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Holland, ND, Holland LZ, Holland PWH.  2015.  Scenarios for the making of vertebrates. Nature. 520:450-455.   10.1038/nature14433   AbstractWebsite

Over the past 200 years, almost every invertebrate phylum has been proposed as a starting point for evolving vertebrates. Most of these scenarios are outdated, but several are still seriously considered. The short-range transition from ancestral invertebrate chordates (similar to amphioxus and tunicates) to vertebrates is well accepted. However, longer-range transitions leading up to the invertebrate chordates themselves are more controversial. Opinion is divided between the annelid and the enteropneust scenarios, predicting, respectively, a complex or a simple ancestor for bilaterian animals. Deciding between these ideas will be facilitated by further comparative studies of multicellular animals, including enigmatic taxa such as xenacoelomorphs.

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.

Venkatesh, TV, Holland ND, Holland LZ, Su MT, Bodmer R.  1999.  Sequence and developmental expression of amphioxus AmphiNk2-1: insights into the evolutionary origin of the vertebrate thyroid gland and forebrain. Development Genes and Evolution. 209:254-259. AbstractWebsite

We characterized an amphioxus NK-2 homeobox gene (AmphiNk2-1), a homologue of vertebrate Nkx2-1, which is involved in the development of the central nervous system and thyroid gland. At the early neurula stage of amphioxus, AmphiNk2-1 expression is first detected medially in the neural plate. By the mid-neurula stage, expression is localized ventrally in the nerve cord and also begins in the endoderm. During the late neurula stage, the ventral neural expression becomes transiently segmented posteriorly and is then down-regulated except in the cerebral vesicle at the anterior end of the central nervous system. Within the cerebral vesicle AmphiNk2-1 is expressed in a broad ventral domain, probably comprising both the floor plate and basal plate regions: this pattern is comparable to Nkx2-1 expression in the mouse diencephalon. In the anterior part of the gut, expression becomes intense in the endostyle (the right wall of the pharynx), which is the presumed homologue of the vertebrate thyroid gland. More posteriorly, there is transitory expression in the midgut and hindgut. In sum, the present results help to support homologies (1) between the amphioxus endostyle and the vertebrate thyroid gland and (2) between the amphioxus cerebral vesicle and the vertebrate diencephalic forebrain.

Holland, ND, Zhang S-C, Clark M, Panopoulou GD, Lehrach H, Holland LZ.  1997.  Sequence and developmental expression of AmphiTob, an amphioxus homolog of vertebrate Tob in the PC3/BTG/Tob family of tumor suppressor genes. Developmental Dynamics. 210:11-18.
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.

Holland, LZ, Pace DA, Blink ML, Kene M, Holland ND.  1995.  Sequence and Expression of Amphioxus Alkali Myosin Light-Chain (Amphimlc-Alk) Throughout Development - Implications for Vertebrate Myogenesis. Developmental Biology. 171:665-676.   10.1006/dbio.1995.1313   AbstractWebsite

The lower chordate amphioxus, widely considered the closest living invertebrate relative of the vertebrates, is a key organism for understanding the relationship between gene duplications and evolution of the complex vertebrate body plan. In tetrapod vertebrates, the alkali myosin light chain genes (MLC-alk), which code for proteins associated with the globular head of the myosin heavy chain, constitute a large family with stage-, tissue-, and fiber-type-specific expression of different isoforms thought to have arisen by duplication of a single ancestral gene. In protostome invertebrates, e.g., arthropods, molluscs, and nematodes, only one MLC-alk gene has been found, but the number of such genes in deuterostome invertebrates and lower vertebrates is unknown. The present report, describing the sequence and expression throughout development of the amphioxus gene for alkali myosin light chain (AmphiMLC-alk), thus fills a major gap in understanding the relation between gene duplication and increasing diversity of muscle-cell types. A full-length clone (1 kb) of AmphiMLC-alk was isolated from a larval amphioxus cDNA Library. It coded for a 149-amino-acid protein most closely related to the vertebrate embryonic form of MLC-alk. Southern blot analysis revealed only one copy of AmphiMLC-alk and suggested that it is the only MLC-alk gene in amphioxus. Northern blot analysis indicated that this gene produces only one transcript, which is expressed at all stages of development and in adults. In situ hybridizations showed expression initially in the myotomes of somites 2-5 of neurula embryos and soon thereafter in the myotomes of somite 1 and of newly forming somites progressively added posteriorly. Myotomal expression continues throughout larval development and into the adult stage as the myotomal cells differentiate into striated, mononucleate muscle cells-unlike vertebrate striated muscle cells, those of amphioxus never become multinucleate. In late larvae and adults myotomal expression of AmphiMLC-alk is localized along the medial edge of the myotome and at the ends of the cells. This is the first demonstration of intracellular localization of MLC transcripts in muscle cells of any animal. Expression of AmphiMLC-alk was also detected in smooth muscles as well as in striated muscles not derived from the myotome. These expression data are consistent with the Southern blot analysis in suggesting that there is only one MLC-alk gene in amphioxus. Thus, duplication of an ancestral vertebrate MLC-alk gene probably occurred after the vertebrate and amphioxus lineages split. We conclude that development of a segmented axial musculature preceded the evolution of multiple MLC-alk isoforms, which evidently arose about the time of multinucleation. Since myogenesis in amphioxus is similar to but far simpler than myogenesis in vertebrates at both the structural and gene levels, an understanding of myogenesis in amphioxus can give insights into both the evolutionary history and the detailed mechanisms of vertebrate myogenesis. (C) 1995 Academic Press, Inc.

