Gene family innovation, conservation and loss on the animal stem lineage

Richter, Daniel J.; Fozouni, Parinaz; Eisen, Michael B.; King, Nicole

doi:10.7554/elife.34226

Cited by 187 publications

(332 citation statements)

References 181 publications

(268 reference statements)

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“…6) to a transition from a holopelagic to a biphasic pelago-benthic life cycle in the stem-benthozoan lineage. This particular result furthers a growing picture of metabolic and chaperone gene loss and gene innovation in early animal evolution (ERIVES AND FASSLER 2015;RICHTER et al 2018).…”

Section: Discussionsupporting

confidence: 52%

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

Erives

Fritzsch

2019

Preprint

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Key words (5 max): animal evolution, gene duplication, Max-like protein (MLX), Max-like interacting protein (MLXIP), transmembrane channel-like proteins (TMCs) Early metazoan gene duplications 2The evolutionary diversification of animals is one of Earth's greatest triumphs, yet its origins are still shrouded in mystery. Animals, the monophyletic clade known as Metazoa, evolved wildly divergent multicellular life strategies featuring ciliated sensory epithelia. In many lineages epithelial sensoria became coupled to increasingly complex nervous systems. Currently, different phylogenetic analyses of single-copy genes support mutually-exclusive possibilities that either Porifera or Ctenophora is sister to all other animals. Resolving this dilemma would advance the ecological and evolutionary understanding of the first animals and the evolution of nervous systems. Here we describe a comparative phylogenetic approach based on gene duplications. We computationally identify and analyze gene families with early metazoan duplications using an approach that mitigates apparent gene loss resulting from the miscalling of paralogs. In the transmembrane channel-like (TMC) family of mechano-transducing channels, we find ancient duplications that define separate clades for Eumetazoa (Placozoa + Cnidaria + Bilateria) versus Ctenophora, and one duplication that is shared only by Eumetazoa and Porifera. In the MLX/MLXIP family of bHLH-ZIP regulators of metabolism, we find that all major lineages from Eumetazoa and Porifera (sponges) share a duplication, absent in Ctenophora. These results suggest a new avenue for deducing deep phylogeny by choosing rather than avoiding ancient gene paralogies.

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Section: Discussionsupporting

confidence: 52%

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

Erives

Fritzsch

2019

Preprint

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“…Some of the genes of this pathway originated in Choanozoans but the core pathway is clearly already established in sponges, tens of million years before the Cambrian explosion. In animals the Wnt pathway has a conserved role in: anterior-posterior axis formation in embryos, in organogenesis, and in tissue homeostasis (1)(2)(3). Dysregulation of the Wnt pathway plays a role in various human diseases including skeletal, cardiac vascular diseases (4), and cancer (5).…”

Section: Introductionmentioning

confidence: 99%

Single molecule dynamics of Dishevelled at the plasma membrane and Wnt pathway activation

Chen

Kang

et al. 2019

Preprint

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Dvl (Dishevelled) is one of several essential non-enzymatic components of the Wnt signaling pathway. In most current models, Dvl forms complexes with Wnt ligand receptors, Fzd and LRP5/6 at the plasma membrane, which then recruits other components of the destruction complex leading to inactivation of β -catenin degradation. Although this model is widespread, direct evidence for this process is lacking. In this study, we tagged mEGFP to C-terminus of dishevlled2 gene using CRISPR/Cas9 induced homologous recombination and observed its dynamics directly at the single molecule level with Total Internal Reflection Fluorescence (TIRF) microscopy. We focused on two questions: 1) What is the native size and the dynamic features of membrane-associated Dvl complexes during Wnt pathway activation? 2) What controls the behavior of these complexes? We found that membrane bound Dvl2 is predominantly monomer in the absent of Wnt (mean size 1.10). Wnt3a stimulation leads to an increase in the total concentration of membrane-bound Dvl2 from 0.08/μm 2 to 0.34/μm 2 . Wnt3a also leads to increased oligomerization which raises the weighted averaged mean size of Dvl2 complexes to 1.4; with 65% of Dvl still as monomers. The driving force for Dvl2 oligomerization is the increased concentration of Dvl2 at the membrane caused by increased affinity of Dvl2 for Fzd, the Dvl2 and Fzd binding is independent of LRP5/6. The oligomerized Dvl2 complexes have greatly increased dwell time, 2~3 minutes compared to less than 1 second for monomeric Dvl2.These properties make Dvl a unique scaffold dynamically changing its state of assembly and stability at the membrane in response to Wnt ligands. Significance Statement:Canonical Wnt signaling is one of the most widely distributed pathways in metazoan development. Despite intense genetic and biochemical study for over 35 years, the major features of signaling across the plasma membrane are still poorly understood. Dishevelled serves as an essential bridge between the membrane receptors and downstream signaling components.Attempts to reconstruct the pathway and analyze its biochemical features in vitro have been hampered by Dishevelled's tendency to aggregate in vitro and to form large aggregates of dubious significance in vivo. To obtain a molecular understanding of the role of Dvl in Wnt signaling, while circumventing these aggregation problems we have expressed a fluorescent tagged Dishevelled in cells at their physiological concentration and quantified the size distribution of Dishevelled before and after Wnt treatment. We found that limited oligomerization in response to the Wnt ligand is very dynamic and provides a key step of signal transduction.

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“…Moreover, S. rosetta is just one tip on the 285 choanoflagellate branch. A recent survey of 21 choanoflagellate transcriptomes revealed that choanoflagellates are at least as genetically diverse as animals (Richter et al, 2018), with other species retaining genetic pathways or exhibiting behaviors that are not found in S. rosetta (e.g., Marron et al, 2013;Leadbeater, 2015;Brunet et al, 2019). Together with future findings from S. rosetta, we anticipate that the establishment of genome editing in other choanoflagellates will 290 provide an increasingly complete portrait of the last common ancestor of choanoflagellates and animals.…”

Section: Discussionmentioning

confidence: 78%

Genome editing enables reverse genetics of multicellular development in the choanoflagellateSalpingoeca rosetta

Booth

King

2020

Preprint

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In a previous study, we established a forward genetic screen to identify genes required for multicellular development in the choanoflagellate, Salpingoeca rosetta (Levin et al., 2014). Yet, the paucity of reverse genetic tools for choanoflagellates has hampered direct tests of gene 25 function and impeded the establishment of choanoflagellates as a model for reconstructing the origin of their closest living relatives, the animals. Here we establish CRISPR/Cas9-mediated genome editing in S. rosetta by engineering a selectable marker to enrich for edited cells. We then use genome editing to disrupt the coding sequence of a S. rosetta C-type lectin gene, rosetteless, and thereby demonstrate its necessity for multicellular rosette development. This 30 work advances S. rosetta as a model system in which to investigate how genes identified from genetic screens and genomic surveys function in choanoflagellates and evolved as critical regulators of animal biology.

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Gene family innovation, conservation and loss on the animal stem lineage

Cited by 187 publications

References 181 publications

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

A screen for gene paralogies delineating evolutionary branching order of early Metazoa

Single molecule dynamics of Dishevelled at the plasma membrane and Wnt pathway activation

Genome editing enables reverse genetics of multicellular development in the choanoflagellateSalpingoeca rosetta

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