Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate

Henriet, Simon; Mungpakdee, Sutada; Aury, Jean‐Marc; Silva, Corinne Da; Brinkmann, Henner; Mikhaleva, Jana; Olsen, Lisbeth Charlotte; Jubin, Claire; Cañestro, Cristian; Bouquet, Jean‐Marie; Danks, Gemma B.; Poulain, Julie; Campsteijn, Coen; Adamski, Marcin; Cross, Ismael; Yadetie, Fekadu; Muffato, Matthieu; Louis, Alexandra; Butcher, Stephen; Tsagkogeorga, Georgia; Konrad, Anke; Singh, Sarabdeep; Jensen, Marit Flo; Cong, Evelyne Huynh; Eikeseth-Otteraa, Helen; Noël, Benjamin; Anthouard, Véronique; Porcel, Betina M.; Kachouri‐Lafond, Rym; Nishino, Atsuo; Ugolini, Matteo; Chourrout, Pascal; Nishida, Hiroki; Aasland, Rein; Huzurbazar, Snehalata; Westhof, Éric; Delsuc, Frédéric; Lehrach, Hans; Reinhardt, Richard; Weissenbach, Jean; Roy, Scott William; Artiguenave, François; Postlethwait, John H.; Manak, J. Robert; Thompson, Eric M.; Jaillon, Olivier; Pasquier, Louis Du; Boudinot, Pierre; Liberles, David A.; Volff, Jean‐Nicolas; Piégay, Hervé; Lenhard, Boris; Crollius, Hugues Roest; Wincker, Patrick; Chourrout, Daniel

doi:10.1126/science.1194167

Cited by 270 publications

(444 citation statements)

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“…9 Since this latter hypothesis was based mainly on data from C. elegans and C. intestinalis we sought to determine if this was also the case in another metazoan; the marine chordate Oikopleura dioica. 5,6 Our work revealed a distinctive role for trans-splicing in the regulation of maternal mRNA. 4 Keywords: Endocycle, growth arrest, maternal RNA, operon, oogenesis, TOP motif, TOR signaling…”

Section: Introductionmentioning

confidence: 99%

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Trans-splicing in metazoans: A link to translational control?

Danks

Thompson

2015

Worm

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T he trans-splicing of a spliced-leader RNA to a subset of mRNAs is a phenomenon that occurs in many species, including Caenorhabditis elegans, and yet the driving force for its evolution in disparate groups of animals remains unclear. Polycistronic mRNA resulting from the transcription of operons is resolved via trans-splicing, but operons comprise only a sub-set of trans-spliced genes. Using the marine chordate, Oikopleura dioica, we recently tested the hypothesis that metazoan operons accelerate recovery from growth arrest. We found no supporting evidence for this in O. dioica. Instead we found a striking relationship between trans-splicing and maternal mRNA in O. dioica, C. elegans and the ascidian, Ciona intestinalis. Furthermore, in O. dioica and C. elegans, we found evidence to suggest a role for mTOR signaling in the translational control of growth-related, trans-spliced maternal mRNAs. We propose that this may be a mechanism for adjusting egg number in response to nutrient levels in these species.

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Section: Introductionmentioning

confidence: 99%

“…3 In the appendicularian Oikopleura dioica, 39% of mRNAs are trans-spliced to a single SL and 28% are found in operons. [4][5][6] Several hypotheses for the functions and evolutionary advantages of both operons and trans-splicing ( Fig. 1) have been proposed.…”

Section: Introductionmentioning

confidence: 99%

Trans-splicing in metazoans: A link to translational control?

Danks

Thompson

2015

Worm

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“…Consistent with the large population sizes of the sequenced species, sequenced tunicate genomes are highly polymorphic. These genomes are surprisingly small (Ciona~160 Mb; Oikopleura~70 Mb, the smallest animal genome so far), owing to several factors: their unduplicated gene complement; substantial gene loss (Holland and Gibson (Satou et al, 2008;Denoeud et al, 2010;Ganot et al, 2004). Frequent or infrequent trans-splicing is also found in most monocistronic genes (Matsumoto et al, 2010).…”

Section: Abstract: Chordates Tunicates Asexual Development Buddinmentioning

confidence: 99%

“…1J). The annotated genome sequences of two ascidians (Ciona savignyi and C. intestinalis) and one appendicularian (O. dioica) have been published (Dehal et al, 2002;Small et al, 2007;Denoeud et al, 2010) (Table 1). Genomic sequences in C. intestinalis have been mapped onto its 14 chromosomes, a prerequisite to studying the global organization of the genome (Shoguchi et al, 2006).…”

