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Yu, JK, Wang MC, Shin T, Kohara Y, Holland LZ, Satoh N, Satou Y.  2008.  A cDNA resource for the cephalochordate amphioxus Branchiostoma floridae. Development Genes and Evolution. 218:723-727.   10.1007/s00427-008-0228-x   AbstractWebsite

Cephalochordates are the basal invertebrate chordates within the phylum Chordata. They are widely used as a model system for research in evolutionary developmental biology (EvoDevo) to understand the basic patterning mechanisms for the chordate body plan and the origin of vertebrates. Recently, the genome of the cephalochordate Branchiostoma floridae was sequenced, which further brings this organism to the front for comparative genomic studies. In this paper, we report the generation of large-scale 5'- and 3'-expressed sequence tags (ESTs) from B. floridae and the complementary deoxyribonucleic acid (cDNA) resource for this species. Both 5'- and 3'-ESTs were sequenced for approximately 140,000 cDNA clones derived from five developmental stages, and the cDNA clones were subsequently grouped into independent clusters using 3'-EST sequences. We identified 21,229 cDNA clusters, and each corresponds to a unique transcript species from B. floridae. We then chose 24,020 cDNA clones representing all of these 21,229 clusters to generate the "Branchiostoma floridae Gene Collection Release 1." We also constructed a database with a searchable interface for this EST dataset and the related information on "Branchiostoma floridae Gene Collection Release 1." This set of cDNA clones along with our cDNA database will serve as an important resource for future research in this basal chordate. This Gene Collection and the original 140,000 individual cDNA clones are available to the research community upon request.

Holland, LZ, Yu JK.  2004.  Cephalochordate (amphioxus) embryos: Procurement, culture, and basic methods. Development of Sea Urchins, Ascidians, and Other Invertebrate Deuterostomes: Experimental Approaches. 74:195-215.Website
Yu, J-K, Holland LZ.  2009.  Cephalochordates (amphioxus or lancelets): a model for understanding the evolution of chordate characters . Cold Spring Harbor Protocols. 2009:pdb.emo130. doi: (9)   10.1101/pdb.emo130  
Holland, LZ, Venkatesh TV, Gorlin A, Bodmer R, Holland ND.  1998.  Characterization and developmental expression of AmphiNk2-2, an NK2 class homeobox gene from amphioxus (Phylum Chordata; Subphylum Cephalochordata). Development Genes and Evolution. 208:100-105.   10.1007/s004270050159   AbstractWebsite

The genome of amphioxus includes AmphiNk2-2, the first gene of the NK2 homeobox class to be demonstrated in any invertebrate deuterostome. AmphiNk2-2 encodes a protein with a TN domain, homeodomain, and NK2-specific domain; on the basis of amino acid identities in these conserved regions, AmphiNk2-2 is a homolog of Drosophila vnd and vertebrate Nkx2-2. During amphioxus development, expression of AmphiNk2-2 is first detected ventrally in the endoderm of late gastrulae. In neurulae, endodermal expression divides into three domains (the pharynx, midgut, and hindgut), and neural expression commences in two longitudinal bands of cells in the anterior neural tube. These neural tube cells occupy a ventrolateral position on either side of the cerebral vesicle (the probable homolog of the vertebrate diencephalic forebrain). The dynamic expression patterns of AmphiNFkx2-2 suggest successive roles, first in regionalizing the endoderm and nervous system and later during differentiation of specific cell types in the gut (possibly peptide endocrine cells) and brain (possibly including axon outgrowth and guidance).

Holland, LZ, Rached LA, Tamme R, Holland ND, Inoko H, Shiina T, Burgtorf C, Lardelli M.  2001.  Characterization and developmental expression of the amphioxus homolog of notch (AmphiNotch): Evolutionary conservation of multiple expression domains in amphioxus and vertebrates. Developmental Biology. 232:493-507.   10.1006/dbio.2001.0160   AbstractWebsite

