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Polyploidy or whole-genome duplication (WGD) is a major event that drastically reshapes genome architecture and is often assumed to be causally associated with organismal innovations and radiations. The 2R hypothesis suggests that two WGD events (1R and 2R) occurred during early vertebrate evolution. However, the timing of the 2R event relative to the divergence of gnathostomes (jawed vertebrates) and cyclostomes (jawless hagfishes and lampreys) is unresolved and whether these WGD events underlie vertebrate phenotypic diversification remains elusive. Here we present the genome of the inshore hagfish, Eptatretus burgeri. Through comparative analysis with lamprey and gnathostome genomes, we reconstruct the early events in cyclostome genome evolution, leveraging insights into the ancestral vertebrate genome. Genome-wide synteny and phylogenetic analyses support a scenario in which 1R occurred in the vertebrate stem-lineage during the early Cambrian, and 2R occurred in the gnathostome stem-lineage, maximally in the late Cambrian-earliest Ordovician, after its divergence from cyclostomes. We find that the genome of stem-cyclostomes experienced an additional independent genome triplication. Functional genomic and morphospace analyses demonstrate that WGD events generally contribute to developmental evolution with similar changes in the regulatory genome of both vertebrate groups. However, appreciable morphological diversification occurred only in the gnathostome but not in the cyclostome lineage, calling into question the general expectation that WGDs lead to leaps of bodyplan complexity.
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Anguila Babosa , Animales , Filogenia , Anguila Babosa/genética , Duplicación de Gen , Vertebrados/genética , Genoma , Lampreas/genéticaRESUMEN
The origin of land plants and their descendants was marked by the evolution of key adaptations to life in terrestrial environments such as roots, vascular tissue and stomata. Though these innovations are well characterized, the evolution of the genetic toolkit underlying their development and function is poorly understood. We analysed molecular data from 532 species to investigate the evolutionary origin and diversification of genes involved in the development and regulation of these adaptations. We show that novel genes in the first land plants led to the single origin of stomata, but the stomatal closure of seed plants resulted from later gene expansions. By contrast, the major mechanism leading to the origin of vascular tissue was cooption of genes that emerged in the first land plants, enabling continuous water transport throughout the ancestral vascular plant. In turn, new key genes in the ancestors of plants with true leaves and seed plants led to the emergence of roots and lateral roots. The analysis highlights the different modes of evolution that enabled plants to conquer land, suggesting that gene expansion and cooption are the most common mechanisms of biological innovation in plant evolutionary history.
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Embryophyta , Agua , Evolución Biológica , Embryophyta/genética , Filogenia , Hojas de la Planta/genética , Raíces de Plantas/genética , Plantas/genéticaRESUMEN
There can be no doubt that early land plant evolution transformed the planet but, until recently, how and when this was achieved was unclear. Coincidence in the first appearance of land plant fossils and formative shifts in atmospheric oxygen and CO2 are an artefact of the paucity of earlier terrestrial rocks. Disentangling the timing of land plant bodyplan assembly and its impact on global biogeochemical cycles has been precluded by uncertainty concerning the relationships of bryophytes to one another and to the tracheophytes, as well as the timescale over which these events unfolded. New genome and transcriptome sequencing projects, combined with the application of sophisticated phylogenomic modelling methods, have yielded increasing support for the Setaphyta clade of liverworts and mosses, within monophyletic bryophytes. We consider the evolution of anatomy, genes, genomes and of development within this phylogenetic context, concluding that many vascular plant (tracheophytes) novelties were already present in a comparatively complex last common ancestor of living land plants (embryophytes). Molecular clock analyses indicate that embryophytes emerged in a mid-Cambrian to early Ordovician interval, compatible with hypotheses on their role as geoengineers, precipitating early Palaeozoic glaciations.
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Briófitas , Embryophyta , Evolución Biológica , Briófitas/genética , Embryophyta/anatomía & histología , Embryophyta/genética , Fósiles , FilogeniaRESUMEN
It is commonly known that drought stress is a major constraint limiting crop production. Drought stress and associated drought tolerance mechanisms are therefore under intense investigation with the view to future production of drought tolerant crops. With an ever-growing population and variable climate, novel approaches need to be considered to sustainably feed future generations. In this context, definitions of drought tolerance are highly variable, which poses a major challenge for the systematic assessment of this trait across the plant kingdom. Furthermore, drought tolerance is a polygenic trait and understanding the evolution of this complex trait may inform us about patterns of gene gain and loss in relation to diverse drought adaptations. We look at the transition of plants from water to land, and the role of drought tolerance in enabling this transition, before discussing the first drought tolerant plant and common drought responses amongst vascular plants. We reviewed the distribution of a combined "drought tolerance" trait in very broad terms to encompass different experimental systems and definitions used in the current literature and assigned a binary trait "tolerance vs. sensitivity" in 178 extant plant species. By simplifying drought responses of plants into this "binary" trait we were able to explore the evolution of drought tolerance across the wider plant kingdom, compared to previous studies. We show how this binary "drought tolerance/sensitivity" trait has evolved and discuss how incorporating this information into an evolutionary genomics framework could provide insights into the molecular mechanisms underlying extreme drought adaptations.
