期刊论文详细信息
BMC Genomics
Differential gene expression between functionally specialized polyps of the colonial hydrozoan Hydractinia symbiolongicarpus (Phylum Cnidaria)
Paulyn Cartwright1  Mariya Shcheglovitova2  Steven M Sanders1 
[1] Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, USA;Department of Biological Sciences, George Washington University, Washington, DC 20052, USA
关键词: Annotation;    Transcriptome assembly;    Differential expression;    Polymorphism;    RNA-Seq;    Hydractinia symbiolongicarpus;   
Others  :  1217179
DOI  :  10.1186/1471-2164-15-406
 received in 2014-02-24, accepted in 2014-05-20,  发布年份 2014
PDF
【 摘 要 】

Background

A colony of the hydrozoan Hydractinia symbiolongicarpus comprises genetically identical yet morphologically distinct and functionally specialized polyp types. The main labor divisions are between feeding, reproduction and defense. In H. symbiolongicarpus, the feeding polyp (called a gastrozooid) has elongated tentacles and a mouth, which are absent in the reproductive polyp (gonozooid) and defensive polyp (dactylozooid). Instead, the dactylozooid has an extended body column with an abundance of stinging cells (nematocysts) and the gonozooid bears gonophores on its body column. Morphological differences between polyp types can be attributed to simple changes in their axial patterning during development, and it has long been hypothesized that these specialized polyps arose through evolutionary alterations in oral-aboral patterning of the ancestral gastrozooid.

Results

An assembly of 66,508 transcripts (>200 bp) were generated using short-read Illumina RNA-Seq libraries constructed from feeding, reproductive, and defensive polyps of H. symbiolongicarpus. Using several different annotation methods, approximately 54% of the transcripts were annotated. Differential expression analyses were conducted between these three polyp types to isolate genes that may be involved in functional, histological, and pattering differences between polyp types. Nearly 7 K transcripts were differentially expressed in a polyp-specific manner, including members of the homeodomain, myosin, toxin and BMP gene families. We report the spatial expression of a subset of these polyp-specific transcripts to validate our differential expression analyses.

Conclusions

While potentially originating through simple changes in patterning, polymorphic polyps in Hydractinia are the result of differentially expressed functional, structural, and patterning genes.

The differentially expressed genes identified in our study provide a starting point for future investigations of the developmental patterning and functional differences that are displayed in the different polyp types that confer a division of labor within a colony of H. symbiolongicarpus.