Notch encodes a transmembrane protein that functions in intercellular signaling. Although there is one Notch gene in Drosophila, vertebrates have three or more with overlapping patterns of embryonic expression. We cloned the entire 7575-bp coding region of an amphioxus Notch gene (AmphiNotch), encoding 2524 amino acids, and obtained the exon/intron organization from a genomic cosmid clone. Southern blot and PCR data indicate that AmphiNotch is the only Notch gene in amphioxus. AmphiNotch, like Drosophila Notch and vertebrate Notch1 and Notch2, has 36 EGF repeats, 3 Notch/lin-12 repeats, a transmembrane region, and B ankyrin repeats. Phylogenetic analysis places it at the base of all the vertebrate genes, suggesting it is similar to the ancestral gene from which the vertebrate Notch family genes evolved. AmphiNotch is expressed in all three embryonic perm layers in spatiotemporal patterns strikingly similar to those of all the vertebrate homologs combined. In the developing nerve cord, AmphiNotch is first expressed in the posteriormost part of the neural plate, then it becomes more broadly expressed and later is localized dorsally in the anteriormost part of the nerve cord corresponding to the diencephalon. In late embryos and larvae, AmphiNotch is also expressed in parts of the pharyngeal endoderm, ill the anterior gut diverticulum, and, like AmphiPax2/5/8, in the rudiment of Hatschek's kidney. A comparison with Notch1 and Pax5 and Pax8 expression in the embryonic mouse kidney helps support homology of the amphioxus and vertebrate kidneys. AmphiNotch is also an early marker for presumptive mesoderm, transcripts first being detectable at the gastrula stage in a ring of mesendoderm just inside the blastopore and subsequently in the posterior mesoderm, notochord, and somites. As in sea urchins and vertebrates, these domains of AmphiNotch expression overlap with those of several Wnt genes and brachyury. These relationships suggest that amphioxus shares with other deuterostomes a common mechanism for patterning along the anterior/posterior axis involving a posterior signaling center in which the Notch and Wnt pathways and brachyury interact. (C) 2001 Academic Press.

Kozmik, Z, Holland LZ, Schubert M, Lacalli TC, Kreslova J, Vlcek C, Holland ND.  2001.  Characterization of amphioxus AmphiVent, an evolutionarily conserved marker for chordate ventral mesoderm. Genesis. 29:172-179.   10.1002/gene.1021   AbstractWebsite

Structure and developmental expression are described for amphioxus AmphiVent, a homolog of vertebrate Vent genes. In amphioxus, AmphiVent-expressing ventral mesoderm arises at midneurula by outgrowth from the paraxial mesoderm, but in vertebrates, Vent-expressing ventral mesoderm originates earlier, at the gastrula stage. In other embryonic tissues (nascent paraxial mesoderm, neural plate, endoderm, and tail-bud), AmphiVent and its vertebrate homologs are expressed in similar spatiotemporal domains, indicating conservation of many Vent gene functions during chordate evolution. the ventral mesoderm evidently develops precociously in vertebrates because their relatively large embryos probably require an early and extensive deployment of the mesoderm-derived circulatory system. The vertebrate ventral mesoderm, in spite of its strikingly early advent, still resembles the nascent ventral mesoderm of amphioxus in expressing Vent homologs, This coincidence may indicate that Vent homologs in vertebrates and amphioxus play comparable roles in ventral mesoderm specification. (C) 2001 Wiley-Liss, Inc.

Schubert, M, Holland LZ, Panopoulou GD, Lehrach H, Holland ND.  2000.  Characterization of amphioxus AmphiWnt8: insights into the evolution of patterning of the embryonic dorsoventral axis. Evolution & Development. 2:85-92.   10.1046/j.1525-142x.2000.00047.x   AbstractWebsite

The full-length sequence and developmental expression of an amphioxus Wnt gene (AmphiWnt8 ) are described. In amphioxus embryos, the expression patterns of AmphiWnt8 suggest patterning roles in the forebrain, in the hindgut, and in the paraxial mesoderm that gives rise to the muscular somites. Phylogenetic analysis indicates that a single Wnt8 subfamily gene in an ancestral chordate duplicated early in vertebrate evolution into a Wnt8 clade and a Wnt8b clade. Coincident with this gene duplication, the functions of the ancestral AmphiWnt8-like gene appear to have been divided between vertebrate Wnt8b (exclusively neurogenic, especially in the forebrain) and vertebrate Wnt8 (miscellaneous, especially in early somitogenesis). Amphioxus AmphiWnt8 and its vertebrate Wnt8 homologs probably play comparable roles in the early dorsoventral patterning of the embryonic body axis.