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Animals display a diversity of life cycles, including larvae in some lineages but not in others. A new study reveals a shared genetic toolkit in many animals that regulates the transition to the juvenile form, from an embryo or a larva.
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Evolución Biológica , Estadios del Ciclo de Vida , Animales , LarvaRESUMEN
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.
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Adaptación Fisiológica/genética , Ephemeroptera/genética , Evolución Molecular , Alas de Animales , Animales , Ephemeroptera/clasificación , Ephemeroptera/crecimiento & desarrollo , Femenino , Regulación del Desarrollo de la Expresión Génica , Genes de Insecto/genética , Genoma de los Insectos/genética , Branquias , Insectos/clasificación , Insectos/genética , Estadios del Ciclo de Vida/genética , Masculino , FilogeniaRESUMEN
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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The animal kingdom shows an astonishing diversity, the product of over 550 million years of animal evolution. The current wealth of genome sequence data offers an opportunity to better understand the genomic basis of this diversity. Here we analyse a sampling of 102 whole genomes including >2.6 million protein sequences. We infer major genomic patterns associated with the variety of animal forms from the superphylum to phylum level. We show that a remarkable amount of gene loss occurred during the evolution of two major groups of bilaterian animals, Ecdysozoa and Deuterostomia, and further loss in several deuterostome lineages. Deuterostomes and protostomes also show large genome novelties. At the phylum level, flatworms, nematodes and tardigrades show the largest reduction of gene complement, alongside gene novelty. These findings paint a picture of evolution in the animal kingdom in which reductive evolution at the protein-coding level played a major role in shaping genome composition.
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Evolución Molecular , Genoma , Secuencia de Aminoácidos , Animales , FilogeniaRESUMEN
Over the last 470 Ma, plant evolution has seen major evolutionary transitions, such as the move from water to land and the origins of vascular tissues, seeds, and flowers [1]. These have resulted in the evolution of terrestrial flora that has shaped modern ecosystems and the diversification of the Plant Kingdom, Viridiplantae, into over 374,000 described species [2]. Each of these transitions was accompanied by the gain and loss of genes in plant genomes. For example, whole-genome duplications are known to be fundamental to the origins of both seed and flowering plants [3, 4]. With the ever-increasing quality and quantity of whole-genome data, evolutionary insight into origins of distinct plant groups using comparative genomic techniques is now feasible. Here, using an evolutionary genomics pipeline to compare 208 complete genomes, we analyze the gene content of the ancestral genomes of the last common ancestor of land plants and all other major groups of plant. This approach reveals an unprecedented level of fundamental genomic novelties in two nodes related to the origin of land plants: the first in the origin of streptophytes during the Ediacaran and another in the ancestor of land plants in the Ordovician. Our findings highlight the biological processes that evolved with the origin of land plants and emphasize the importance of conserved gene novelties in plant diversification. Comparisons to other eukaryotic studies suggest a separation of the genomic origins of multicellularity and terrestrialization in plants.
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Embryophyta/genética , Evolución Molecular , Genoma de Planta , Evolución Biológica , FilogeniaRESUMEN
Traditional evolutionary scenarios posit that land plants emerged from land plant-like relatives, the charophytes. New phylogenies suggest a closer affinity to simpler pond scum relatives, and evidence the gradual assembly of the land plant genome, revealing a phenotypic simplification from the complex ancestors envisaged by traditional scenarios.
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Carofíceas/genética , Embryophyta/genética , Genoma de Planta , Filogenia , PlantasRESUMEN
Nature is adept at utilising highly similar protein folds to carry out very different functions, yet the mechanisms by which this functional divergence occurs remain poorly characterised. In certain methanotrophic bacteria, two homologous pentacoordinate c-type heme proteins have been identified: a cytochrome P460 (cyt P460) and a cytochrome c'-ß (cyt cp-ß). Cytochromes P460 are able to convert hydroxylamine to nitrous oxide (N2O), a potent greenhouse gas. This reactivity is similar to that of hydroxylamine oxidoreductase (HAO), which is a key enzyme in nitrifying and methanotrophic bacteria. Cyt P460 and HAO both have unusual protein-heme cross-links, formed by a Tyr residue in HAO and a Lys in cyt P460. In contrast, cyts cp-ß (the only known cytochromes c' with a ß-sheet fold) lack this crosslink and appears to be optimized for binding non-polar molecules (including NO and CO) without enzymatic conversion. Our bioinformatics analysis supports the proposal that cyt cp-ß may have evolved from cyt P460 via a gene duplication event. Using high-resolution X-ray crystallography, UV-visible absorption, electron paramagnetic resonance (EPR) and resonance Raman spectroscopy, we have characterized the overall protein folding and active site structures of cyt cp-ß and cyt P460 from the obligate methanotroph, Methylococcus capsulatus (Bath). These proteins display a similar ß-sheet protein fold, together with a pattern of changes to the heme pocket regions and localised tertiary structure that have converted a hydroxylamine oxidizing enzyme into a gas-binding protein. Structural comparisons provide insights relevant to enzyme redesign for synthetic enzymology and engineering of gas sensor proteins. We also show the widespread occurrence of cyts cp-ß and characterise their phylogeny.
