Characterization of testis-specific serine/threonine kinase 1-like (TSSK1-like) gene and expression patterns in diploid and triploid Pacific abalone (Haliotis discus hannai; Gastropoda; Mollusca) males
Autoři:
Eun Jeong Kim aff001; So Jeong Kim aff001; Choul Ji Park aff002; Yoon Kwon Nam aff001
Působiště autorů:
Department of Marine Bio-Materials and Aquaculture, Pukyong National University, Busan, Republic of Korea
aff001; Genetics and Breeding Research Center, National Institute of Fisheries Science, Geoje, Republic of Korea
aff002
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0226022
Souhrn
Testis-specific serine/threonine kinase 1-like (TSSK1-like), which plays important roles in late-phase spermatogenesis and male fertility, was characterized in Pacific abalone Haliotis discus hannai, an important commercial marine gastropod. Further, its expression patterns were assessed in diploid and induced triploid males showing differential degrees of testis maturation. Abalone TSSK1-like shared conserved structural features with mammalian TSSK1s and other potential metazoan orthologs, especially regarding the catalytic STKc domain. Phylogenetically, abalone TSSK1-like displayed a genetic affiliation with its molluscan TSSK1-like orthologs and human TSSK1. Additionally, abalone TSSK1-like gene showed a tetrapartite exon-intron organization, unlike the intronless structure of most amniotic tetrapodian TSSK1s. Molecular phylogenetic analysis in the metazoan lineage suggested a possible revision in the origin of the earliest ancestral TSSK1. Further, abalone TSSK1-like showed testis-predominant expression, which was significantly influenced by both age and seasonal reproductive cycles. Comparative expression analyses between diploid and triploid abalone males suggested that robust TSSK1-like expression occurred primarily at the post-meiotic stage. Additionally, RT-PCR assay indicates that mature abalone sperms retain TSSK1-like transcripts after release. Taken together, this study provides useful insights for further studies to assess male reproduction and sterility and/or partial fertility of induced male triploidy in abalone species.
Klíčová slova:
Gene expression – Sequence alignment – Phylogenetic analysis – Testes – Sperm – Introns – Multiple alignment calculation – Triploidy
Zdroje
1. Visconti PE, Hao Z, Purdon MA, Stein P, Balsara BR, Testa JR, et al. Cloning and chromosomal localization of a gene encoding a novel serine/threonine kinase belonging to the subfamily of testis-specific kinases. Genomics. 2001;77: 163–170. doi: 10.1006/geno.2001.6628 11597141
2. Shang P, Baarends WM, Hoogerbrugge J, Ooms MP, Cappellen WA, Jong AAW, et al. Functional transformation of the chromatoid body in mouse spermatids requires testis-specific serine/threonine kinases. J Cell Sci. 2010;123(3): 331–339. doi: 10.1242/jcs.059949 20053632
3. Jha KN, Coleman AR, Wong L, Salicioni AM, Howcroft E, Johnson GR. Heat shock protein 90 functions to stabilize and activate the testis-specific serine/threonine kinases, a family of kinases essential for male fertility. J Biol Chem. 2013;288: 16308–16320. doi: 10.1074/jbc.M112.400978 23599433
4. Hao Z, Jha KN, Kim YH, Vemuganti S, Westbrook VA, Chertihin O, et al. Expression analysis of the human testis-specific serine/ threonine kinase (TSSK) homologues. A TSSK member is present in the equatorial segment of human sperm. Mol Hum Reprod. 2004;10: 433–444. doi: 10.1093/molehr/gah052 15044604
5. Li Y, Sosnik J, Brassard L, Reese M, Spiridonov NA, Bates TC, et al. Expression and localization of five members of the testis-specific serine kinase (TSSK) family in mouse and human sperm and testis. Mol Hum Reprod. 2011;17: 42–56. doi: 10.1093/molehr/gaq071 20729278
6. Volff JN, Brosius J. Modern genomes with retro-look: Retrotransposed elements, retroposition and the origin of new genes. Genome Dyn. 2007;3: 175–190. doi: 10.1159/000107611 18753792
7. Shang P, Hoogerbrugge J, Baarends WM, Grootegoed JA. Evolution of testis-specific kinases TSSK1B and TSSK2 in primates. Andrology. 2013;1: 160–168. doi: 10.1111/j.2047-2927.2012.00021.x 23258646
8. Han MV, Demuth JP, McGrath CL, Casola C, Hahn MW. Adaptive evolution of young gene duplicates in mammals. Genome Res. 2009;19: 859–867. doi: 10.1101/gr.085951.108 19411603
9. Ciocan CM, Cubero-Leon E, Minier C, Rotchell JM. Identification of reproduction-specific genes associated with maturation and estrogen exposure in a marine bivalve Mytilus edulis. PLoS One. 2011;6: e22326. doi: 10.1371/journal.pone.0022326 21818309
10. Li HH, Kong LF, Yu R, Yu H, Li Q. Characterization, expression, and functional analysis of testis-specific serine/threonine kinase 1 (Tssk1) in the pen shell Atrina pectinata. Invertebr Reprod Dev. 2016;60: 118–125. doi: 10.1080/07924259.2016.1161667
11. Park CJ, Kim SY. Abalone aquaculture in Korea. J. Shellfish Res. 2013;32: 17–19.
12. Cook PA. The worldwide abalone industry. Mod. Econ. 2014;5: 1181–1186.
13. Park CJ, Kwon MS, Kim EJ, Nam YK. Improvement of cold-shock treatment conditions for triploidy induction in Pacific abalone Haliotis discus hannai. Korean J. Malacol. 2018;34(4): 191–200.