Kozmik, Z, Holland ND, Kalousova A, Paces J, Schubert M, Holland LZ.  1999.  Characterization of an amphioxus paired box gene, AmphiPax2/5/8: developmental expression patterns in optic support cells, nephridium, thyroid-like structures and pharyngeal gill slits, but not in the midbrain-hindbrain boundary region. Development. 126:1295-1304. AbstractWebsite

On the basis of developmental gene expression, the vertebrate central nervous system comprises: a forebrain plus anterior midbrain, a midbrain-hindbrain boundary region (MHB) having organizer properties, and rhombospinal domain. The vertebrate MHB is characterized by position, by organizer properties and by being the early site of action of Wnt1 and engrailed genes, and of genes of the Pax2/5/8 subfamily. Wada and others (Wada, H., Saiga, H., Satoh, N. and Holland, P.W.H. (1998) Development 125, 1113-1122) suggested that ascidian tunicates have a vertebrate-like MHB on the basis of ascidian Pax258 expression there. In another invertebrate chordate, amphioxus, comparable gene expression evidence for a vertebrate-like MHB is lacking, We, therefore, isolated and characterized AmphiPax2/5/8, the sole member of this subfamily in amphioxus, AmphiPax2/5/8 is initially expressed well back in the rhombospinal domain and not where a MHB would be expected. In contrast, most of the other expression domains of AmphiPax2/5/8 correspond to expression domains of vertebrate Pax2, Pax5 and Pax8 in structures that are probably homologous - support cells of the eye, nephridium, thyroid-like structures and pharyngeal gill slits; although AmphiPax2/5/8 is not transcribed in any structures that could be interpreted as homologues of vertebrate otic placodes or otic vesicles. In sum, the developmental expression of AmphiPax2/5/8 indicates that the amphioxus central nervous system lacks a MHB resembling the vertebrate isthmic region, Additional gene expression data for the developing ascidian and amphioxus nervous systems would help determine whether a MHB is a basal chordate character secondarily lost in amphioxus, The alternative is that the MHB is a vertebrate innovation.

Schubert, M, Holland LZ, Holland ND.  2000.  Characterization of an amphioxus Wnt gene, AmphiWnt11, with possible roles in myogenesis and tail outgrowth. Genesis. 27:1-5. AbstractWebsite

The full-length sequence and developmental expression of an amphioxus Wnt gene (AmphiWnt11) are described. A phylogenetic analysis of all known full-length Wnt11 sequences indicates that a gene duplication occurred at the base of the vertebrate Wnt11 clade. The developmental expression domains of AmphiWnt11 resemble those of Wnt11 homologs in vertebrates. The earliest detectable expression is transiently associated with the dorsal lip of the blastopore. At the neurula stage, AmphiWnt11 is expressed in myotomal muscle cells; however, AmphiWnt11 transcription is not associated with metameric pre-patterning prior to morphological segmentation. Finally, in amphioxus and the vertebrates, Wnt11 homologs are expressed in anteroventral ectoderm and in association with the tailbud and the tail fin. Thus, in amphioxus and lower vertebrates, the posterior expression of Wnt11 may be involved in tail fin outgrowth, and this ancient genetic program might have been cc-opted at least in part for lateral appendage development during vertebrate evolution. genesis 27: 1-5, 2000, (C) 2000 Wiley-Liss, Inc.

Schubert, M, Holland LZ, Holland ND.  2000.  Characterization of two amphioxus Wnt genes (AmphiWnt4 and AmphiWnt7b) with early expression in the developing central nervous system. Developmental Dynamics. 217:205-215.   10.1002/(sici)1097-0177(200002)217:2<205::aid-dvdy7>;2-f   AbstractWebsite

Full-length sequences and developmental expression patterns of two amphioxus Wnt genes (AmphiWnt4 and AmphiWnt7b) are described for the first time. The dynamic expression pattern of AmphiWnt4 suggests roles in the development of the posterior mesoderm, central nervous system, muscular somites, heart, and endostyle (a homolog of the vertebrate thyroid). The less diverse expression domains of AmphiWnt7b indicate that this gene may be involved only in the development of the central nervous system and the endostyle, In contrast to amphioxus, vertebrate embryos do not express Wnt4 homologues in the posterior mesoderm, somites, or heart; instead, Wnt genes of other subfamilies are expressed in these developing vertebrate organs, Because the developmental genetic programs of amphioxus may approximate those in the invertebrate chordate ancestor of the vertebrates, it is possible that some developmental functions of an ancestral Wnt4 gene may have been assumed by genes of other Wnt subfamilies during vertebrate evolution, possibly as a result of functional redundancy among Wnt subfamilies. (C) 2000 Wiley-Liss, Inc.

