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Holland, LZ.  2015.  Evolution of basal deuterostome nervous systems. Journal of Experimental Biology. 218:637-645.   10.1242/jeb.109108   AbstractWebsite

Understanding the evolution of deuterostome nervous systems has been complicated by the by the ambiguous phylogenetic position of the Xenocoelomorpha (Xenoturbellids, acoel flat worms, nemertodermatids), which has been placed either as basal bilaterians, basal deuterostomes or as a sister group to the hemichordate/echinoderm clade (Ambulacraria), which is a sister group of the Chordata. None of these groups has a single longitudinal nerve cord and a brain. A further complication is that echinoderm nerve cords are not likely to be evolutionarily related to the chordate central nervous system. For hemichordates, opinion is divided as to whether either one or none of the two nerve cords is homologous to the chordate nerve cord. In chordates, opposition by two secreted signaling proteins, bone morphogenetic protein (BMP) and Nodal, regulates partitioning of the ectoderm into central and peripheral nervous systems. Similarly, in echinoderm larvae, opposition between BMP and Nodal positions the ciliary band and regulates its extent. The apparent loss of this opposition in hemichordates is, therefore, compatible with the scenario, suggested by Dawydoff over 65 years ago, that a true centralized nervous system was lost in hemichordates.

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.

Holland, LZ.  2002.  Heads or tails? Amphioxus and the evolution of anterior-posterior patterning in deuterostomes Developmental Biology. 241:209-228.   10.1006/dbio.2001.0503   AbstractWebsite

In Xenopus, the canonical Wnt-signaling pathway acting through (beta-catenin functions both in establishing the dorso-ventral axis and in patterning the anterior-posterior axis. This pathway also acts in patterning the animal-vegetal axis in sea urchins. However, because sea urchin development is typically indirect, and adult sea urchins have pentamerous symmetry and lack a longitudinal nerve cord, it has not been clear how the roles of the canonical Wnt-signaling pathway in axial patterning in sea urchins and vertebrates are evolutionarily related. The developmental expression patterns of Notch, brachyury, caudal, and eight Wnt genes have now been determined for the invertebrate chordate amphioxus, which, like sea urchins, has an early embryo that gastrulates by invagination, but like vertebrates, has a later embryo with a dorsal hollow nerve cord that elongates posteriorly from a tail bud. Comparisons of amphioxus with other deuterostomes suggest that patterning of the ancestral deuterostome embryo along its anterior-posterior axis during the late blastula and subsequent stages involved a posterior signaling center including Writs, Notch, and transcription factors such as brachyury and caudal. In tunicate embryos, in which cell numbers are reduced and cell fates largely determined during cleavage stages, only vestiges of this signaling center are still apparent; these include localization of Wnt-5 mRNA to the posterior cytoplasm shortly after fertilization and localization of beta-catenin to vegetal nuclei during cleavage stages. Neither in tunicates nor in amphioxus is there any evidence that the canonical Wnt-signaling pathway functions in establishment of the dorso-ventral axis. Thus, roles for Wnt-signaling in dorso-ventral patterning of embryos may be a vertebrate innovation that arose in connection with the evolution of yolky eggs and gastrulation by extensive involution. (C) 2001 Elsevier Science.

Holland, LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK.  2013.  Evolution of bilaterian central nervous systems: a single origin? Evodevo. 4   10.1186/2041-9139-4-27   AbstractWebsite

The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the anterior/posterior axis, this ancestor used gene networks homologous to those patterning three organizing centers in the vertebrate brain: the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer, and subsequent evolution of the vertebrate brain involved elaboration of these ancestral signaling centers; however, all or part of these signaling centers were lost from the CNS of invertebrate chordates. The present review analyzes the evidence for and against these theories. The bulk of the evidence indicates that a CNS evolved just once - in the ancestral bilaterian. Importantly, in both protostomes and deuterostomes, the CNS represents a portion of a generally neurogenic ectoderm that is internalized and receives and integrates inputs from sensory cells in the remainder of the ectoderm. The expression patterns of genes involved in medio/lateral (dorso/ventral) patterning of the CNS are similar in protostomes and chordates; however, these genes are not similarly expressed in the ectoderm outside the CNS. Thus, their expression is a better criterion for CNS homologs than the expression of anterior/posterior patterning genes, many of which (for example, Hox genes) are similarly expressed both in the CNS and in the remainder of the ectoderm in many bilaterians. The evidence leaves hemichordates in an ambiguous position - either CNS centralization was lost to some extent at the base of the hemichordates, or even earlier, at the base of the hemichordates + echinoderms, or one of the two hemichordate nerve cords is homologous to the CNS of protostomes and chordates. In any event, the presence of part of the genetic machinery for the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer in invertebrate chordates together with similar morphology indicates that these organizers were present, at least in part, at the base of the chordates and were probably elaborated upon in the vertebrate lineage.

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.

Holland, LZ.  2000.  Body-plan evolution in the Bilateria: early antero-posterior patterning and the deuterostome-protostome dichotomy. Current Opinion in Genetics & Development. 10:434-442.   10.1016/s0959-437x(00)00109-x   AbstractWebsite

Recent molecular analyses reveal common themes in early antero-posterior patterning in the four major groups of invertebrate deuterostomes and vertebrates in spite of large differences in the mode of gastrulation. Comparisons with Drosophila and Cnidarians suggest a scheme for evolution of the Bilaterian body plan and emphasize the pressing need for similar studies in a wider variety of organisms, especially more basal protostomes.

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Onai, T, Yu JK, Blitz IL, Cho KWY, Holland LZ.  2010.  Opposing Nodal/Vg1 and BMP signals mediate axial patterning in embryos of the basal chordate amphioxus. Developmental Biology. 344:377-389.   10.1016/j.ydbio.2010.05.016   AbstractWebsite

The basal chordate amphioxus resembles vertebrates in having a dorsal, hollow nerve cord, a notochord and somites However, it lacks extensive gene duplications, and its embryos are small and gastrulate by simple invagination Here we demonstrate that Nodal/Vg1 signaling acts from early cleavage through the gastrula stage to specify and maintain dorsal/anterior development while, starting at the early gastrula stage, BMP signaling promotes ventral/posterior identity Knockdown and gain-of-function experiments show that these pathways act in opposition to one another Signaling by these pathways is modulated by dorsally and/or anteriorly expressed genes including Chordin, Cerberus, and Blimp1. Overexpression and/or reporter assays in Xenopus demonstrate that the functions of these proteins are conserved between amphioxus and vertebrates. Thus, a fundamental genetic mechanism for axial patterning involving opposing Nodal and BMP signaling is present in amphioxus and probably also in the common ancestor of amphioxus and vertebrates or even earlier in deuterostome evolution (C) 2010 Elsevier Inc. All rights reserved

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.