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[This corrects the article DOI: 10.1039/C8SC05210G.].
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[This corrects the article DOI: 10.1039/C8SC05210G.].
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Although animals are among the best studied organisms, we still lack a full description of their diversity, especially for microscopic taxa. This is partly due to the time-consuming and costly nature of surveying animal diversity through morphological and molecular studies of individual taxa. A powerful alternative is the use of high-throughput environmental sequencing, providing molecular data from all organisms sampled. We here address the unknown diversity of animal phyla in marine environments using an extensive dataset designed to assess eukaryotic ribosomal diversity among European coastal locations. A multi-phylum assessment of marine animal diversity that includes water column and sediments, oxic and anoxic environments, and both DNA and RNA templates, revealed a high percentage of novel 18S rRNA sequences in most phyla, suggesting that marine environments have not yet been fully sampled at a molecular level. This novelty is especially high among Platyhelminthes, Acoelomorpha, and Nematoda, which are well studied from a morphological perspective and abundant in benthic environments. We also identified, based on molecular data, a potentially novel group of widespread tunicates. Moreover, we recovered a high number of reads for Ctenophora and Cnidaria in the smaller fractions suggesting their gametes might play a greater ecological role than previously suspected.
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Organismos Acuáticos , Biodiversidad , Código de Barras del ADN Taxonómico , Nematodos , Platelmintos , Animales , Organismos Acuáticos/clasificación , Organismos Acuáticos/genética , ADN de Helmintos/genética , Europa (Continente) , Nematodos/clasificación , Nematodos/genética , Platelmintos/clasificación , Platelmintos/genética , ARN de Helminto/genética , ARN Ribosómico 18S/genéticaRESUMEN
Understanding the emergence of the Animal Kingdom is one of the major challenges of modern evolutionary biology. Many genomic changes took place along the evolutionary lineage that gave rise to the Metazoa. Recent research has revealed the role that co-option of old genes played during this transition, but the contribution of genomic novelty has not been fully assessed. Here, using extensive genome comparisons between metazoans and multiple outgroups, we infer the minimal protein-coding genome of the first animal, in addition to other eukaryotic ancestors, and estimate the proportion of novelties in these ancient genomes. Contrary to the prevailing view, this uncovers an unprecedented increase in the extent of genomic novelty during the origin of metazoans, and identifies 25 groups of metazoan-specific genes that are essential across the Animal Kingdom. We argue that internal genomic changes were as important as external factors in the emergence of animals.
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Evolución Biológica , Biología Computacional/métodos , Genoma , Familia de Multigenes , Proteínas/genética , Animales , Células Eucariotas/citología , Células Eucariotas/metabolismo , Regulación de la Expresión Génica , Filogenia , Proteínas/clasificación , Proteínas/metabolismo , Transducción de SeñalRESUMEN
What makes an animal? To find the answer we need to integrate data from disciplines such as phylogenetics, paleontology, ecology, development, anatomy, and physiology, as well as molecular biology and genomics. Knowledge of which groups branched before and after the origin of animals is essential. Recent advances in molecular phylogenetics, together with the discovery of new eukaryotic lineages, have drawn a new picture of the ancestry of animals. The nature of the early diverging animal lineages and the timing of the transition are in a state of flux. Various factors have been linked to this striking transition to multicellularity, including changes in environmental conditions and the ecological interactions between unicellular eukaryotes. The current wealth of genomic data has also shed new light on this question. The analysis of the genome of various close relatives of animals has revealed the importance that recycling of ancient genes into metazoan biological functions played into animal origins. A recent study reconstructing the genome of the last common ancestor of extant animals has unveiled an unprecedented emergence of new genes, highlighting the role of genomic novelty in the origin of metazoans.
