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Unexpected Variation of Hox Genes' Homeodomains in Cephalopods

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Unexpected Variation of Hox Genes' Homeodomains in Cephalopods Molecular Phylogenetics and Evolution 40 (2006) 872–879 www.elsevier.com/locate/ympev Short communication Unexpected variation of Hox genes’ homeodomains in cephalopods Mathieu Pernice b, Jean S. Deutsch a, Aude Andouche b, Renata Boucher-Rodoni b, Laure Bonnaud b,¤ a Développement et Evolution, UMR 7622, CNRS et Université P et M Curie (Paris 6), Case 24, 9 quai St Bernard, 75252 Paris Cedex 05, France b Muséum National d’Histoire Naturelle, Département Milieux et Peuplements Aquatiques, Biologie des Organismes Marins et Ecosystèmes (UMR 5178 CNRS), 55 rue BuVon, CP51, 75005 Paris, France Received 2 September 2005; revised 24 February 2006; accepted 4 April 2006 Available online 26 April 2006 1. Introduction derived from the foot, a condensed nervous system associ- ated with several sensory structures and a speciWc direct Hox genes encode a family of transcription factors con- development. Among the eight recognised classes of extant taining a homeodomain-binding motif of 60 aminoacids molluscs six have been explored, few Hox genes have been (Gehring et al., 1994). They are extensively conserved identiWed and the number of genes in each cluster is far throughout Eu-metazoans (de Rosa et al., 1999). As they from being determined. The amount of available data have a role in the determination of the anterior-posterior recently increased with the characterisation of 11 Hox par- axis during development, they may give information about alogues in a bivalve, Pecten maximus, the highest number the history of bilaterian lineages (de Rosa et al., 1999; Bal- found at present (Canapa et al., 2005). In gastropods, con- avoine et al., 2002). In bilaterians, they are organised in sidered as the sister group of cephalopods, six Hox genes clusters, the last common ancestor of protostomes and have been characterised in Patella vulgata (de Rosa et al., deuterostomes having a cluster of 8–10 Hox genes (Cook 1999). In cephalopods, nine genes have been identiWed in et al., 2004). They appear to have undergone various inde- Euprymna scolopes, a sepiolid (Callaerts et al., 2002). The pendent duplications in the three clades Ecdysozoa, Lopho- aim of the present work was to compare Hox genes trochozoa and Deuterostomia. They present some between cephalopod species issued from the basal lineage conserved features that allowed determining lophotrocho- Nautiloidea ( D Tetrabranchiata) and those issued from the zoan signatures (de Rosa et al., 1999) but they have not derived lineage Coleoidea ( D Dibranchiata). In the present been used to distinguish between the main phyla within the study, we identiWed Hox genes in Sepia oYcinalis, a cuttle- Lophotrochozoa yet. Wsh belonging to the Decabrachia group like E. scolopes, To study Hox gene evolution it is crucial to include more and two nautiloids, Nautilus macromphalus and Nautilus sequences from lophotrochozoan species. Among them, the pompilius. The latter have preserved a number of ancestral phylum Mollusca is a Cambrian lineage showing a great morphological characters (e.g. external shell, numerous ten- diversity of body plans. It is considered as a monophyletic tacles without suckers) that were present in the Ammonites, group based on shared derived characters such as a foot, a a lineage close to extant nautiloids, which became extinct in radula, a mantle secreting the shell and a palleal cavity har- the Mesozoic era. We then compared our homeodomain bouring gills (Brusca and Brusca, 1990). sequences with those of available data from other molluscs Here we report the cloning of Hox genes from three and metazoans. cephalopod species. Cephalopods are distinct from other molluscs in numerous features. Cephalopoda is a mono- 2. Materials and methods phyletic group based on common derived characters (syna- pomorphies): a funnel and a brachial crown probably 2.1. Biological material and DNA extraction Nautilus pompilius was collected on the east coast of * Corresponding author. Fax: +33 1 40 79 57 34. Cebu island (Philippines), N. macromphalus in New Cale- E-mail address: [email protected] (L. Bonnaud). donia and S. oYcinalis oV the coast of Banyuls (France). 