Holland, ND, Holland LZ.  1993.  Serotonin-Containing Cells in the Nervous-System and Other Tissues During Ontogeny of a Lancelet, Branchiostoma-Floridae. Acta Zoologica. 74:195-204. AbstractWebsite

Serotonin-containing cells are described by immunohistochemistry throughout lancelet ontogeny. Such cells are first detected in the 2-day larva: these are (1) enterochromaffin cells in the inner epithelium of the gut and (2) anterior serotonergic neurons at the rostral end of the nerve cord. In the 6-day larva, relatively low levels of serotonin appear in ventro-lateral perikarya and cell processes of intraspinal serotonergic neurons scattered along the nerve cord. In the 18-day (early metamorphic) larva, antero-lateral serotonergic neurons are detected near the rostral end of the nerve cord as two small, bilateral clusters of perikarya with axons that descend the nerve cord; at later developmental stages, these axons extend almost to the posterior end of the body. In the 21-day (mid-metamorphic) larva, serotonin can no longer be detected in the anterior serotonergic neurons, but serotonin-containing cells are found subjacent to the inner epithelium of the digestive caecum and in the peribranchial epithelium covering the primary gill bars. In the discussion, we suggest that the anterior serotonergic neurons may play a role in larval photoreception and that the antero-lateral serotonergic neurons may be homologous to vertebrate hindbrain neurons with axons descending the spinal cord to modulate undulation (if this homology is valid, the anterior limit of the lancelet hindbrain would be roughly 100 mum behind the rostral tip of the nerve cord).

Holland, LZ.  2006.  A SINE in the genome of the cephalochordate amphioxus is an Alu element. International Journal of Biological Sciences. 2.(2):61-65.
Holland, ND, Holland LZ.  2006.  Stage- and tissue-specific patterns of cell division in embryonic and larval tissues of amphioxus during normal development. Evolution & Development. 8:142-149.   10.1111/j.1525-142X.2006.00085.x   AbstractWebsite

The distribution of dividing cells is described for embryos and larvae of amphioxus (Branchiostoma floridae) pulse labeled with bromodeoxyuridine. Because cell division is assessed for all of the developing tissues, this is the first comprehensive study of developmental cell proliferation for an animal lacking a stereotyped cell lineage. In amphioxus, cell divisions are virtually synchronous during cleavage, but become asynchronous at the blastula stage. Starting at the neurula stage, after the origin of the mesoderm, the proportion of dividing cells progressively declines in the somitic mesoderm and notochord. Other tissues, however, deviate from this pattern. For example, in the mid-neurula, there is a brief, intense burst of mitosis at the anterior end of the neural plate. Also, from the neurula through the early larval stage, all of the ectoderm cells cease dividing and develop cilia that propel the animal through the water; subsequently, in the epidermis of later larvae, mitosis resumes and the proportion of ciliated cells declines as muscular undulation gradually replaces ciliation for swimming. Finally, in the early larvae, there is a terminal arrest of cell division in three cell types that differentiate early to participate in feeding as soon as the mouth opens-namely the ciliated pharyngeal cells that produce the feeding current and the secretory cells of the club-shaped gland and endostyle that export food-trapping mucus into the pharynx. In sum, these stage- and tissue-specific changes in cell proliferation intensity illustrate how the requirements of embryonic and larval natural history can shape developmental programs.

Jaffe, LA, Gould-Somero M, Holland LZ.  1982.  Studies of the Mechanism of the Electrical Polyspermy Block Using Voltage Clamp During Cross-Species Fertilization. Journal of Cell Biology. 92:616-621.   10.1083/jcb.92.3.616   Website
Holland, LZ, Giese AC, Phillips JH.  1967.  Studies on Perivisceral Coelomic Fluid Protein Concentration During Seasonal and Nutritional Changes in Purple Sea Urchin. Comparative Biochemistry and Physiology. 21:361-371.   10.1016/0010-406x(67)90798-0   Website