Tianying Lan

The coffee genome provides insight into the convergent evolution of caffeine biosynthesis

Coffee, tea, and chocolate converge Caffeine has evolved multiple times among plant species, but no one knows whether these events involved similar genes. Denoeud et al. sequenced the Coffea canephora (coffee) genome and identified a conserved gene order (see the Perspective by Zamir). Although this species underwent fewer genome duplications than related species, the relevant caffeine genes experienced tandem duplications that expanded their numbers within this species. Scientists have seen similar but independent expansions in distantly related species of tea and cacao, suggesting that caffeine might have played an adaptive role in coffee evolution. Science, this issue p. 1181; see also p. 1124 The genetic origins of coffee’s constituents reveal intriguing links to cacao and tea. Coffee is a valuable beverage crop due to its characteristic flavor, aroma, and the stimulating effects of caffeine. We generated a high-quality draft genome of the species Coffea canephora, which displays a conserved chromosomal gene order among asterid angiosperms. Although it shows no sign of the whole-genome triplication identified in Solanaceae species such as tomato, the genome includes several species-specific gene family expansions, among them N-methyltransferases (NMTs) involved in caffeine production, defense-related genes, and alkaloid and flavonoid enzymes involved in secondary compound synthesis. Comparative analyses of caffeine NMTs demonstrate that these genes expanded through sequential tandem duplications independently of genes from cacao and tea, suggesting that caffeine in eudicots is of polyphyletic origin.

Architecture and evolution of a minute plant genome

It has been argued that the evolution of plant genome size is principally unidirectional and increasing owing to the varied action of whole-genome duplications (WGDs) and mobile element proliferation. However, extreme genome size reductions have been reported in the angiosperm family tree. Here we report the sequence of the 82-megabase genome of the carnivorous bladderwort plant Utricularia gibba. Despite its tiny size, the U. gibba genome accommodates a typical number of genes for a plant, with the main difference from other plant genomes arising from a drastic reduction in non-genic DNA. Unexpectedly, we identified at least three rounds of WGD in U. gibba since common ancestry with tomato (Solanum) and grape (Vitis). The compressed architecture of the U. gibba genome indicates that a small fraction of intergenic DNA, with few or no active retrotransposons, is sufficient to regulate and integrate all the processes required for the development and reproduction of a complex organism.

Assembly and Validation of the Genome of the Nonmodel Basal Angiosperm Amborella

Shaping Plant Evolution Amborella trichopoda is understood to be the most basal extant flowering plant and its genome is anticipated to provide insights into the evolution of plant life on Earth (see the Perspective by Adams). To validate and assemble the sequence, Chamala et al. (p. 1516) combined fluorescent in situ hybridization (FISH), genomic mapping, and next-generation sequencing. The Amborella Genome Project (p. 10.1126/science.1241089) was able to infer that a whole-genome duplication event preceded the evolution of this ancestral angiosperm, and Rice et al. (p. 1468) found that numerous genes in the mitochondrion were acquired by horizontal gene transfer from other plants, including almost four entire mitochondrial genomes from mosses and algae. Fluorescence in situ hybridization allows for next-generation sequencing of a large, difficult genome. [Also see Perspective by Adams; Research Articles by Amborella Genome Project and Rice et al.] Genome sequencing with next-generation sequence (NGS) technologies can now be applied to organisms pivotal to addressing fundamental biological questions, but with genomes previously considered intractable or too expensive to undertake. However, for species with large and complex genomes, extensive genetic and physical map resources have, until now, been required to direct the sequencing effort and sequence assembly. As these resources are unavailable for most species, assembling high-quality genome sequences from NGS data remains challenging. We describe a strategy that uses NGS, fluorescence in situ hybridization, and whole-genome mapping to assemble a high-quality genome sequence for Amborella trichopoda, a nonmodel species crucial to understanding flowering plant evolution. These methods are applicable to many other organisms with limited genomic resources.

Dynamic distribution patterns of ribosomal DNA and chromosomal evolution in Paphiopedilum, a lady's slipper orchid

