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Holland, LZ, Schubert M, Holland ND, Neuman T.  2000.  Evolutionary conservation of the presumptive neural plate markers AmphiSox1/2/3 and AmphiNeurogenin in the invertebrate chordate amphioxus. Developmental Biology. 226:18-33.   10.1006/dbio.2000.9810   AbstractWebsite

Amphioxus, as the closest living invertebrate relative of the vertebrates, can give insights into the evolutionary origin of the vertebrate body plan. Therefore, to investigate the evolution of genetic mechanisms for establishing and patterning the neuroectoderm, we cloned and determined the embryonic expression of two amphioxus transcription factors, AmphiSox1/2/3 and AmphiNeurogenin. These genes are the earliest known markers for presumptive neuroectoderm in amphioxus. By the early neurula stage, AmphiNeurogenin expression becomes restricted to two bilateral columns of segmentally arranged neural plate cells, which probably include precursors of motor neurons. This is the earliest indication of segmentation in the amphioxus nerve cord, Later, expression extends to dorsal cells in the nerve cord, which may include precursors of sensory neurons. By the midneurula, AmphiSox1/2/3 expression becomes limited to the dorsal part of the forming neural tube. These patterns resemble those of their vertebrate and Drosophila homologs. Taken together with the evolutionarily conserved expression of the dorsoventral patterning genes, BLP2/4 and chordin, in nonneural and neural ectoderm, respectively, of chordates and Drosophila, our results are consistent with the evolution of the chordate dorsal nerve cord and the insect ventral nerve cord from a longitudinal nerve cord in a common bilaterian ancestor. However, AmphiSox1/2/3 differs from its vertebrate homologs in not being expressed outside the CNS, suggesting that additional roles for this gene have evolved in connection with gene duplication in the vertebrate lineage. In contrast, expression in the midgut of AmphiNeurogenin together with the gene encoding the insulin-like peptide suggests that amphioxus may have homologs of vertebrate pancreatic islet cells, which express neurogenin3. In addition, AmphiNeurogenin, like its vertebrate and Drosophila homologs, is expressed in apparent precursors of epidermal chemosensory and possibly mechanosensory cells, suggesting a common origin for protostome and deuterostome epidermal sensory cells in the ancestral bilaterian. (C) 2000 Academic Press.

Holland, ND, Holland LZ, Davis CA, Honma Y.  1991.  Expression domains of engrailed gene in lamprey embryos. American Zoologist. 31:A46-A46. AbstractWebsite
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Holland, LZ, Holland ND.  1996.  Expression of AmphiHox-1 and AmphiPax-1 in amphioxus embryos treated with retinoic acid: Insights into evolution and patterning of the chordate nerve cord and pharynx. Development. 122:1829-1838. AbstractWebsite

Excess all-trans retinoic acid (RA) causes severe craniofacial malformations in vertebrate embryos: pharyngeal arches are fused or absent, and a rostrad expansion of Hoxb-1 expression in the hindbrain shows that anterior rhombomeres are homeotically respecified to a more posterior identity. As a corollary, neural crest migration into the pharyngeal arches is abnormal. We administered excess RA to developing amphioxus, the closest invertebrate relative of the vertebrates and thus a key organism for understanding evolution of the vertebrate body plan. In normal amphioxus, the nerve cord has only a slight anterior swelling, the cerebral vesicle, and apparently lacks migratory neural crest. Nevertheless, excess RA similarly affects amphioxus and vertebrates. The expression domain of AmphiHox-1 (homologous to mouse Hoxb-1) in the amphioxus nerve cord is also extended anteriorly. For both the amphioxus and mouse genes, excess RA causes either (1) continuous expression throughout the preotic hindbrain (mouse) and from the level of somite 7 to the anterior end of the nerve cord (amphioxus) or (2) discontinuous expression with a gap in rhombomere 3 (mouse) and a gap at the posterior end of the cerebral vesicle (amphioxus). A comparison of these expression patterns suggests that amphioxus has a homolog of the vertebrate hindbrain, both preotic and postotic. Although RA alters the expression of AmphiHox-1 expression in the amphioxus nerve cord, it does not alter the expression of AmphiHox-1 in presomitic mesoderm or of alkali myosin light chain (AmphiMlc-alk) in somites, and the axial musculature and notochord develop normally. The most striking morphogenetic effect of RA on amphioxus larvae is the failure of mouth and gill slits to form. In vertebrates effects of excess RA on pharyngeal development have been attributed solely to the abnormal migratory patterns of Hox-expressing cranial neural crest cells. This cannot be true for amphioxus because of the lack of migratory neural crest. Furthermore, expression of Hox genes in pharyngeal tissues of amphioxus has not yet been detected. However, the absence of gill slits in RA-treated amphioxus embryos correlates with an RA-induced failure of AmphiPax-1 to become down-regulated in regions of pharyngeal endoderm that would normally fuse with the overlying ectoderm. In vertebrates, RA might similarly act via Pax-1/9, also expressed in pharyngeal endoderm, to impair pharyngeal patterning.