1055-7903/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2006.04.004 Table 1 Species name, taxonomic position and Hox genes analysed with their accession numbers in EMBL database (except ¤ in Swissprot database) Phylum Species Abr. Hox1 lab Hox2 pb Hox3 zen Hox4 Dfd Hox5 Scr Hox6 ftz/Lox5 Hox7 Antp Hox8 Ubx/ Hox9 Post1 Hox10 AbdB/Post2 Cdx cad Xlox Lox2 abdA/Lox4 Mollusca Cephalopoda Euprymna Esc AY052753 AY052755 AF127335 AY052756 AY052757 AY052758 AY052759 AY052760 AY052761 AF127341 scolopes Sepia Sof AJ937220 AJ937221 AJ937222 AJ937223 AM050636 AJ937224 oYcinalis Nautilus pompilius Npo AJ937214 AJ937215 AJ937216 AJ937219 AJ937217 Nautilus macromphalus Nma AM050632 AM050631 AM050634 AM050633 AM050630 Gastropoda M. Pernice Molecular etal./ Phylogenetics and Evolution40 (2006)872–879 Patella vulgata Pvu AF144666 AF144667 AF144669 AF144668 AF144670 AJ518062 AF144671 Ilyanassa obsoleta Iob AF118831 AY736276 AF118833 AF118832 AY736274 Haliotis asinina Has AF327746 AF327747 AF328863 Haliotis rufescens Hru X79374 X79372 X79377 AF275310 X79371 Bivalvia Yoldia eightsi Yei YEI534462 YEI534464 YEI534463 Ensis ensis Een EEN534448 EEN534449 EEN534450 Ruditapes philippinarum Rph TPH534460 TPH534459 TPH534461 Mytilus galloprovincialis Mga AJ629073 MGA534452 AJ629072 AJ629071 Pecten maximus Pma AJ876619 AJ876620 AJ876621 AJ876622 AJ876623 PMA534457 AJ876625 AJ876626 AJ876628 AJ876629 AJ575213 AJ876631 AJ876627 Annelida Polychaeta Nereis virens Nvi AF151663 AF151664 AF151665 AF151666 AF151667 AF151671 AF151668 AF151672 AF151673 AY117546 AF151669 Ctenodrilus serratus Cse U26539 U26625 U26626 U26627 U26629 U26628 U26635 U26633 Chaetopterus variopedatus Cva AF163856 AF163857 AF163858 CVU68284 AF163860 AF163859 Oligochaeta Eisenia andrei Ean AF400169 AF400165 AF400167 AF400164 AF400162 AF400166 AF400180 AF400181 AF00168 AF400163 AF400170 AF400177 AF400175 Perionyx excavatus Pex AY439315 AY439318 AY439319 AY439321 AY439323 AY439325 AY439324 AY439326 AY439328 AY439329 AY439316 AY439320 AY439327 AY439330 AY439317 AY439322 Stylaria lacustris Sla S76355 S76357 S76361 S76354 Hirudinida Hellobdella robusta Hro AF004386 AF004387 Hellobdella triserialis Htr AF006638 Y10888 AF137385 Hirudo medicinalis Hme AF017253 LO7298 S79240 X17566 Nemerta Anopla Lineus sanguineus Lsa Y16570 Y16571 Y16572 Y16573 Y16574 P81193¤ Ectoprocta Bugula turrita Btu AY497421 AY497422 AY497423 AY497425 AY497426 AY497424 Brachiopoda Lingula anatina Lan AF144672 AF144673 AF144674 AF144676 AF144675 AF144677 AF144679 AF144680 AF144678 Plathyhelmintha Polycelis nigra Pni L41847 L41850 L41852 L41854 L41849 L41848 L41851 L41846 (continued on next page) 873 874 M. Pernice et al. / Molecular Phylogenetics and Evolution 40 (2006) 872–879 Tissue samples (mantle and brain) were either frozen or preserved in alcohol and stored at 4 °C. DNA was extracted using the Dneasy Tissue Kit (Qiagen) and stored in aliquots at ¡20 °C. 2.2. PCR ampliWcation The central part of the homeodomain Hox gene was ampliWed by PCR from Nautilus and Sepia DNA using degenerate primers HoxA and HoxB (5Ј-GARY TNGARAARGARTT-3Ј corresponding to amino acids sequence ELEKEF and 3Ј-CKNCKRTTYTGRAACCA- 5Ј corresponding to WFQNRR, respectively). Lox2 was ampliWed in N. pompilius using HoxB and 5Ј-CCNAAYT CNTMNCARAGRAGRAAR-3Ј corresponding to amino Hox9 Post1 Hox10 AbdB/Post2 Cdx cad Xlox acids sequence PNS(S/Y)QRRK. Post2 homeodomain gene was ampliWed in S. oYcinalis only using 5Ј-MGNTAYCA RACNATGGTNYTNGARAAYGARTTY-3Ј corre- AJ007434 AJ007436 AF241657 X54453 AF017415 AJ005422 Lox2 abdA/Lox4 sponding to amino acids sequence RYQTMVLENEF and 3Ј-YTTYTTNCKYTTCATNCKNCKRTTYTGRAACC A-5Ј corresponding to amino acids sequence WFQNRR MKRKK. The reaction mixture contained 0.6 mol of each primer, 0.4 mmol of each deoxynucleoside triphosphate, 1X SuperTaq buVer and 2.5 U of SuperTaq polymerase 4 M20704 X76210 X51663 X03062 (ATGC) in a total volume of 50 l. PCR were conducted with an initial denaturing step (94 °C for 5 min) followed by 40 cycles at 94°C for 1min, 42°C for 2min and 72°C for 1 min and a Wnal elongation step at 72 °C for 7 min. PCR products of the expected size (150 bp) were puriWed with a Qiaquick gel extraction Kit (Qiagen). 2.3. Cloning and sequencing PuriWed PCR products were then cloned by insertion into the plasmid vector PCR 2.1 TOPO TA Cloning (Invitrogen) following the manufacturer’s instructions. Plasmids were pre- pared from pelleted cells with a QIAprep Miniprep kit (Qiagen). A total of 30 clones for each species, i.e. S. oYcinalis, N. pompilius and N. macromphalus, were sequenced. AF362086 AF3620892.4. AF362092 AF362094 Alignments and sequence comparison The central part of the homeodomain (aminoacids) Z35142 Z35143 X68045 AB028208sequences Z35145 Z35146 of Z35147lophotrochozoans, Z35148 Z35150 ecdysozoans AF052465 AF052464 and deuter- X ostomes were aligned using the Bioedit program. Species Alo AF071407 Csa AJ007431B Pma AJ005643Omy AJ007432 AJ007433 AJ007435 AAM19473 AY567802 CSA131397 Z35149 ScaSla U79468 AF148935 U79469 AF148936 AF148937 U79476 AF1011431 AF393441 AF393444 AF393443 AF393442 AF241662 AF241661 AF481736 AY779183 U79471 Tdo AF104008Tca AF104009 AF231104 AY456922 AF187068Dme X97819 X13103 AF104005 AF104010 X63728 AAB393556 AAK16422 AF321227 X05136 AF104003 AF104001 AY074761 X14475 X0085 AF104002 AF227923 AJ005421 Lfo AF362084 AF362085 AF362087 AF362088 AF362090 AF362091 AF362093name,
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