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confidence: 99%

Evolutionary crossroads in developmental biology: the tunicates

2011

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The tunicates, or urochordates, constitute a large group of marine animals whose recent common ancestry with vertebrates is reflected in the tadpole-like larvae of most tunicates. Their diversity and key phylogenetic position are enhanced, from a research viewpoint, by anatomically simple and transparent embryos, compact rapidly evolving genomes, and the availability of powerful experimental and computational tools with which to study these organisms. Tunicates are thus a powerful system for exploring chordate evolution and how extreme variation in genome sequence and gene regulatory network architecture is compatible with the preservation of an ancestral chordate body plan. Key words: Chordates, Tunicates, Asexual development, Budding, Embryogenesis, EvolutionIntroduction Cephalochordates (including Amphioxus; see Glossary, Box 1), tunicates (or urochordates, see Glossary, Box 1) and vertebrates constitute the chordate phylum, which is characterized by a tadpolelike body plan at the end of embryogenesis. The rigidity of the tail of these tadpoles is ensured by a unique structure, the notochord, which gave its name to the phylum. Fossil evidence, although sometimes controversial, suggests that ancestral chordates roamed Cambrian oceans more than 550 million years ago (Morris, 1999;Shu et al., 1996).It is now thought that cephalochordates are the most basal chordates. Tunicates and vertebrates are sister taxa (see Glossary, Box 1), which diverged more recently (Delsuc et al., 2006;Bourlat et al., 2006;Putnam et al., 2008). This molecular classification is supported at the anatomical level by the presence in tunicate larvae, but not in those of cephalochordates or of any other invertebrate, of cells similar to vertebrate migratory neural crest cells (Jeffery, 2007).The tunicates constitute a diverse group of animals that are united by the cellulose-containing tunic that covers their body (Nakashima et al., 2004). They are traditionally split into three major classes: the ascidians, thaliaceans and appendicularians, whose phylogenetic relationships are depicted in Fig. 1 (Tsagkogeorga et al., 2009;Govindarajan et al., 2010). Ascidians, also called sea squirts, are the most diverse tunicate group and include several developmental models such as Ciona intestinalis, Halocynthia roretzi and Botryllus schlosseri. These vase-like benthic filter feeders (see Glossary, Box 1) ('ascidian' derives from Development 138, 2143Development 138, -2152Development 138, (2011 Filter feeder. Organisms that feed on particulate food suspended in water. In tunicates, water enters the body via the oral siphon, is filtered on the branchial basket and expelled through an atrial siphon (in appendicularians, water is expelled through gill slits).Hybridization. The production of offspring by interbreeding between two individuals of different species. Kernel. A small region of a gene regulatory network that is evolutionarily highly conserved, the retention of which might underlie the conservation of body plans and the development of major ...

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“…(Baumgarten et al 2015) were downloaded from http://reefgenomics.org. Assembly and annotation for Oikopleura dioica (Denoeud et al 2010) were downloaded from Genoscope (http://www.genoscope. cns.fr/externe/GenomeBrowser/Oikopleura/).…”

Section: Genomic Data Sourcesmentioning

confidence: 99%

Similar ratios of introns to intergenic sequence across animal genomes

Francis

Wörheide

2016

Preprint

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One central goal of genome biology is to understand how the usage of the genome differs between organisms. Our knowledge of genome composition, needed for downstream inferences, is critically dependent on gene annotations, yet problems associated with gene annotation and assembly errors are usually ignored in comparative genomics. Here, we analyze the genomes of 68 species across 12 animal phyla and some single-cell eukaryotes for general trends in genome composition and transcription, taking into account problems of gene annotation. We show that, regardless of genome size, the ratio of introns to intergenic sequence is comparable across essentially all animals, with nearly all deviations dominated by increased intergenic sequence. Genomes of model organisms have ratios much closer to 1:1, suggesting that the majority of published genomes of nonmodel organisms are underannotated and consequently omit substantial numbers of genes, with likely negative impact on evolutionary interpretations. Finally, our results also indicate that most animals transcribe half or more of their genomes arguing against differences in genome usage between animal groups, and also suggesting that the transcribed portion is more dependent on genome size than previously thought.

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Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate

Cited by 270 publications

References 25 publications

Trans-splicing in metazoans: A link to translational control?

Trans-splicing in metazoans: A link to translational control?

Evolutionary crossroads in developmental biology: the tunicates

Similar ratios of introns to intergenic sequence across animal genomes

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