BackgroundPaphiopedilum is a horticulturally and ecologically important genus of ca. 80 species of ladys slipper orchids native to Southeast Asia. These plants have long been of interest regarding their chromosomal evolution, which involves a progressive aneuploid series based on either fission or fusion of centromeres. Chromosome number is positively correlated with genome size, so rearrangement processes must include either insertion or deletion of DNA segments. We have conducted Fluorescence In Situ Hybridization (FISH) studies using 5S and 25S ribosomal DNA (rDNA) probes to survey for rearrangements, duplications, and phylogenetically-correlated variation within Paphiopedilum. We further studied sequence variation of the non-transcribed spacers of 5S rDNA (5S-NTS) to examine their complex duplication history, including the possibility that concerted evolutionary forces may homogenize diversity.Results5S and 25S rDNA loci among Paphiopedilum species, representing all key phylogenetic lineages, exhibit a considerable diversity that correlates well with recognized evolutionary groups. 25S rDNA signals range from 2 (representing 1 locus) to 9, the latter representing hemizygosity. 5S loci display extensive structural variation, and show from 2 specific signals to many, both major and minor and highly dispersed. The dispersed signals mainly occur at centromeric and subtelomeric positions, which are hotspots for chromosomal breakpoints. Phylogenetic analysis of cloned 5S rDNA non-transcribed spacer (5S-NTS) sequences showed evidence for both ancient and recent post-speciation duplication events, as well as interlocus and intralocus diversity.ConclusionsPaphiopedilum species display many chromosomal rearrangements - for example, duplications, translocations, and inversions - but only weak concerted evolutionary forces among highly duplicated 5S arrays, which suggests that double-strand break repair processes are dynamic and ongoing. These results make the genus a model system for the study of complex chromosomal evolution in plants.

Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida (Asteraceae)

The complex inflorescences (capitula) of Asteraceae consist of different types of flowers. In Gerbera hybrida (gerbera), the peripheral ray flowers are bilaterally symmetrical and lack functional stamens while the central disc flowers are more radially symmetrical and hermaphroditic. Proteins of the CYC2 subclade of the CYC/TB1-like TCP domain transcription factors have been recruited several times independently for parallel evolution of bilaterally symmetrical flowers in various angiosperm plant lineages, and have also been shown to regulate flower-type identity in Asteraceae. The CYC2 subclade genes in gerbera show largely overlapping gene expression patterns. At the level of single flowers, their expression domain in petals shows a spatial shift from the dorsal pattern known so far in species with bilaterally symmetrical flowers, suggesting that this change in expression may have evolved after the origin of Asteraceae. Functional analysis indicates that GhCYC2, GhCYC3 and GhCYC4 mediate positional information at the proximal-distal axis of the inflorescence, leading to differentiation of ray flowers, but that they also regulate ray flower petal growth by affecting cell proliferation until the final size and shape of the petals is reached. Moreover, our data show functional diversification for the GhCYC5 gene. Ectopic activation of GhCYC5 increases flower density in the inflorescence, suggesting that GhCYC5 may promote the flower initiation rate during expansion of the capitulum. Our data thus indicate that modification of the ancestral network of TCP factors has, through gene duplications, led to the establishment of new expression domains and to functional diversification.

Phylogeny and biogeography of New World Stachydeae (Lamiaceae) with emphasis on the origin and diversification of Hawaiian and South American taxa

Due to its unique geological history and isolated location, the Hawaiian Archipelago provides an ideal setting for studies on biogeography, phylogeny and population biology. Species richness in these islands has been attributed to unique colonization events. The Hawaiian mints comprising of three endemic genera represent one of the largest radiations in the island. Previous studies have shown the Hawaiian mints to be nested within the dry-fruited Stachys, probably resulting from one or more hybridization events. Stachydeae, the largest tribe in the subfamily Lamioideae (Lamiaceae), is a taxonomically complex and widespread lineage exhibiting remarkable chromosomal diversity. In this paper we attempted at untangling the relationships between the New World and Hawaiian mint taxa, as well as investigate the origin and diversification of the mints in the New World. There seem to have been at least two independent migration events of Stachys to the New World during the Middle to Late Miocene and towards the beginning of the Pliocene, respectively. Results indicate incongruence between the rDNA and cpDNA phylogenies suggesting a reticulate, New World origin for the Hawaiian mints, although dispersal to Hawaii appears to have happened only once during the Pliocene. South American Stachys diversified from their Mesoamerican relatives around Late Pliocene and may also have arisen from similar reticulate events indicated by their intercalating position among the Mesoamerican Stachys species. Further insights into the phylogenetic relationships between the New World mints may be gathered through the study of low copy nuclear loci.

Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch

Silver birch (Betula pendula) is a pioneer boreal tree that can be induced to flower within 1 year. Its rapid life cycle, small (440-Mb) genome, and advanced germplasm resources make birch an attractive model for forest biotechnology. We assembled and chromosomally anchored the nuclear genome of an inbred B. pendula individual. Gene duplicates from the paleohexaploid event were enriched for transcriptional regulation, whereas tandem duplicates were overrepresented by environmental responses. Population resequencing of 80 individuals showed effective population size crashes at major points of climatic upheaval. Selective sweeps were enriched among polyploid duplicates encoding key developmental and physiological triggering functions, suggesting that local adaptation has tuned the timing of and cross-talk between fundamental plant processes. Variation around the tightly-linked light response genes PHYC and FRS10 correlated with latitude and longitude and temperature, and with precipitation for PHYC. Similar associations characterized the growth-promoting cytokinin response regulator ARR1, and the wood development genes KAK and MED5A.

Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome

Significance Carnivorous plants capture and digest animal prey for nutrition. In addition to being carnivorous, the humped bladderwort plant, Utricularia gibba, has the smallest reliably assembled flowering plant genome. We generated an updated genome assembly based on single-molecule sequencing to address questions regarding the bladderwort’s genome adaptive landscape. Among encoded genes, we segregated those that could be confidently distinguished as having derived from small-scale versus whole-genome duplication processes and showed that conspicuous expansions of gene families useful for prey trapping and processing derived mainly from localized duplication events. Such small-scale, tandem duplicates are therefore revealed as essential elements in the bladderwort’s carnivorous adaptation. Utricularia gibba, the humped bladderwort, is a carnivorous plant that retains a tiny nuclear genome despite at least two rounds of whole genome duplication (WGD) since common ancestry with grapevine and other species. We used a third-generation genome assembly with several complete chromosomes to reconstruct the two most recent lineage-specific ancestral genomes that led to the modern U. gibba genome structure. Patterns of subgenome dominance in the most recent WGD, both architectural and transcriptional, are suggestive of allopolyploidization, which may have generated genomic novelty and led to instantaneous speciation. Syntenic duplicates retained in polyploid blocks are enriched for transcription factor functions, whereas gene copies derived from ongoing tandem duplication events are enriched in metabolic functions potentially important for a carnivorous plant. Among these are tandem arrays of cysteine protease genes with trap-specific expression that evolved within a protein family known to be useful in the digestion of animal prey. Further enriched functions among tandem duplicates (also with trap-enhanced expression) include peptide transport (intercellular movement of broken-down prey proteins), ATPase activities (bladder-trap acidification and transmembrane nutrient transport), hydrolase and chitinase activities (breakdown of prey polysaccharides), and cell-wall dynamic components possibly associated with active bladder movements. Whereas independently polyploid Arabidopsis syntenic gene duplicates are similarly enriched for transcriptional regulatory activities, Arabidopsis tandems are distinct from those of U. gibba, while still metabolic and likely reflecting unique adaptations of that species. Taken together, these findings highlight the special importance of tandem duplications in the adaptive landscapes of a carnivorous plant genome.

Genome-wide evidence for a hybrid origin of modern polar bears

Interspecific hybridization is recognized as a widespread phenomenon but measuring its extent, directionality, and adaptive importance in the evolution of species remain challenging. Polar bears possess unique adaptations to life on the Arctic sea ice, whereas their closest relatives -brown bears - are boreal and subarctic generalists. Despite largely non-overlapping modern distributions, genomic evidence demonstrates ancient admixture between these species. Here, we analyze new genomes from contemporary zones of species overlap as well as a previously sequenced 120,000-year old polar bear subfossil. We use explicit statistical fitting of data to admixture graphs to provide a framework for testing alternative scenarios of population relationships and gene flow directionality. Our analyses favor a single, parsimonious introgression event from relatives of extant Southeast Alaskan coastal brown bears into the ancestor of extant polar bears, which inverts the current paradigm of unidirectional gene flow from polar into brown bear. This conclusion has clear implications for our understanding of the impact of climate change: a specialist Arctic lineage may have been the recipient of generalist, boreal genetic variants at crucial times during critical phases of Northern Hemisphere glacial oscillations.

Evolutionary history of enigmatic bears in the Tibetan Plateau–Himalaya region and the identity of the yeti

Although anecdotally associated with local bears (Ursus arctos and U. thibetanus), the exact identity of ‘hominid’-like creatures important to folklore and mythology in the Tibetan Plateau–Himalaya region is still surrounded by mystery. Recently, two purported yeti samples from the Himalayas showed genetic affinity with an ancient polar bear, suggesting they may be from previously unrecognized, possibly hybrid, bear species, but this preliminary finding has been under question. We conducted a comprehensive genetic survey of field-collected and museum specimens to explore their identity and ultimately infer the evolutionary history of bears in the region. Phylogenetic analyses of mitochondrial DNA sequences determined clade affinities of the purported yeti samples in this study, strongly supporting the biological basis of the yeti legend to be local, extant bears. Complete mitochondrial genomes were assembled for Himalayan brown bear (U. a. isabellinus) and black bear (U. t. laniger) for the first time. Our results demonstrate that the Himalayan brown bear is one of the first-branching clades within the brown bear lineage, while Tibetan brown bears diverged much later. The estimated times of divergence of the Tibetan Plateau and Himalayan bear lineages overlap with Middle to Late Pleistocene glaciation events, suggesting that extant bears in the region are likely descendants of populations that survived in local refugia during the Pleistocene glaciations.