Skip to main content
SpringerLink
Log in

Exploring developmental gene toolkit and associated pathways in a potential new model crustacean using transcriptomic analysis

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

The crustaceans are one of the largest, most diverse, and most successful groups of invertebrates. The diversity among the crustaceans is also reflected in embryonic development models. However, the molecular genetics that regulates embryonic development is not known in those crustaceans that have a short germ-band development with superficial cleavage, such as Macrobrachium olfersi. This species is a freshwater decapod and has great potential to become a model for developmental biology, as well as for evolutionary and environmental studies. To obtain sequence data of M. olfersi from an embryonic developmental perspective, we performed de novo assembly and annotation of the embryonic transcriptome. Using a pooling strategy of total RNA, paired-end Illumina sequencing, and assembly with multiple k-mers, a total of 25,636,097 pair reads were generated. In total, 99,751 unigenes were identified, and 20,893 of these returned a Blastx hit. KEGG pathway analysis mapped a total of 6866 unigenes related to 129 metabolic pathways. In general, 21,845 unigenes were assigned to gene ontology (GO) categories: molecular function (19,604), cellular components (10,254), and biological processes (13,841). Of these, 2142 unigenes were assigned to the developmental process category. More specifically, a total of 35 homologs of embryonic development toolkit genes were identified, which included maternal effect (one gene), gap (six), pair-rule (six), segment polarity (seven), Hox (four), Wnt (eight), and dorsoventral patterning genes (three). In addition, genes of developmental pathways were found, including TGF-β, Wnt, Notch, MAPK, Hedgehog, Jak-STAT, VEGF, and ecdysteroid-inducible nuclear receptors. RT-PCR analysis of eight genes related to embryonic development from gastrulation to late morphogenesis/organogenesis confirmed the applicability of the transcriptome analysis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abzhanov A, Kaufman TC (2000a) Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 210:493–506. doi:10.1007/s004270000090

    Article  CAS  Google Scholar 

  • Abzhanov A, Kaufman TC (2000b) Embryonic expression patterns of the Hox genes of the crayfish Procambarus clarkii (Crustacea, Decapoda). Evol Dev 2:271–283. doi:10.1046/j.1525-142x.2000.00066.x

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alwes F, Hinchen B, Extavour CG (2011) Patterns of cell lineage, movement, and migration from germ layer specification to gastrulation in the amphipod crustacean Parhyale hawaiensis. Dev Biol 359:110–123. doi:10.1016/j.ydbio.2011.07.029

    Article  CAS  PubMed  Google Scholar 

  • Biffis C, Alwes F, Scholtz G (2009) Cleavage and gastrulation of the dendrobranchiate shrimp Penaeus monodon (Crustacea, Malacostraca, Decapoda). Arthropod Struct Dev 38:527–540. doi:10.1016/j.asd.2009.06.003

    Article  PubMed  Google Scholar 

  • Brown S, Denell RE (1996) Segmentation and dorsoventral patterning in Tribolium. Semin Cell Dev Biol 7:553–560. doi:10.1006/scdb.1996.0069

    Article  Google Scholar 

  • Browne WE, Price AL, Gerberding M, Patel NH (2005) Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149. doi:10.1002/gene.20145

    Article  PubMed  Google Scholar 

  • Brusca RS, Brusca GJ (1990) Invertebrates. Sinauer Associates, Massachussets

    Google Scholar 

  • Clark MS, Thorne MAS, Toullec JY, Meng Y, Guan LL, Peck LS, Moore S (2011) Antarctic krill 454 pyrosequencing reveals chaperone and stress transcriptome. PLoS One 6:e15919. doi:10.1371/journal.pone.0015919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Cáceres CE, Carmel L, Casola C, Choi JH, Detter JC, Dong Q, Dusheyko S, Eads BD, Fröhlich T, Geiler-Samerotte KA, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kültz D, Laforsch C, Lindquist E, Lopez J, Manak JR, Muller J, Pangilinan J, Patwardhan RP, Pitluck S, Pritham EJ, Rechtsteiner A, Rho M, Rogozin IB, Sakarya O, Salamov A, Schaack S, Shapiro H, Shiga Y, Skalitzky C, Smith Z, Souvorov A, Sung W, Tang Z, Tsuchiya D, Tu H, Vos H, Wang M, Wolf YI, Yamagata H, Yamada T, Ye Y, Shaw JR, Andrews J, Crease TJ, Tang H, Lucas SM, Robertson HM, Bork P, Koonin EV, Zdobnov EM, Grigoriev IV, Lynch M, Boore JL (2011) The ecoresponsive genome of Daphnia pulex. Science 331:555–561. doi:10.1126/science.1197761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832. doi:10.1155/2008/619832

