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Leitch, I. J.

Publications and source records attributed to Leitch, I. J..

14 recordsLinked to original sources

Genome dynamics across the radiation of a mega-diverse genus

Understanding the drivers of species diversity and rapid radiations is a major goal in evolutionary biology. Begonia is one of the most species-rich angiosperm genera with 2,164 species currently identified. This genus exhibits considerable variation in chromosome number and a wide range of genome sizes, allowing us to associate genome dynamics with divergence and speciation at a range of temporal scales. We investigate all main radiations within the Begoniaceae family using five previously published Begonia genomes and seven new genome assemblies. We show that Begonia species show more complex, repetitive and dynamic genomes overall than their close relative, the monotypic Hillebrandia sandwicensis. We identify families of repetitive elements that have recently expanded in species from two different highly speciose Southeast Asian sections and two large Neotropical radiations. Detailed characterisation of genomes from species belonging to two parallel radiations, one in Southeast Asia (Begonia section Coelocentrum) and the other in the Neotropics (Begonia section Gireoudia), revealed recent expansion in LTR retrotransposons (LTR-RTs) and satellite DNA, in contrast to more species-poor closely related clades. We further investigate variation in repetitive elements within species, finding that accessions from a population of the widespread Begonia heracleifolia with unusually large genomes show a markedly higher satellite repeat and Ty3/Gypsy LTR-RT content associated with the expansion of a few abundant repeat lineages. We find that accessions derived from this population show lower seed viability in crosses with other conspecific populations, and thus identify a direct link between expansions of repetitive DNA and the process of genetic isolation. These results show how genome dynamics may promote speciation in one of the most diverse flowering plant genera.

genomics↗

Gene turnover and contingency facilitated the repeated evolution of C4 photosynthesis in grasses

SummaryO_LIIn grasses, almost all species belong to two evenly sized clades (BOP and PACMAD), yet the >20 independent origins of C4 photosynthesis in this family only occur in the PACMAD lineage. Here, we identify potential genetic precursors for C4 photosynthesis that were present at the base of the PACMAD clade, representing the last common ancestor of all C4 grasses. C_LIO_LIWe generated the first reference genomes for Aristidoideae species (Aristida adscensionis and Stipagrostis hirtigluma), the sister lineage of all other PACMAD grasses. In combination with 34 other Poales genomes, we identify gene gains at the base of the PACMAD clade, and genes lost in the sister BOP lineage. C_LIO_LICandidate C4 precursors include {beta}-carbonic anhydrase, as well as genes involved in amino acid and nitrate transport, carbon metabolism, oxidative stress management and transcription regulation. C_LIO_LIGene turnover created the necessary genetic contingency, facilitating the independent recruitment and refinement of C4 genes in multiple independent origins. Our results support the idea that the repeated evolution of C4 photosynthesis in PACMAD grasses was not driven by a single genetic event but was instead underwritten by chance genetic changes that originated long before there was selection for the trait itself. C_LI

evolutionary biology↗

Recurrent evolution of cryptic triploids in cultivated enset increases yield

The high incidence of polyploidy in crops could be explained if domestication involved the selection of polyploids (cytotypes with more than two sets of chromosomes). Ancestral horticulture could have targeted desirable traits including yield, robustness to stress and to disease, rather than requiring knowledge of polyploidy itself. We find evidence for this process underway in enset (Ensete ventricosum, Musaceae) - a highly resilient crop constituting the main staple for over 20 million people in Ethiopia, which is clonally propagated and cultivated for its starch-rich corm and pseudostem. Prior to this study, enset was thought to be exclusively diploid (2n = 2x = 18). Using a newly-assembled chromosome-scale reference genome, and sequence data from 723 wild and domesticated enset individuals from southwestern Ethiopia, we demonstrate that around 20% of cultivated enset clones are triploid. We show that triploidy has arisen multiple times independently, that the triploid lineages have been given distinct landrace names, and planted disproportionately frequently. As well as providing evidence for enduring selection on triploids, our results reveal valuable genetic diversity captured by these triploid lines. They represent key resources for scientifically directed breeding of this major crop in the Ethiopian agrosystem, and could improve food security in sub-saharan Africa. Author SummaryDuplication of a species entire genome (polyploidization) plays an important part in evolution. Domestication may have favoured polyploid crops including wheat, coffee, potato, cotton, strawberry, and banana. It has been proposed that this trend is explained by the selection of advantageous traits exhibited by polyploids compared to their relatives with unduplicated genomes. These desirable traits include bigger fruits, seeds or other edible organs, and better tolerance to stress and disease. We unexpectedly find that a large proportion of cultivated enset lines have three copies of their genome (triploidy) instead of two (diploid). Enset is a highly resilient crop in the banana family; its stem and leaves are processed to provide one of the main food sources for over 20 million people in Ethiopia. Prior to our study, enset was thought to be exclusively diploid. Farmers use landrace names that distinguish diploids from triploids without having this new genetic information, showing the differences between them are recognised and given importance. Triploids were planted disproportionately and appear to grow faster, suggesting they are being selected for their higher productivity. These triploid ensets are an important genetic resource for scientifically directed breeding of new varieties, which could improve food security in sub-saharan Africa.

