The genomes of Darwin's primroses reveal chromosome-scale adaptive introgression and differential permeability of species boundaries

Introgression is an important source of genetic variation that can determine species adaptation to environmental conditions. Yet, definitive evidence of the genomic and adaptive implications of introgression in nature remains scarce. The widespread hybrid zones of Darwin's primroses (Primula elatior, Primula veris, and Primula vulgaris) provide a unique natural laboratory for studying introgression in flowering plants and the varying permeability of species boundaries. Through analysis of 650 genomes, we provide evidence of an introgressed genomic region likely to confer adaptive advantage in conditions of soil toxicity. We also document unequivocal evidence of chloroplast introgression, an important precursor to species-wide chloroplast capture. Finally, we provide the first evidence that the S-locus supergene, which controls heterostyly in primroses, does not introgress in this clade. Our results contribute novel insights into the adaptive role of introgression and demonstrate the importance of extensive genomic and geographical sampling for illuminating the complex nature of species boundaries

Parallel adaptation in autopolyploid Arabidopsis arenosa is dominated by repeated recruitment of shared alleles

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms

Lateral transfers of large DNA fragments spread functional genes among grasses

A fundamental tenet of multicellular eukaryotic evolution is that vertical inheritance is paramount, with natural selection acting on genetic variants transferred from parents to offspring. This lineal process means that an organism's adaptive potential can be restricted by its evolutionary history, the amount of standing genetic variation, and its mutation rate. Lateral gene transfer (LGT) theoretically provides a mechanism to bypass many of these limitations, but the evolutionary importance and frequency of this process in multicellular eukaryotes, such as plants, remains debated. We address this issue by assembling a chromosome-level genome for the grass Alloteropsis semialata, a species surmised to exhibit two LGTs, and screen it for other grass-to-grass LGTs using genomic data from 146 other grass species. Through stringent phylogenomic analyses, we discovered 57 additional LGTs in the A. semialata nuclear genome, involving at least nine different donor species. The LGTs are clustered in 23 laterally acquired genomic fragments that are up to 170 kb long and have accumulated during the diversification of Alloteropsis. The majority of the 59 LGTs in A. semialata are expressed, and we show that they have added functions to the recipient genome. Functional LGTs were further detected in the genomes of five other grass species, demonstrating that this process is likely widespread in this globally important group of plants. LGT therefore appears to represent a potent evolutionary force capable of spreading functional genes among distantly related grass species

Transcriptional activity of transposable elements along an elevational gradient in Arabidopsis arenosa

Background Plant genomes can respond rapidly to environmental changes and transposable elements (TEs) arise as important drivers contributing to genome dynamics. Although some elements were reported to be induced by various abiotic or biotic factors, there is a lack of general understanding on how environment influences the activity and diversity of TEs. Here, we combined common garden experiment with short-read sequencing to investigate genomic abundance and expression of 2245 consensus TE sequences (containing retrotransposons and DNA transposons) in an alpine environment in Arabidopsis arenosa. To disentangle general trends from local differentiation, we leveraged four foothill-alpine population pairs from different mountain regions. Seeds of each of the eight populations were raised under four treatments that differed in temperature and irradiance, two factors varying with elevation. RNA-seq analysis was performed on leaves of young plants to test for the effect of elevation and subsequently of temperature and irradiance on expression of TE sequences. Results Genomic abundance of the 2245 consensus TE sequences varied greatly between the mountain regions in line with neutral divergence among the regions, representing distinct genetic lineages of A. arenosa. Accounting for intraspecific variation in abundance, we found consistent transcriptomic response for some TE sequences across the different pairs of foothill-alpine populations suggesting parallelism in TE expression. In particular expression of retrotransposon LTR Copia (e.g. Ivana and Ale clades) and LTR Gypsy (e.g. Athila and CRM clades) but also non-LTR LINE or DNA transposon TIR MuDR consistently varied with elevation of origin. TE sequences responding specifically to temperature and irradiance belonged to the same classes as well as additional TE clades containing potentially stress-responsive elements (e.g. LTR Copia Sire and Tar, LTR Gypsy Reina). Conclusions Our study demonstrated that the A. arenosa genome harbours a considerable diversity of TE sequences whose abundance and expression response varies across its native range. Some TE clades may contain transcriptionally active elements responding to a natural environmental gradient. This may further contribute to genetic variation between populations and may ultimately provide new regulatory mechanisms to face environmental challenges

