Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

Schierwater, Bernd; Holland, Peter; Miller, David J.; Stadler, Peter F.; Wiegmann, Brian M.; Wörheide, Gert; Wray, Gregory A.; DeSalle, Rob

doi:10.3389/fevo.2016.00005

Cited by 21 publications

(21 citation statements)

References 128 publications

(146 reference statements)

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“…microRNA candidates are not found in ctenophore Mnemiopsis leidyi, nor are Drosha or Pasha orthologs (Maxwell et al 2012). These support various scenarios of acquisition and loss, or basal absence depending on relative phylogenetic position of Ctenophora and Placozoa (Schierwater et al 2016), yet all are consistent with the assumption that Drosha and Pasha orthologs represent presence of a canonical metazoan biogenesis pathway.…”

Section: Drosha and Pasha Orthology Are Not Adequate To Assert Sharedsupporting

confidence: 61%

The Meaning of the Microprocessor: Accounting for Evolution of Structural-Functional Novelty in the Canonical microRNA Biogenesis Pathway

Robinson¹

2019

Preprint

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It is standard to identify and compare genomic or mRNA sequence of the Drosha and Pasha genes subsidiary to detection and identification of novel microRNAs in newly sequenced taxa or review of previous deep sequencing data. Drosha and Pasha are the key, conserved gene members of the ‘microprocessor’ protein complex which facilitates nuclear nuclear-localized, pri- to pre-miRNA processing miRNAs of the canonical eumetazoan complement. Because of the necessity of the microprocessor for production of canonical eumetazoan miRNA, the detection of both (1) bona fide microRNAs and (2) presence of Drosha/Pasha orthologs (or homologs) is often presented as sufficient to represent a functional canonical eumetazoan microRNA biogenesis pathway. However, the functional role of the Drosha and Pasha homologs is not commonly experimentally investigated in non-model taxa, and therefore the assumption is not necessarily valid. Differentiation of ‘bona fide miRNAs’, opposed to ‘non-bona fide’ small RNAs of similar size, are also necessary for miRNA sequencing projects. Recent rubrics are based on structural and sequence elements of the miRNAs themselves, however these inclusion criteria include paraphyletic groupings of miRNAs, for example eumetazoan miRNAs and streptophyte (green plant) miRNAs which are not produced by the Drosha/Pasha microprocessor mechanism. Therefore, a dichotomy exists between the structural definitions for miRNAs and understanding of the evolutionarily conserved function of the microprocessor and its components. In this article, I review literature in the context of this topic and discuss philosophical ramifications for understanding the importance of the microprocessor in understanding the evolutionary and molecular origins of miRNA.

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Section: Drosha and Pasha Orthology Are Not Adequate To Assert Sharedsupporting

confidence: 61%

The Meaning of the Microprocessor: Accounting for Evolution of Structural-Functional Novelty in the Canonical microRNA Biogenesis Pathway

Robinson¹

2019

Preprint

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“…The remaining two lineages – the major actors in the controversy – are sponges and ctenophores, a marine phylum of gelatinous metazoans that bear distinctive “combs” of cilia, earning them the moniker “comb jellies.” The debate centers on which of these two, sponges or ctenophores, is the sister lineage (see Glossary) to the rest of the metazoans (Figure 1). The uncertainty stemming from this controversy has major implications for understanding the origin of metazoan multicellularity and development, deciphering the biology of early metazoans [4, 5], and unraveling the evolution of many marquee metazoan traits, including muscles and the nervous system [6–8]. …”

Section: Introductionmentioning

confidence: 99%

Embracing Uncertainty in Reconstructing Early Animal Evolution

2017

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The origin of metazoans, one of the major transitions in evolution, remains mysterious. While many key aspects of metazoan origins can be reconstructed by comparing living organisms within a robust phylogenetic framework, uncertainty regarding the evolutionary relationships among sponges, ctenophores and the remainder of metazoan diversity has proven to be a major barrier. Comparative morphology and some phylogenomic analyses support the view that sponges represent the sister lineage to the rest of the metazoans, while other competing phylogenomic analyses strongly support ctenophores, a phylum of carnivorous, gelatinous marine organisms, as the sister lineage. Here, we explore why different phylogenomic studies yield different answers and discuss the implications of the two alternative hypotheses for understanding the origin of metazoan multicellularity. Reconstruction of ancient evolutionary radiations, like the one that gave rise to metazoans, is devilishly difficult and will likely require broader sampling of sponge and ctenophore genomes, improved analytical strategies, and critical analyses of the phylogenetic distribution and molecular mechanisms underlying apparently conserved traits. Rather than staking out positions in favor of the ctenophore-sister or the sponge-sister hypothesis, we submit that research programs aimed at understanding the biology of the first metazoans should embrace the uncertainty surrounding early metazoan evolution in their experimental designs.

