ABSTRACT
P‐element‐induced wimpy testis (PIWI)‐interacting RNAs (piRNAs) are small, noncoding RNAs known for silencing transposable elements (TEs) in the germline of animals. Most genomes host TEs, ...which are notorious for mobilizing themselves and endangering survival of the host if not controlled. By silencing TEs in the germline, piRNAs prevent harmful mutations from being passed on to the next generation. How piRNAs are generated and how they silence TEs were the focus of researchers ever since their discovery. Now a spate of recent papers are beginning to tell us that piRNAs can play roles beyond TE silencing and are involved in diverse cellular processes from mRNA regulation to development or genome rearrangement. In this review, we discuss some of these recently reported roles. Data on these new roles are often rudimentary, and the involvement of piRNAs in these processes is yet to be definitely established. What is interesting is that the reports are on animals widely separated on the phylogenetic tree of life and that piRNAs were also found outside the gonadal tissues. Some of these piRNAs map to TE sequences, prompting us to hypothesize that genomes may have co‐opted the TE‐derived piRNA system for their own regulation.—Sarkar, A., Volff, J.‐N., Vaury, C. piRNAs and their diverse roles: a transposable element‐driven tactic for gene regulation~ FASEB J. 31, 436–446 (2017). www.fasebj.org
Transposable elements (TEs) are major components of vertebrate genomes, with major roles in genome architecture and evolution. In order to characterize both common patterns and lineage-specific ...differences in TE content and TE evolution, we have compared the mobilomes of 23 vertebrate genomes, including 10 actinopterygian fish, 11 sarcopterygians, and 2 nonbony vertebrates. We found important variations in TE content (from 6% in the pufferfish tetraodon to 55% in zebrafish), with a more important relative contribution of TEs to genome size in fish than in mammals. Some TE superfamilies were found to be widespread in vertebrates, but most elements showed a more patchy distribution, indicative of multiple events of loss or gain. Interestingly, loss of major TE families was observed during the evolution of the sarcopterygian lineage, with a particularly strong reduction in TE diversity in birds and mammals. Phylogenetic trends in TE composition and activity were detected: Teleost fish genomes are dominated by DNA transposons and contain few ancient TE copies, while mammalian genomes have been predominantly shaped by nonlong terminal repeat retrotransposons, along with the persistence of older sequences. Differences were also found within lineages: The medaka fish genome underwent more recent TE amplification than the related platyfish, as observed for LINE retrotransposons in the mouse compared with the human genome. This study allows the identification of putative cases of horizontal transfer of TEs, and to tentatively infer the composition of the ancestral vertebrate mobilome. Taken together, the results obtained highlight the importance of TEs in the structure and evolution of vertebrate genomes, and demonstrate their major impact on genome diversity both between and within lineages.
Lungfishes belong to lobe-fined fish (Sarcopterygii) that, in the Devonian period, 'conquered' the land and ultimately gave rise to all land vertebrates, including humans
. Here we determine the ...chromosome-quality genome of the Australian lungfish (Neoceratodus forsteri), which is known to have the largest genome of any animal. The vast size of this genome, which is about 14× larger than that of humans, is attributable mostly to huge intergenic regions and introns with high repeat content (around 90%), the components of which resemble those of tetrapods (comprising mainly long interspersed nuclear elements) more than they do those of ray-finned fish. The lungfish genome continues to expand independently (its transposable elements are still active), through mechanisms different to those of the enormous genomes of salamanders. The 17 fully assembled lungfish macrochromosomes maintain synteny to other vertebrate chromosomes, and all microchromosomes maintain conserved ancient homology with the ancestral vertebrate karyotype. Our phylogenomic analyses confirm previous reports that lungfish occupy a key evolutionary position as the closest living relatives to tetrapods
, underscoring the importance of lungfish for understanding innovations associated with terrestrialization. Lungfish preadaptations to living on land include the gain of limb-like expression in developmental genes such as hoxc13 and sall1 in their lobed fins. Increased rates of evolution and the duplication of genes associated with obligate air-breathing, such as lung surfactants and the expansion of odorant receptor gene families (which encode proteins involved in detecting airborne odours), contribute to the tetrapod-like biology of lungfishes. These findings advance our understanding of this major transition during vertebrate evolution.
Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of ...sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to the current debate about heterogametic sex-chromosome decay, we find that massive gene loss occurred in the wake of sex-chromosome 'birth'.
Actinopterygian fishes harbor at least eight distinct pigment cell types, leading to a fascinating diversity of colors. Among this diversity, the cellular origin of the white color appears to be ...linked to several pigment cell types such as iridophores or leucophores. We used the clownfish Amphiprion ocellaris, which has a color pattern consisting of white bars over a darker body, to characterize the pigment cells that underlie the white hue. We observe by electron microscopy that cells in white bars are similar to iridophores. In addition, the transcriptomic signature of clownfish white bars exhibits similarities with that of zebrafish iridophores. We further show by pharmacological treatments that these cells are necessary for the white color. Among the top differentially expressed genes in white skin, we identified several genes (fhl2a, fhl2b, saiyan, gpnmb, and apoD1a) and show that three of them are expressed in iridophores. Finally, we show by CRISPR/Cas9 mutagenesis that these genes are critical for iridophore development in zebrafish. Our analyses provide clues to the genomic underpinning of color diversity and allow identification of new iridophore genes in fish.