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.

Holland, LZ, Holland ND.  1999.  Chordate origins of the vertebrate central nervous system. Current Opinion in Neurobiology. 9:596-602.   10.1016/s0959-4388(99)00003-3   AbstractWebsite

Fine structural, computerized three-dimensional (3D) mapping of cell connectivity in the amphioxus nervous system and comparative molecular genetic studies of amphioxus and tunicates have provided recent insights into the phylogenetic origin of the vertebrate nervous system. The results suggest that several of the genetic mechanisms for establishing and patterning the vertebrate nervous system already operated in the ancestral chordate and that the nerve cord of the proximate invertebrate ancestor of the vertebrates included a diencephalon, midbrain, hindbrain, and spinal cord. In contrast, the telencephalon, a midbrain-hindbrain boundary region with organizer properties, and the definitive neural crest appear to be vertebrate innovations.

Holland, LZ.  2009.  Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nature Reviews Neuroscience. 10:736-746.   10.1038/nrn2703   AbstractWebsite

The vertebrate brain is highly complex with millions to billions of neurons. During development, the neural plate border region gives rise to the neural crest, cranial placodes and, in anamniotes, to Rohon-Beard sensory neurons, whereas the boundary region of the midbrain and hindbrain develops organizer properties. Comparisons of developmental gene expression and neuroanatomy between vertebrates and the basal chordate amphioxus, which has only thousands of neurons and lacks a neural crest, most placodes and a midbrain-hindbrain organizer, indicate that these vertebrate features were built on a foundation already present in the ancestral chordate. Recent advances in genomics have provided insights into the elaboration of the molecular toolkit at the invertebrate-vertebrate transition that may have facilitated the evolution of these vertebrate characteristics.

Holland, LZ, Gibson-Brown JJ.  2003.  The Ciona intestinalis genome: when the constraints are off. Bioessays. 25:529-532.   10.1002/bies.10302   AbstractWebsite

The recent genome sequencing of a non-vertebrate deuterostome, the ascidian tunicate Ciona intestinalis, makes a substantial contribution to the fields of evolutionary and developmental biology.((1)) Tunicates have some of the smallest bilaterian genomes, embryos with relatively few cells, fixed lineages and early determination of cell fates. Initial analyses of the C. intestinalis genome indicate that it has been evolving rapidly. Comparisons with other bilaterians show that C. intestinalis has lost a number of genes, and that many genes linked together in most other bilaterians have become uncoupled. In addition, a number of independent, lineage-specific gene duplications have been detected. These new results, although interesting in themselves, will take on a deeper significance once the genomes of additional invertebrate deuterostomes (e.g. echinoderms, hemichordates and amphioxus) have been sequenced. With such a broadened database, comparative genomics can begin to ask pointed questions about the relationship between the evolution of genomes and the evolution of bodyplans. BioEssays25:529-532,2003. (C) 2003 Wiley Periodicals, Inc.

Beaster-Jones, L, Schubert M, Holland LZ.  2007.  Cis-regulation of the amphioxus engrailed gene: Insights into evolution of a muscle-specific enhancer. Mechanisms of Development. 124:532-542.   10.1016/j.mod.2007.06.002   AbstractWebsite