Bardet, PL, Schubert M, Horard B, Holland LZ, Laudet V, Holland ND, Vanacker JM.  2005.  Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition. Evolution & Development. 7:223-233.   10.1111/j.1525-142X.2005.05025.x   AbstractWebsite

The evolutionary origin of vertebrate hindbrain segmentation is unclear since the amphioxus, the closest living invertebrate relative to the vertebrates, possesses a hindbrain homolog that displays no gross morphological segmentation. Three of the estrogen-receptor related (ERR) receptors are segmentally expressed in the zebrafish hindbrain, suggesting that their common ancestor was expressed in a similar, reiterated manner. We have also cloned and determined the developmental expression of the single homolog of the vertebrate ERR genes in the amphioxus (AmphiERR). This gene is also expressed in a segmented manner in a region considered homologous to the vertebrate hindbrain. In contrast to the expression of amphioxus islet (a LIM-homeobox gene that also labels motoneurons), AmphiERR expression persists longer in the hindbrain homolog and does not later extend to additional posterior cells. In addition, AmphiERR and one of its vertebrate homologs (ERR alpha) are expressed in the developing somitic musculature of amphioxus and zebrafish, respectively. Altogether, our results are consistent with fine structural evidence suggesting that the amphioxus hindbrain is segmented, and indicate that chordate ERR gene expression is a marker for both hindbrain and muscle segmentation. Furthermore, our data support an evolution model of chordate brain segmentation: originally, the program for anterior segmentation in the protochordate ancestors of the vertebrates resided in the developing axial mesoderm which imposed reiterated patterning on the adjacent neural tube; during early vertebrate evolution, this segmentation program was transferred to and controlled by the neural tube.

Beaster-Jones, L, Kaltenbach S, Koop D, Yuan SC, Chastain R, Holland LZ.  2008.  Expression of somite segmentation genes in amphioxus: a clock without a wavefront? Development Genes and Evolution. 218:599-611.   10.1007/s00427-008-0257-5   AbstractWebsite

In the basal chordate amphioxus (Branchiostoma), somites extend the full length of the body. The anteriormost somites segment during the gastrula and neurula stages from dorsolateral grooves of the archenteron. The remaining ones pinch off, one at a time, from the tail bud. These posterior somites appear to be homologous to those of vertebrates, even though the latter pinch off from the anterior end of bands of presomitic mesoderm rather than directly from the tail bud. To gain insights into the evolution of mesodermal segmentation in chordates, we determined the expression of ten genes in nascent amphioxus somites. Five (Uncx4.1, NeuroD/atonal-related, IrxA, Pcdh delta 2-17/18, and Hey1) are expressed in stripes in the dorsolateral mesoderm at the gastrula stage and in the tail bud while three (Paraxis, Lcx, and Axin) are expressed in the posterior mesendoderm at the gastrula and neurula stages and in the tail bud at later stages. Expression of two genes (Pbx and OligA) suggests roles in the anterior somites that may be unrelated to initial segmentation. Together with previous data, our results indicate that, with the exception that Engrailed is only segmentally expressed in the anterior somites, the genetic mechanisms controlling formation of both the anterior and posterior somites are probably largely identical. Thus, the fundamental pathways for mesodermal segmentation involving Notch-Delta, Wnt/beta-catenin, and Fgf signaling were already in place in the common ancestor of amphioxus and vertebrates although budding of somites from bands of presomitic mesoderm exhibiting waves of expression of Notch, Wnt, and Fgf target genes was likely a vertebrate novelty. Given the conservation of segmentation gene expression between amphioxus and vertebrate somites, we propose that the clock mechanism may have been established in the basal chordate, while the wavefront evolved later in the vertebrate lineage.

