The small non-coding RNA processing machinery of two living fossil species, lungfish and coelacanth, gives new insights into the evolution of the Argonaute protein family.
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ABSTRACT:
SUBMITTER: Biscotti M.A.
PROVIDER: S-EPMC5381642 | biostudies-literature | 2017 Mar
REPOSITORIES: biostudies-literature
Publications
The small non-coding RNA processing machinery of two living fossil species, lungfish and coelacanth, gives new insights into the evolution of the Argonaute protein family.
Biscotti Maria Assunta M.A. Canapa Adriana A Forkoni Mariko M Gerdol Marco M Pallavicini Alberto A Schartl Manifred M Barucca Marco M
Genome biology and evolution 20170216 3
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Project description:The colonization of land by tetrapod ancestors is one of the major questions in the evolution of vertebrates. Despite intense molecular phylogenetic research on this problem during the last 15 years, there is, until now, no statistically supported answer to the question of whether coelacanths or lungfish are the closest living relatives of tetrapods. We determined DNA sequences of the nuclear-encoded recombination activating genes (Rag1 and Rag2) from all three major lungfish groups, the Australian Neoceratodis forsteri, the South American Lepidosiren paradoxa and the African lungfish Protopterus dolloi, and the Indonesian coelacanth Latimeria menadoensis. Phylogenetic analyses of both the single gene and the concatenated data sets of RAG1 and RAG2 found that the lungfishes are the closest living relatives of the land vertebrates. These results are supported by high bootstrap values, Bayesian posterior probabilities, and likelihood ratio tests.
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Project description:Emerging data from the coelacanth genome are beginning to shed light on the origin and evolution of tetrapod genes and noncoding elements. Of particular relevance is the realization that coelacanth retains active copies of transposable elements that once served as raw material for the evolution of new functional sequences in the vertebrate lineage. Recognizing the evolutionary significance of coelacanth genome in this regard, we employed an ab initio search strategy to further classify its repetitive complement. This analysis uncovered a class of interspersed elements (Latimeria Harbinger 1-LatiHarb1) that is a major contributor to coelacanth genome structure and gene content (?1% to 4% or the genome). Sequence analyses indicate that 1) each ?8.7 kb LatiHarb1 element contains two coding regions, a transposase gene and a gene whose function is as yet unknown (MYB-like) and 2) copies of LatiHarb1 retain biological activity in the coelacanth genome. Functional analyses verify transcriptional and enhancer activities of LatiHarb1 in vivo and reveal transcriptional decoupling that could permit MYB-like genes to play functional roles not directly linked to transposition. Thus, LatiHarb1 represents the first known instance of a harbinger-superfamily transposon with contemporary activity in a vertebrate genome. Analyses of LatiHarb1 further corroborate the notion that exaptation of anciently active harbinger elements gave rise to at least two vertebrate genes (harbi1 and naif1) and indicate that the vertebrate gene tsnare1 also traces its ancestry to this transposon superfamily. Based on our analyses of LatiHarb1, we speculate that several functional features of harbinger elements may predispose the transposon superfamily toward recurrent exaptive evolution of cellular coding genes. In addition, these analyses further reinforce the broad utility of the coelacanth genome and other "outgroup" genomes in understanding the ancestry and evolution of vertebrate genes and genomes.
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Project description:BACKGROUND: One of the greatest challenges facing the early land vertebrates was the need to effectively interpret a terrestrial environment. Interpretation was based on ocular adaptations evolved for an aquatic environment millions of years earlier. The Australian lungfish Neoceratodus forsteri is thought to be the closest living relative to the first terrestrial vertebrate, and yet nothing is known about the visual pigments present in lungfish or the early tetrapods. RESULTS: Here we identify and characterise five visual pigments (rh1, rh2, lws, sws1 and sws2) expressed in the retina of N. forsteri. Phylogenetic analysis of the molecular evolution of lungfish and other vertebrate visual pigment genes indicates a closer relationship between lungfish and amphibian pigments than to pigments in teleost fishes. However, the relationship between lungfish, the coelacanth and tetrapods could not be absolutely determined from opsin phylogeny, supporting an unresolved trichotomy between the three groups. CONCLUSION: The presence of four cone pigments in Australian lungfish suggests that the earliest tetrapods would have had a colorful view of their terrestrial environment.
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Project description:The coelacanth has long been regarded as a "living fossil," with extant specimens looking very similar to fossils dating back to the Cretaceous period. The hypothesis of a slowly or even not evolving genome has been proposed to account for this apparent morphological stasis. While this assumption seems to be sustained by different evolutionary analyses on protein-coding genes, recent studies on transposable elements have provided more conflicting results. Indeed, the coelacanth genome contains many transposable elements and has been shaped by several major bursts of transposition during evolution. In addition, comparison of orthologous genomic regions from the genomes of the 2 extant coelacanth species L. chalumnae and L. menadoensis revealed multiple species-specific insertions, indicating transposable element recent activity and contribution to post-speciation genome divergence. These observations, which do not support the genome stasis hypothesis, challenge either the impact of transposable elements on organismal evolution or the status of the coelacanth as a "living fossil." Closer inspection of fossil and molecular data indicate that, even if coelacanths might evolve more slowly than some other lineages due to demographic and/or ecological factors, this variation is still in the range of a "non-fossil" vertebrate species.
