo Genético , Genoma de Planta , Característica Quantitativa HerdávelRESUMO
BACKGROUND: High resolution and high throughput genotype to phenotype studies in plants are underway to accelerate breeding of climate ready crops. In the recent years, deep learning techniques and in particular Convolutional Neural Networks (CNNs), Recurrent Neural Networks and Long-Short Term Memories (LSTMs), have shown great success in visual data recognition, classification, and sequence learning tasks. More recently, CNNs have been used for plant classification and phenotyping, using individual static images of the plants. On the other hand, dynamic behavior of the plants as well as their growth has been an important phenotype for plant biologists, and this motivated us to study the potential of LSTMs in encoding these temporal information for the accession classification task, which is useful in automation of plant production and care. METHODS: In this paper, we propose a CNN-LSTM framework for plant classification of various genotypes. Here, we exploit the power of deep CNNs for automatic joint feature and classifier learning, compared to using hand-crafted features. In addition, we leverage the potential of LSTMs to study the growth of the plants and their dynamic behaviors as important discriminative phenotypes for accession classification. Moreover, we collected a dataset of time-series image sequences of four accessions of Arabidopsis, captured in similar imaging conditions, which could be used as a standard benchmark by researchers in the field. We made this dataset publicly available. CONCLUSION: The results provide evidence of the benefits of our accession classification approach over using traditional hand-crafted image analysis features and other accession classification frameworks. We also demonstrate that utilizing temporal information using LSTMs can further improve the performance of the system. The proposed framework can be used in other applications such as in plant classification given the environment conditions or in distinguishing diseased plants from healthy ones.
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Summary: We describe a rapid algorithm for demultiplexing DNA sequence reads with in-read indices. Axe selects the optimal index present in a sequence read, even in the presence of sequencing errors. The algorithm is able to handle combinatorial indexing, indices of differing length and several mismatches per index sequence. Availability and implementation: Axe is implemented in C, and is used as a command-line program on Unix-like systems. Axe is available online at https://github.com/kdmurray91/axe, and is available in Debian/Ubuntu distributions of GNU/Linux as the package axe-demultiplexer. Supplementary information: Supplementary data are available at Bioinformatics online.
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Algoritmos , Análise de Sequência de DNA/métodos , Software , Biologia ComputacionalRESUMO
This article comments on: Genome-wide signatures of flowering adaptation to climate temperature: Regional analyses in a highly diverse native range of Arabidopsis thaliana.
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Arabidopsis , Aclimatação , Clima , Genômica , TemperaturaRESUMO
As species face rapid environmental change, we can build resilient populations through restoration projects that incorporate predicted future climates into seed sourcing decisions. Eucalyptus melliodora is a foundation species of a critically endangered community in Australia that is a target for restoration. We examined genomic and phenotypic variation to make empirical based recommendations for seed sourcing. We examined isolation by distance and isolation by environment, determining high levels of gene flow extending for 500 km and correlations with climate and soil variables. Growth experiments revealed extensive phenotypic variation both within and among sampling sites, but no site-specific differentiation in phenotypic plasticity. Model predictions suggest that seed can be sourced broadly across the landscape, providing ample diversity for adaptation to environmental change. Application of our landscape genomic model to E. melliodora restoration projects can identify genomic variation suitable for predicted future climates, thereby increasing the long term probability of successful restoration.
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Variação Biológica da População , Mudança Climática , Recuperação e Remediação Ambiental/métodos , Eucalyptus/crescimento & desenvolvimento , Eucalyptus/genética , Variação Genética , Aclimatação , Adaptação Fisiológica , AustráliaRESUMO
Stress recovery may prove to be a promising approach to increase plant performance and, theoretically, mRNA instability may facilitate faster recovery. Transcriptome (RNA-seq, qPCR, sRNA-seq, and PARE) and methylome profiling during repeated excess-light stress and recovery was performed at intervals as short as 3 min. We demonstrate that 87% of the stress-upregulated mRNAs analyzed exhibit very rapid recovery. For instance, HSP101 abundance declined 2-fold every 5.1 min. We term this phenomenon rapid recovery gene downregulation (RRGD), whereby mRNA abundance rapidly decreases promoting transcriptome resetting. Decay constants (k) were modeled using two strategies, linear and nonlinear least squares regressions, with the latter accounting for both transcription and degradation. This revealed extremely short half-lives ranging from 2.7 to 60.0 min for 222 genes. Ribosome footprinting using degradome data demonstrated RRGD loci undergo cotranslational decay and identified changes in the ribosome stalling index during stress and recovery. However, small RNAs and 5'-3' RNA decay were not essential for recovery of the transcripts examined, nor were any of the six excess light-associated methylome changes. We observed recovery-specific gene expression networks upon return to favorable conditions and six transcriptional memory types. In summary, rapid transcriptome resetting is reported in the context of active recovery and cellular memory.
