Umeå University's logo

Gymnosperms, particularly conifers, exhibit a high abundance of transposable elements (TEs) in their giga-scale genomes. TEs interact both antagonistically and cooperatively with the host genome, promoting structural and genetic innovations across evolutionary lineages. However, how TEs shape the coding space of gymnosperm genomes remains a key unresolved question. Here, we present a high-quality genome assembly for the keystone conifer Platycladus orientalis , with a contig N50 of 57.54 Mb—the highest continuity reported to date—to investigate the role of TEs. Comparative genomics confirms the absence of recent whole-genome duplication and the presence of genome expansion in gymnosperms, revealing complex interactions among recurrent TE proliferation, low DNA removal rates, and DNA methylation-mediated silencing. Computational evidence indicates that TE-mediated gene duplication and pseudogenization provide a genetic basis for adaptive evolution and functional innovation, significantly shaping gene family dynamics and the emergence of species-specific genes. Additionally, TEs capture and duplicate an average of ∼400,000 coding gene fragments per gymnosperm genome, facilitating exon shuffling and triggering epigenetic conflicts between source genes and captured exon fragments. Genes from which fragments are captured (donor genes) show significantly higher levels of exon methylation than genes not captured by TEs (free genes), whereas syntenic donor genes exhibit lower levels of silencing responses than non-syntenic donor genes. This study provides valuable genomic resources and offers insights into the evolutionary patterns and principles underlying the large genome size and complexity of gymnosperms.

Rosa, a genus esteemed worldwide for its ornamental plants, has encountered barriers in functional genomic studies and further genetic enhancement due to incomplete sequences and floating regions in previously sequenced genomes. Our groundbreaking study introduced a meticulously assembled, continuous, and fully bridged reference genome for Rosa rugosa, constructed through a sophisticated combination of PacBio High-Fidelity, ONT ultra-long reads, and Hi-C data. This robust assembly spanned 444.55 Mb and encompassed 34 109 protein-coding genes. We have uniquely assembled each chromosome into single, gap-free structures, successfully identifying all 14 telomeres and seven centromeres, a feat not achieved previously. The centromeric regions were distinguished by tandem repeats, primarily composed of centromere-specific 159-bp monomers, and a significant enrichment of ATHILA/Gypsy long terminal repeat retrotransposons in proximal regions. Our research highlighted recent tandem duplications as instrumental in bolstering R. rugosa's stress tolerance, environmental adaptability, and enhanced anthocyanin synthesis. Furthermore, our study ventured into uncharted territory by predicting transcription factors potentially regulating anthocyanin biosynthesis through the employment of gene co-expression networks, providing new avenues for research. This comprehensive reference genome not only serves as a cornerstone for in-depth exploration of genomic architecture and functionalities in R. rugosa but also acts as a catalyst for innovative breeding strategies and genetic refinement within the genus.

Karyotype diversity plays an important role in speciation and diversification. However, gymnosperms, particularly conifers, exhibit remarkable karyotype uniformity. To explore the evolutionary processes shaping karyotypes in gymnosperms, the karyotype evolutionary history is reconstructed through comparative genomic analyses. Synteny analysis confirms the absence of ancient polyploidy in conifers and its rarity across the gymnosperms as a whole. Further analysis reveals convergent patterns of reciprocal translocations between nonhomologous chromosomes in conifer genomes. Centromeric-centromeric reciprocal translocations (CRTs) have been identified as the primary mechanism of karyotype evolution in conifers, while telomeric-centromeric reciprocal translocations (TRTs) significantly contributed to descending dysploidy within Cupressales. A graph-based method is utilized to infer the detailed evolutionary pathways from the proto-gymnosperm karyotype (n = 12) to modern conifer karyotypes (n = 11–12). In conclusion, the scarcity of both polyploidy and dysploidy contributes to the karyotype uniformity of gymnosperms and potentially also to their lower species richness compared to angiosperms. However, the pervasive CRTs and occasional TRTs underlie this “apparent uniformity”, supporting the “karyotype orthoselection” hypothesis. This study provides new insights into the mechanisms maintaining karyotype uniformity in conifers and the role of karyotype evolution in their diversification.