evolutionary biology↗

Chromosome-scale genome assembly and de novo annotation of Alopecurus aequalis.

Alopecurus aequalis is a winter annual or short-lived perennial bunchgrass which has in recent years emerged as the dominant agricultural weed of barley and wheat in certain regions of China and Japan, causing significant yield losses. Its robust tillering capacity and high fecundity, combined with the development of both target and non-target-site resistance to herbicides means it is a formidable challenge to food security. Here we report on a chromosome-scale assembly of A. aequalis with a genome size of 2.83 Gb. The genome contained 33,758 high-confidence protein-coding genes with functional annotation. Comparative genomics revealed that the genome structure of A. aequalis is more similar to Hordeum vulgare rather than the more closely related Alopecurus myosuroides and has undergone an expansion of cytochrome P450 genes, a gene family involved in non-target-site herbicide resistance.

plant biology↗

Early Cretaceous Origin and Evolutionary History of Palms (Arecaceae) inferred from 1,033 Nuclear Genes and a New Synthesis of Fossil Evidence

AO_SCPLOWBSTRACTC_SCPLOWTropical rainforests are home to almost half of all known plant diversity, yet a shortfall in tropical plant phylogenetic hypotheses is hindering our understanding of how rainforests have formed and adapted to past global changes. Phylogenetic and historical biogeographic evidence from key rainforest lineages, including palms (Arecaceae), are required to illuminate the history of these ecosystems. However, our current understanding of the palm tree of life is based on uneven sampling of data from the plastid and nuclear genome, and numerous palm genera and palm fossils have been described or revised over the past decade, casting doubt on many palm relationships, ages and ancestral ranges inferred in previous studies. Here, we infer the phylogenetic relationships of all palm genera based on data from 1,033 nuclear genes generated using target sequence capture. Our palm tree of life is highly resolved and supported. Remaining areas of ambiguity reflect the complex dynamics of palm evolution, including many rapid diversification events in subfamily Arecoideae and putative cases of ancient reticulation throughout the family. We review the phylogenetic placement and age of hundreds of palm fossils and use a vetted selection to estimate divergence times and ancestral ranges for all palm genera. We show that the family is older than previously thought, likely first diversifying in the Early Cretaceous in Laurasia, and that three quarters of the genera had originated by the Oligocene. The early spread of palms across the world involved at least 40 long-distance dispersals across oceanic gaps. Dispersals away from northern latitudes vastly outnumber dispersals into these latitudes, consistent with the ancient affinity of palms for megathermal climates, and suggesting that global cooling during the Oligocene was a major constraint on early palm distribution. Our dated phylogenomic tree and curated fossil dataset provide a new foundation for evolutionary studies on palms, opening the door to deeper research on the rainforest biome in which they thrive.

