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Holland, LZ.  2015.  The origin and evolution of chordate nervous systems. Philosophical Transactions of the Royal Society B-Biological Sciences. 370   10.1098/rstb.2015.0048   AbstractWebsite

In the past 40 years, comparisons of developmental gene expression and mechanisms of development (evodevo) joined comparative morphology as tools for reconstructing long-extinct ancestral forms. Unfortunately, both approaches typically give congruent answers only with closely related organisms. Chordate nervous systems are good examples. Classical studies alone left open whether the vertebrate brain was a new structure or evolved from the anterior end of an ancestral nerve cord like that of modern amphioxus. Evodevo plus electron microscopy showed that the amphioxus brain has a diencephalic forebrain, small midbrain, hindbrain and spinal cord with parts of the genetic mechanisms for the midbrain/hindbrain boundary, zona limitans intrathalamica and neural crest. Evodevo also showed how extra genes resulting from whole-genome duplications in vertebrates facilitated evolution of new structures like neural crest. Understanding how the chordate central nervous system (CNS) evolved from that of the ancestral deuterostome has been truly challenging. The majority view is that this ancestor had a CNS with a brain that gave rise to the chordate CNS and, with loss of a discrete brain, to one of the two hemichordate nerve cords. The minority view is that this ancestor had no nerve cord; those in chordates and hemichordates evolved independently. New techniques such as phylostratigraphy may help resolve this conundrum.

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.

Onai, T, Lin HC, Schubert M, Koop D, Osborne PW, Alvarez S, Alvarez R, Holland ND, Holland LZ.  2009.  Retinoic acid and Wnt/beta-catenin have complementary roles in anterior/posterior patterning embryos of the basal chordate amphioxus. Developmental Biology. 332:223-233.   10.1016/j.ydbio.2009.05.571   AbstractWebsite

A role for Wnt/beta-catenin signaling in axial patterning has been demonstrated in animals as basal as cnidarians, while roles in axial patterning for retinoic acid (RA) probably evolved in the deuterostomes and may be chordate-specific. In vertebrates, these two pathways interact both directly and indirectly. To investigate the evolutionary origins of interactions between these two pathways, we manipulated Wnt/beta-catenin and RA signaling in the basal chordate amphioxus during the gastrula stage, which is the RA-sensitive period for anterior/posterior (A/P) patterning. The results show that Wnt/beta-catenin and RA signaling have distinctly different roles in patterning the A/P axis of the amphioxus gastrula. Wnt/beta-catenin specifies the identity of the ends of the embryo (high Wnt = posterior; low Wnt = anterior) but not intervening positions. Thus, Upregulation of Wnt/beta-catenin signaling induces ectopic expression of posterior markers at the anterior tip of the embryo. In contrast, RA specifies position along the A/P axis, but not the identity of the ends of the embryo-increased RA signaling strongly affects the domains of Hox expression along the A/P axis but has little or no effect on the expression of either anterior or posterior markers. Although the two pathways may both influence such things as specification of neuronal identity, interactions between them in A/P patterning appear to be minimal. (C) 2009 Elsevier Inc. All rights reserved.

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.

Schubert, M, Holland ND, Laudet V, Holland LZ.  2006.  A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Developmental Biology. 296:190-202.   10.1016/j.ydbio.2006.04.457   AbstractWebsite

Retinoic acid (RA) mediates both anterior/posterior patterning and neuronal specification in the vertebrate central nervous system (CNS). However, the molecular mechanisms downstream of RA are not well understood. To investigate these mechanisms, we used the invertebrate chordate amphioxus, in which the CNS, although containing only about 20,000 neurons in adults, like the vertebrate CNS, has a forebrain, midbrain, hindbrain, and spinal cord and is regionalized by RA-signaling. Here we show, first, that domains of genes with expression normally limited to diencephalon and midbrain are generally not affected by altered RA-signaling, second, that contrary to previous reports, not only Hox1, 3, and 4, but also Hox2 and Hox6 are collinearly expressed in the amphioxus CNS, and third, that collinear expression of all these Hox genes is controlled by RA-signaling. Finally, we show that Hox1 is involved in mediating both the role of RA-signaling in regionalization of the hindbrain and in specification of hindbrain motor neurons. Thus, morpholino knock-down of the single amphioxus Hox1 mimics the effects of treatments with an RA-antagonist. This analysis establishes RA-dependent regulation of collinear Hox expression as a feature common to the chordate CNS and indicates that the RA-Hox hierarchy functions both in proper anterior/posterior patterning of the developing CNS and in specification of neuronal identity. (c) 2006 Elsevier Inc. All rights reserved.