    Article  PubMed  Google Scholar 

  • Davis GK, Patel NH (2002) Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47:669–699. doi:10.1146/annurev.ento.47.091201.145251

    Article  CAS  PubMed  Google Scholar 

  • De Grave S, Chan T-Y, Chu KH, Yang C-H, Landeira JM (2015) Phylogenetics reveals the crustacean order Amphionidacea to be larval shrimps (Decapoda: Caridea). Sci Rep 5:17464. doi:10.1038/srep17464

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellis JR, Burke JM (2007) EST-SSRs as a resource for population genetic analyses. Heredity (Edinb) 99:125–132. doi:10.1038/sj.hdy.6801001

    Article  CAS  Google Scholar 

  • Gallardo-Escárate C, Valenzuela-Muñoz V, Nuñez-Acuña G (2014) RNA-seq analysis using de novo transcriptome assembly as a reference for the salmon louse Caligus rogercresseyi. PLoS One 9:e92239. doi:10.1371/journal.pone.0092239

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao J, Wang X, Zou Z, Jia X, Wang Y, Zhang Z (2014) Transcriptome analysis of the differences in gene expression between testis and ovary in green mud crab (Scylla paramamosain). BMC Genomics 15:585. doi:10.1186/1471-2164-15-585

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghaffari N, Sanchez-Flores A, Doan R, Garcia-Orozco KD, Chen PL, Ochoa-Leyva A, Lopez-Zavala AA, Carrasco JS, Hong C, Brieba LG, Rudiño-Piñera E, Blood PD, Sawyer JE, Johnson CD, Dindot SV, Sotelo-Mundo RR, Criscitiello MF (2014) Novel transcriptome assembly and improved annotation of the whiteleg shrimp (Litopenaeus vannamei), a dominant crustacean in global seafood mariculture. Sci Rep 4:7081. doi:10.1038/srep07081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • He L, Jiang H, Cao D, Liu L, Hu S, Wang Q (2013) Comparative transcriptome analysis of the accessory sex gland and testis from the chinese mitten crab (Eriocheir sinensis). PLoS One 8:e53915. doi:10.1371/journal.pone.0053915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L, Wang Q, Jin X, Wang Y, Chen L, Liu L, Wang Y (2012) Transcriptome profiling of testis during sexual maturation stages in Eriocheir sinensis using Illumina sequencing. PLoS One 7:e33735. doi:10.1371/journal.pone.0033735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertzler PL (2005) Cleavage and gastrulation in the shrimp Penaeus (litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct Dev 34:455–469. doi:10.1016/j.asd.2005.01.009

    Article  Google Scholar 

  • Holthuis LB (1952) A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. II. The subfamily Palaemoninae. Allan Hancock Found Publ Occas Pap 12:1–396

    Google Scholar 

  • Jin S, Fu H, Zhou Q, Sun S, Jiang S, Xiong Y, Gong Y, Qiao H, Zhang W (2013) Transcriptome analysis of androgenic gland for discovery of novel genes from the oriental river prawn, Macrobrachium nipponense, using Illumina Hiseq 2000. PLoS One 8:e76840. doi:10.1371/journal.pone.0076840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenny NJ, Sin YW, Shen X, Zhe Q, Wang W, Chan TF, Tobe SS, Shimeld SM, Chu KH, Hui JHL (2014) Genomic sequence and experimental tractability of a new decapod shrimp model, Neocaridina denticulata. Mar Drugs 12:1419–1437. doi:10.3390/md12031419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim WJ, Jung H, Gaffney PM (2011) Development of type I genetic markers from expressed sequence tags in highly polymorphic species. Mar Biotechnol (NY) 13:127–132. doi:10.1007/s10126-010-9280-4

    Article  CAS  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. doi:10.1186/gb-2009-10-3-r25

    Article  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404

    Article  CAS  PubMed  Google Scholar 

  • Lenz PH, Roncalli V, Hassett RP, Wu LS, Cieslak MC, Hartline DK, Christie AE (2014) De novo assembly of a transcriptome for Calanus finmarchicus (Crustacea, Copepoda)—the dominant zooplankter of the North Atlantic Ocean. PLoS One 9:e88589. doi:10.1371/journal.pone.0088589

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. doi:10.1093/bioinformatics/btp352

    Article  PubMed  PubMed Central  Google Scholar 

  • Li S, Zhang X, Sun Z, Li F, Xiang J (2013) Transcriptome analysis on chinese shrimp Fenneropenaeus chinensis during WSSV acute infection. PLoS One 8:e58627. doi:10.1371/journal.pone.0058627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. doi:10.1093/bioinformatics/btl158