In eukaryotes, genome size correlates little with the number of coding genes or the level of organismal complexity (C-value paradox). The underlying causes of variations in genome size, whether ...adaptive or neutral, remain unclear, although several biological traits often covary with it 1–5. Rapid increases in genome size occur mainly through whole-genome duplications or bursts in the activity of transposable elements (TEs) 6. The very small and compact genome of Oikopleura dioica, a tunicate of the larvacean class, lacks elements of most ancient families of animal retrotransposons 7, 8. Here, we sequenced the genomes of six other larvaceans, all of which are larger than that of Oikopleura (up to 12 times) and which increase in size with greater body length. Although no evidence was found for whole-genome duplications within the group of species, the global amount of TEs strongly correlated with genome size. Compared to other metazoans, however, the TE diversity was reduced in all species, as observed previously in O. dioica, suggesting a common ancestor with a compacted genome. Strikingly, non-autonomous elements, particularly short interspersed nuclear elements (SINEs), massively contributed to genome size variation through species-specific independent amplifications, ranging from 3% in the smallest genome up to 49% in the largest. Variations in SINE abundance explain as much as 83% of interspecific genome size variation. These data support an indirect influence of autonomous TEs on genome size via their ability to mobilize non-autonomous elements.
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•Genome size varies up to 12× in larvaceans, chordates with a distinctive anatomy•Small and large species have the smallest and largest genomes, respectively•Transposable elements have driven multiple independent genome expansions•Genomes mainly increased through accumulations of non-autonomous elements (SINEs)
The causes of genome size variation and their relation with life traits are poorly understood. Naville, Henriet, et al. show that, in tunicate larvaceans, close relatives of vertebrates, multiplications of non-autonomous transposable elements were the main drive of remarkable genome expansions.
Teleost fish have been shown to contain many superfamilies of transposable elements (TEs) that are absent from most tetrapod genomes. Since theories predict an increase in TE activity following ...polyploidization, such diversity might be linked to the 3R whole‐genome duplication that occurred approximately 300 million years ago before the teleost radiation. To test this hypothesis, we have analyzed the genome of the spotted gar Lepisosteus oculatus, which diverged from the teleost lineage before the 3R duplication. Our results indicate that TE diversity and copy numbers are similar in gar and teleost genomes, suggesting that TE diversity was ancestral and not linked to the 3R whole‐genome duplication. We propose that about 25 distinct superfamilies of TEs were present in the last ancestor of gars and teleost fish about 300 million years ago in the ray‐finned fish lineage.
GRAPHICAL ABSTRACT
Transposable element diversity in gar suggests absence of causative link between ancestral genome duplication and transposon diversification in teleost fish.
Several attributes intuitively considered to be typical mammalian features, such as complex behavior, live birth and malignant disease such as cancer, also appeared several times independently in ...lower vertebrates. The genetic mechanisms underlying the evolution of these elaborate traits are poorly understood. The platyfish, X. maculatus, offers a unique model to better understand the molecular biology of such traits. We report here the sequencing of the platyfish genome. Integrating genome assembly with extensive genetic maps identified an unexpected evolutionary stability of chromosomes in fish, in contrast to in mammals. Genes associated with viviparity show signatures of positive selection, identifying new putative functional domains and rare cases of parallel evolution. We also find that genes implicated in cognition show an unexpectedly high rate of duplicate gene retention after the teleost genome duplication event, suggesting a hypothesis for the evolution of the behavioral complexity in fish, which exceeds that found in amphibians and reptiles.
Coloration and color patterning belong to the most diverse phenotypic traits in animals. Particularly, teleost fishes possess more pigment cell types than any other group of vertebrates. As the ...result of an ancient fish-specific genome duplication (FSGD), teleost genomes might contain more copies of genes involved in pigment cell development than tetrapods. No systematic genomic inventory allowing to test this hypothesis has been drawn up so far for pigmentation genes in fish, and almost nothing is known about the evolution of these genes in different fish lineages.
Using a comparative genomic approach including phylogenetic reconstructions and synteny analyses, we have studied two major pigment synthesis pathways in teleost fish, the melanin and the pteridine pathways, with respect to different types of gene duplication. Genes encoding three of the four enzymes involved in the synthesis of melanin from tyrosine have been retained as duplicates after the FSGD. In the pteridine pathway, two cases of duplicated genes originating from the FSGD as well as several lineage-specific gene duplications were observed. In both pathways, genes encoding the rate-limiting enzymes, tyrosinase and GTP-cyclohydrolase I (GchI), have additional paralogs in teleosts compared to tetrapods, which have been generated by different modes of duplication. We have also observed a previously unrecognized diversity of gchI genes in vertebrates. In addition, we have found evidence for divergent resolution of duplicated pigmentation genes, i.e., differential gene loss in divergent teleost lineages, particularly in the tyrosinase gene family.
Mainly due to the FSGD, teleost fishes apparently have a greater repertoire of pigment synthesis genes than any other vertebrate group. Our results support an important role of the FSGD and other types of duplication in the evolution of pigmentation in fish.
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