14. Okumura SI, Arai K, Harigaya Y, Eguchi H, Sakai M, Senbokuya H, et al. Highly efficient induction of triploid Pacific abalone Haliotis discus hannai by caffeine treatment. Fish Sci. 2007;73: 237–243. https://doi.org/10.1111/j.1444-2906.2007.01329.x.
15. Kim SJ. Gonad development and reproductive characteristics of induced triploidy in Pacific abalone, Haliotis discus hannai. M.Sc. Thesis, Pukyong National University. 2017. http://pknu.dcollection.net/public_resource/pdf/000002381588_20190623202227.pdf
16. Lee SY, Nam YK. Transcriptional responses of metallothionein gene to different stress factors in Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol. 2016;58: 530–541. doi: 10.1016/j.fsi.2016.09.030 27693328
17. Lee SY, Nam YK. Molecular cloning of metal-responsive transcription factor-1 (MTF-1) and transcriptional responses to metal and heat stresses in Pacific abalone Haliotis discus hannai. Fish Aquatic Sci. 2017;20: 9. doi: 10.1186/s41240-017-0055-y
18. Kim H, Kim BH, Son MH, Jeon MA, Lee YG, Lee JS. Gonadal development and reproductive cycle of cultured abalone, Haliotis discus hannai (gastropoda: haliotidae) in Korea: implications for seed production. J Shellfish Res. 2016;35: 653–659. doi: 10.2983/035.035.0311
19. NFRDI. Standard manual of abalone culture. 1st ed. Busan: National Fisheries Research and Development Institute Press; 2008.
20. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008;3: 1101–1108. doi: 10.1038/nprot.2008.73 18546601
21. Libus J, Štorchová H, Quantification of cDNA generated by reverse transcription of total RNA provides a simple alternative tool for quantitative RT-PCR normalization. BioTechniques. 2006;41: 156–162. doi: 10.2144/000112232 16925017
22. Roux A, Lambrechts H, Roodt-Wilding R. Reproductive histology of cultured Haliotis midae (Linnaeus, 1758) and preliminary evaluation of maturation. J Shellfish Res. 2013;32: 143–153. doi: 10.2983/035.032.0120
23. Xu B, Hao Z, Jha KN, Zhang Z, Urekar C, Digilio L, et al. Targeted deletion of Tssk1 and 2 causes male infertility due to haploinsufficiency. Dev Biol. 2008;319: 211–222. doi: 10.1016/j.ydbio.2008.03.047 18533145
24. Costa MM, Dios S, Alonso-Gutierrez, Romero A, Novoa B, Figueras A. Evidence of high individual diversity on myticin C in mussel (Mytilus galloprovincialis). Dev Comp Immunol. 2009;33: 162–170. doi: 10.1016/j.dci.2008.08.005 18789353
25. Gao D, Qiu L, Gao Q, Hou Z, Wang L, Song L. Repertoire and evolution of TNF superfamily in Crassostrea gigas: Implications for expansion and diversification of this superfamily in Mollusca. Dev Comp Immunol. 2015;51: 251–260. doi: 10.1016/j.dci.2015.04.006 25910814
26. Song K, Li L, Zhang G. Relationship among intron length, gene expression, and nucleotide diversity in the pacific oyster Crassostrea gigas. Mar Biotechnol. 2018;20: 676–684. doi: 10.1007/s10126-018-9838-0 29967965
27. Su D, Zhang W, Yang Y, Deng Y, Ma Y, Song H, et al. Mutation screening and association study of the TSSK4 gene in Chinese infertile men with impaired spermatogenesis. J Androl. 2008;29: 374–378. doi: 10.2164/jandrol.107.004598 18390560
28. Zhang H, Su D, Yang Y, Zhang W, Liu Y, Bai G, et al. Some single-nucleotide polymorphisms of the TSSK2 gene may be associated with human spermatogenesis impairment. J Androl. 2010;31: 388–392. doi: 10.2164/jandrol.109.008466 19926886
29. Ohresser M, Borsa P, Delsert C. Intron-length polymorphism at the actin gene locus mac-1: a genetic marker for population studies in the marine mussels Mytilus galloprovincialis Lmk. and M. edulis L. Mol Mar Biol Biotechnol. 1997;6(2): 123–130. 9200839
30. Daguin C, Bonhomme F, Borsa P. The zone of sympatry and hybridization of Mytilus edulis and M. galloprovincialis, as described by intron length polymorphism at locus mac-1. Heredity. 2001;86: 342–354. https://doi.org/10.1046/j.1365-2540.2001.00832.x 11488971
31. Arias A, Freire R, Mendez J, Insua A. Intron characterization and their potential as molecular markers for population studies in the scallops Aequipecten opercularis and Mimachlamys varia. Hereditas. 2009;146: 46–57. doi: 10.1111/j.1601-5223.2008.02075.x 19490165
32. Teixeira KN, Souza KN, Vidigal THDA, Brito C, Santos AMC, Santoro MM. Size polymorphism in alleles of the myoglobin gene from Biomphalaria mollusks. Genes. 2010;1 357–370. doi: 10.3390/genes1030357 24710092
33. Vera M, Martinez P, Poisa-Beiro L, Figueras A, Novoa B. Genomic organization, molecular diversification, and evolution of antimicrobial peptide myticin-C genes in the mussel (Mytilus galloprovincialis). PLoS One. 2011;6(8): e24041. doi: 10.1371/journal.pone.0024041 21904604
34. Li L, Zhao J, Wang L, Qiu L, Song L. Genomic organization, polymorphisms and molecular evolution of the goose-type lysozyme gene from Zhikong scallop Chlamys farreri. Gene. 2013;513: 40–52. doi: 10.1016/j.gene.2012.10.080 23142386
35. Dunn CW. Giribet G, Edgecombe GD, Hejnol A. Animal phylogeny and its evolutionary implications. Annu Rev Ecol Evol Syst. 2014;45: 371–395. https://doi.org/10.1146/annurev-ecolsys-120213-091627.