evolutionary biology↗

The Origin And Speciation Of Orchids

Orchids constitute one of the most spectacular radiations of flowering plants. However, their geographical origin, historical spread across the globe, and hotspots of speciation remain uncertain due to the lack of a broad phylogenomic framework. We present a new Orchidaceae phylogeny based on high-throughput and Sanger sequencing datasets, covering all five subfamilies, 17/22 tribes, 40/49 subtribes, 285/736 genera, and [~]7% (1,921) of the currently 29,524 accepted species. We then use it to infer geographic range evolution, diversity, and speciation patterns by adding curated geographical distribution data through the World Checklist of Vascular Plants. Orchids most recent common ancestor is traced back to the Late Cretaceous in Laurasia. The modern Southeast Asian range of subfamily Apostasioideae is interpreted as relictual, matching the history of numerous clades that went extinct at higher latitudes following the global climate cooled during the Oligocene. Despite their ancient origins, modern orchid species diversity mainly originated over the last 5 Ma, with the fastest speciation rates found in south-eastern Central America. Our results substantially alter our understanding of the geographic origin of orchids, previously proposed as Australian, and further pinpoint the role of Central American as a region of recent and explosive speciation.

evolutionary biology↗

Genome size is positively correlated with extinction risk in herbaceous angiosperms

O_LIAngiosperms with large genomes experience nuclear-, cellular- and organism-level constraints that may limit their phenotypic plasticity and ecological niche. These constraints have been documented to vary across lineages, life-history strategies, ecogeographic patterns and environmental conditions. Therefore, we test the hypotheses that extinction risk is higher in large-genomed compared to small-genomed species, and that the effect of genome size varies across three selected covariates: life form, endemism, and climatic zones. C_LIO_LIWe collated genome size and extinction risk information for a representative sample of angiosperms comprising 3,250 species, which we analyzed alongside life form, endemism and climate variables using a phylogenetic framework. C_LIO_LIAngiosperm genome size is positively correlated with extinction risk, a pattern driven by a signal in herbaceous but not woody species, regardless of climate and endemism. The influence of genome size is stronger in endemic herbaceous species, but is relatively homogenous across different climates. Beyond its indirect link via endemism and climate, genome size also influences extinction risk directly and significantly. C_LIO_LIGenome size may serve as a proxy for difficult-to-measure parameters associated with resilience and vulnerability in herbaceous angiosperms. Therefore, it merits further exploration as a useful biological attribute for understanding intrinsic extinction risk and augmenting plant conservation efforts. C_LI

plant biology↗

The global biogeography of angiosperm genome size is shaped by climate and range size

O_LIAngiosperms, which inhabit diverse environments across all continents, exhibit significant variation in genome sizes, making them an excellent model system for examining hypotheses about the global distribution of genome size. These include the previously proposed large-genome-constraint, mutational-hazard, polyploidy-mediated, and climate-mediated hypotheses. C_LIO_LIWe compiled the largest genome size dataset to date, encompassing >5% of known angiosperm species, and analyzed genome size distribution using a comprehensive geographic distribution dataset for all angiosperms. C_LIO_LIWe observed that angiosperms with large range sizes generally had small genomes, supporting the large-genome-constraint hypothesis. Climate was shown to exert a strong influence on genome size distribution along the global latitudinal gradient, while the frequency of polyploidy and the type of growth form had negligible effects. In contrast to the unimodal patterns along the global latitudinal gradient shown by plant size traits and polyploid proportions, the increase in angiosperm genome size from the equator to 40-50{degrees}N/S is probably mediated by different (mostly climatic) mechanisms than the decrease in genome sizes observed from 40-50{degrees}N northwards. C_LIO_LIOur analysis suggests that the global distribution of genome sizes in angiosperms is mainly shaped by climatically-mediated purifying selection, genetic drift, relaxed selection, and environmental filtering. C_LI

evolutionary biology↗

The Ecology of Palm Genomes: Repeat-associated genome size expansion is constrained by aridity

O_LIGenome size varies 2,400-fold across plants, influencing their evolution through changes in cell size and cell division rates which impact plants environmental stress tolerance. Repetitive element expansion explains much genome size diversity, and the processes structuring repeat communities are analogous to those structuring ecological communities. However, which environmental stressors influence repeat community dynamics has not yet been examined from an ecological perspective. C_LIO_LIWe measured genome size and leveraged climatic data for 91% of genera within the ecologically diverse palm family (Arecaceae). We then generated genomic repeat profiles for 141 palm species, and analysed repeats using phylogenetically-informed linear models to explore relationships between repeat dynamics and environmental factors. C_LIO_LIWe show that palm genome size and repeat community composition are best explained by aridity. Specifically, EnSpm CACTA repeats were more abundant in palm species from wetter environments, which generally had larger genomes (>2.15Gbp/1C), suggesting amplification. In contrast, Ty1-copia Angela elements were more abundant in drier environments. C_LIO_LIOur results suggest water stress inhibits the expansion of repeats through selection on upper genome size limits. However, Ty1-copia Angela elements, which may associate with stress-response genes, have amplified in arid-adapted palm species. Overall, we provide novel evidence of climate influencing the assembly of repeat communities. C_LI

evolutionary biology↗

The nature of intraspecific genome size variation in taxonomically complex eyebrights