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“…Recent discussions about the phylogenetic position of placozoans have been based on the T. adhaerens genome . A better sampling of the placozoan genomic diversity is, however, needed [29] to address the current dispute over the phylogenetic relationships between early-branching metazoan phyla [30][31][32] and the placement of the Placozoa in the metazoan tree of life. In this context, it is important to first assess if adding another placozoan species would break up the long placozoan branch, because the inclusion of a single representative of a clade with a very long terminal branch, or fast-evolving taxa that can have random amino acid sequence similarities, may result in erroneous groupings in a phylogeny (so-called "long-branch attraction artefacts") [32,33] .…”

Section: Placozoa In the Animal Tree Of Lifementioning

confidence: 99%

A taxogenomics approach uncovers a new genus in the phylum Placozoa

Eitel¹,

Francis

Osigus³

et al. 2017

Preprint

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The Placozoa [1] is a monotypic phylum of non-bilaterian marine animals. Its only species, Trichoplax adhaerens , was described in 1883 [2] . Despite the worldwide distribution of placozoans [3][4][5][6] , morphological differences are lacking among isolates from different geographic areas and, consequently, no other species in this phylum has been described and accepted for more than 130 years. However, recent single-gene studies on the genetic diversity of this "species" have revealed deeply divergent lineages of, as yet, undefined taxonomic ranks [3,5,6] . Since single genes are not considered sufficient to define species[7] , a whole nuclear genome comparison appears the most appropriate approach to determine relationships between placozoan lineages. Such a "taxogenomics" approach can help discover and diagnose potential additional species and, therefore, develop a much-needed, more robust, taxonomic framework for this phylum. To achieve this we sequenced the genome of a placozoan lineage isolated from Hong Kong (lineage H13), which is distantly related to T. adhaerens [6] . The 87 megabase genome assembly contains 12,010 genes .Comparison to the T. adhaerens genome [8] identified an average protein distance of 24.4% in more than 2,700 screened one-to-one orthologs, similar to levels observed between the chordate classes mammals and birds. Genome rearrangements are commonplace and >25% of genes are not collinear (i.e. they are not in the same order in the two genomes). Finally, a multi-gene distance comparison with other non-bilaterian phyla indicate genus level differences to T. adhaerens . These data highlight the large genomic diversity within the Placozoa and justifies the designation of lineage H13 as a new species, Xxxxxxxxx yyyyyyyyyyyyy gen. et spec. nov., now the second described placozoan species and the first in 1 1 NOTE RELATING TO TAXONOMIC RULES: According to the International Code of Zoological Nomenclature preprint publication of taxonomic names is discouraged. Consequently, the " Xxxxxxxxx yyyyyyyyyyyyy / X. yyyyyyyyyyyyy " given here is a dummy only. The valid name will be available upon formal journal publication. high-quality and contamination filtered contigs with an gap-free N50 of 407 kb (Table S1; Figures S1-S3), seven megabases smaller than the T. adhaerens contig assembly. The overall calculated genome heterozygosity was 1.6% (based on SNP counts, see Table S2).We annotated the genome with a combination of 15.3 Gb of RNAseq and ab initio methods to yield 12,010 genes (Table S1 and Supplemental Information). A high percentage of raw reads mapped back to the genome (Table S3) and between 89-93% of the 978 genes in the Metazoa BUSCO v2.0 dataset were identified in the different annotation sets (Table S4). 2. CC-BY-NC-ND 4.0 International license not peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/202119 doi: bioRxiv preprint first posted online Oct. 12, 2017; Together this suggest...

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Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

Cited by 21 publications

References 128 publications

The Meaning of the Microprocessor: Accounting for Evolution of Structural-Functional Novelty in the Canonical microRNA Biogenesis Pathway

The Meaning of the Microprocessor: Accounting for Evolution of Structural-Functional Novelty in the Canonical microRNA Biogenesis Pathway

Embracing Uncertainty in Reconstructing Early Animal Evolution

A taxogenomics approach uncovers a new genus in the phylum Placozoa

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