Abstract
Lophotrochozoa is a sister taxon of Ecdysozoa in the Protostomia that includes mollusks, annelids, brachiopods, and platyhelminths. Recent studies have clarified the structure, expression, and roles of lophotrochozoan Zic family genes. Zic genes in oligochaete annelid Tubifex tubifex (freshwater sludge worm) and polychaete annelid Capitella teleta (bristle worm) are commonly expressed in a subset of developing brain and mesoderm derivatives. The latter includes the naïve mesoderm and the associated chaetal sacs in each body segment, although the segmentation processes differ between the two species. Furthermore, in brachiopod Terebratalia transversa (lamp shell), Zic is expressed in the anterior ectodermal domains and mesodermal derivatives, including those associated with the chaetal sacs. This result suggests the common involvement of Zic genes in the development of chaetae, a lophotrochozoan novelty acquired in the course of evolution. In addition, the highly simplified lophotrochozoan Dicyema acuticephalum (dicyemid mesozoan, a cephalopod endoparasite), which lost its gut, nervous system, and muscles during evolution, expresses its Zic genes in hermaphroditic gonads, highlighting the role of Zic genes in germ cell development. The role of Zic in head regeneration was revealed in studies on platyhelminth Schmidtea mediterranea (freshwater planarian). Planarian Zic expression was induced in a subpopulation of neoblasts that includes adult pluripotent stem cells. It is needed for head regeneration and production of an anterior signaling center. Suppression of Wnt-β-catenin signaling underlies Zic-mediated head regeneration, reminiscent of Wnt-β-catenin suppression by vertebrate Zic genes. Taken together, studies on the lophotrochozoan Zic genes are essential to understanding not only the roles of these genes in body plan evolution but also the molecular mechanism underlying adult stem cell regulation.
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References
Aruga J, Kamiya A, Takahashi H, Fujimi TJ, Shimizu Y, Ohkawa K, Yazawa S, Umesono Y, Noguchi H, Shimizu T, Saitou N, Mikoshiba K, Sakaki Y, Agata K, Toyoda A (2006) A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity. Genomics 87(6):783–792. https://doi.org/10.1016/j.ygeno.2006.02.011
Aruga J, Odaka YS, Kamiya A, Furuya H (2007) Dicyema Pax6 and Zic: tool-kit genes in a highly simplified bilaterian. BMC Evol Biol 7:201. https://doi.org/10.1186/1471-2148-7-201
Bao Y, Xu F, Shimeld SM (2017) Phylogenetics of lophotrochozoan bHLH genes and the evolution of lineage-specific gene duplicates. Genome Biol Evol. https://doi.org/10.1093/gbe/evx047
Biscotti MA, Canapa A, Forconi M, Barucca M (2014) Hox and ParaHox genes: a review on molluscs. Genesis 52(12):935–945. https://doi.org/10.1002/dvg.22839
Brown SA, Warburton D, Brown LY, Yu CY, Roeder ER, Stengel-Rutkowski S, Hennekam RC, Muenke M (1998) Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired. Nat Genet 20(2):180–183. https://doi.org/10.1038/2484
Dray N, Tessmar-Raible K, Le Gouar M, Vibert L, Christodoulou F, Schipany K, Guillou A, Zantke J, Snyman H, Behague J, Vervoort M, Arendt D, Balavoine G (2010) Hedgehog signaling regulates segment formation in the annelid Platynereis. Science 329(5989):339–342. https://doi.org/10.1126/science.1188913
Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sorensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452(7188):745–749. https://doi.org/10.1038/nature06614