O_LIGenome size (GS) is a key trait related to morphology, life history, and evolvability. Although GS is, by definition, affected by presence/absence variants (PAVs), which are ubiquitous in population sequencing studies, GS is often treated as an intrinsic property of a species. Here, we studied intra- and interspecific GS variation in taxonomically complex British eyebrights (Euphrasia). C_LIO_LIWe generated GS data for 192 individuals of diploid and tetraploid Euphrasia and analysed GS variation in relation to ploidy, taxonomy, population affiliation, and geography. We further compared the genomic repeat content of 30 samples. C_LIO_LIWe found considerable genuine intraspecific GS variation, and observed isolation-by-distance for GS in outcrossing diploids. Tetraploid Euphrasia showed contrasting patterns, with GS increasing with latitude in outcrossing Euphrasia arctica, but little GS variation in the highly selfing Euphrasia micrantha. Interspecific differences in GS genomic repeat percentages were small. C_LIO_LIWe show the utility of treating GS as the outcome of polygenic variation. Like other types of genetic variation, such as single nucleotide polymorphisms, GS variation may be increased through hybridisation and population subdivision. In addition to selection on associated traits, GS is predicted to be affected indirectly by selection due to pleiotropy of the underlying PAVs. C_LI

evolutionary biology↗

A Comprehensive Phylogenomic Platform for Exploring the Angiosperm Tree of Life

The tree of life is the fundamental biological roadmap for navigating the evolution and properties of life on Earth, and yet remains largely unknown. Even angiosperms (flowering plants) are fraught with data gaps, despite their critical role in sustaining terrestrial life. Today, high-throughput sequencing promises to significantly deepen our understanding of evolutionary relationships. Here, we describe a comprehensive phylogenomic platform for exploring the angiosperm tree of life, comprising a set of open tools and data based on the 353 nuclear genes targeted by the universal Angiosperms353 sequence capture probes. This paper (i) documents our methods, (ii) describes our first data release and (iii) presents a novel open data portal, the Kew Tree of Life Explorer (https://treeoflife.kew.org). We aim to generate novel target sequence capture data for all genera of flowering plants, exploiting natural history collections such as herbarium specimens, and augment it with mined public data. Our first data release, described here, is the most extensive nuclear phylogenomic dataset for angiosperms to date, comprising 3,099 samples validated by DNA barcode and phylogenetic tests, representing all 64 orders, 404 families (96%) and 2,333 genera (17%). Using the multi-species coalescent, we inferred a "first pass" angiosperm tree of life from the data, which totalled 824,878 sequences, 489,086,049 base pairs, and 532,260 alignment columns. The tree is strongly supported and highly congruent with existing taxonomy, while challenging numerous hypothesized relationships among orders and placing many genera for the first time. The validated dataset, species tree and all intermediates are openly accessible via the Kew Tree of Life Explorer. This major milestone towards a complete tree of life for all flowering plant species opens doors to a highly integrated future for angiosperm phylogenomics through the systematic sequencing of standardised nuclear markers. Our approach has the potential to serve as a much-needed bridge between the growing movement to sequence the genomes of all life on Earth and the vast phylogenomic potential of the worlds natural history collections.

evolutionary biology↗

Archaeogenomics of a ~2,100-year-old Egyptian leaf provides a new timestamp on date palm domestication