    Article  CAS  PubMed  Google Scholar 

  • Lin F-J, Liu Y, Sha Z, Tsang LM, Chu KH, Chan T-Y, Liu R, Cui Z (2012) Evolution and phylogeny of the mud shrimps (Crustacea: Decapoda) revealed from complete mitochondrial genomes. BMC Genomics 13:631. doi:10.1186/1471-2164-13-631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv J, Liu P, Gao B, Wang Y, Wang Z, Chen P, Li J (2014) Transcriptome analysis of the Portunus trituberculatus: de novo assembly, growth-related gene identification and marker discovery. PLoS One 9:e94055. doi:10.1371/journal.pone.0094055

    Article  PubMed  PubMed Central  Google Scholar 

  • Lv J, Liu P, Wang Y, Gao B, Chen P, Li J (2013) Transcriptome analysis of Portunus trituberculatus in response to salinity stress provides insights into the molecular basis of osmoregulation. PLoS One 8:e82155. doi:10.1371/journal.pone.0082155

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch JA, El-Sherif E, Brown SJ (2012) Comparisons of the embryonic development of Drosophila, Nasonia, and Tribolium. Wiley Interdiscip Rev Dev Biol 1:16–39. doi:10.1002/wdev.3

    Article  CAS  PubMed  Google Scholar 

  • Ma K, Qiu G, Feng J, Li J (2012) Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7:e39727. doi:10.1371/journal.pone.0039727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mark M, Rijli FM, Chambon P (1997) Homeobox genes in embryogenesis and pathogenesis. Pediatr Res 42:421–429. doi:10.1203/00006450-199710000-00001

  • Martin JW, David GE (2001) An updated classification of the recent crustacea. Natural history museum of Los Angeles country, LA

  • Materna SC, Howard-Ashby M, Gray RF, Davidson EH (2006) The C2H2 zinc finger genes of Strongylocentrotus purpuratus and their expression in embryonic development. Dev Biol 300:108–120. doi:10.1016/j.ydbio.2006.08.032

  • McLaughlin PA (1980) Comparative morphology of recent Crustacea. W. H. Freeman and Company, San Francisco

    Google Scholar 

  • Meng XL, Liu P, Jia FL, Li J, Gao BQ (2015) De novo transcriptome analysis of Portunus trituberculatus ovary and testis by RNA-seq: identification of genes involved in gonadal development. PLoS One 10:e0128659. doi:10.1371/journal.pone.0128659

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller YMR, Ammar D, Nazari EM (2004) Embryonic development of four species of palaemonid prawns (Crustacea, Decapoda): pre-naupliar, naupliar and post-naupliar periods. Rev Bras Zool 21:27–32. doi:10.1590/S0101-81752004000100005

    Article  Google Scholar 

  • Müller YMR, Nazari EM, Simões-Costa MS (2003) Embryonic stages of the freshwater prawn Macrobrachium olfersi (Decapoda, Palaemonidae). J Crustac Biol 23:869–875. doi:10.1651/C-2408

    Article  Google Scholar 

  • Nazari EM, Ammar D, de Bem AF, Latini A, Müller YMR, Allodi S (2010) Effects of environmental and artificial UV-B radiation on freshwater prawn Macrobrachium olfersi embryos. Aquat Toxicol 98:25–33. doi:10.1016/j.aquatox.2010.01.010

    Article  CAS  PubMed  Google Scholar 

  • Nazari EM, Ammar D, Müller YMR, Allodi S (2013) Impacts of ultraviolet-B radiation on aquatic embryos. In: Allodi S, EM N (eds) Exploring themes on aquatic toxicology vol. 1. Research Signpost, Kerala, pp. 103–118

    Google Scholar 

  • Nazari EM, Simões-Costa MS, Müller YMR, Ammar D, Dias M (2003) Comparisons of fecundity, egg size, and egg mass volume of the freshwater prawns Macrobrachium potiuna and Macrobrachium olfersi (Decapoda, Palaemonidae). J Crustac Biol 23:862–868. doi:10.1651/C-2387

    Article  Google Scholar 

  • Perera OP, Shelby KS, Popham HJR, Gould F, Adang MJ, Jurat-Fuentes JL (2015) Generation of a transcriptome in a model lepidopteran pest, Heliothis virescens, using multiple sequencing strategies for profiling midgut gene expression. PLoS One 10:e0128563. doi:10.1371/journal.pone.0128563

  • Pires-da Silva A, Sommer RJ (2003) The evolution of signaling pathways in animal development. Nat Rev Genet 4:39–49. doi:10.1038/nrg977