Endo M, Sakai C, Shimizu T (2016) Embryonic expression patterns of Hox genes in the oligochaete annelid Tubifex tubifex. Gene Expr Patterns: GEP 22(1):1–14. https://doi.org/10.1016/j.gep.2016.09.002
Fujimi TJ, Hatayama M, Aruga J (2012) Xenopus Zic3 controls notochord and organizer development through suppression of the Wnt/beta-catenin signaling pathway. Dev Biol 361(2):220–231. https://doi.org/10.1016/j.ydbio.2011.10.026
Furuya H, Tsuneki K (2003) Biology of dicyemid mesozoans. Zool Sci 20(5):519–532. https://doi.org/10.2108/zsj.20.519
Garcia-Fernandez J, Baguna J, Salo E (1993) Genomic organization and expression of the planarian homeobox genes Dth-1 and Dth-2. Development 118(1):241–253
Goto A, Kitamura K, Shimizu T (1999) Cell lineage analysis of pattern formation in the Tubifex embryo. I Segmentation in the mesoderm. Int J Dev Biol 43(4):317–327
Gustus RM, Cloney RA (1972) Ultrastructural similarities between setae of brachiopods and polychaetes. Acta Zool 53:229–233
Halanych KM (2016) Diversification of Lophotrochozoa. In: Kliman RM (ed) Encyclopedia of evolutionary biology. Elsevier Science, Waltham, pp 405–408
Halanych KM, Bacheller JD, Aguinaldo AM, Liva SM, Hillis DM, Lake JA (1995) Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267(5204):1641–1643
Hayashi M, Shinozuka Y, Shigenobu S, Sato M, Sugimoto M, Ito S, Abe K, Kobayashi S (2017) Conserved role of Ovo in germline development in mouse and Drosophila. Sci Rep 7:40056. https://doi.org/10.1038/srep40056
Kenny NJ, Namigai EK, Dearden PK, Hui JH, Grande C, Shimeld SM (2014) The Lophotrochozoan TGF-beta signalling cassette – diversification and conservation in a key signalling pathway. Int J Dev Biol 58(6–8):533–549. https://doi.org/10.1387/ijdb.140080nk
Kobayashi M, Furuya H, Holland PW (1999) Dicyemids are higher animals. Nature 401(6755):762. https://doi.org/10.1038/44513
Kobayashi M, Furuya H, Wada H (2009) Molecular markers comparing the extremely simple body plan of dicyemids to that of lophotrochozoans: insight from the expression patterns of Hox, Otx, and brachyury. Evol Dev 11(5):582–589. https://doi.org/10.1111/j.1525-142X.2009.00364.x
Kuo JS, Patel M, Gamse J, Merzdorf C, Liu X, Apekin V, Sive H (1998) Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 125(15):2867–2882
Lapan SW, Reddien PW (2011) dlx and sp6-9 control optic cup regeneration in a prototypic eye. PLoS Genet 7(8):e1002226. https://doi.org/10.1371/journal.pgen.1002226
Layden MJ, Meyer NP, Pang K, Seaver EC, Martindale MQ (2010) Expression and phylogenetic analysis of the zic gene family in the evolution and development of metazoans. EvoDevo 1(1):12. https://doi.org/10.1186/2041-9139-1-12
Lee PN, Callaerts P, De Couet HG, Martindale MQ (2003) Cephalopod Hox genes and the origin of morphological novelties. Nature 424(6952):1061–1065. https://doi.org/10.1038/nature01872
Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94(5):465–477. https://doi.org/10.1038/sj.hdy.6800664
Mallatt J, Winchell CJ (2002) Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol 19(3):289–301
Meyer NP, Seaver EC (2009) Neurogenesis in an annelid: characterization of brain neural precursors in the polychaete Capitella sp. I. Dev Biol 335(1):237–252. https://doi.org/10.1016/j.ydbio.2009.06.017
Meyer NP, Boyle MJ, Martindale MQ, Seaver EC (2010) A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta. EvoDevo 1(1):8. https://doi.org/10.1186/2041-9139-1-8
Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K (2000) Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci U S A 97(4):1618–1623
Nakata K, Nagai T, Aruga J, Mikoshiba K (1997) Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci U S A 94(22):11980–11985
