POU genes are expressed during the formation of individual ganglia of the cephalopod central nervous system

EvoDevo

Andreas Wanninger²  Bernard M Degnan¹  Carmel McDougall¹  Tim Wollesen² 

[1]School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia

[2]Department of Integrative Zoology, Faculty of Sciences, University of Vienna, Althanstr. 14, 1090 Vienna, Austria

关键词: ontogeny;    mollusk;    Lophotrochozoa;    invertebrate;    homeobox genes;    development;    evolution;    complex;    brain;   

Others  :  1093208
DOI  :  10.1186/2041-9139-5-41

 received in 2014-07-22, accepted in 2014-09-29,  发布年份 2014

【 摘 要 】

Background

Among the Lophotrochozoa, cephalopods possess the highest degree of central nervous system (CNS) centralization and complexity. Although the anatomy of the developing cephalopod CNS has been investigated, the developmental mechanisms underlying brain development and evolution are unknown. POU genes encode key transcription factors controlling nervous system development in a range of bilaterian species, including lophotrochozoans. In this study, we investigate the expression of POU genes during early development of the pygmy squid Idiosepius notoides and make comparisons with other bilaterians to reveal whether these genes have conserved or divergent roles during CNS development in this species.

Results

POU2, POU3, POU4 and POU6 orthologs were identified in transcriptomes derived from developmental stages and adult brain tissue of I. notoides. All four POU gene orthologs are expressed in different spatiotemporal combinations in the early embryo. Ino-POU2 is expressed in the gills and the palliovisceral, pedal, and optic ganglia of stage 19 to 20 embryos, whereas the cerebral and palliovisceral ganglia express Ino-POU3. Ino-POU4 is expressed in the optic and palliovisceral ganglia and the arms/intrabrachial ganglia of stage 19 to 20 individuals. Ino-POU6 is expressed in the palliovisceral ganglia during early development. In stage 25 embryos expression domains include the intrabrachial ganglia (Ino-POU3) and the pedal ganglia (Ino-POU6). All four POU genes are strongly expressed in large areas of the brain of stage 24 to 26 individuals. Expression could not be detected in late prehatching embryos (approximately stage 27 to 30).

Conclusions

The expression of four POU genes in unique spatiotemporal combinations during early neurogenesis and sensory organ development of I. notoides suggests that they fulfill distinct tasks during early brain development. Comparisons with other bilaterian species reveal that POU gene expression is associated with anteriormost neural structures, even between animals for which these structures are unlikely to be homologous. Within lophotrochozoans, POU3 and POU4 are the only two genes that have been comparatively investigated. Their expression patterns are broadly similar, indicating that the increased complexity of the cephalopod brain is likely due to other unknown factors.

