Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa

Medina, Mónica; Collins, Allen G.; Taylor, John W.; Valentine, James W.; Lipps, Jere H.; Amaral‐Zettler, Linda; Sogin, Mitchell L.

doi:10.1017/s1473550403001551

Cited by 102 publications

(69 citation statements)

References 41 publications

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“…Thus, Proterospongia choanojuncta is simply the colonial phase of Choanoeca perplexa, both species of which have identical sequences for all genes examined (Fig. S1 A) (18), and Proterospongia sp. ATCC 50818 is the colonial stage of an unnamed species of Salpingoeca (B.S.C.L., unpublished data).…”

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confidence: 95%

Molecular phylogeny of choanoflagellates, the sister group to Metazoa

Carr

Leadbeater

Hassan

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

193

173

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Choanoflagellates are single-celled aquatic flagellates with a unique morphology consisting of a cell with a single flagellum surrounded by a ''collar'' of microvilli. They have long interested evolutionary biologists because of their striking resemblance to the collared cells (choanocytes) of sponges. Molecular phylogeny has confirmed a close relationship between choanoflagellates and Metazoa, and the first choanoflagellate genome sequence has recently been published. However, molecular phylogenetic studies within choanoflagellates are still extremely limited. Thus, little is known about choanoflagellate evolution or the exact nature of the relationship between choanoflagellates and Metazoa. We have sequenced four genes from a broad sampling of the morphological diversity of choanoflagellates including most species currently available in culture. Phylogenetic analyses of these sequences, alone and in combination, reject much of the traditional taxonomy of the group. The molecular data also strongly support choanoflagellate monophyly rejecting proposals that Metazoa were derived from a true choanoflagellate ancestor. Mapping of a complementary matrix of morphological and ecological traits onto the phylogeny allows a reinterpretation of choanoflagellate character evolution and predicts the nature of their last common ancestor.evolution ͉ morphology ͉ holozoa ͉ animals ͉ protists

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confidence: 95%

Molecular phylogeny of choanoflagellates, the sister group to Metazoa

Carr

Leadbeater

Hassan

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

193

173

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“…Over the past decade or so, evidence supporting this relationship has accumulated from phylogenetic analyses of nuclear and mitochondrial genes [3][4][5][6] , comparative genomics between the mitochondrial genomes of choanoflagellates, sponges and other metazoans 7,8 , and the finding that choanoflagellates express homologues of metazoan signalling and adhesion genes 9-12 . Furthermore, species-rich phylogenetic analyses demonstrate that choanoflagellates are not derived from metazoans, but instead represent a distinct lineage that evolved before the origin and diversification of metazoans (Fig.…”

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confidence: 99%

The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans

King

Westbrook²,

Young³

et al. 2008

Nature

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Choanoflagellates are the closest known relatives of metazoans. To discover potential molecular mechanisms underlying the evolution of metazoan multicellularity, we sequenced and analysed the genome of the unicellular choanoflagellate Monosiga brevicollis. The genome contains approximately 9,200 intron-rich genes, including a number that encode cell adhesion and signalling protein domains that are otherwise restricted to metazoans. Here we show that the physical linkages among protein domains often differ between M. brevicollis and metazoans, suggesting that abundant domain shuffling followed the separation of the choanoflagellate and metazoan lineages. The completion of the M. brevicollis genome allows us to reconstruct with increasing resolution the genomic changes that accompanied the origin of metazoans.Choanoflagellates have long fascinated evolutionary biologists for their marked similarity to the 'feeding cells' (choanocytes) of sponges and the possibility that they might represent the closest living relatives of metazoans 1,2 . Over the past decade or so, evidence supporting this relationship has accumulated from phylogenetic analyses of nuclear and mitochondrial genes [3][4][5][6] , comparative genomics between the mitochondrial genomes of choanoflagellates, sponges and other metazoans 7,8 , and the finding that choanoflagellates express homologues of metazoan signalling and adhesion genes 9-12 . Furthermore, species-rich phylogenetic analyses demonstrate that choanoflagellates are not derived from metazoans, but instead represent a distinct lineage that evolved before the origin and diversification of metazoans (Fig. 1a, Supplementary Fig. 1 and Supplementary Note 3.1) 8,13 . By virtue of their position on the tree of life, studies of choanoflagellates provide an unparallelled window into the nature of the unicellular and colonial progenitors of metazoans 14 .Choanoflagellates are abundant and globally distributed microbial eukaryotes found in marine and freshwater environments 15,16 . Like sponge choanocytes, each cell bears an apical flagellum surrounded by a distinctive collar of actin-filled microvilli, with which choanoflagellates trap bacteria and detritus (Fig. 1b). Using this highly effective means of prey capture, choanoflagellates link bacteria to higher trophic levels and thus have critical roles in oceanic carbon cycling and in the microbial food web 17,18 .More than 125 choanoflagellate species have been identified, and all species have a unicellular life-history stage. Some can also form simple colonies of equipotent cells, although these differ substantially from the obligate associations of differentiated cells in metazoans 19 . Studies of basal metazoans indicate that the ancestral metazoan was multicellular and had differentiated cell types, an epithelium, a body plan and regulated development including gastrulation. In contrast, the last common ancestor of choanoflagellates and metazoans was unicellular or possibly capable of forming simple colonies, underscoring the abundant biologi...

