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Escriva, H, Bertrand S, Germain P, Robinson-Rechavi M, Umbhauer M, Cartry J, Duffraisse M, Holland L, Gronemeyer H, Laudet V.  2006.  Neofunctionalization in vertebrates: The example of retinoic acid receptors. Plos Genetics. 2:955-965.   10.1371/journal.pgen.0020102   AbstractWebsite

Understanding the role of gene duplications in establishing vertebrate innovations is one of the main challenges of Evo-Devo (evolution of development) studies. Data on evolutionary changes in gene expression (i.e., evolution of transcription factor-cis-regulatory elements relationships) tell only part of the story; protein function, best studied by biochemical and functional assays, can also change. In this study, we have investigated how gene duplication has affected both the expression and the ligand-binding specificity of retinoic acid receptors (RARs), which play a major role in chordate embryonic development. Mammals have three paralogous RAR genes-RAR alpha, beta, and gamma-which resulted from genome duplications at the origin of vertebrates. By using pharmacological ligands selective for specific paralogues, we have studied the ligand-binding capacities of RARs from diverse chordates species. We have found that RAR beta-like binding selectivity is a synapomorphy of all chordate RARs, including a reconstructed synthetic RAR representing the receptor present in the ancestor of chordates. Moreover, comparison of expression patterns of the cephalochordate amphioxus and the vertebrates suggests that, of all the RARs, RAR beta expression has remained most similar to that of the ancestral RAR. On the basis of these results together, we suggest that while RAR beta kept the ancestral RAR role, RAR alpha and RAR gamma diverged both in ligand-binding capacity and in expression patterns. We thus suggest that neofunctionalization occurred at both the expression and the functional levels to shape RAR roles during development in vertebrates.

H
Holland, LZ.  2005.  Non-neural ectoderm is really neural: Evolution of developmental patterning mechanisms in the non-neural ectoderm of chordates and the problem of sensory cell homologies. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 304B:304-323.   10.1002/jez.21038   AbstractWebsite

In chordates, the ectoderm is divided into the neuroectoderm and the so-called non-neural ectoderm. In spite of its name, however, the non-neural ectoderm contains. numerous sensory cells. Therefore, the term "non-neural" ectoderm should be replaced by "general ectoderm." At least in amphioxus and tunicates and possibly in vertebrates as well, both the neuroectoderm and the general ectoderm are patterned anterior/posteriorly by mechanisms involving retinoic acid and Hox genes. In amphioxus and tunicates the ectodermal sensory cells, which have a wide range of ciliary and microvillar configurations, are mostly primary neurons sending axons to the CNS, although a minority lack axons. In contrast, vertebrate mechanosensory cells, called hair cells, are all secondary neurons that lack axons and have a characteristic eccentric cilium adjacent to a group of microvilli of graded lengths. It has been highly controversial whether the ectodermal sensory cells in the oral siphons of adult tunicates are homologous to vertebrate hair cells. In some species of tunicates, these cells appear to be secondary neurons, and microvillar and ciliary configurations of some of these cells approach those of vertebrate hair cells. However, none of the tunicate cells has all the characteristics of a hair cell, and there is a high degree of variation among ectodermal sensory cells within and between different species. Thus, similarities between the ectodermal sensory cells of any one species of tunicate and craniate hair cells may well represent convergent evolution rather than homology.

Holland, LZ, Ocampo Daza D.  2018.  A new look at an old question: when did the second whole genome duplication occur in vertebrate evolution? Genome Biology. 19   10.1186/s13059-018-1592-0   AbstractWebsite

A recent study used 61 extant animal genomes to reconstruct the chromosomes of the hypothetical amniote ancestor. Comparison of this karyotype to the 17 chordate linkage groups previously inferred in the ancestral chordate indicated that two whole genome duplications probably occurred in the lineage preceding the ancestral vertebrate.

Holland, LZ, Panfilio KA, Chastain R, Schubert M, Holland ND.  2005.  Nuclear beta-catenin promotes non-neural ectoderm and posterior cell fates in amphioxus embryos. Developmental Dynamics. 233:1430-1443.   10.1002/dvdy.20473   AbstractWebsite

In vertebrate development, Wnt/beta-catenin signaling has an early role in specification of dorsal/anterior identity and a late one in posterior specification. To understand the evolution of these roles, we cloned beta-catenin from the invertebrate chordate amphioxus. The exon/intron organization of beta-catenin is highly conserved between amphioxus and other animals including a cnidarian, but not Drosophila. In development, amphioxus P-catenin is concentrated in all nuclei from the 16-cell stage until the onset of gastrulation when it becomes undetectable in presumptive mesendoderm. Li+, which up-regulates Wnt/beta-catenin signaling, had no detectable effect on axial patterning when applied before the late blastula stage, suggesting that a role for P-catenin in specification of dorsal/anterior identity may be a vertebrate innovation. From the mid-gastrula through the neurula stage, the highest levels of nuclear R-catenin are around the blastopore. In the early neurula, P-catenin is down-regulated in the neural plate, but remains high in adjacent non-neural ectoderm. Embryos treated with Li+ at the late blastula stage are markedly posteriorized and lack a neural plate. These results suggest that in amphioxus, as in vertebrates, downregulation of Wnt/beta-catenin signaling in the neural plate is necessary for maintenance of the neuroectoderm and that a major evolutionarily conserved role of Wnt/beta-catenin signaling is to specify posterior identity and pattern the anterior/posterior axis. (c) 2005 Wiley-Liss, Inc.

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Ono, H, Koop D, Holland LZ.  2018.  Nodal and Hedgehog synergize in gill slit formation during development of the cephalochordate Branchiostoma floridae. Development. 145   10.1242/dev.162586   AbstractWebsite

The larval pharynx of the cephalochordate Branchiostoma (amphioxus) is asymmetrical. The mouth is on the left, and endostyle and gill slits are on the right. At the neurula, Nodal and Hedgehog (Hh) expression becomes restricted to the left. To dissect their respective roles in gill slit formation, we inhibited each pathway separately for 20 min at intervals during the neurula stage, before gill slits penetrate, and monitored the effects on morphology and expression of pharyngeal markers. The results pinpoint the short interval spanning the gastrula/neurula transition as the critical period for specification and positioning of future gill slits. Thus, reduced Nodal signaling shifts the gill slits ventrally, skews the pharyngeal domains of Hh, Pax1/9, Pax2/5/8, Six1/2 and IrxC towards the left, and reduces Hh and Tbx1/10 expression in endoderm and mesoderm, respectively. Nodal auto-regulates. Decreased Hh signaling does not affect gill slit positions or Hh or Nodal expression, but it does reduce the domain of Gli, the Hh target, in the pharyngeal endoderm. Thus, during the neurula stage, Nodal and Hh cooperate in gill slit development - Hh mediates gill slit formation and Nodal establishes their left-right position.

S
Striedter, GF, Belgard TG, Chen CC, Davis FP, Finlay BL, Gunturkun O, Hale ME, Harris JA, Hecht EE, Hof PR, Hofmann HA, Holland LZ, Iwaniuk AN, Jarvis ED, Karten HJ, Katz PS, Kristan WB, Macagno ER, Mitra PP, Moroz LL, Preuss TM, Ragsdale CW, Sherwood CC, Stevens CF, Stuttgen MC, Tsumoto T, Wilczynski W.  2014.  NSF workshop report: Discovering general principles of nervous system organization by comparing brain maps across species. Journal of Comparative Neurology. 522:1445-1453.   10.1002/cne.23568   AbstractWebsite

Efforts to understand nervous system structure and function have received new impetus from the federal Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative. Comparative analyses can contribute to this effort by leading to the discovery of general principles of neural circuit design, information processing, and gene-structure-function relationships that are not apparent from studies on single species. We here propose to extend the comparative approach to nervous system maps' comprising molecular, anatomical, and physiological data. This research will identify which neural features are likely to generalize across species, and which are unlikely to be broadly conserved. It will also suggest causal relationships between genes, development, adult anatomy, physiology, and, ultimately, behavior. These causal hypotheses can then be tested experimentally. Finally, insights from comparative research can inspire and guide technological development. To promote this research agenda, we recommend that teams of investigators coalesce around specific research questions and select a set of reference species' to anchor their comparative analyses. These reference species should be chosen not just for practical advantages, but also with regard for their phylogenetic position, behavioral repertoire, well-annotated genome, or other strategic reasons. We envision that the nervous systems of these reference species will be mapped in more detail than those of other species. The collected data may range from the molecular to the behavioral, depending on the research question. To integrate across levels of analysis and across species, standards for data collection, annotation, archiving, and distribution must be developed and respected. To that end, it will help to form networks or consortia of researchers and centers for science, technology, and education that focus on organized data collection, distribution, and training. These activities could be supported, at least in part, through existing mechanisms at NSF, NIH, and other agencies. It will also be important to develop new integrated software and database systems for cross-species data analyses. Multidisciplinary efforts to develop such analytical tools should be supported financially. Finally, training opportunities should be created to stimulate multidisciplinary, integrative research into brain structure, function, and evolution. J. Comp. Neurol. 522:1445-1453, 2014. (c) 2014 Wiley Periodicals, Inc.