【 授权许可】

   
2014 Wollesen et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Wells MJ: Octopus, Physiology and Behavior of an Advanced Invertebrate. London: Chapman and Hall; 1978.
• [2]Cummins SF, Boal JG, Buresch KC, Kuanpradit C, Sobhon P, Holm JB, Degnan BM, Nagle GT, Hanlon RT: Extreme aggression in male squid induced by a β-MSP-like pheromone. Curr Biol 2011, 21:322-327.
• [3]Romagny S, Darmaillacq AS, Guibé M, Bellanger C, Dickel L: Feel, smell and see in an egg: emergence of perception and learning in an immature invertebrate, the cuttlefish embryo. J Exp Biol 2012, 215:4125-4130.
• [4]Young JZ: The Anatomy of the Nervous System of Octopus vulgaris. Oxford: Clarendon; 1971.
• [5]Meister G: Organogenese von Loligo vulgaris LAM. Mollusca, Cephalopoda, Teuthoidea, Myopsida, Loliginidae. Zool Jb Anat 1972, 89:247-300.
• [6]Marquis VF: Die Embryonalentwicklung des Nervensystem von Octopus vulgaris Lam. (Cephalopoda, Octopoda), eine histologische Analyse. Verhandl Naturf Ges Basel 1989, 99:23-76.
• [7]Shigeno S, Tsuchiya K, Segawa S: Embryonic and paralarval development of the central nervous system of the loliginid squid Sepioteuthis lessoniana. J Comp Neurol 2001, 437:449-475.
• [8]Yamamoto M, Shimazaki Y, Shigeno S: Atlas of the embryonic brain in the pygmy squid, Idiosepius paradoxus. Zoolog Sci 2003, 20:163-179.
• [9]Shigeno S, Takenori S, Moritaki T, Kasugai T, Vecchione M, Agata K: Evolution of the cephalopod head complex by assembly of multiple molluscan body parts: Evidence from Nautilus embryonic development. J Morphol 2008, 69:1-17.
• [10]Nixon M, Young JZ: The Brains and Lives of Cephalopods. New York: Oxford University Press; 2003.
• [11]Baratte S, Bonnaud L: Evidence of early nervous differentiation and early catecholaminergic sensory system during Sepia officinalis embryogenesis. J Comp Neurol 2009, 517:539-549.
• [12]Wollesen T, Cummins SF, Degnan BM, Wanninger A: FMRFamide gene and peptide expression during central nervous system development of the cephalopod mollusk, Idiosepius notoides. Evol Dev 2010, 12:113-130.
• [13]Wollesen T, Degnan BM, Wanninger A: Expression of serotonin (5-HT) during CNS development of the cephalopod mollusk, Idiosepius notoides. Cell Tissue Res 2010, 342:161-718.
• [14]Aroua S, Andouche A, Martin M, Baratte S, Bonnaud L: FaRP cell distribution in the developing CNS suggests the involvement of FaRPs in all parts of the chromatophore control pathway in Sepia officinalis (Cephalopoda). Zoology 2011, 114:113-122.
• [15]Wollesen T, Nishiguchi MK, Seixas P, Degnan BM, Wanninger A: The VD1/RPD2 α1-neuropeptide is highly expressed in the brain of cephalopod mollusks. Cell Tissue Res 2012, 348:439-452.
• [16]Wollesen T, Sukhsangchan C, Seixas P, Nabhitabhata J, Wanninger A: Analysis of neurotransmitter distribution in brain development of benthic and pelagic octopod cephalopods. J Morphol 2012, 273:776-790.
• [17]Herr W, Sturm RA, Clerc RG, Corcoran LM, Baltimore D, Sharp PA, Ingraham HA, Rosenfeld MG, Finney M, Ruvkun G, Horvitz HR: The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products. Genes Dev 1988, 2:1513-1516.
• [18]Larroux C, Luke GN, Koopman P, Rokhsar DS, Shimeld SM, Degnan BM: Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 2008, 25:980-996.
• [19]Veenstra GJC, van der Vliet PC, Destrée OHJ: POU domain transcription factors in embryonic development. Mol Biol Rep 1997, 24:139-155.
• [20]Ryan AK, Rosenfeld MG: POU domain family values: flexibility, partnerships, and developmental codes. Genes Dev 1997, 11:1207-1225.
• [21]Orii H, Agata K, Watanabe K: POU-domain genes in planarian Dugesia japonica: the structure and expression. Biochem Biophys Res Commun 1993, 192:1395-1402.
• [22]Muñoz-Mármol AM, Casali A, Miralles A, Bueno D, Bayascas JR, Romero R, Saló E: Characterization of platyhelminth POU domain genes: ubiquitous and specific anterior nerve cell expression of different epitopes of GtPOU-1. Mech Dev 1998, 76:127-140.
• [23]Lozano V, Martínez-Escauriaza R, Bernardo-Castiñeira C, Mesías-Gansbiller C, Pazos AJ, Sánchez JL, Pérez-Parallé ML: A novel class of Pecten maximus POU gene, PmaPOU-IV: characterization and expression in adult tissues. J Exp Mar Biol Ecol 2014, 453:154-161.
• [24]O’Brien EK, Degnan BM: Expression of POU, Sox, and Pax genes in the brain ganglia of the tropical abalone Haliotis asinina. Mar Biotechnol 2000, 2:545-557.
• [25]O’Brien EK, Degnan BM: Pleiotropic developmental expression of HasPOU-III, a class III POU gene, in the gastropod Haliotis asinina. Mech Dev 2002, 114:129-132.
• [26]O’Brien EK, Degnan BM: Developmental expression of a class IV POU gene in the gastropod Haliotis asinina supports a conserved role in sensory cell development in bilaterians. Dev Genes Evol 2002, 212:394-398.
• [27]Backfisch B, Veedin Rajan VB, Fischer RM, Lohs C, Arboleda E, Tessmar-Raible K, Raible F: Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proc Natl Acad Sci U S A 2013, 110:193-198.
• [28]Bassaglia Y, Bekel T, Da Silva C, Poulain J, Andouche A, Navet S, Bonnaud L: ESTs library from embryonic stages reveals tubulin and reflectin diversity in Sepia officinalis (Mollusca-Cephalopoda). Gene 2012, 498:203-211.
• [29]Lemaire J: Table de developpement embryonnaire de Sepia officinalis. L. (Mollusque Céphalopode). Bull Soc Zool 1970, 95:773-782.