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“…Finally, another node in the tree of life that has gained recent interest is that of the choanoflagellates, a unicellular sister group to metazoans (10). Ribosomal phylogenies suggest that choanoflagellates are the most likely unicellular lineage to have shared common ancestry with the multicellular animals (11), but there are a few other unicellular protists that also fall out in this part of the tree in other gene phylogenies (12). A choanoflagellate genome project is now in progress, and multiple EST initiatives for unicellular opisthokont protists are also in place.…”

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confidence: 99%

“…Consensus phylogenies of fungi place the Chitridiomycota as the most basal lineage, followed by the Zygomycota, with Ascomycota and Basidiomycota as sister crown clades (13,14). Ribosomal phylogenies suggest that the Nuclearid amoeba are the likely unicellular sister group to Fungi (11,15).…”

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confidence: 99%

Genomes, phylogeny, and evolutionary systems biology

Medina

2005

Proc. Natl. Acad. Sci. U.S.A.

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With the completion of the human genome and the growing number of diverse genomes being sequenced, a new age of evolutionary research is currently taking shape. The myriad of technological breakthroughs in biology that are leading to the unification of broad scientific fields such as molecular biology, biochemistry, physics, mathematics, and computer science are now known as systems biology. Here, I present an overview, with an emphasis on eukaryotes, of how the postgenomics era is adopting comparative approaches that go beyond comparisons among model organisms to shape the nascent field of evolutionary systems biology.postgenomics ͉ eukaryotic genomics ͉ network evolution Systems biology is in the eye of the beholder.Leroy Hood O nly in the last decade have we had access to nearly complete genomes of a diversity of organisms allowing for large-scale comparative analysis. The access to this immense amount of data is providing profound insight into the tree of life at all levels of divergence ( Fig. 1 A). It is thus not surprising that understanding phylogenetic relationships is a prevalent research goal among not only evolutionary biologists but also all scientists interested in the organization and function of the genome. New genome sequences and analysis methods are helping improve our understanding of phylogeny, and at the same time improved phylogenies and phylogenetic theory are generating a better understanding of genome evolution. Currently however, the level of genome sequencing for different branches of the tree of life is far from equivalent. Prokaryotic genome projects are abundant, mainly due to their small genome sizes, with Ͼ200 genomes already published and at least 500 currently in progress (www. genomesonline.org). In contrast, Ͻ300 eukaryotic genomes are either finished or in progress (www.genomesonline.org). Nevertheless, these data are starting to have a major impact on our understanding of eukaryotic evolution.These new genomic data have informed our understanding of phylogenetic relationships, and the emerging consensus topologies are adding new insight to the small subunit ribosomal RNA phylogenies. For example, the topology of the ribosomal eukaryotic tree has been recently redrawn with the use of genomic signatures that place the root of all eukaryotic life between two newly uncovered major clades, Unikonts and Bikonts (Fig. 1 A). Unikonts, which contain the heterotrophic groups Opisthokonta and the Amebozoa, share a derived three-gene fusion of enzymeencoding genes in the pyrimidine synthesis pathway (1), whereas Bikonts, which contain the remaining eukaryotic clades, share another derived gene fusion between dihydrofolate reductase and thymidine synthase (2). All photosynthetic groups of primary and secondary plastid symbiotic origins are now thought to be within the Bikonts. Although the animal, fungal, and plant lineages are the most widely represented in terms of genome initiatives (Fig. 1 B-D), it is significant that multiple protistan genome projects have also been initiated by th...

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Phylogeny of Opisthokonta and the evolution of multicellularity and complexity in Fungi and Metazoa

Cited by 102 publications

References 41 publications

Molecular phylogeny of choanoflagellates, the sister group to Metazoa

Molecular phylogeny of choanoflagellates, the sister group to Metazoa

The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans

Genomes, phylogeny, and evolutionary systems biology

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