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Freeman, Robert

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Freeman

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Robert

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Freeman, Robert
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    The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii
    (BioMed Central, 2014) Fritzenwanker, Jens H; Gerhart, John; Freeman, Robert; Lowe, Christopher J
    Background: The Fox gene family is a large family of transcription factors that arose early in organismal evolution dating back to at least the common ancestor of metazoans and fungi. They are key components of many gene regulatory networks essential for embryonic development. Although much is known about the role of Fox genes during vertebrate development, comprehensive comparative studies outside vertebrates are sparse. We have characterized the Fox transcription factor gene family from the genome of the enteropneust hemichordate Saccoglossus kowalevskii, including phylogenetic analysis, genomic organization, and expression analysis during early development. Hemichordates are a sister group to echinoderms, closely related to chordates and are a key group for tracing the evolution of gene regulatory mechanisms likely to have been important in the diversification of the deuterostome phyla. Results: Of the 22 Fox gene families that were likely present in the last common ancestor of all deuterostomes, S. kowalevskii has a single ortholog of each group except FoxH, which we were unable to detect, and FoxQ2, which has three paralogs. A phylogenetic analysis of the FoxQ2 family identified an ancestral duplication in the FoxQ2 lineage at the base of the bilaterians. The expression analyses of all 23 Fox genes of S. kowalevskii provide insights into the evolution of components of the regulatory networks for the development of pharyngeal gill slits (foxC, foxL1, and foxI), mesoderm patterning (foxD, foxF, foxG), hindgut development (foxD, foxI), cilia formation (foxJ1), and patterning of the embryonic apical territory (foxQ2). Conclusions: Comparisons of our results with data from echinoderms, chordates, and other bilaterians help to develop hypotheses about the developmental roles of Fox genes that likely characterized ancestral deuterostomes and bilaterians, and more recent clade-specific innovations.
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    Hemichordate genomes and deuterostome origins
    (2015) Simakov, Oleg; Kawashima, Takeshi; Marlétaz, Ferdinand; Jenkins, Jerry; Koyanagi, Ryo; Mitros, Therese; Hisata, Kanako; Bredeson, Jessen; Shoguchi, Eiichi; Gyoja, Fuki; Yue, Jia-Xing; Chen, Yi-Chih; Freeman, Robert; Sasaki, Akane; Hikosaka-Katayama, Tomoe; Sato, Atsuko; Fujie, Manabu; Baughman, Kenneth W.; Levine, Judith; Gonzalez, Paul; Cameron, Christopher; Fritzenwanker, Jens H.; Pani, Ariel M.; Goto, Hiroki; Kanda, Miyuki; Arakaki, Nana; Yamasaki, Shinichi; Qu, Jiaxin; Cree, Andrew; Ding, Yan; Dinh, Huyen H.; Dugan, Shannon; Holder, Michael; Jhangiani, Shalini N.; Kovar, Christie L.; Lee, Sandra L.; Lewis, Lora R.; Morton, Donna; Nazareth, Lynne V.; Okwuonu, Geoffrey; Santibanez, Jireh; Chen, Rui; Richards, Stephen; Muzny, Donna M.; Gillis, Andrew; Peshkin, Leon; Wu, Michael; Humphreys, Tom; Su, Yi-Hsien; Putnam, Nicholas H.; Schmutz, Jeremy; Fujiyama, Asao; Yu, Jr-Kai; Tagawa, Kunifumi; Worley, Kim C.; Gibbs, Richard A.; Kirschner, Marc; Lowe, Christopher J.; Satoh, Noriyuki; Rokhsar, Daniel S.; Gerhart, John
    Acorn worms, also known as enteropneust (literally, ‘gut-breathing’) hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal ‘gill’ slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor.
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    Cephalopod genomics: A plan of strategies and organization
    (Michigan State University, 2012) Albertin, Caroline B.; Bonnaud, Laure; Brown, C. Titus; Crookes-Goodson, Wendy J.; da Fonseca, Rute R.; Di Cristo, Carlo; Dilkes, Brian P.; Edsinger-Gonzales, Eric; Freeman, Robert; Hanlon, Roger T.; Koenig, Kristen M.; Lindgren, Annie R.; Martindale, Mark Q.; Minx, Patrick; Moroz, Leonid L.; Nödl, Marie-Therese; Nyholm, Spencer V.; Ogura, Atsushi; Pungor, Judit R.; Rosenthal, Joshua J. C.; Schwarz, Erich M.; Shigeno, Shuichi; Strugnell, Jan M.; Wollesen, Tim; Zhang, Guojie; Ragsdale, Clifton W.
    The Cephalopod Sequencing Consortium (CephSeq Consortium) was established at a NESCent Catalysis Group Meeting, “Paths to Cephalopod Genomics- Strategies, Choices, Organization,” held in Durham, North Carolina, USA on May 24-27, 2012. Twenty-eight participants representing nine countries (Austria, Australia, China, Denmark, France, Italy, Japan, Spain and the USA) met to address the pressing need for genome sequencing of cephalopod mollusks. This group, drawn from cephalopod biologists, neuroscientists, developmental and evolutionary biologists, materials scientists, bioinformaticians and researchers active in sequencing, assembling and annotating genomes, agreed on a set of cephalopod species of particular importance for initial sequencing and developed strategies and an organization (CephSeq Consortium) to promote this sequencing. The conclusions and recommendations of this meeting are described in this white paper.