To gain insights into the relation between evolution of cis-regulatory DNA and evolution of gene function, we identified tissue-specific enhancers of the engrailed gene of the basal chordate amphioxus (Branch iostoma floridae) and compared their ability to direct expression in both amphioxus and its nearest chordate relative, the tunicate Ciona intestinalis. In amphioxus embryos, the native engrailed gene is expressed in three domains - the eight most anterior somites, a few cells in the central nervous system (CNS) and a few ectodermal cells. In contrast, in C. intestinalis, in which muscle development is highly divergent, engrailed expression is limited to the CNS. To characterize the tissue-specific enhancers of amphioxus engrailed, we first showed that 7.8 kb of upstream DNA of amphioxus engrailed directs expression to all three domains in amphioxus that express the native gene. We then identified the amphioxus engrailed muscle-specific enhancer as the 1.2 kb region of upstream DNA with the highest sequence identity to the mouse en-2 jaw muscle enhancer. This amphioxus enhancer directed expression to both the somites in amphioxus and to the larval muscles in C intestinalis. These results show that even though expression of the native engrailed has apparently been lost in developing C intestinalis muscles, they express the transcription factors necessary to activate transcription from the amphioxus engrailed enhancer, suggesting that gene networks may not be completely disrupted if an individual component is lost. (c) 2007 Elsevier Ireland Ltd. All rights reserved.

Holland, PWH, Koschorz B, Holland LZ, Herrmann BG.  1995.  Conservation of Brachyury (T) genes in amphioxus and vertebrates: Developmental and evolutionary implications. Development. 121:4283-4291. AbstractWebsite

Homologues of the murine Brachyury (T) gene have been cloned from several vertebrates, and are implicated in mesoderm formation and in differentiation of the notochord, In contrast, the roles of the ascidian Brachyury gene may be restricted to presumptive notochord, To understand the evolution of Brachyury genes and their developmental roles, we have searched for homologues in amphioxus, representing the third chordate subphylum and the probable closest relative of the vertebrates. We report the isolation of two amphioxus cDNA clones with clear homology to Brachyury genes, and demonstrate that these derive from separate loci resultant from a recent gene duplication. This finding represents an exception to the emerging consensus of an archetypal prevertebrate genome in amphioxus, The spatial and temporal distribution of Brachyury transcripts during amphioxus development is remarkably similar to vertebrate Brachyury, in presumptive mesoderm, posterior mesoderm and the notochord, Gene expression extends throughout the anteroposterior axis of the notochord, despite the most rostral regions being a more recent specialization; it also persists into larval stages, despite differentiation into contractile tissue, We propose that roles of Brachyury in notochord differentiation are more ancient than roles in mesoderm formation, and that the latter are shared by cephalochordates and all vertebrates.

Yue, JX, Kozmikova I, Ono H, Nossa CW, Kozmik Z, Putnam NH, Yu JK, Holland LZ.  2016.  Conserved noncoding elements in the most distant genera of cephalochordates: The Goldilocks principle. Genome Biology and Evolution. 8:2387-2405.   10.1093/gbe/evw158   AbstractWebsite

Cephalochordates, the sister group of vertebrates + tunicates, are evolving particularly slowly. Therefore, genome comparisons between two congeners of Branchiostoma revealed so many conserved noncoding elements (CNEs), that it was not clear how many are functional regulatory elements. To more effectively identify CNEs with potential regulatory functions, we compared noncoding sequences of genomes of the most phylogenetically distant cephalochordate genera, Asymmetron and Branchiostoma, which diverged approximately 120-160 million years ago. We found 113,070 noncoding elements conserved between the two species, amounting to 3.3% of the genome. The genomic distribution, target gene ontology, and enriched motifs of these CNEs all suggest that many of them are probably cis-regulatory elements. More than 90% of previously verified amphioxus regulatory elements were re-captured in this study. A search of the cephalochordate CNEs around 50 developmental genes inseveral vertebrate genomes revealed eight CNEs conserved between cephalochordates and vertebrates, indicating sequence conservation over > 500 million years of divergence. The function of five CNEs was tested in reporter assays in zebrafish, and one was also tested in amphioxus. All five CNEs proved to be tissue-specific enhancers. Taken together, these findings indicate that even though Branchiostoma and Asymmetron are distantly related, as they are evolving slowly, comparisons between them are likely optimal for identifying most of their tissue-specific cis-regulatory elements laying the foundation for functional characterizations and a better understanding of the evolution of developmental regulation in cephalochordates.

Gould-Somero, M, Holland LZ, Paul M.  1977.  Cytochalasin-B Inhibits Sperm Penetration into eggs of Urechis caupo (Echiura). Developmental Biology. 58(1):11-22.   10.1016/0012-1606(77)90071-9