    Article  CAS  Google Scholar 

  • Rao R, Bing Zhu Y, Alinejad T, Tiruvayipati S, Lin Thong K, Wang J, Bhassu S (2015) RNA-seq analysis of Macrobrachium rosenbergii hepatopancreas in response to Vibrio parahaemolyticus infection. Gut Pathog 7:6. doi:10.1186/s13099-015-0052-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz MH, Zerbino DR, Vingron M, Birney E (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086–1092. doi:10.1093/bioinformatics/bts094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sengupta S, Bolin JM, Ruotti V, Nguyen BK, Thomson JA, Elwell AL, Stewart R (2011) Single read and paired end mRNA-seq Illumina libraries from 10 nanograms total RNA. J Vis Exp 56:e3340. doi:10.3791/3340

    PubMed  Google Scholar 

  • Shigenobu S, Bickel RD, Brisson JA, Butts T, Chang CC, Christiaens O, Davis GK, Duncan EJ, Ferrier DEK, Iga M, Janssen R, Lin GW, Lu HL, McGregor AP, Miura T, Smagghe G, Smith JM, Van Der Zee M, Velarde RA, Wilson MJ, Dearden PK, Stern DL (2010) Comprehensive survey of developmental genes in the pea aphid, Acyrthosiphon pisum: Frequent lineage-specific duplications and losses of developmental genes. Insect Mol Biol 19:47–62. doi:10.1111/j.1365-2583.2009.00944.x

  • Simões-Costa MS, Pacheco C, Nazari EM, Müller YMR, Ammar D (2005) Estagiamento de embriões de Macrobrachium olfersi (Wiegman) (Crustacea, Palaemonidae) através de critérios morfológicos nos dias embrionários. Rev Bras Zool 22:501–508. doi:10.1590/S0101-81752005000200029

    Article  Google Scholar 

  • Sookruksawong S, Sun F, Liu Z, Tassanakajon A (2013) RNA-seq analysis reveals genes associated with resistance to Taura syndrome virus (TSV) in the Pacific white shrimp Litopenaeus vannamei. Dev Comp Immunol 41:523–533. doi:10.1016/j.dci.2013.07.020

    Article  CAS  PubMed  Google Scholar 

  • Surget-Groba Y, Montoya-Burgos JI (2010) Optimization of de novo transcriptome assembly from next-generation sequencing data. Genome Res 20:1432–1440. doi:10.1101/gr.103846.109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, Chen Z, Childers CP, Glastad KM, Gokhale K, Gowin J, Gronenberg W, Hermansen RA, Hu H, Hunt BG, Huylmans AK, Khalil SMS, Mitchell RD, Munoz-Torres MC, Mustard JA, Pan H, Reese JT, Scharf ME, Sun F, Vogel H, Xiao J, Yang W, Yang Z, Yang Z, Zhou J, Zhu J, Brent CS, Elsik CG, Goodisman MAD, Liberles DA, Roe RM, Vargo EL, Vilcinskas A, Wang J, Bornberg-Bauer E, Korb J, Zhang G, Liebig J (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun 5:3636. doi:10.1038/ncomms4636

    Article  CAS  PubMed  Google Scholar 

  • Wägele JW (1989) On the influence of fishes on the evolution of benthic crustaceans. Z Zool Syst Evol 27:297–309. doi:10.1111/j.1439-0469.1989.tb00352.x

    Article  Google Scholar 

  • Waloszek D (2003) The ‘Orsten’ window—a three-dimensionally preserved upper Cambrian meiofauna and its contribution to our understanding of the evolution of Arthropoda. Paleontol Res 7(1):71–88. doi:10.2517/prpsj.7.71

    Article  Google Scholar 

  • Waloszek D, Müller KJ (1998) Cambrian “Orsten”-type arthropods and the phylogeny of Crustacea. In: Fortey RA, Thomas RH (eds) Arthropod relationships, Systematics association special volume series, vol 55. Chapman & Hall, London, pp. 139–153

    Chapter  Google Scholar 

  • Wei J, Zhang X, Yu Y, Huang H, Li F, Xiang J (2014) Comparative transcriptomic characterization of the early development in Pacific white shrimp Litopenaeus vannamei. PLoS One 9:e106201. doi:10.1371/journal.pone.0106201

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolff C, Scholtz G (2002) Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev Biol 250:44–58. doi:10.1006/dbio.2002.0789

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Sun F, Yang Z, Li H (2014) Comprehensive transcriptome study to develop molecular resources of the copepod Calanus sinicus for their potential ecological applications. Biomed Res Int 2014:1–12. doi:10.1155/2014/493825

