Skip to main content
Log in

Expression of the prospective mesoderm genes twist, snail, and mef2 in penaeid shrimp

  • Short Communication
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

In penaeid shrimp, mesoderm forms from two sources: naupliar mesoderm founder cells, which invaginate during gastrulation, and posterior mesodermal stem cells called mesoteloblasts, which undergo characteristic teloblastic divisions. The primordial mesoteloblast descends from the ventral mesendoblast, which arrests in cell division at the 32-cell stage and ingresses with its sister dorsal mesendoblast prior to naupliar mesoderm invagination. The naupliar mesoderm forms the muscles of the naupliar appendages (first and second antennae and mandibles), while the mesoteloblasts form the mesoderm, including the muscles, of subsequently formed posterior segments. To better understand the mechanism of mesoderm and muscle formation in penaeid shrimp, twist, snail, and mef2 cDNAs were identified from transcriptomes of Penaeus vannamei, P. japonicus, P. chinensis, and P. monodon. A single Twist ortholog was found, with strong inferred amino acid conservation across all three species. Multiple Snail protein variants were detected, which clustered in a phylogenetic tree with other decapod crustacean Snail sequences. Two closely-related mef2 variants were found in P. vannamei. The developmental mRNA expression of these genes was studied by qPCR in P. vannamei embryos, larvae, and postlarvae. Expression of Pv-twist and Pv-snail began during the limb bud stage and continued through larval stages to the postlarva. Surprisingly, Pv-mef2 expression was found in all stages from the zygote to the postlarva, with the highest expression in the limb bud and protozoeal stages. The results add comparative data on the development of anterior and posterior mesoderm in malacostracan crustaceans, and should stimulate further studies on mesoderm and muscle development in penaeid shrimp.

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

Access this article

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

Instant access to the full article PDF.

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

Abbreviations

qPCR:

Quantitative real-time PCR

twi :

Twi twist nucleic acid, Twist protein

sna :

Sna snail nucleic acid, Snail protein

mef2:

Mef2 myocyte enhancer factor 2 nucleic acid, mef2 protein

References

  • Biffis C, Alwes F, Scholtz G (2010) Cleavage and gastrulation of the dendrobranchiate shrimp Penaeus monodon (Crustacea, Malacostraca, Decapoda). Arthropod Struct Dev 38:527–540

  • Brown WE, Price AL, Gerberding M, Patel NH (2005) Stages of embryonic development I the amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149

    Article  Google Scholar 

  • Castanon I, Baylies MK (2002) A twist in fate: evolutionary comparison of twist structure and function. Gene 287:11–22

    Article  CAS  PubMed  Google Scholar 

  • Gunthorpe D, Beatty KE, Taylor MV (1999) Different levels, but not different isoforms, of the Drosophila transcription factor Dmef2 affect distinct aspects of muscle differentiation. Dev Biol 215:130–145

    Article  CAS  PubMed  Google Scholar 

  • Hannibal RL, Price AL, Rachem RJ, Patel NH (2012) Analysis of snail genes in the crustacean Parhyale hawaiensis: insight into snail gene family evolution. Dev Genes Evol 222:139–151

    Article  CAS  PubMed  Google Scholar 

  • Hertzler PL (2002) Development of the mesendoderm in the dendrobranchiate shrimp Sicyonia ingentis. Arthropod Struct Dev 31:33–49

    Article  PubMed  Google Scholar 

  • Hertzler PL (2005) Cleavage and gastrulation in the shrimp Litopenaeus vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct Dev 34:455–469

    Article  Google Scholar 

  • Hertzler PL, Clark WH (1992) Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116:127–140

  • Kiernan DA, Hertzler PL (2006) Muscle development in dendrobranchiate shrimp, with comparison with Artemia. Evol Dev 8:537–549

    Article  PubMed  Google Scholar 

  • Li SH, Zhang XJ, Sun Z, Li FH, Xiang JH (2013) Transcriptome analysis on Chinese shrimp Fenneropenaeus chinensis during WSSV acute infection. PLoS One 8. doi: 10.1371/journal.pone.00058627

  • Ma KY, Chan TY, Chu KH (2009) Phylogeny of penaeoid shrimps (Decapoda: Penaeoidea) inferred from nuclear protein-coding genes. Mol Phylogenet Evol 53:45–55

    Article  CAS  PubMed  Google Scholar 

  • Ma KY, Chan TY, Chu KH (2011) Refuting the six-genus classification of Penaeus s.l. (Dendrobranchiata, Penaeidae): a combined analysis of mitochondrial and nuclear genes. Zool Scr 40:498–508

    Article  Google Scholar 

  • Nishikawa T, Ota T, Isogai T (2000) Prediction of whether a human cDNA sequence contains initiation codon by combining statistical information and similarity with protein sequences. Bioinformatics 16:960–967

    Article  CAS  PubMed  Google Scholar 

  • Pawlak JB, Wood A, Sellars MJ, Hertzler PL (2010) Cleavage and gastrulation in the Kuruma shrimp Penaeus (Marsupenaeus) japonicus (Bate): a revised cell lineage and identification of a presumptive germ cell marker. Develop Growth Differ 52:677–692

    Article  CAS  Google Scholar 

  • Price AL, Patel NH (2008) Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. J Exp Zool (Mol Dev Evol) 310B:24–40

    Article  CAS  Google Scholar 

  • Scholtz G, Abzhanov A, Alwes F, Biffis C, Pint J (2009) Development, genes, and decapod evolution. In: Martin JW, Crandal KA, Felder DL (eds) Decapod crustacean phylogenetics. CRC Press, Boca Raton, pp 31–46

    Chapter  Google Scholar 

  • Sellars MJ, Trewin C, McWilliam SM, Glaves RSE, Hertzler PL (2015) Transcriptome profiles of Penaeus (Marsupenaeus) japonicus animal and vegetal half-embryos: identification of sex determination, germ line, mesoderm, and other developmental genes. Mar Biotechnol 17:252–265

    Article  CAS  PubMed  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 doi: 10.1371/journal.pone.0106201

  • Zilch R (1978) Embryologische Untersuchungen an der holoblastischen Ontogenese von Penaeus trisulcatus Leach (Crustacea, Decapoda). Zoomorphology 90:67–100

    Article  Google Scholar 

  • Zilch R (1979) Cell lineage in arthropods? In: Siewing I (ed) Erlanger Symposium für Strukturanalyse und Evolutionforschung, Erlangen 1977. Verlag Paul Parey, Hamburg, pp 19–41

    Google Scholar 

Download references

Acknowledgments

This work was originally undertaken within the CSIRO Marine and Atmospheric Research Capability Development Fund, CSIRO Office of the Chief Executive Payne Scott Award Program to MJS, and CSIRO Food Futures Flagship Cluster on “Sex ratio and sterility for commercial animal production” to PLH. Further support was provided by a FRCE Research Grant from Central Michigan University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Philip L. Hertzler.

Additional information

Communicated by Siegfried Roth

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 17 kb)

ESM 2

(DOCX 15 kb)

ESM 3

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, J., Glaves, R.S.E., Sellars, M.J. et al. Expression of the prospective mesoderm genes twist, snail, and mef2 in penaeid shrimp. Dev Genes Evol 226, 317–324 (2016). https://doi.org/10.1007/s00427-016-0544-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-016-0544-5

Keywords

Navigation