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Evolución Biológica , Genómica/métodos , Invertebrados/genética , Biología Molecular/métodos , Filogenia , Animales , Evolución Molecular , Genoma , Invertebrados/clasificación , Vertebrados/clasificación , Vertebrados/genéticaRESUMEN
Hox genes exert fundamental roles for proper regional specification along the main rostro-caudal axis of animal embryos. They are generally expressed in restricted spatial domains according to their position in the cluster (spatial colinearity)-a feature that is conserved across bilaterians. In jawed vertebrates (gnathostomes), the position in the cluster also determines the onset of expression of Hox genes (a feature known as whole-cluster temporal colinearity (WTC)), while in invertebrates this phenomenon is displayed as a subcluster-level temporal colinearity. However, little is known about the expression profile of Hox genes in jawless vertebrates (cyclostomes); therefore, the evolutionary origin of WTC, as seen in gnathostomes, remains a mystery. Here, we show that Hox genes in cyclostomes are expressed according to WTC during development. We investigated the Hox repertoire and Hox gene expression profiles in three different species-a hagfish, a lamprey and a shark-encompassing the two major groups of vertebrates, and found that these are expressed following a whole-cluster, temporally staggered pattern, indicating that WTC has been conserved during the past 500 million years despite drastically different genome evolution and morphological outputs between jawless and jawed vertebrates.
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Evolución Molecular , Regulación del Desarrollo de la Expresión Génica , Genes Homeobox , Anguila Babosa/genética , Lampreas/genética , Animales , Genoma , Anguila Babosa/crecimiento & desarrollo , Lampreas/crecimiento & desarrollo , Tiburones/genética , Tiburones/crecimiento & desarrollo , TranscriptomaRESUMEN
Streptomyces lividans has a distinct dependence on the bioavailability of copper for its morphological development. A cytosolic copper resistance system is operative in S. lividans that serves to preclude deleterious copper levels. This system comprises of several CopZ-like copper chaperones and P1-type ATPases, predominantly under the transcriptional control of a metalloregulator from the copper sensitive operon repressor (CsoR) family. In the present study, we discover a new layer of cytosolic copper resistance in S. lividans that involves a protein belonging to the newly discovered family of copper storage proteins, which we have named Ccsp (cytosolic copper storage protein). From an evolutionary perspective, we find Ccsp homologues to be widespread in Bacteria and extend through into Archaea and Eukaryota. Under copper stress Ccsp is upregulated and consists of a homotetramer assembly capable of binding up to 80 cuprous ions (20 per protomer). X-ray crystallography reveals 18 cysteines, 3 histidines and 1 aspartate are involved in cuprous ion coordination. Loading of cuprous ions to Ccsp is a cooperative process with a Hill coefficient of 1.9 and a CopZ-like copper chaperone can transfer copper to Ccsp. A Δccsp mutant strain indicates that Ccsp is not required under initial copper stress in S. lividans, but as the CsoR/CopZ/ATPase efflux system becomes saturated, Ccsp facilitates a second level of copper tolerance.
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Proteínas Bacterianas/metabolismo , Cobre/toxicidad , Citosol/metabolismo , Metalochaperonas/metabolismo , Streptomyces lividans/metabolismo , Proteínas Bacterianas/química , Proteínas Bacterianas/genética , Clonación Molecular , Cristalografía por Rayos X , Metalochaperonas/química , Metalochaperonas/genética , Operón , Unión Proteica , Conformación Proteica , Streptomyces lividans/crecimiento & desarrolloRESUMEN
Analysis of genome sequences within a phylogenetic context can give insight into the mode and tempo of gene and protein evolution, including inference of gene ages. This can reveal whether new genes arose on particular evolutionary lineages and were recruited for new functional roles. Here, we apply MCL clustering with all-versus-all reciprocal BLASTP to identify and phylogenetically date 'Homology Groups' among vertebrate proteins. Homology Groups include new genes and highly divergent duplicate genes. Focusing on the origin of the placental mammals within the Eutheria, we identify 357 novel Homology Groups that arose on the stem lineage of Placentalia, 87 of which are deduced to play core roles in mammalian biology as judged by extensive retention in evolution. We find the human homologues of novel eutherian genes are enriched for expression in preimplantation embryo, brain, and testes, and enriched for functions in keratinization, reproductive development, and the immune system.
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Euterios/genética , Evolución Molecular , Genoma , Animales , FilogeniaRESUMEN
Gene duplications and gene losses have been frequent events in the evolution of animal genomes, with the balance between these two dynamic processes contributing to major differences in gene number between species. After gene duplication, it is common for both daughter genes to accumulate sequence change at approximately equal rates. In some cases, however, the accumulation of sequence change is highly uneven with one copy radically diverging from its paralogue. Such 'asymmetric evolution' seems commoner after tandem gene duplication than after whole-genome duplication, and can generate substantially novel genes. We describe examples of asymmetric evolution in duplicated homeobox genes of moths, molluscs and mammals, in each case generating new homeobox genes that were recruited to novel developmental roles. The prevalence of asymmetric divergence of gene duplicates has been underappreciated, in part, because the origin of highly divergent genes can be difficult to resolve using standard phylogenetic methods.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.