    Google Scholar 

  • Yu Y, Zhang X, Yuan J, Li F, Chen X, Zhao Y, Huang L, Zheng H, Xiang J (2015) Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific white shrimp Litopenaeus vannamei. Sci Rep 5:15612. doi:10.1038/srep15612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan J-B, Zhang X-J, Liu C-Z, Wei J-K, Li F-H, Xiang J-H (2013) Horizontally transferred genes in the genome of Pacific white shrimp, Litopenaeus vannamei. BMC Evol Biol 13:165. doi:10.1186/1471-2148-13-165

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng D, Chen X, Xie D, Zhao Y, Yang C, Li Y, Ma N, Peng M, Yang Q, Liao Z, Wang H, Chen X (2013) Transcriptome analysis of Pacific white shrimp (Litopenaeus vannamei) hepatopancreas in response to Taura syndrome virus (TSV) experimental infection. PLoS One 8:e57515. doi:10.1186/1471-2164-12-581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng V, Villanueva KE, Ewen-Campen BS, Alwes F, Browne WE, Extavour CG (2011) De novo assembly and characterization of a maternal and developmental transcriptome for the emerging model crustacean Parhyale hawaiensis. BMC Genomics 12:581. doi:10.1371/journal.pone.0057515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeni EC, Ammar D, Leal ML, da Silva HS, Allodi S, Muller YMR, Nazari EM (2015) Light-mediated DNA repair prevents UVB-induced cell cycle arrest in embryos of the crustacean Macrobrachium olfersi. Photochem Photobiol 91:869–878. doi:10.1111/php.12457

    Article  CAS  PubMed  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. doi:10.1101/gr.074492.107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Zhang X, Liu C, Huan P, Li F, Xiang J, Huang C (2012) BAC end sequencing of Pacific white shrimp Litopenaeus vannamei: a glimpse into the genome of Penaeid shrimp. Chin J Oceanol Limnol 30:456–470. doi:10.1007/s00343-012-1159-y

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, 425/2010) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, 475788/2011-7).

Author information

Authors and Affiliations

  1. Departamento de Biologia Celular, Embriologia e Genética, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil

    Michael L. Jaramillo, Christian L. B. Paese, Evelise M. Nazari, Dib Ammar & Yara Maria Rauh Müller

  2. PPGGBM, Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Frank Guzman

  3. Departamento de Biofisica, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Rogerio Margis

Authors
  1. Michael L. Jaramillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frank Guzman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian L. B. Paese
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rogerio Margis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Evelise M. Nazari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dib Ammar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yara Maria Rauh Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yara Maria Rauh Müller.

Ethics declarations

The procedures for collecting of M. olfersi were approved by the National Environmental Agency (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, number 15294-1/IBAMA/2008).

Additional information

Communicated by Siegfried Roth

Dib Ammar and Yara M. R. Müller contributed equally to this work.

Electronic supplementary material

Table S1

Primer sequences of genes related to embryonic development of M. olfersi employed in RT-PCR. (DOCX 15 kb)

Table S2

The 60 most frequently occurring InterPro domains/families in M. olfersi unigenes. (XLSX 12 kb)

Table S3

Genes related to embryonic development identified in the transcriptome of M. olfersi. (XLSX 19 kb)

Table S4

Developmental pathways identified in the transcriptome of M. olfersi embryos. (XLSX 21 kb)

Table S5

Summary of SSRs in the transcriptome of M. olfersi embryos. (DOCX 18 kb)

Fig. S1

Alignment of eight genes related to embryonic development from arthropods species using ClustalW. The colors indicate the degree of conservation of the different amino acids. Species and accession numbers are indicated (left). The homeobox domain of the genes is denoted by the box in the alignment. (PDF 377 kb)

Fig. S2

Neighbor-joining (NJ) trees from an alignment of eight genes related to embryonic development from arthropods species. NJ trees under the TN93 + G (Ubx, Antp, Scr and En), Tajime-Nei + G (Ftz) and JTT + G (Eve) models and analysis of 1000 bootstrap replicates and the Poisson correction model for MEGA5 program were used. Orthologs of these genes from Onychophora species were used to root the tree. Hox genes of Neocaridina were obtained from published paper by Kenny et al. 2014. The scale bar shows the number of substitutions per site. (PDF 95 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaramillo, M.L., Guzman, F., Paese, C.L.B. et al. Exploring developmental gene toolkit and associated pathways in a potential new model crustacean using transcriptomic analysis. Dev Genes Evol 226, 325–337 (2016). https://doi.org/10.1007/s00427-016-0551-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-016-0551-6

Keywords

Search

Navigation