Lin, HC, Holland LZ, Holland ND.  2006.  Expression of the AmphiTcf gene in amphioxus: Insights into the evolution of the TCF/LEF gene family during vertebrate evolution. Developmental Dynamics. 235:3396-3403.   10.1002/dvdy.20971   AbstractWebsite

T-cell factor (TCF) and lymphoid enhancer factors (LEF) genes encode proteins that are transcription factors mediating beta-catenin/Wnt signaling. Whereas mammals have four such genes, the Florida amphioxus (Branchiostoma floridae) apparently has only one such gene (AmphiTcF). From cleavage through early gastrula, cytoplasmic maternal transcripts of this gene are localized toward the animal pole. In gastrulae, AmphiTcf expression begins in the mesendoderm. In neurulae, there is expression in the pharynx, hindgut, anterior notochord, somites, and at the anterior end of the neural plate. In early larvae, expression is detectable in the floor of the diencephalon, notochord, tail bud, forming somites, pharynx, and ciliated pit (a presumed homolog of the vertebrate adenohypophysis). Phylogenetic analysis of TCF/LEF proteins placed AmphiTcf as the sister group of a clade comprising vertebrate Tcf1, Lef1, Tcf3, and Tcf4. Comparison of developmental expression for amphioxus AmphiTcf and vertebrate TCF/LEF genes indicates that this gene family has undergone extensive subfunctionalization and neofunctionalization during vertebrate evolution.

Yu, J-K, Holland LZ.  2009.  Extraction of DNA from adult amphioxus tissue. . Cold Spring Harbor Protocols. 2009:pdb.prot5287(9)   10.1101/pdb.prot5287  
Yu, J-K, Holland LZ.  2009.  Extraction of RNA from amphioxus embryos or adult amphioxus tissues. . Cold Spring Harbor Protocols. 2009:pdb.prot5288. (9)   10.1101/pdb.prot5288.  
Yu, J-K, Holland LZ.  2009.  Extraction of RNA from small amounts of amphioxus embryos. Cold Spring Harbor Protocols. 2009:pdb.prot5289.   10.1101/pdb.prot5289  
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Holland, LZ, Gould-Somero M.  1982.  Fertilization Acid of Sea-Urchin Eggs - Evidence That It Is H+, Not Co2. Developmental Biology. 92:549-552.   10.1016/0012-1606(82)90200-7   Website
Gould-Somero, M, Holland LZ.  1975.  Fine-structural Investigation of Insemination Response in Urechis caupo . Developmental Biology . 46(2):358-369.   10.1016/0012-1606(75)90112-8  
Holland, ND, Holland LZ.  1991.  The Fine-Structure of the Growth Stage Oocytes of a Lancelet (= Amphioxus), Branchiostoma-Lanceolatum. Invertebrate Reproduction & Development. 19:107-122.   10.1080/07924259.1991.9672164   AbstractWebsite

Oocytes of the European lancelet (Branchiostoma lanceolatum) were fixed for transmission electron microscopy at Banyuls (French Mediterranean) in mid spring, which is just before the spawning season. Special attention is given to the growth stage (= diplotene) oocytes and to their relations with non-germinal cells of the ovary. At the time of year studied, the ovaries contain both relatively small (7-57-mu-m) and relatively large (97-127-mu-m) oocytes, but none of medium-size. In addition to the usual cell organelles (like free ribosomes, mitochondria, and endoplasmic reticulum), the oocytes include a number of more specialized structures. Nuage is present throughout the growth stage, both adjacent to the nucleus and scattered elsewhere in the cytoplasm. Other specialized structures do not begin to appear until the oocytes attain a certain diameter. The following structures are first detected at the following oocyte diameters: cortical granules, always in close association with Golgi complexes (20-mu-m); vacuoles containing presumed precursors of the vitelline layer (30-mu-m); yolk granules (35-mu-m); and a central vacuole within the nucleolus (50-mu-m). The cytoplasm of the largest oocytes includes a few annulate lamellae and some very unusual striated fibers resembling ciliary rootlets. These fibers, which are banded with a 70-nm periodicity (but are evidently not associated with centrioles), occur only at the animal pole of the oocyte, and their functional significance is unknown. The smaller oocytes have relatively smooth plasma membranes, except where endocytotic pits are abundant, whereas the larger oocytes bear abundant microvilli and are covered by a vitelline layer of dense, granular material. During oocyte growth, areas of contact between the oocytes and neighboring non-germinal cells shrink progressively. In the large oocytes, such contacts are limited to the animal pole, where a few processes from non-germinal cells pass through the vitelline layer and terminate on the oocyte plasma membrane at adhaerens type junctions (perhaps mixed with gap junctions). The possible functions and phylogenetic significance of such junctions are discussed.