O_LIThe date palm (Phoenix dactylifera) has been a cornerstone of Middle Eastern and North African agriculture for millennia. It is presumed that date palms were first domesticated in the Persian Gulf and subsequently introduced into North Africa, where their evolution in the latter region appears to have been influenced by gene flow from the wild relative P. theophrasti, which is restricted to Crete and Turkey. However, the timing of gene flow from P. theophrasti to P. dactylifera remains unknown due to the limited archaeobotanical evidence of P. theophrasti and their exclusion from population genomic studies. C_LIO_LIWe addressed this issue by investigating the relatedness and ancestry of a ~2,100-year-old P. dactylifera leaf from Saqqara (Egypt), combining genome sequencing of this ancient specimen with a broad sample of date palm cultivars and closely related species. C_LIO_LIThe ancient Saqqara date palm shares close genetic ancestry with North African date palm populations. We find clear genomic admixture between the Saqqara date palm, P. theophrasti and the closest known relative P. sylvestris. C_LIO_LIOur study highlights that gene flow from P. theophrasti and P. sylvestris to North African date palms had already occurred at least ~2,100 years ago, providing a minimum timestamp for hybridisation between species. C_LI

evolutionary biology↗

Hundreds of nuclear and plastid loci yield insights into orchid relationships

Premise of the studyEvolutionary relationships in the species-rich Orchidaceae have historically relied on organellar DNA sequences and limited taxon sampling. Previous studies provided a robust plastid-maternal phylogenetic framework, from which multiple hypotheses on the drivers of orchid diversification have been derived. However, the extent to which the maternal evolutionary history of orchids is congruent with that of the nuclear genome has remained uninvestigated. MethodsWe inferred phylogenetic relationships from 294 low-copy nuclear genes sequenced/obtained using the Angiosperms353 universal probe set from 75 species representing 69 genera, 16 tribes and 24 subtribes. To test for topological incongruence between nuclear and plastid genomes, we constructed a tree from 78 plastid genes, representing 117 genera, 18 tribes and 28 subtribes and compared them using a co-phylogenetic approach. The phylogenetic informativeness and support of the Angiosperms353 loci were compared with those of the 78 plastid genes. Key ResultsPhylogenetic inferences of nuclear datasets produced highly congruent and robustly supported orchid relationships. Comparisons of nuclear gene trees and plastid gene trees using the latest co-phylogenetic tools revealed strongly supported phylogenetic incongruence in both shallow and deep time. Phylogenetic informativeness analyses showed that the Angiosperms353 genes were in general more informative than most plastid genes. ConclusionsOur study provides the first robust nuclear phylogenomic framework for Orchidaceae plus an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely documented: nuclear and plastid phylogenetic trees are not fully congruent and therefore should not be considered interchangeable.

evolutionary biology↗

A Universal Probe Set for Targeted Sequencing of 353 Nuclear Genes from Any Flowering Plant Designed Using k-medoids Clustering

Sequencing of target-enriched libraries is an efficient and cost-effective method for obtaining DNA sequence data from hundreds of nuclear loci for phylogeny reconstruction. Much of the cost associated with developing targeted sequencing approaches is preliminary data needed for identifying orthologous loci for probe design. In plants, identifying orthologous loci has proven difficult due to a large number of whole-genome duplication events, especially in the angiosperms (flowering plants). We used multiple sequence alignments from over 600 angiosperms for 353 putatively single-copy protein-coding genes to design a set of targeted sequencing probes for phylogenetic studies of any angiosperm lineage. To maximize the phylogenetic potential of the probes while minimizing the cost of production, we introduce a k-medoids clustering approach to identify the minimum number of sequences necessary to represent each coding sequence in the final probe set. Using this method, five to 15 representative sequences were selected per orthologous locus, representing the sequence diversity of angiosperms more efficiently than if probes were designed using available sequenced genomes alone. To test our approximately 80,000 probes, we hybridized libraries from 42 species spanning all higher-order lineages of angiosperms, with a focus on taxa not present in the sequence alignments used to design the probes. Out of a possible 353 coding sequences, we recovered an average of 283 per species and at least 100 in all species. Differences among taxa in sequence recovery could not be explained by relatedness to the representative taxa selected for probe design, suggesting that there is no phylogenetic bias in the probe set. Our probe set, which targeted 260 kbp of coding sequence, achieved a median recovery of 137 kbp per taxon in coding regions, a maximum recovery of 250 kbp, and an additional median of 212 kbp per taxon in flanking non-coding regions across all species. These results suggest that the Angiosperms353 probe set described here is effective for any group of flowering plants and would be useful for phylogenetic studies from the species level to higher-order lineages, including all angiosperms.

evolutionary biology↗