Hybridization is a driving force in ecological transitions and speciation, yet direct evidence linking it to adaptive differentiation in natural systems remains limited. This study evaluates the role of hybridization in the speciation of Pinus densata, a keystone forest species on the southeastern Tibetan Plateau. By creating artificial interspecific F1s and a long-term common garden experiment on the plateau, we provide in situ assessments on 44 growth and physiological traits across four seasons, along with RNA sequencing. We found significant phenotypic divergence between P. densata and its putative parental species P. tabuliformis and P. yunnanensis, with P. densata demonstrating superior growth and dynamic balance between photosynthesis and photoprotection. The F1s closely resembled P. densata in most traits. Gene expression revealed 19%–10% of 34,000 examined genes as differentially expressed in P. densata and F1s relative to mid-parent expression values. Both additive (4%) and non-additive gene actions (5%–6% in F1s, 10%–12% in P. densata) were common, while transgressive expression occurred more frequently in the stabilized natural hybrids, illustrating transcriptomic reprogramming brought by hybridization and further divergence by natural selection. We provide compelling evidence for hybridization-derived phenotypic divergence at both physiological and gene expression levels that could have contributed to the adaptation of P. densata to high plateau habitat where both parental species have low fitness. The altered physiology and gene expression in hybrids serve both as a substrate for novel ecological adaptation and as a mechanism for the initiation of reproductive isolation.

The genetic base of local adaptation has been extensively studied in natural populations. However, a comprehensive genome-wide perspective on the contribution of structural variants (SVs) and adaptive introgression to local adaptation remains limited. In this study, we performed de novo assembly and annotation of 22 representative accessions of Quercus variabilis, identifying a total of 543,372 SVs. These SVs play crucial roles in shaping genomic structure and influencing gene expression. By analyzing range-wide genomic data, we identified both SNPs and SVs associated with local adaptation in Q. variabilis and Quercus acutissima. Notably, SV-outliers exhibit selection signals that did not overlap with SNP-outliers, indicating that SNP-based analyses may not detect the same candidate genes associated with SV-outliers. Remarkably, 29%-37% of candidate SNPs were located in a 250 kb region on chromosome 9, referred to as Chr9-ERF. This region contains 8 duplicated ethylene-responsive factor (ERF) genes, which may have contributed to local adaptation of Q. variabilis and Q. acutissima. We also found that a considerable number of candidate SNPs were shared between Q. variabilis and Q. acutissima in the Chr9-ERF region, suggesting a pattern of repeated selection. We further demonstrated that advantageous variants in this region were introgressed from western populations of Q. acutissima into Q. variabilis, providing compelling evidence that introgression facilitates local adaptation. This study offers a valuable genomic resource for future studies on oak species and highlights the importance of pan-genome analysis in understating mechanism driving adaptation and evolution.

Evolutionary radiation, a pivotal aspect of macroevolution, offers valuable insights into evolutionary processes. The genus Pinus is the largest genus in conifers with (Formula presented.) 90% of the extant species emerged in the Miocene, which signifies a case of rapid diversification. Despite this remarkable history, our understanding of the mechanisms driving radiation within this expansive genus has remained limited. Using exome capture sequencing and a fossil-calibrated phylogeny, we investigated the divergence history, niche diversification, and introgression among 13 closely related Eurasian species spanning climate zones from the tropics to the boreal Arctic. We detected complex introgression among lineages in subsection Pinus at all stages of the phylogeny. Despite this widespread gene exchange, each species maintained its genetic identity and showed clear niche differentiation. Demographic analysis unveiled distinct population histories among these species, which further influenced the nucleotide diversity and efficacy of purifying and positive selection in each species. Our findings suggest that radiation in the Eurasian pines was likely fueled by interspecific recombination and further reinforced by their adaptation to distinct environments. Our study highlights the constraints and opportunities for evolutionary change, and the expectations of future adaptation in response to environmental changes in different lineages.

Poplar (Populus) is a well-established model system for tree genomics and molecular breeding, and hybrid poplar is widely used in forest plantations. However, distinguishing its diploid homologous chromosomes is difficult, complicating advanced functional studies on specific alleles. In this study, we applied a trio-binning design and PacBio high-fidelity long-read sequencing to obtain haplotype-phased telomere-to-telomere genome assemblies for the 2 parents of the well-studied F1 hybrid “84K” (Populus alba × Populus tremula var. glandulosa). Almost all chromosomes, including the telomeres and centromeres, were completely assembled for each haplotype subgenome apart from 2 small gaps on one chromosome. By incorporating information from these haplotype assemblies and extensive RNA-seq data, we analyzed gene expression patterns between the 2 subgenomes and alleles. Transcription bias at the subgenome level was not uncovered, but extensive-expression differences were detected between alleles. We developed machine-learning (ML) models to predict allele-specific expression (ASE) with high accuracy and identified underlying genome features most highly influencing ASE. One of our models with 15 predictor variables achieved 77% accuracy on the training set and 74% accuracy on the testing set. ML models identified gene body CHG methylation, sequence divergence, and transposon occupancy both upstream and downstream of alleles as important factors for ASE. Our haplotype-phased genome assemblies and ML strategy highlight an avenue for functional studies in Populus and provide additional tools for studying ASE and heterosis in hybrids.