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Project description:The complete nucleotide sequence of the 16,407-bp mitochondrial genome of the coelacanth (Latimeria chalumnae) was determined. The coelacanth mitochondrial genome order is identical to the consensus vertebrate gene order which is also found in all ray-finned fishes, the lungfish, and most tetrapods. Base composition and codon usage also conform to typical vertebrate patterns. The entire mitochondrial genome was PCR-amplified with 24 sets of primers that are expected to amplify homologous regions in other related vertebrate species. Analyses of the control region of the coelacanth mitochondrial genome revealed the existence of four 22-bp tandem repeats close to its 3' end. The phylogenetic analyses of a large data set combining genes coding for rRNAs, tRNAs, and proteins (16,140 characters) confirmed the phylogenetic position of the coelacanth as a lobe-finned fish; it is more closely related to tetrapods than to ray-finned fishes. However, different phylogenetic methods applied to this largest available molecular data set were unable to resolve unambiguously the relationship of the coelacanth to the two other groups of extant lobe-finned fishes, the lungfishes and the tetrapods. Maximum parsimony favored a lungfish/coelacanth or a lungfish/tetrapod sistergroup relationship depending on which transversion:transition weighting is assumed. Neighbor-joining and maximum likelihood supported a lungfish/tetrapod sistergroup relationship.
| S-EPMC1208067 | biostudies-other
Project description:BackgroundSince the discovery of the "living fossil" in 1938, the coelacanth (Latimeria chalumnae) has generally been considered to be the closest living relative of the land vertebrates, and this is still the prevailing opinion in most general biology textbooks. However, the origin of tetrapods has not been resolved for decades. Three principal hypotheses (lungfish-tetrapod, coelacanth-tetrapod, or lungfish-coelacanth sister group) have been proposed.FindingsWe used the Bayesian method under the coalescence model with the latest published program (Bayesian Estimation of Species Trees, or BEST) to perform a phylogenetic analysis for seven relevant taxa and 43 nuclear protein-coding genes with the jackknife method for taxon sub-sampling. The lungfish-coelacanth sister group was consistently reconstructed with the Bayesian method under the coalescence model in 17 out of 21 taxon sets with a Bayesian posterior probability as high as 99%. Lungfish-tetrapod was only inferred from BCLS and BACLS. Neither coelacanth-tetrapod nor lungfish-coelacanth-tetrapod was recovered out of all 21 taxon sets.ConclusionsOur results provide strong evidence in favor of accepting the hypothesis that lungfishes and coelacanths form a monophyletic sister-group that is the closest living relative of tetrapods. This clade was supported by high Bayesian posterior probabilities of the branch (a lungfish-coelacanth clade) and high taxon jackknife supports.
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Project description:To understand how nuclear machineries are targeted to accurate locations during nuclear assembly, we investigated the pathway of the ribosomal RNA (rRNA) processing machinery towards ribosomal genes (nucleolar organizer regions [NORs]) at exit of mitosis. To follow in living cells two permanently transfected green fluorescence protein-tagged nucleolar proteins, fibrillarin and Nop52, from metaphase to G1, 4-D time-lapse microscopy was used. In early telophase, fibrillarin is concentrated simultaneously in prenucleolar bodies (PNBs) and NORs, whereas PNB-containing Nop52 forms later. These distinct PNBs assemble at the chromosome surface. Analysis of PNB movement does not reveal the migration of PNBs towards the nucleolus, but rather a directional flow between PNBs and between PNBs and the nucleolus, ensuring progressive delivery of proteins into nucleoli. This delivery appeared organized in morphologically distinct structures visible by electron microscopy, suggesting transfer of large complexes. We propose that the temporal order of PNB assembly and disassembly controls nucleolar delivery of these proteins, and that accumulation of processing complexes in the nucleolus is driven by pre-rRNA concentration. Initial nucleolar formation around competent NORs appears to be followed by regroupment of the NORs into a single nucleolus 1 h later to complete the nucleolar assembly. This demonstrates the formation of one functional domain by cooperative interactions between different chromosome territories.