【 授权许可】

   
2014 Sanders et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150705020238536.pdf 3143KB PDF download
Figure 7. 43KB Image download
Figure 6. 172KB Image download
Figure 5. 59KB Image download
Figure 4. 106KB Image download
Figure 3. 58KB Image download
Figure 2. 59KB Image download
Figure 1. 68KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】
  • [1]Muller W: Experimentelle Untersuchungen Über Stockentwicklung, Polypendifferenzierung, und sexualchimären bei Hydractinia echinata. Wilhelm Roux’ Arch Entwicklungsmech Org 1964, 155:181-268.
  • [2]Berrill NJ: Growth and form in gymnoblastic hydroids; polymorphism within the Hydractiniidae. J Morph 1953, 92:241-272.
  • [3]Burnett AL, Sindelar W, Diehl N: An examination of polymorphism in the hydroid Hydractinia echinata. J Mar Biol Assoc UK 1967, 47:645-658.
  • [4]Cartwright P, Nawrocki AM: Character evolution in Hydrozoa (phylum Cnidaria). J Integ Comp Biol 2010, 50:456-472.
  • [5]Agassiz A: North American Acalephae. Welsh, Bigelow, Cambridge, U.K: University Press; 1865.
  • [6]Haeckel E: Report on the Siphonophorae Collected by H. M. S. Challenger During the Years 1873–76. London: The Challenger Reports; 1888.
  • [7]Huxley TH: The Oceanic Hydrozoa: A Description of the Calycophoridae and Physophoridae Observed During the Voyage of the H. M. S. “Rattlesnake” in the years 1846–1850: With a General Introduction. London: Ray Society; 1859.
  • [8]Cartwright P, Bowsher J, Buss LW: Expression of the HOX type gene, Cnox-2, and the division of labor in a colonial hydroid. Proc Natl Acad Sci USA 1999, 96:2183-2186.
  • [9]Mokady O, Dick MH, Lackschewitz D, Schierwater B, Buss LW: Over one-half billion years of head conservation? Expression of an ems class gene in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa). Proc Natl Acad Sci USA 1998, 95:3673-3678.
  • [10]Siebert S, Robinson MD, Tintori SC, Goetz F, Helm RR, Smith SA, Shaner N, Haddock SHD, Dunn CW: Differential gene expression in the siphonophore Nanomia bijuga (Cnidaria) assessed with multiple next-generation sequencing workflows. PLoS One 2011, 6:e22953.
  • [11]Hao DC, Ge G, Xiao P, Zhang Y, Yang L: The first insight into the tissue specific Taxus transcriptome via Illumina second generation sequencing. PLoS One 2011, 6:e21220.
  • [12]Helm RR, Siebert S, Tulin S, Smith J, Dunn CW: Characterization of differential transcript abundance through time during Nematostella vectensis development. BMC Genomics 2013, 14:266. BioMed Central Full Text
  • [13]Lui S, Lin L, Jiang P, Wang D, Xing Y: A comparison of RNA-Seq and high-density exon array for detecting differential expression between closely related species. Nucl Acids Res 2010, 39:578-588.
  • [14]Kanska J, Frank U: Novels roles for Nanos in neural cell fate determination revealed by studies in a cnidarian. J Cell Science 2013. doi:10.1242/ jcs.127233
  • [15]Rebscher N, Volk C, Teo R, Plickert G: The germ plasm component vasa allows tracing of the interstitial stem cells in the Cnidarian Hydractinia echinata. Dev Dynamics 2008, 237:1736-1745.
  • [16]Seipel K, Yanze N, Schmid V: The germ line and somatic stem cell gene Cniwi in the jellyfish Podocoryne carnea. J Dev Biol 2004, 48:1-7.
  • [17]Bebenek HG, Gates RD, Morris J, Hartenstein V, Jacobs DK: sine oculis in basal Metazoa. Dev Genes Evol 2004, 214:342-351.
  • [18]Martindale MQ, Pang K, Finnerty JR: Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Dev 2004, 131:2463-2474.
  • [19]Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS: Early evolution of the LIM homeobox gene family. BMC Biol 2010, 8:4. BioMed Central Full Text
  • [20]Mazza ME, Pang K, Reitzel AM, Martindale MQ, Finnerty JR: A conserved cluster of three PRD-class homeobox genes (homeobrain, rx and orthopedia) in the Cnidaria and Protostomia. EvoDevo 2010, 1:3. BioMed Central Full Text
  • [21]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.
  • [22]Stierwald M, Yanze N, Bamert RP, Kammermeier L, Schmid V: The Sine oculis/Six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration. Dev Biol 2004, 274:70-81.
  • [23]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.
  • [24]Millane RC, Kanska J, Duffy DJ, Seoighe C, Cunningham S, Plickert G, Frank U: Induced stem cell neoplasia in a cnidarian by ectopic expression of a POU domain transcription factor. Dev 2011, 138:2429-2439.