Holland, ND, Campbell TG, Garey JR, Holland LZ, Wilson NG.  2009.  The Florida amphioxus (Cephalochordata) hosts larvae of the tapeworm Acanthobothrium brevissime: natural history, anatomy and taxonomic identification of the parasite. Acta Zoologica. 90:75-86.   10.1111/j.1463-6395.2008.00343.x   AbstractWebsite

Holland, N. D., Campbell, T. G., Garey, J. R., Holland, L. Z. and Wilson, N. G. 2009. The Florida amphioxus (Cephalochordata) hosts larvae of the tapeworm Acanthobothrium brevissime: natural history, anatomy and taxonomic identification of the parasite. - Acta Zoologica (Stockholm) 90: 75-86. Plerocercoid larvae of a tapeworm are frequently found in the hindgut lumen of the Florida amphioxus (Branchiostoma floridae) in central west Florida. About three-quarters of the adult amphioxus are parasitized. On average, each adult amphioxus hosts about five tapeworm larvae. The residence time of the parasites in the amphioxus gut appears to be in the order of several months, which is considerably shorter than the potential lifetime of the host. The living larvae range in length (when fully extended) from 300 to 850 mu m and are approximately cone-shaped, tapering to a point posteriorly and bearing a single large sucker anteriorly. Toward the anterior end of the body are four hookless bothridia, each indented by three loculi plus an inconspicuous accessory sucker. The larvae initiate the early stages of hook formation when they are cultured for a few days in urea-saline (mimicking the gut fluid of the definitive host, which is an elasmobranch). The tapeworm larvae are identifiable to genus and species on the basis of correspondences between their nuclear ribosomal DNA genes and those of adult specimens of Acanthobothrium brevissime recovered from the spiral valve of a stingray from the same environment.

Short, S, Kozmik Z, Holland LZ.  2012.  The Function and Developmental Expression of Alternatively Spliced Isoforms of Amphioxus and Xenopus laevis Pax2/5/8 Genes: Revealing Divergence at the Invertebrate to Vertebrate Transition . Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 318B(7):555-571.   10.1002/jez.b.22460  
Kreslova, J, Holland LZ, Schubert M, Burgtorf C, Benes V, Kozmik Z.  2002.  Functional equivalency of amphioxus and vertebrate Pax258 transcription factors suggests that the activation of mid-hindbrain specific genes in vertebrates occurs via the recruitment of Pax regulatory elements. Gene. 282:143-150.   10.1016/s0378-1119(01)00840-x   AbstractWebsite

Pax genes encode transcription factors that control key developmental decisions in various animal phyla. The Pax2/5/8 subfamily plays a key role in specification and/or maintenance of vertebrate mid-hindbrain boundary (MHB) region by directly regulating expression of other genes, most notably En2. In the invertebrate chordate amphioxus, expression of AmphiPax2/5/8 is found in many sites that are homologous to the regions of the vertebrate embryo expressing orthologous genes Pax2, Pax5 or Pax8. However, no co-expression of AmphiPax2/5/8 and AmphiEn is detected in the region of the neural tube that might correspond to the vertebrate MHB. Based on this observation and the absence of AmphiWnt expression in this region it appears that amphioxus does not have a MHB. Here we investigated the possibility that the AmphiPax2/5/8, as a key component of MHB development, has lost some of the properties of its vertebrate counterparts. We have analyzed both the DNA-binding and transactivation properties of AmphiPax2/5/8 as well as its ability to interact with the groucho co-repressor. In all these assays AmphiPax2/5/8 is indistinguishable from the human Pax5. In addition, we found two alternatively spliced AmphiPax2/5/8 isoforms that function similarly to the alternatively spliced isoforms of human Pax8. Analysis of the AmphiEn regulatory region provided no evidence for AmphiPax2/5/8 binding and transactivation. Therefore, in amphioxus, AmphiPax2/5/8, although capable of performing all the necessary functions has not been recruited for a developmental mechanism which usually sets up MHB development in vertebrates. (C) 2002 Elsevier Science B.V. All rights reserved.