Holland, LZ, Panfilio KA, Chastain R, Schubert M, Holland ND.  2005.  Nuclear beta-catenin promotes non-neural ectoderm and posterior cell fates in amphioxus embryos. Developmental Dynamics. 233:1430-1443.   10.1002/dvdy.20473   AbstractWebsite

In vertebrate development, Wnt/beta-catenin signaling has an early role in specification of dorsal/anterior identity and a late one in posterior specification. To understand the evolution of these roles, we cloned beta-catenin from the invertebrate chordate amphioxus. The exon/intron organization of beta-catenin is highly conserved between amphioxus and other animals including a cnidarian, but not Drosophila. In development, amphioxus P-catenin is concentrated in all nuclei from the 16-cell stage until the onset of gastrulation when it becomes undetectable in presumptive mesendoderm. Li+, which up-regulates Wnt/beta-catenin signaling, had no detectable effect on axial patterning when applied before the late blastula stage, suggesting that a role for P-catenin in specification of dorsal/anterior identity may be a vertebrate innovation. From the mid-gastrula through the neurula stage, the highest levels of nuclear R-catenin are around the blastopore. In the early neurula, P-catenin is down-regulated in the neural plate, but remains high in adjacent non-neural ectoderm. Embryos treated with Li+ at the late blastula stage are markedly posteriorized and lack a neural plate. These results suggest that in amphioxus, as in vertebrates, downregulation of Wnt/beta-catenin signaling in the neural plate is necessary for maintenance of the neuroectoderm and that a major evolutionarily conserved role of Wnt/beta-catenin signaling is to specify posterior identity and pattern the anterior/posterior axis. (c) 2005 Wiley-Liss, Inc.

Gibson-Brown, JJ, Osoegawa K, McPherson JD, Waterston RH, de Jong PJ, Rokhsar DS, Holland LZ.  2003.  A proposal to sequence the amphioxus genome submitted to the joint genome institute of the US department of energy. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 300B:5-22.   10.1002/jez.b.00042   Website
Lacalli, TC, Holland LZ.  1998.  The developing dorsal ganglion of the salp Thalia democratica, and the nature of the ancestral chordate brain. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences. 353:1943-1967. AbstractWebsite

The development of the dorsal ganglion of the salp, Thalia democratica, is described from electron microscope reconstructions up to the stage of central neuropile formation. The central nervous system (CNS) rudiment is initially tubular with an open central canal. Early developmental events include: (i) the formation of a thick dorsal mantle of neuroblasts from which paired dorsal paraxial neuropiles arise; (ii) the differentiation of clusters of primary motor neurons along the ventral margin of the mantle; and (iii) the development from the latter of a series of peripheral nerves. The dorsal paraxial neuropiles ultimately connect to the large central neuropile, which develops later. Direct contact between neuroblasts and muscle appears to be involved in the development of some anterior nerves. The caudal nerves responsible for innervating more distant targets in the posterior part of the body develop without such contacts, which suggests that a different patterning mechanism may be employed in this part of the neuromuscular system. The results are compared with patterns of brain organization in other chordates. Because the salp CNS is symmetrical and generally less reduced than that of ascidian larvae, it is more easily compared with the CNS of amphioxus and vertebrates. The dorsal paraxial centres in the salp resemble the dorsolateral tectal centres in amphioxus in both position and organization; the central neuropile in salps likewise resembles the translumenal system in amphioxus. The neurons themselves are similar in that many of their neurites appear to be derived from the apical surface instead of the basal surface of the cell. Such neurons, with extensively developed apical neurites, may represent a new cell type that evolved in the earliest chordates in conjunction with the formation of translumenal or intralumenal integrative centres. In comparing the salp ganglion with vertebrates, we suggest that the main core of the ganglion is most like the mes-metencephalic region of the vertebrate brain, i.e. the zone occupied by the midbrain, isthmus, and anterior hindbrain. Counterparts of more anterior regions (forebrain) and posterior ones (segmented hindbrain) appear to be absent in salps, but are found in other tunicates, suggesting that evolution has acted quite differently on the main subdivisions of the CNS in different types of tunicates.

Kusakabe, R, Kusakabe T, Satoh N, Holland ND, Holland LZ.  1997.  Differential gene expression and intracellular mRNA localization of amphioxus actin isoforms throughout development: Implications for conserved mechanisms of chordate development. Development Genes and Evolution. 207:203-215.   10.1007/s004270050109   AbstractWebsite

The cephalochordate amphioxus is thought to share a common ancestor with vertebrates. To investigate the evolution of developmental mechanisms in chordates, cDNA clones for two amphioxus actin genes, BfCA1 and BfCA1, were isolated. BfCA1 encodes a cytoplasmic actin and is expressed in a variety of tissues during embryogenesis, beginning in the dorsolateral mesendoderm of the mid-gastrula. At the open neural plate stage, BfCA1 transcripts accumulate at the bases of the neuroectodermal cells adjacent the presumptive notochord. The 3' untranslated region of BfCA1 contains a sequence that is similar to the ''zipcode'' sequence of chicken beta-cytoplasmic actin gene, which is thought to direct intracellular mRNA localization. BfCA1 is also expressed in the notochord through the early larval stage, in the pharynx and in the somites at the onset of muscle-cell differentiation. BfMA1 is a vertebrate-type muscle actin gene, although the deduced amino acid sequence is fairly divergent. Transcripts first appear in the early neurula in the somites as they begin to differentiate into axial muscle cells and persist into the adult stage. In young adults, transcripts are localized in the Z-discs of the muscle cells. Smooth muscle cells around the gill slits and striated muscle cells in the pterygeal muscle also express BfMA1; however, there is never any detectable expression in the notochord, which is a modified striated muscle. Together with the alkali myosin light chain gene AmphiMLC-alk, the sequence and muscle-specific expression of BfMA1 implies a conserved mechanism of muscle cell differentiation between amphioxus and vertebrates. Evolution of the chordate actin gene family is discussed based on molecular phylogenetic analysis and expression patterns of amphioxus actin genes.

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.