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    MAGIC-SPP: A Database-Driven DNA Sequence Processing Package with Associated Management Tools
    (BioMed Central, 2006) Liang, Chun; Sun, Feng; Wang, Haiming; Qu, Junfeng; Freeman, Robert; Pratt, Lee H; Cordonnier-Pratt, Marie-Michèle
    Background: Processing raw DNA sequence data is an especially challenging task for relatively small laboratories and core facilities that produce as many as 5000 or more DNA sequences per week from multiple projects in widely differing species. To meet this challenge, we have developed the flexible, scalable, and automated sequence processing package described here. Results: MAGIC-SPP is a DNA sequence processing package consisting of an Oracle 9i relational database, a Perl pipeline, and user interfaces implemented either as JavaServer Pages (JSP) or as a Java graphical user interface (GUI). The database not only serves as a data repository, but also controls processing of trace files. MAGIC-SPP includes an administrative interface, a laboratory information management system, and interfaces for exploring sequences, monitoring quality control, and troubleshooting problems related to sequencing activities. In the sequence trimming algorithm it employs new features designed to improve performance with respect to concerns such as concatenated linkers, identification of the expected start position of a vector insert, and extending the useful length of trimmed sequences by bridging short regions of low quality when the following high quality segment is sufficiently long to justify doing so. Conclusion: MAGIC-SPP has been designed to minimize human error, while simultaneously being robust, versatile, flexible and automated. It offers a unique combination of features that permit administration by a biologist with little or no informatics background. It is well suited to both individual research programs and core facilities.
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    Dorsoventral Patterning in Hemichordates: Insights into Early Chordate Evolution
    (Public Library of Science, 2006) Lowe, Christopher J; Terasaki, Mark; Runft, Linda; Kwan, Kristen; Haigo, Saori; Aronowicz, Jochanan; Gruber, Chris; Gerhart, John; Wu, Michael; Freeman, Robert; Lander, Eric; Smith, Mark; Kirschner, Marc
    We have compared the dorsoventral development of hemichordates and chordates to deduce the organization of their common ancestor, and hence to identify the evolutionary modifications of the chordate body axis after the lineages split. In the hemichordate embryo, genes encoding bone morphogenetic proteins (Bmp) 2/4 and 5/8, as well as several genes for modulators of Bmp activity, are expressed in a thin stripe of ectoderm on one midline, historically called “dorsal.” On the opposite midline, the genes encoding Chordin and Anti-dorsalizing morphogenetic protein (Admp) are expressed. Thus, we find a Bmp-Chordin developmental axis preceding and underlying the anatomical dorsoventral axis of hemichordates, adding to the evidence from Drosophila and chordates that this axis may be at least as ancient as the first bilateral animals. Numerous genes encoding transcription factors and signaling ligands are expressed in the three germ layers of hemichordate embryos in distinct dorsoventral domains, such as pox neuro, pituitary homeobox, distalless, and tbx2/3 on the Bmp side and netrin, mnx, mox, and single-minded on the Chordin-Admp side. When we expose the embryo to excess Bmp protein, or when we deplete endogenous Bmp by small interfering RNA injections, these expression domains expand or contract, reflecting their activation or repression by Bmp, and the embryos develop as dorsalized or ventralized limit forms. Dorsoventral patterning is independent of anterior/posterior patterning, as in Drosophila but not chordates. Unlike both chordates and Drosophila, neural gene expression in hemichordates is not repressed by high Bmp levels, consistent with their development of a diffuse rather than centralized nervous system. We suggest that the common ancestor of hemichordates and chordates did not use its Bmp-Chordin axis to segregate epidermal and neural ectoderm but to pattern many other dorsoventral aspects of the germ layers, including neural cell fates within a diffuse nervous system. Accordingly, centralization was added in the chordate line by neural-epidermal segregation, mediated by the pre-existing Bmp-Chordin axis. Finally, since hemichordates develop the mouth on the non-Bmp side, like arthropods but opposite to chordates, the mouth and Bmp-Chordin axis may have rearranged in the chordate line, one relative to the other.