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

Archiv für Entwicklungsmechanik der Organismen - Tập 226 - Trang 317-324 - 2016
Jiankai Wei1,2,3, Richard Samuel Elliot Glaves4, Melony J. Sellars5, Jianhai Xiang1,2, Philip L. Hertzler4
1University of Chinese Academy of Sciences, Beijing, China
2Key Laboratory of Experimental Marine Biology, Institute of Oceanography, Chinese Academy of Sciences, Qingdao, China
3Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China
4Department of Biology, Central Michigan University, Mount Pleasant, USA
5ARC Research Hub for Advanced Prawn Breeding, Integrated Sustainable Aquaculture Production, Agriculture Flagship, CSIRO, Lucia, Australia

Tóm tắt

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.

Tài liệu tham khảo

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 Castanon I, Baylies MK (2002) A twist in fate: evolutionary comparison of twist structure and function. Gene 287:11–22 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 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 Hertzler PL (2002) Development of the mesendoderm in the dendrobranchiate shrimp Sicyonia ingentis. Arthropod Struct Dev 31:33–49 Hertzler PL (2005) Cleavage and gastrulation in the shrimp Litopenaeus vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct Dev 34:455–469 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 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 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 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 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 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 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 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 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 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