Newmark PA, Sanchez Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220(2):142–153. https://doi.org/10.1006/dbio.2000.9645
Ogino K, Tsuneki K, Furuya H (2010) Unique genome of dicyemid mesozoan: highly shortened spliceosomal introns in conservative exon/intron structure. Gene 449(1–2):70–76. https://doi.org/10.1016/j.gene.2009.09.002
Petersen CP, Reddien PW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332(6031):852–855. https://doi.org/10.1126/science.1202143
Pourebrahim R, Houtmeyers R, Ghogomu S, Janssens S, Thelie A, Tran HT, Langenberg T, Vleminckx K, Bellefroid E, Cassiman JJ, Tejpar S (2011) Transcription factor Zic2 inhibits Wnt/beta-catenin protein signaling. J Biol Chem 286(43):37732–37740. https://doi.org/10.1074/jbc.M111.242826
Ruppert EE, Fox RS, Barns RD (2004) Invertebrate zoology. Thomson-Brooks/Cole, Belmonte
Schiemann SM, Martin-Duran JM, Borve A, Vellutini BC, Passamaneck YJ, Hejnol A (2017) Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties. Proc Natl Acad Sci U S A 114(10):E1913–E1922. https://doi.org/10.1073/pnas.1614501114
Seaver EC (2014) Variation in spiralian development: insights from polychaetes. Int J Dev Biol 58(6–8):457–467. https://doi.org/10.1387/ijdb.140154es
Shimizu T (1982) Ooplasmic segregation in the Tubifex egg: mode of pole plasm accumulation and possible involvement of microfilaments. Wilehm Roux Arch Dev Biol 191(4):246–256. https://doi.org/10.1007/BF00848412
Steinmetz PR, Kostyuchenko RP, Fischer A, Arendt D (2011) The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol Dev 13(1):72–79. https://doi.org/10.1111/j.1525-142X.2010.00457.x
Struck TH, Wey-Fabrizius AR, Golombek A, Hering L, Weigert A, Bleidorn C, Klebow S, Iakovenko N, Hausdorf B, Petersen M, Kuck P, Herlyn H, Hankeln T (2014) Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of spiralia. Mol Biol Evol 31(7):1833–1849. https://doi.org/10.1093/molbev/msu143
Suzuki TG, Ogino K, Tsuneki K, Furuya H (2010) Phylogenetic analysis of dicyemid mesozoans (phylum Dicyemida) from innexin amino acid sequences: dicyemids are not related to Platyhelminthes. J Parasitol 96(3):614–625. https://doi.org/10.1645/GE-2305.1
Takahashi H, Shimizu T, Aruga J (2008) Expression pattern of annelid Zic in embryonic development of the oligochaete Tubifex tubifex. Dev Genes Evol 218(10):553–560. https://doi.org/10.1007/s00427-008-0252-x
Telford MJ (2006) Animal phylogeny. Curr Biol 16(23):R981–R985. https://doi.org/10.1016/j.cub.2006.10.048
Umesono Y, Watanabe K, Agata K (1997) A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain. Develop Growth Differ 39(6):723–727
Vasquez-Doorman C, Petersen CP (2014) zic-1 expression in planarian neoblasts after injury controls anterior pole regeneration. PLoS Genet 10(7):e1004452. https://doi.org/10.1371/journal.pgen.1004452
Vogg MC, Owlarn S, Perez Rico YA, Xie J, Suzuki Y, Gentile L, Wu W, Bartscherer K (2014) Stem cell-dependent formation of a functional anterior regeneration pole in planarians requires Zic and Forkhead transcription factors. Dev Biol 390(2):136–148. https://doi.org/10.1016/j.ydbio.2014.03.016
Wagner DE, Wang IE, Reddien PW (2011) Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332(6031):811–816. https://doi.org/10.1126/science.1203983
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Aruga, J. (2018). Lophotrochozoan Zic Genes. In: Aruga, J. (eds) Zic family. Advances in Experimental Medicine and Biology, vol 1046. Springer, Singapore. https://doi.org/10.1007/978-981-10-7311-3_5
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