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Koop, D, Holland LZ, Setiamarga D, Schubert M, Holland ND.  2011.  Tail regression induced by elevated retinoic acid signaling in amphioxus larvae occurs by tissue remodeling, not cell death. Evolution & Development. 13:427-435.   10.1111/j.1525-142X.2011.00501.x   AbstractWebsite

The vitamin A derived morphogen retinoic acid (RA) is known to function in the regulation of tissue proliferation and differentiation. Here, we show that exogenous RA applied to late larvae of the invertebrate chordate amphioxus can reverse some differentiated states. Although treatment with the RA antagonist BMS009 has no obvious effect on late larvae of amphioxus, administration of excess RA alters the morphology of the posterior end of the body. The anus closes over, and gut contents accumulate in the hindgut. In addition, the larval tail fin regresses, although little apoptosis takes place. This fin normally consists of columnar epidermal cells, each characterized by a ciliary rootlet running all the way from an apical centriole to the base of the cell and likely contributing substantial cytoskeletal support. After a few days of RA treatment, the rootlet becomes disrupted, and the cell shape changes from columnar to cuboidal. Transmission electron microscopy (TEM) shows fragments of the rootlet in the basal cytoplasm of the cuboidal cell. A major component of the ciliary rootlet in amphioxus is the protein Rootletin, which is encoded by a single AmphiRootletin gene. This gene is highly expressed in the tail epithelial cells of control larvae, but becomes downregulated after about a day of RA treatment, and the breakup of the ciliary rootlet soon follows. The effect of excess RA on these epidermal cells of the larval tail in amphioxus is unlike posterior regression in developing zebrafish, where elevated RA signaling alters connective tissues of mesodermal origin. In contrast, however, the RA-induced closure of the amphioxus anus has parallels in the RA-induced caudal regression syndrome of mammals.

Schubert, M, Holland LZ, Stokes MD, Holland ND.  2001.  Three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) associated with the tail bud: The evolution of somitogenesis in chordates. Developmental Biology. 240:262-273.   10.1006/dbio.2001.0460   AbstractWebsite

The amphioxus tail bud is similar to the amphibian tail bud in having an epithelial organization without a mesenchymal component. We characterize three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) and show that their early expression around the blastopore can subsequently be traced into the tail bud; in vertebrate embryos, there is a similar progression of expression domains for Wnt3, Wnt5, and Wnt6 genes from the blastopore lip (or its equivalent) to the tail bud. In amphioxus, AmphiWnt3, AmphiWnt5, and AmphiWnt6 are each expressed in a specific subregion of the tail bud, tentatively suggesting that a combinatorial code of developmental gene expression may help generate specific tissues during posterior elongation and somitogenesis. In spite of similarities within their tail buds, vertebrate and amphioxus embryos differ markedly in the relation between the tail bud and the nascent somites: vertebrates have a relatively extensive zone of unsegmented mesenchyme (i.e., presomitic mesoderm) intervening between the tail bud and the forming somites, whereas the amphioxus tail bud gives rise to new somites directly. It is likely that presomitic mesoderm is a vertebrate innovation made possible by developmental interconversions between epithelium and mesenchyme that first became prominent at the dawn of vertebrate evolution. (C) 2001 Academic Press.

Gould-Somero, M, Holland LZ.  1974.  Timing of RNA-synthesis for Spermiogenesis in Organ-cultures of Drosophila melanogaster testes. TIWilhelm Roux Archiv fur Entwicklungsmechanik der Organismen . 174(2):133-148.
Yu, JK, Holland ND, Holland LZ.  2004.  Tissue-specific expression of FoxD reporter constructs in amphioxus embryos. Developmental Biology. 274:452-461.   10.1016/j.ydbio.2004.07.010   AbstractWebsite

Cephalochordates (amphioxus), the closest living invertebrate relatives of the vertebrates, are key to understanding the evolution of developmental mechanisms during the invertebrate-to-vertebrate transition. However, a major impediment to amphioxus as a model organism for developmental biology has been the inability to introduce transgenes or other macromolecules into the embryos. Here, we report the development of a reproducible method for microinjection of amphioxus eggs. Specifically, we show that expression of a LacZ reporter construct including 6.3 kb of AmphiFoxD upstream regulatory DNA recapitulates expression of the endogenous gene in the nerve cord, somites, and notochord. We have also identified the 1.6 kb at the 5' end of this region as essential for expression in the first two of these domains and the 4.7 kb at the 3' end as sufficient for expression in the notochord. This study, which is the first report of a method for introduction of large molecules such as DNA into amphioxus embryos, opens the way for studies of gene regulation and function in amphioxus and for comparative studies with vertebrates to understand the relationship between the extensive gene duplications that occurred within the vertebrate lineage and the evolution of vertebrate innovations such as neural crest. (C) 2004 Elsevier Inc. All rights reserved.

Zhang, SC, Holland ND, Holland LZ.  1997.  Topographic changes in nascent and early mesoderm in amphioxus embryos studied by Dil labeling and by in situ hybridization for a Brachyury gene. Development Genes and Evolution. 206:532-535.   10.1007/s004270050083   AbstractWebsite

In amphioxus embryos, the nascent and early mesoderm (including chorda-mesoderm) was visualized by expression of a Brachyury gene (AmBra-2). A band of mesoderm is first detected encircling the earliest (vegetal plate stage) gastrula sub-equatorially. Soon thereafter, the vegetal plate invaginates. resulting in a cap-shaped gastrula with the mesoderm localized at the blastoporal lip and completely encircling the blastopore. As the gastrula stage progresses, DiI (a vital dye) labeling demonstrates that the entire mesoderm is internalized by a slight involution of the epiblast into the hypoblast all around the perimeter of the blastopore. Subsequently. during the early neurula stage, the internalized mesoderm undergoes anterior extension mid-dorsally (as notochord) and dorsolaterally (in paraxial regions when segments will later form). By the late neurula stage, AmBra-2 is no longer transcribed throughout the mesoderm as a whole; instead. expression is detectable only in the posterior mesoderm and in the notochord, but not in par axial mesoderm where definitive somites have formed.

Yue, JX, Yu JK, Putnam NH, Holland LZ.  2014.  The transcriptome of an Amphioxus, Asymmetron lucayanum, from the Bahamas: A window into chordate evolution. Genome Biology and Evolution. 6:2681-2696.   10.1093/gbe/evu212   AbstractWebsite

Cephalochordates, the sister group of tunicates plus vertebrates, have been called "living fossils" due to their resemblance to fossil chordates from Cambrian strata. The genome of the cephalochordate Branchiostoma floridae shares remarkable synteny with vertebrates and is free from whole-genome duplication. We performed RNA sequencing from larvae and adults of Asymmetron lucayanum, a cephalochordate distantly related to B. floridae. Comparisons of about 430 orthologous gene groups among both cephalochordates and 10 vertebrates using an echinoderm, a hemichordate, and a mollusk as outgroups showed that cephalochordates are evolving more slowly than the slowest evolving vertebrate known (the elephant shark), with A. lucayanum evolving even more slowly than B. floridae. Against this background of slow evolution, some genes, notably several involved in innate immunity, stand out as evolving relatively quickly. This may be due to the lack of an adaptive immune system and the relatively high levels of bacteria in the inshore waters cephalochordates inhabit. Molecular dating analysis including several time constraints revealed a divergence time of similar to 120 Ma for A. lucayanum and B. floridae. The divisions between cephalochordates and vertebrates, and that between chordates and the hemichordate plus echinoderm clade likely occurred before the Cambrian.