• [30]Ramachandra NB, Gates RD, Ladurner P, Jacobs DK, Hartenstein V: Embryonic development in the primitive bilaterian Neochildia fusca: normal morphogenesis and isolation of POU genes Brn-1 and Brn-3. Dev Genes Evol 2002, 212:55-69.
• [31]Hroudova M, Vojta P, Strnad H, Krejcik Z, Ridl J, Paces J, Vlcek C, Paces V: Diversity, phylogeny and expression patterns of Pou and Six homeodomain transcription factors in hydrozoan jellyfish Craspedacusta sowerbyi. PLoS One 2012, 7:e36420.
• [32]Nakanishi N, Yuan D, Hartenstein V, Jacobs DK: Evolutionary origin of rhopalia: insights from cellular-level analyses of Otx and POU expression patterns in the developing rhopalial nervous system. Evol Dev 2010, 12:404-415.
• [33]Treacy MN, Rosenfeld MG: Expression of a family of pou-domain protein regulatory genes during development of the central nervous system. Annu Rev Neurosci 1992, 15:139-165.
• [34]Dick T, Yang XH, Yeo SL, Chia W: Two closely linked Drosophila POU domain genes are expressed in neuroblasts and sensory elements. Proc Natl Acad Sci USA 1991, 88:7645-7649.
• [35]Anderson MG, Perkins GL, Chittick P, Shrigley RJ, Johnson WA: drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes Dev 1995, 9:123-137.
• [36]Finney M, Ruvkun G, Horvitz HR: The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors. Cell 1988, 55:757-769.
• [37]Finney M, Ruvkun G: The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 1990, 63:895-905.
• [38]Greenstein D, Hird S, Plasterk RH, Andachi Y, Kohara Y, Wang B, Finney M, Ruvkun G: Targeted mutations in the Caenorhabditis elegans POU homeobox gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. Genes Dev 1994, 8:1935-1948.
• [39]Candiani S, Pennati R, Oliveri D, Locascio A, Branno M, Castagnola P, Pestarino M, De Bernardi F: Ci-POU-IV expression identifies PNS neurons in embryos and larvae of the ascidian Ciona intestinalis. Dev Genes Evol 2005, 215:41-45.
• [40]Candiani S, Oliveri D, Parodi M, Bertini E, Pestarino M: Expression of AmphiPOU-IV in the developing neural tube and epidermal sensory neural precursors in amphioxus supports a conserved role of class IV POU genes in the sensory cells development. Dev Genes Evol 2006, 216:623-633.
• [41]Candiani S, Castagnola P, Oliveri D, Pestarino M: Cloning and developmental expression of AmphiBrn1/2/4, a POU III gene in amphioxus. Mech Dev 2002, 116:231-234.
• [42]Spaniol P, Bornmann C, Hauptmann G, Gerster T: Class III POU genes of zebrafish are predominantly expressed in the central nervous system. Nucleic Acids Res 1996, 24:4874-4881.
• [43]Agarwal VR, Sato SM: XLPOU 1 and XLPOU 2, two novel POU domain genes expressed in the dorsoanterior region of Xenopus embryos. Dev Biol 1991, 147:363-373.
• [44]Matsuo-Takasaki M, Lim JH, Sato SM: The POU domain gene, XlPOU 2 is an essential downstream determinant of neural induction. Mech Dev 1999, 89:75-85.
• [45]Baltzinger M, Relaix F, Remy P: Transcription of XLPOU3, a brain-specific gene, during Xenopus laevis early embryogenesis. Mech Dev 1996, 58:103-114.
• [46]Andersen B, Schonemann MD, Pearse RV II, Jenne K, Sugarman J, Rosenfeld MG: Brn-5 is a divergent POU domain factor highly expressed in layer IV of the neocortex. J Biol Chem 1993, 268:23390-23398.
• [47]Yamamoto M: Normal embryonic stages of the pygmy cuttlefish, Idiosepius pygmaeus paredoxus Ortmann. Zool Sci 1988, 5:989-998.
• [48]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 2011, 15:644-652.
• [49]Shigeno S, Yamamoto M: Organization of the nervous system in the pygmy cuttlefish, Idiosepius paradoxus Ortmann (Idiosepiidae, Cephalopoda). J Morphol 2002, 254:65-80.
• [50]Bürglin TR, Ruvkun G: Regulation of ectodermal and excretory function by the C. elegans POU homeobox gene ceh-6. Development 2001, 128:779-790.
• [51]Bullock TH: Mollusca: Cephalopoda. In Structure and Function in the Nervous Systems of Invertebrates. Edited by Bullock TH, Horridge GA. San Francisco: Freeman; 1965:1433-1515.
• [52]Lee PN, Callaerts P, de Couet HG, Martindale MQ: Cephalopod Hox genes and the origin of morphological novelties. Nature 2003, 424:1061-1065.
• [53]Samadi L, Steiner G: Involvement of Hox genes in shell morphogenesis in the encapsulated development of a top shell gastropod (Gibbula varia L.). Dev Genes Evol 2009, 219:523-530.
• [54]Samadi L, Steiner G: Expression of Hox genes during the larval development of the snail, Gibbula varia (L.) - further evidence of non-colinearity in molluscs. Dev Genes Evol 2010, 220:161-172.
• [55]Hashimoto N, Kurita Y, Wada H: Developmental role of dpp in the gastropod shell plate and co-option of the dpp signaling pathway in the evolution of the operculum. Dev Biol 2012, 366:367-373.
• [56]Reichert H: A tripartite organization of the urbilaterian brain: developmental genetic evidence from Drosophila. Brain Res Bull 2005, 66:491-494.
• [57]Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WE, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW: Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc Biol Sci 2009, 276:4261-4270.
• [58]Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SH, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G: Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.