  • [25]Gröger H, Callaerts P, Gehring WJ, Schmid V: Gene duplication and recruitment of a specific tropomyosin into striated muscle cells in the jellyfish Podocoryne carnea. J Exp Zoo 1999, 285:378-386.
  • [26]Baader CD, Schmid V, Schuchert P: Characterization of a tropomyosin cDNA from the hydrozoan Podocoryne carnea. Fed Eur Biochem Soc 1993, 328:63-66.
  • [27]Miglietta MP, Cunningham CW: Evolution of life cycle, colony morphology, and host specificity in the family Hydractiniidae (Hydrozoa, Cnidaria). Evol 2012. doi:10.1111/j.1558-5646.2012.01717.x
  • [28]Bouillon J, Medel D, Cantero ALP: The taxonomic status of the genus Stylactaria Stechow, 1921 (Hydroidomedusae, Anthomedusae, Hydractiniidae), with the description of a new species. Sci 1997, 61:471-486.
  • [29]Boero F, Sará M: Motile sexual stages and evolution of Leptomedusae (Cnidaria). Boll Zool 1987, 54:131-139.
  • [30]Frazão B, Vasconcelos V, Antunes A: Sea anemone (Cnidaria, Anthozoa, Actiniaria) toxins: an overview. Mar Drugs 2012, 10:1812-1851.
  • [31]Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K: Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatching enzyme of Oryzias latipes, and concurrent expression of their mRNAs during development. Dev Biol 1992, 153:250-258.
  • [32]Hishida R, Ishihara T, Kondo K, Katsura I: hch-1, a gene required for normal hatching and normal migration of a neuroblast in C. elegans, encodes a protein related to TOLLOID and BMP-1. EMBO J 1996, 15:411-4122.
  • [33]Geier G, Zwilling R: Cloning and characterization of a cDNA coding for Astacus embryonic astacin, a member of the astacin family of metalloproteases from the crayfish Astacus astacus. Eur J Biochem 1998, 253:796-803.
  • [34]Fan TJ, Katagiri C: Properties of the hatching enzyme from Xenopus laevis. Eur J Biochem 2001, 268:4892-4898.
  • [35]Pan T, Gröger H, Schmid V, Spring J: A toxin homology domain in an astacing-like metallopteinase of the jellyfish of Podocoryne carnea with a dual role in digestion and development. Dev Genes Evol 1998, 208:259-266.
  • [36]Yan L, Pollock GH, Nagase H, Sarras MP Jr: A 25.7×103Mr hydra metalloproteinase (HMP1), a member of the astacin family, localizes to the extracellular matrix of Hydra vulgaris in a head-specific manner and has a developmental function. Dev 1995, 121:1591-1602.
  • [37]Kumpfmüller G, Rybakine V, Takahashi T, Fujisawa T, Bosch TCG: Identification of an astacin matrix metalloprotease as target gene for Hydra foot activator peptides. Dev Genes Evol 1995, 209:601-607.
  • [38]Möhrlen F, Maniura M, Plickert G, Frohme M, Frank U: Evolution of astacin-like metalloproteases in animals and their function in development. Evol Dev 2006, 8:223-231.
  • [39]Hazen AP: Regeneration in Hydractinia and Podocoryne. Amer Nat 1902, 36:193-200.
  • [40]Campbell RD: Cell proliferation and morphological patterns in the hydroids Tubularia and Hydractinia. J Embryol Exp Morph 1967, 17:607-616.
  • [41]Braverman M: Studies on hydroid differentiation; the replacement of hypostomal gland cells of Podocoryne carnea. J Morph 1968, 126:95-106.
  • [42]Bouillon J: Les cellules glandulaires des hydroïdes et des hydroméduses; leur structure et la mature de leurs sécrétions. Cahiers Biologie Marine 1966, 7:157-205.
  • [43]Hsu DR, Economides AN, Wang X, Eimon PM, Harland RM: The Xenpus dorsalizing factor Gremlin indentifies a novel family of secreted proteins that antagonize BMP activities. Mol Cell 1998, 1:673-683.
  • [44]Piccolo S, Agius E, Leyns L, Bhattacharyya B, Grunz H, Bouwmeester T, De Robertis EM: The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 1999, 397:707-710.
  • [45]Duffy DJ, Plickert G, Kuenzel T, Tilmann W, Frank U: Wnt signaling promotes oral but suppresses aboral structures in Hydractinia metamorphosis and regeneration. Dev 2010, 137:3057-3066.
  • [46]Müller W, Frank U, Teo R, Mokady O, Guette C, Plickert G: Wnt signaling in hydroid development: ectopic heads and giant buds induced by GSK-3ß inhibitors. Int J Dev Biol 2007, 51:211-220.
  • [47]Plickert G, Jacoby V, Frank U, Müller WA, Mokady O: Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 2006, 298:368-378.
  • [48]Broun M, Gee L, Reinhardt B, Bode HR: Formation of the head organizer in hydra involves the canonical Wnt pathway. Dev 2005, 132:2907-2916.
  • [49]Gee L, Hartig J, Law L, Wittlieb J, Khalturin K, Bosch TCG, Bode HR: ß-catenin plays a central role in setting up the head organizer in Hydra. Dev Biol 2010, 340:116-124.