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Castro, LFC, Rasmussen SLK, Holland PWH, Holland ND, Holland LZ.  2006.  A Gbx homeobox gene in amphioxus: Insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Developmental Biology. 295:40-51.   10.1016/j.ydbio.2006.03.003   AbstractWebsite

In the vertebrate central nervous system (CNS), mutual antagonism between posteriorly expressed Gbx2 and anteriorly expressed OtX2 positions the midbrain/hindbrain boundary (MHB), but does not induce MHB organizer genes such as En, Pax2/5/8 and Wnt1. In the CNS of the cephalochordate amphioxus, Otx is also expressed anteriorly, but En, Pax2/5/8 and Wnt1 are not expressed near the caudal limit of Otx, raising questions about the existence of an MHB organizer in amphioxus. To investigate the evolutionary origins of the MHB, we cloned the single amphioxus Gbx gene. Fluorescence in situ hybridization showed that, as in vertebrates, amphioxus Gbx and the Hox cluster are on the same chromosome. From analysis of linked genes, we argue that during evolution a single ancestral Gbx gene duplicated fourfold in vertebrates, with subsequent loss of two duplicates. Amphioxus Gbx is expressed in all germ layers in the posterior 75% of the embryo, and in the CNS, the Gbx and Otx domains abut at the boundary between the cerebral vesicle (forebrain/midbrain) and the hindbrain. Thus, the genetic machinery to position the MHB was present in the protochordate ancestors of the vertebrates, but is insufficient for induction of organizer genes. Comparison with hemichordates suggests that anterior Otx and posterior Gbx domains were probably overlapping in the ancestral deuterostome and came to abut at the MHB early in the chordate lineage before MHB organizer properties evolved. (c) 2006 Elsevier Inc. All rights reserved.

Holland, LZ, Short S.  2008.  Gene Duplication, Co-Option and Recruitment during the Origin of the Vertebrate Brain from the Invertebrate Chordate Brain. Brain Behavior and Evolution. 72:91-105.   10.1159/000151470   AbstractWebsite

The brain of the basal chordate amphioxus has been compared to the vertebrate diencephalic forebrain, midbrain, hindbrain and spinal cord on the basis of the cell architecture from serial electron micrographs and patterns of developmental gene expression. In addition, genes specifying the neural plate and neural plate border as well as Gbx and Otx, that position the midbrain/hindbrain boundary (MHB), are expressed in comparable patterns in amphioxus and vertebrates. However, migratory neural crest is lacking in amphioxus, and although it has homologs of the genes that specify neural crest, they are not expressed at the edges of the amphioxus neural plate. Similarly, amphioxus has the genes that specify organizer properties of the MHB, but they are not expressed at the Gbx/Otx boundary as in vertebrates. Thus, the genetic machinery that created migratory neural crest and an MHB organizer was present in the ancestral chordate, but only co-opted for these new roles in vertebrates. Analyses with the amphioxus genome project strongly support the idea of two rounds of whole genome duplication with subsequent gene losses in the vertebrate lineage. Duplicates of developmental genes were preferentially retained. Although some genes apparently acquired roles in neural crest prior to these genome duplications, other key genes (e. g., FoxD3 in neural crest and Wnt1 at the MHB) were recruited into the respective gene networks after one or both genome duplications, suggesting that such an expansion of the genetic toolkit was critical for the evolution of these structures. The toolkit has also increased by alternative splicing. Contrary to the general rule, for at least one gene family with key roles in neural crest and the MHB, namely Pax genes, alternative splicing has not decreased subsequent to gene duplication. Thus, vertebrates have a much larger number of proteins available for mediating new functions in these tissues. The creation of new splice forms typically changes protein structure more than evolution of the protein after gene duplication. The functions of particular isoforms of key proteins expressed at the MHB and in neural crest have only just begun to be studied. Their roles in modulating gene networks may turn out to rival gene duplication for facilitating the evolution of structures such as neural crest and the MHB. Copyright (c) 2008 S. Karger AG, Basel