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Project description:Previously considered an actinopterygian or an osteichthyan incertae sedis, the Devonian (Givetian-Frasnian) Holopterygius nudus is reinterpreted as a coelacanth. This genus is among the oldest coelacanths known from articulated remains, but its eel-like morphology marks a considerable departure from the conventional coelacanth body plan. A cladistic analysis places Holopterygius as the sister taxon of the Carboniferous (Serpukhovian) genus Allenypterus. Despite the specialized morphology of these genera, they occupy a surprisingly basal position in coelacanth phylogeny; only Diplocercides and Miguashaia are further removed from the crown. A morphometric analysis reveals that coelacanths were anatomically disparate early in their history. Conflicts between this result and those of previous studies challenge the adequacy of systematic character sets for describing historical patterns of morphological variety. Coelacanths have long had an iconic place in the study of vertebrate evolution for their apparent anatomical conservatism over geological time, but Holopterygius provides clear evidence for rapid morphological evolution early in the history of this clade.
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Project description:BackgroundThe Notostraca is a small but ancient crustacean order with a contrasting combination of a conservative morphology and a wide range of reproductive modes. The tadpole shrimp Triops cancriformis, includes bisexual - the putatively ancestral state -, androdioecious and hermaphrodite populations. As hermaphroditism and androdioecy confer a colonisation advantage, we expect the postglacial colonisation of northern Europe to have been effected by lineages with such reproductive modes. Therefore, N European populations should be composed of closely related lineages reflecting a recent range expansion. In contrast, glacial refugia in the south should contain bisexual populations with high haplotype diversity and more population structuring. To test these hypotheses, we analysed the geographic distribution of reproductive modes based on new and published sex ratio data. In addition, we investigated the European phylogeography of T. cancriformis by sequencing over a 1000 bp of mitochondrial DNA (mtDNA) in individuals from a large sample of populations of the three recognised subspecies.ResultsBisexual populations were only found in the Iberian Peninsula, with the rest of European populations showing low male proportions or no males. Androdioecious populations were found in Central and Eastern Europe. Regarding mtDNA diversity, Spanish and Moroccan populations of T. c. mauritanicus were highly divergent, and showed strong population structure. In contrast, Triops c. cancriformis and T. c. simplex formed a single mtDNA lineage with low haplotype diversity. This diversity was structured into two phylogenetic clades (A, B), coexisting in E Germany. Basal haplotypes of both lineages were found in the Iberian Peninsula. Most of the populations in clade A and B are either hermaphroditic or androdioecious, with the only bisexual population in these clades found in the Iberian Peninsula. The genetic divergence between these two clades suggests a split in the Late Pleistocene and their geographic distribution reflects a complex evolutionary history of European Triops populations, with possibly two episodes of range expansions - one of them by clade A - involving androdioecious and hermaphroditic populations.ConclusionAs we predicted, N European populations of T. cancriformis are closely related, with few widely distributed haplotypes and indications of a recent range expansion involving hermaphroditic/androdioecious lineages. A possible second range expansion or long distance colonisation may have created the secondary contact zone between T. c. cancriformis/simplex clades A and B. The large haplotype diversity and strong genetic subdivision in the Iberian Peninsula, which is known to contain only bisexual populations, strongly suggest that this area was a Pleistocene refugium for T. cancriformis, although the occurrence of additional eastern refugia cannot be ruled out. Our data support the status of T. c. mauritanicus as a separate species and the colonisation of N Africa from the Iberian Peninsula. We suggest that hermaphroditism/androdioecy has evolved recently in T. cancriformis and has facilitated the postglacial colonisation of northern Europe.
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Project description:Morphological and developmental similarities, and interactions among developing structures are interpreted as evidences of modularity. Such similarities exist between the dorsal and anal fins of living actinopterygians, on the anteroposterior axis: (1) both fins differentiate in the same direction [dorsal and anal fin patterning module (DAFPM)], and (2) radials and lepidotrichia differentiate in the same direction [endoskeleton and exoskeleton module (EEM)]. To infer the evolution of these common developmental patternings among osteichthyans, we address (1) the complete description and quantification of the DAFPM and EEM in a living actinopterygian (the rainbow trout Oncorhynchus mykiss) and (2) the presence of these modules in fossil osteichthyans (coelacanths, lungfishes, porolepiforms and 'osteolepiforms'). In Oncorhynchus, sequences of skeletal elements are determined based on (1) apparition (radials and lepidotrichia), (2) chondrification (radials), (3) ossification (radials and lepidotrichia), and (4) segmentation plus bifurcation (lepidotrichia). Correlations are then explored between sequences. In fossil osteichthyans, sequences are determined based on (1) ossification (radials and lepidotrichia), (2) segmentation, and (3) bifurcation of lepidotrichia. Segmentation and bifurcation patterns were found crucial for comparisons between extant and extinct osteichthyan taxa. Our data suggest that the EEM is plesiomorphic at least for actinopterygians, and the DAFPM is plesiomorphic for osteichthyans, with homoplastic dissociation. Finally, recurrent patterns suggest the presence of a Lepidotrichia Patterning Module (LPM).
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