Southeast Asia (SEA) has seen strong climatic oscillations and fluctuations in sea levels during the Quaternary. The impact of past climate changes on the evolution and distribution of local flora in SEA is still poorly understood. Here we aim to infer how the Quaternary climate change affects the evolutionary process and range shifts in two pine species. We investigated the population genetic structure and diversity using cytoplasmic DNA markers, and performed ecological niche modeling to reconstruct the species past distribution and to project range shift under future climates. We found substantial gene flow across the continuous distribution of the subtropical Pinus yunnanensis. In contrast, the tropical Pinus kesiya showed a strong population structure in accordance with its disjunct distribution across montane islands in Indochina and the Philippines. A broad hybrid zone of the two species occurs in southern Yunnan. Asymmetric introgression from the two species was detected in this zone with dominant mitochondrial gene flow from P. yunnanensis and chloroplast gene flow from P. kesiya. The observed population structure suggests a typical postglaciation expansion in P. yunnanensis, and a glacial expansion and interglacial contraction in P. kesiya. Ecological niche modeling supports the inferred demographic history and predicts a decrease in range size for P. kesiya under future climates. Our results suggest that tropical pine species in SEA have undergone evolutionary trajectories different from high latitude species related to their Quaternary climate histories. We also illustrate the need for urgent conservation actions in this fragmented landscape.

Long non-coding RNAs (lncRNAs) play essential roles in various biological processes, such as chromatin remodeling, post-transcriptional regulation, and epigenetic modifications. Despite their critical functions in regulating plant growth, root development, and seed dormancy, the identification of plant lncRNAs remains a challenge due to the scarcity of specific and extensively tested identification methods. Most mainstream machine learning-based methods used for plant lncRNA identification were initially developed using human or other animal datasets, and their accuracy and effectiveness in predicting plant lncRNAs have not been fully evaluated or exploited. To overcome this limitation, we retrained several models, including CPAT, PLEK, and LncFinder, using plant datasets and compared their performance with mainstream lncRNA prediction tools such as CPC2, CNCI, RNAplonc, and LncADeep. Retraining these models significantly improved their performance, and two of the retrained models, LncFinder-plant and CPAT-plant, alongside their ensemble, emerged as the most suitable tools for plant lncRNA identification. This underscores the importance of model retraining in tackling the challenges associated with plant lncRNA identification. Finally, we developed a pipeline (Plant-LncPipe) that incorporates an ensemble of the two best-performing models and covers the entire data analysis process, including reads mapping, transcript assembly, lncRNA identification, classification, and origin, for the efficient identification of lncRNAs in plants. The pipeline, Plant-LncPipe, is available at: https://github.com/xuechantian/Plant-LncRNA-pipline.

Scots pine is the foundation species of diverse forested ecosystems across Eurasia and displays remarkable ecological breadth, occurring in environments ranging from temperate rainforests to arid tundra margins. Such expansive distributions can be favored by various demographic and adaptive processes and the interactions between them.

To understand the impact of neutral and selective forces on genetic structure in Scots pine, we conducted range-wide population genetic analyses on 2321 trees from 202 populations using genotyping-by-sequencing, reconstructed the recent demography of the species and examined signals of genetic adaptation.

We found a high and uniform genetic diversity across the entire range (global FST 0.048), no increased genetic load in expanding populations and minor impact of the last glacial maximum on historical population sizes. Genetic-environmental associations identified only a handful of single-nucleotide polymorphisms significantly linked to environmental gradients.

The results suggest that extensive gene flow is predominantly responsible for the observed genetic patterns in Scots pine. The apparent missing signal of genetic adaptation is likely attributed to the intricate genetic architecture controlling adaptation to multi-dimensional environments. The panmixia metapopulation of Scots pine offers a good study system for further exploration into how genetic adaptation and plasticity evolve under gene flow and changing environment.