36. Brazeau MD, Friedman M. The origin and early phylogenetic history of jawed vertebrates. Nature. 2015;520: 490–497. doi: 10.1038/nature14438 25903631
37. Qiao T, King B, Long JA, Ahlberg PE, Zhu M. Early gnathostome phylogeny revisited: Multiple method consensus. PLoS One. 2016;11(9): e0163157. doi: 10.1371/journal.pone.0163157 27649538
38. Erwin DH, Davidson EH. The last common bilaterian ancestor. Development. 2002;129: 3021–3032. Available from https://dev.biologists.org/content/develop/129/13/3021.full.pdf. 12070079
39. Blair JE, Hedges SB. Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol. 2005;22(11): 2275–2284. doi: 10.1093/molbev/msi225 16049193
40. Vinckenbosch N, Dupanloup I, Kaessmann H. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA. 2006;103: 3220–3225. doi: 10.1073/pnas.0511307103 16492757
41. Wang Z, Dong X, Ding G, LI Y. Comparing the retention mechanisms of tandem duplicates and retrogenes in human and mouse genomes. Genet Sel Evol. 2010;42: 24. doi: 10.1186/1297-9686-42-24 20584267
42. Wang P, Huo HL, Wang SY, Miao YW, Zhang YY, Zhang QL, et al. Cloning, sequence characterization, and expression patterns of members of the porcine TSSK family. Genet Mol Res. 2015;14(4): 14908–14919. doi: 10.4238/2015.October.18.56 26600552
43. Kim H, Jeon MA, Choi JS, Kim BH, Son MH, Lee JS. Morphological Sex Differentiation of the Abalone Haliotis discus hannai. Korean J. Malacol. 2015;31(4) 273–277. doi: 10.9710/kjm.2015.31.4.273
44. Boutet I, Moraga D, Marinovic L, Obreque J, Chavez-Crooker P. Characterization of reproduction-specific genes in a marine bivalve mollusc: Influence of maturation stage and sex on mRNA expression. Gene. 2008;407: 130–138. doi: 10.1016/j.gene.2007.10.005 17976928
45. Piferrer F, Beaumont A, Falguiere J-C, Flajshans M, Haffray P, Colombo L. Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture. 2009;293: 125–156. doi: 10.1016/j.aquaculture.2009.04.036
46. Dheilly NM, Jouaux A, Boudry P, Favrel P, Lelong C. Transcriptomic profiling of gametogenesis in triploid pacific oysters Crassostrea gigas: Towards an understanding of partial sterility associated with triploidy. PLoS One. 2014;9(11): e112094. doi: 10.1371/journal.pone.0112094 25375782
47. Suquet M, Malo F, Quere C, Ledu C, Grand JL, Benabdelmouna A. Gamete quality in triploid Pacific oyster (Crassostrea gigas). Aquaculture. 2016;451: 11–15. doi: 10.1016/j.aquaculture.2015.08.032
48. Jee YJ, Nam BH, Lee JY, Chang YJ. Maturity and spawning of the triploid pacific abalone, Haliotis discus hannai. Korean J. Malacol. 2013;29(2): 105–111. doi: 10.9710/kjm.2013.29.2.105
49. Fischer BE, Wasbrough E, Meadows LA, Randlet O, Dorus S, Karr TL, Russell S. Conserved properties of Drosophila and human spermatozoal mRNA repertoires. Proc Biol Sci. 2012;279: 2636–2644. doi: 10.1098/rspb.2012.0153 22378807
50. Ren X, Chen X, Wang Z, Wang D. Is transcription in sperm stationary or dynamic? J Repro Dev. 2017;63: 439–443. doi: 10.1262/jrd.2016-093 28845020
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts