Publications

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2017
Holland, ND, Holland LZ.  2017.  The ups and downs of amphioxus biology: a history. International Journal of Developmental Biology. 61:575-583.   10.1387/ijdb.160395LH   AbstractWebsite

Humans (at least a select few) have long known about the cephalochordate amphioxus, first as something to eat and later as a subject for scientific study. The rate of publication on these animals has waxed and waned several times. The first big surge, in the late nineteenth century, was stimulated by Darwin's evolutionary ideas and by Kowalevsky's embryologic findings suggesting that an amphioxus-like creature might have bridged the gap between the invertebrates and the vertebrates. Interest declined sharply in the early twentieth century and remained low for the next 50 years. An important contributing factor (in addition to inhibition by two world wars and the Great Depression) was the indifference of the new evolutionary synthesis toward broad phylogenetic problems like the origin of the vertebrates. Then, during the 1960s and 1970s, interest in amphioxus resurged, driven especially by increased government support for basic science as well as opportunities presented by electron microscopy. After faltering briefly in the 1980s (electron microscopists were running out of amphioxus tissues to study), a third and still-continuing period of intensive amphioxus research began in the early 1990s, stimulated by the advent of evolutionary developmental biology (evo-devo) and genomics. The volume of studies peaked in 2008 with the publication of the genome of the Florida amphioxus. Since then, although the number of papers per year has dropped somewhat, sequencing of additional genomes and transcriptomes of several species of amphioxus (both in the genus Branchiostoma and in a second genus, Asymmetron) is providing the raw material for addressing the major unanswered question of the relationship between genotype and phenotype.

2004
Holland, LZ, Laudet V, Schubert M.  2004.  The chordate amphioxus: an emerging model organism for developmental biology. Cellular and Molecular Life Sciences. 61:2290-2308.   10.1007/s00018-004-4075-2   AbstractWebsite

The cephalochordate amphioxus is the closest living invertebrate relative of the vertebrates. It is vertebrate-like in having a dorsal, hollow nerve cord, notochord, segmental muscles, pharyngeal gill slits and a post-anal tail that develops from a tail bud. However, amphioxus is less complex than vertebrates, lacking neural crest and having little or no mesenchyme. The genetic programs patterning the amphioxus embryo are also similar to those patterning vertebrate embryos, although the amphioxus genome lacks the extensive gene duplications characteristic of vertebrates. This relative structural and genomic simplicity in a vertebrate-like organism makes amphioxus ideal as a model organism for understanding mechanisms of vertebrate development.

1997
Holland, LZ, Kene M, Williams NA, Holland ND.  1997.  Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): The metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. Development. 124:1723-1732. AbstractWebsite

Vertebrate segmentation has been proposed as an evolutionary inheritance either from some metameric protostome or from a more closely related deuterostome, To address this question, we studied the developmental expression of AmphiEn, the engrailed gene of amphioxus, the closest living invertebrate relative of the vertebrates, In neurula embryos of amphioxus, AmphiEn is expressed along the anteroposterior axis as metameric stripes, each located in the posterior part of a nascent or newly formed segment, This pattern resembles the expression stripes of the segment-polarity gene engrailed, which has a key role in establishing and maintaining the metameres in embryos of Drosophila and other metameric protostomes, Later, amphioxus embryos express AmphiEn in non-metameric patterns - transiently in the embryonic ectoderm and dorsal nerve cord. Nerve cord expression occurs in a few cells approximately midway along the rostrocaudal axis and also in a conspicuous group of anterior cells in the cerebral vesicle at a level previously identified as corresponding to the vertebrate diencephalon. Compared to vertebrate engrailed expression at the midbrain/hindbrain boundary, AmphiEn expression in the cerebral vesicle is relatively late, Thus, it is uncertain whether the cerebral vesicle expression marks the rostral end of the amphioxus hindbrain; if it does, then amphioxus may have little or no homolog of the vertebrate midbrain, The segmental expression of AmphiEn in forming somites suggests that the functions of engrailed homologs in establishing and maintaining a metameric body plan may have arisen only once during animal evolution, If so, the protostomes and deuterostomes probably shared a common segmented ancestor.

1996
Holland, ND, Panganiban G, Henyey EL, Holland LZ.  1996.  Sequence and developmental expression of AmphiDII, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: Insights into evolution of craniate forebrain and neural crest. Development. 122:2911-2920. AbstractWebsite

The dynamic expression patterns of the single amphioxus Distal-less homolog (AmphiDll) during development are consistent with successive roles of this gene in global regionalization of the ectoderm, establishment of the dorsoventral axis, specification of migratory epidermal cells early in neurulation and the specification of forebrain, Such a multiplicity of Distal-less functions probably represents an ancestral chordate condition and, during craniate evolution, when this gene diversified into a family of six or so members, the original functions evidently tended to be parcelled out among the descendant genes, In the amphioxus gastrula, AmphiDll is expressed throughout the animal hemisphere (presumptive ectoderm), but is soon downregulated dorsally (in the presumptive neural plate), During early neurulation, AmphiDll-expressing epidermal cells flanking the neural plate extend lamellipodia, appear to migrate over it and meet mid-dorsally, Midway in neurulation, cells near the anterior end of the neural plate begin expressing AmphiDll and, as neurulation terminates, these cells are incorporated into the dorsal part of the neural tube, which forms by a curling of the neural plate, This group of AmphiDII-expressing neural cells and a second group expressing the gene a little later and even more anteriorly in the neural tube demarcate a region that comprises the anterior three/fourths of the cerebral vesicle; this region of the amphioxus neural tube, as judged by neural expression domains of craniate Distal-less-related genes, is evidently homologous to the craniate forebrain, Our results suggest that craniates evolved from an amphioxus-like creature that had the beginnings of a forebrain and possibly a precursor of neural crest - namely, the cell population leading the epidermal overgrowth of the neural plate during early neurulation.

1994
Holland, PWH, Garcia-Fernandez J, Holland LZ, Williams NA, Holland ND.  1994.  The Molecular Control of Spatial Patterning in Amphioxus. Journal of the Marine Biological Association of the United Kingdom. 74:49-60. AbstractWebsite

The embryology of amphioxus (Chordata: Cephalochordata) has features in common with vertebrate embryology, reflecting a dose phylogenetic relationship between the two taxa. Amphioxus differs from vertebrates, however, in having less complex organogenesis and cranial morphogenesis, and less specialization along the anteroposterior body axis. Here we illustrate this by describing the embryology of an amphioxus species, Branchiostoma floridae. To gain further insight into the origins, evolutionary divergence and comparative embryology of these taxa, we are comparing the molecular control of embryonic development in amphioxus and vertebrates. For these analyses, we are focusing on homeobox genes: a diverse multigene family implicated in developmental control in many Metazoa. We report the results of PCR-based experiments which reveal that the amphioxus genome has homeobox genes from several recognized gene classes. The PCR experiments also suggest that amphioxus has fewer 'Hox' and 'Msx' class homeobox genes than do vertebrates. We suggest, therefore, that amphioxus may be a living descendant from an intermediate stage in the evolution of homeobox gene family complexity, and the complexity of vertebrate developmental control. The pattern of gene expression during embryogenesis has been described for one amphioxus homeobox gene of the Hox class. This gene is primarily expressed in the presumptive neural tube of amphioxus neurulae, later embryos and larvae, in a spatially-restricted manner. The expression data lead us to suggest that Hox genes are involved in the control of spatial patterning in the neural tube of amphioxus; the data are also interpreted as giving insight into possible homology between the amphioxus and vertebrate body plans.

1992
Holland, PWH, Holland LZ, Williams NA, Holland ND.  1992.  An Amphioxus Homeobox Gene - Sequence Conservation, Spatial Expression During Development and Insights into Vertebrate Evolution. Development. 116:653-&. AbstractWebsite

The embryology of amphioxus has much in common with vertebrate embryology, reflecting a close phylogenetic relationship between the two groups. Amphioxus embryology is simpler in several key respects, however, including a lack of pronounced craniofacial morphogenesis. To gain an insight into the molecular changes that accompanied the evolution of vertebrate embryology, and into the relationship between the amphioxus and vertebrate body plans, we have undertaken the first molecular level investigation of amphioxus embryonic development. We report the cloning, complete DNA sequence determination, sequence analysis and expression analysis of an amphioxus homeobox gene, AmphiHox3, evolutionarily homologous to the third-most 3' paralogous group of mammalian Hox genes. Sequence comparison to a mammalian homologue, mouse Hox-2.7 (HoxB3), reveals several stretches of amino acid conservation within the deduced protein sequences. Whole mount in situ hybridization reveals localized expression of AmphiHox3 in the posterior mesoderm (but not in the somites), and region-specific expression in the dorsal nerve cord, of amphioxus neurulae, later embryos and larvae. The anterior limit to expression in the nerve cord is at the level of the four/five somite boundary at the neurula stage, and stabilises to just anterior to the first nerve cord pigment spot to form. Comparison to the anterior expression boundary of mouse Hox-2.7 (HoxB3) and related genes suggests that the vertebrate brain is homologous to an extensive region of the amphioxus nerve cord that contains the cerebral vesicle (a region at the extreme rostral tip) and extends posterior to somite four. This proposed homology implies that the vertebrate brain probably did not evolve solely from the cerebral vesicle of an amphioxus-like ancestor, nor did it arise entirely de novo anterior to the cerebral vesicle.