Jumping genes: Genomic ballast or powerhouse of biological diversification

Studying hybridization has the potential to elucidate challenging questions in evolutionary biology such as the nature of adaptive genetic variation and reproductive isolation. A growing body of work highlights that the merging of divergent genomes goes beyond the reshuffling of standing variation from related species and promotes mutations (Abbott et al., 2013). However, to what extent such genome instability generates evolutionary significant variation remains largely elusive. In this issue of Molecular Ecology, Dennenmoser et al. (2017) report considerable dynamics of transposable elements (TEs) in a recent invasive fish species of hybrid origin (Cottus; Figure 1). It adds to the recent examples from plants to support TE-specific genome variation following hybridization. Insights from early, as well as established, hybrids are largely coherent with increased TE activity, and this fish system thus represents an inspiring opportunity to further address the possible association between genome dynamics and “rapid evolution of hybrid species.” This work based on genome (re)sequencing contrasts with prior transcriptomics or PCR-based studies of TEs and illustrates how unprecedented amount of information promises a better understanding of the multiple patterns of variation across eukaryotic genomes; provided that we get the better of methodological advances. As discussed here, unbiased assessment of TE variation from genome surveys indeed remains a challenge precluding firm conclusions to be reached about the evolutionary significance of TEs. Despite methodological and conceptual developments that appear necessary to unambiguously uncover the unexplored iceberg below the known tip, the role of coding genes vs. TEs in promoting adaptation and speciation might be clarified in a not so remote future

SNPs data

SNPs dataset (containing also SNPs within the transposable element sequences) in vcf format. Called with FreeBayes v.1.0.2 from whole genome sequencing (Illumina Hiseq 2500) 304 individuals from four regions: Ma: Martinet Pa: Para Es: Essets Pi: Pierreda

non-TE SNPs dataset

SNPs dataset that do not contain the SNPs within the transposable elements sequences in a vcf format called with FreeBayes v.1.0.2 from whole genome sequencing (Illumina Hiseq 2500). 304 individuals from four regions: Ma: Martinet Pa: Para Es: Essets Pi: Pierreda

Comparative Genomics Elucidates the Origin of a Supergene Controlling Floral Heteromorphism

Supergenes are nonrecombining genomic regions ensuring the coinheritance of multiple, coadapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterostyly is characterized by the cooccurrence of two complementary, self-incompatible floral morphs and is controlled by five genes clustered in the hemizygous, ca. 300-kb S locus. Here, we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula

The genome of Draba nivalis shows signatures of adaptation to the extreme environmental stresses of the Arctic

The Arctic is one of the most extreme terrestrial environments on the planet. Here, we present the first chromosome-scale genome assembly of a plant adapted to the high Arctic, Draba nivalis (Brassicaceae), an attractive model species for studying plant adaptation to the stresses imposed by this harsh environment. We used an iterative scaffolding strategy with data from short-reads, single-molecule long reads, proximity ligation data, and a genetic map to produce a 302 Mb assembly that is highly contiguous with 91.6% assembled into eight chromosomes (the base chromosome number). To identify candidate genes and gene families that may have facilitated adaptation to Arctic environmental stresses, we performed comparative genomic analyses with nine non-Arctic Brassicaceae species. We show that the D. nivalis genome contains expanded suites of genes associated with drought and cold stress (e.g., related to the maintenance of oxidation-reduction homeostasis, meiosis, and signaling pathways). The expansions of gene families associated with these functions appear to be driven in part by the activity of transposable elements. Tests of positive selection identify suites of candidate genes associated with meiosis and photoperiodism, as well as cold, drought, and oxidative stress responses. Our results reveal a multifaceted landscape of stress adaptation in the D. nivalis genome, offering avenues for the continued development of this species as an Arctic model plant

Changes in the Chlorophyll Content and Cytokinin Levels in the Top Three Leaves of New Plant Type Rice During Grain Filling

This paper reports the ways that the differences in leaf senescence are related to grain filling, grain yield, and the dynamics of cytokinins (CKs) in the top three leaves of four field-grown new plant type (NPT) rice, a tropical japonica developed at the International Rice Research Institute, Philippines, to increase the yield potential of rice. The chlorophyll content in leaves decreased from flowering to maturity in all the NPT lines, whereas the grain filling percentage was higher in the fast-senescing NPT line than in slow-senescing NPT line. Grain yield was positively correlated with senescence in the flag leaf. Rapid changes in the CK levels were recorded in the leaves of the fast-senescing line, whereas the CK levels were relatively stable in leaves of the slow-senescing line, suggesting that the dynamics of CKs in the fast-senescing line are vital for fast senescence. There were no significant changes in bioactive CKs, CK O-glucosides (storage CKs), and cis-zeatin derivatives in different leaves of the slow-senescing NPT line between 0 and 3 weeks after flowering, suggesting that the content of these CKs is relatively stable during grain filling. A progressive increase in levels of bioactive CKs was positively correlated with gradual accumulation of CK N-glucosides (inactive CKs) in the top three leaves of the slow-senescing NPT line, whereas the decrease of bioactive CKs in the flag leaf of the fast-senescing line was accompanied by accumulation of CK O-glucosides. These results suggest that there is a higher rate of biosynthesis and/or import of bioactive CKs as well as their turnover which may favor delay of leaf senescence in the slow-senescing NPT line