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Arabidopsis/genética , Arabidopsis/efeitos da radiação , Regulação para Baixo/genética , Regulação da Expressão Gênica de Plantas/efeitos da radiação , Genes de Plantas , Luz , Estresse Fisiológico/genética , Arabidopsis/fisiologia , Proteínas de Arabidopsis/genética , Proteínas de Arabidopsis/metabolismo , Metilação de DNA/genética , Perfilação da Expressão Gênica , Inativação Gênica , Loci Gênicos , Meia-Vida , Dinâmica não Linear , Biossíntese de Proteínas , Estabilidade de RNA/genética , RNA Mensageiro/genética , RNA Mensageiro/metabolismo , RNA Interferente Pequeno/metabolismo , Reação em Cadeia da Polimerase em Tempo Real , Análise de Sequência de RNA , Estresse Fisiológico/efeitos da radiação , Fatores de Tempo , Transcrição Gênica/efeitos da radiação , Transcriptoma/genéticaRESUMO
Background and Aims: Species are often used as the unit for conservation, but may not be suitable for species complexes where taxa are difficult to distinguish. Under such circumstances, it may be more appropriate to consider species groups or populations as evolutionarily significant units (ESUs). A population genomic approach was employed to investigate the diversity within and among closely related species to create a more robust, lineage-specific conservation strategy for a nationally endangered terrestrial orchid and its relatives from south-eastern Australia. Methods: Four putative species were sampled from a total of 16 populations in the Victorian Volcanic Plain (VVP) bioregion and one population of a sub-alpine outgroup in south-eastern Australia. Morphological measurements were taken in situ along with leaf material for genotyping by sequencing (GBS) and microsatellite analyses. Key Results: Species could not be differentiated using morphological measurements. Microsatellite and GBS markers confirmed the outgroup as distinct, but only GBS markers provided resolution of population genetic structure. The nationally endangered Diuris basaltica was indistinguishable from two related species ( D. chryseopsis and D. behrii ), while the state-protected D. gregaria showed genomic differentiation. Conclusions: Genomic diversity identified among the four Diuris species suggests that conservation of this taxonomically complex group will be best served by considering them as one ESU rather than separately aligned with species as currently recognized. This approach will maximize evolutionary potential among all species during increased isolation and environmental change. The methods used here can be applied generally to conserve evolutionary processes for groups where taxonomic uncertainty hinders the use of species as conservation units.
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Conservação dos Recursos Naturais , Variação Genética , Genoma de Planta , Orchidaceae/genética , Genética Populacional , Genômica , Genótipo , Repetições de Microssatélites , Orchidaceae/classificação , Austrália do SulRESUMO
Variation in the presence or absence of transposable elements (TEs) is a major source of genetic variation between individuals. Here, we identified 23,095 TE presence/absence variants between 216 Arabidopsis accessions. Most TE variants were rare, and we find these rare variants associated with local extremes of gene expression and DNA methylation levels within the population. Of the common alleles identified, two thirds were not in linkage disequilibrium with nearby SNPs, implicating these variants as a source of novel genetic diversity. Many common TE variants were associated with significantly altered expression of nearby genes, and a major fraction of inter-accession DNA methylation differences were associated with nearby TE insertions. Overall, this demonstrates that TE variants are a rich source of genetic diversity that likely plays an important role in facilitating epigenomic and transcriptional differences between individuals, and indicates a strong genetic basis for epigenetic variation.