  • [50]Guder C, Pinho S, Nacak TG, Schmidt HA, Hobmayer B, Niehrs C, Holstein TW: An ancient Wnt-Dickkopf anatagonism in Hydra. Dev 2005, 133:901-911.
  • [51]Lengfeld T, Watanabe H, Simakov O, Lindgens D, Gee L, Law L, Schmidt HA, Özbek S, Bode H, Holstein TW: Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev Biol 2009, 330:186-199.
  • [52]Nakamura Y, Tsiairis CD, Özbek S, Holstein TW: Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer. Proc Natl Acad Sci USA 2011, 108:9137-9142.
  • [53]Bunting M: The origin of the sex-cells in Hydractinia and Podocoryne; and the development of Hydractinia. J Morph 1894, 9:203-236.
  • [54]Jiménez G, Guichet A, Ephrussi A, Casanova J: Relief of gene repression by Torso RTK signaling: role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev 1894, 14:224-231.
  • [55]Monteiro R, van Dinther M, Bakkers J, Wilkinson R, Patient R, ten Diijke P, Mummery C: Two novel type II receptors mediate BMP signaling and are required to establish left-right asymmetry in zebrafish. Dev Biol 2008, 315:55-71.
  • [56]Deshpande G, Swanhart L, Chiang P, Schedl P: Hedgehog signaling in germ cell migration. Cell 2001, 106:759-769.
  • [57]Bitgood MJ, Shen L, McMahon AP: Sertoli cell signaling by Desert hedgehog regulates the male germline. Current Biol 1996, 6:298-304.
  • [58]Matus DQ, Magie CR, Pang K, Martindale MQ, Thomsen GH: The Hedgehog gene family of the cnidarian, Nematostella vectensis, and implications for understanding metazoan Hedgehog pathway evolution. Dev Biol 2008, 313:501-518.
  • [59]Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL: TopHat2: accurate alignment of transcriptomes in the presence of insertation, deletions and gene fusions. Genome Biol 2013, 14:R36. BioMed Central Full Text
  • [60]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotech 2010, 28:511-515.
  • [61]This Transcriptome Shotgun Assembly project has been deposited at DDBJ/EMBL/GenBank under the accession GAWH00000000. The version described in this paper is the first version, GAWH01000000
  • [62]Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
  • [63]Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J, Conesa A: High-throughput functional annotation and data mining with the Blast2GO suite. Nucl Acids Res 2008, 36:3420-3435.
  • [64]Parra G, Bradnam K, Korf I: CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 2007, 23:1061-1067.
  • [65]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD: The Pfam protein families database. Nucl Acid Res 2012., Database Issuedoi:10.1093/nar/gkr1065
  • [66]TIGR Database http://blast.jcvi.org/web-hmm/ webcite
  • [67]Min XJ, Butler G, Storms R, Tsang A: OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res 2005, (Web Server Issue):W677-W680. http://proteomics.ysu.edu/tools/OrfPredictor.html webcite
  • [68]HMMER. http://hmmer.org/ webcite
  • [69]Li L, Stoeckert CJ, Roos DS: OrthoMCL: identification of orthologous groups for Eukaryotic genomes. Genome Res 2003, 13:2178-2189.
  • [70]Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9:35-359.
  • [71]Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol 2010, 11:R106. BioMed Central Full Text
  • [72]Robinson MD, McCarthy DJ, Smyth GK: edgeR: a Bioconductorpackage for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
  • [73]Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, Mason CE, Socci ND, Betel D: Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol 2013, 14:R95. BioMed Central Full Text
  • [74]Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, Robinson MD: Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature Prot 2013, 8:1765-1786.
  • [75]Soneson C, Delorenzi M: A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics 2013, 14:91. BioMed Central Full Text
  • [76]Nawrocki AM, Cartwright P: Expression of Wnt pathway genes in polyps and medusa-like structures of Ectopleura larynx (Cnidaria: Hydrozoa). Evol Dev 2013, 15:373-384.
  • [77]Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in the accuracy of multiple sequence alignment. Nucl Acids Res 2005, 33:511-518.
  • [78]Stamatakis A, Hoover P, Rougemont J: A fast bootstrapping alogorithm for the RAxML web-servers. Sys Biol 2008, 57:758-771.
  • [79]CIPRES Science Gateway. http://www.phylo.org/index.php/portal/ webcite
  文献评价指标  
  下载次数:33次 浏览次数:22次