Abstract
Macrobrachium rosenbergii is a typical aquatic organism with reversible gonadal development that is regulated by gene expression. The role of transcription factors in gonadal in adult shrimps remains unclear in M. rosenbergii. In this study, we sequenced the transcriptomes of adult shrimp testes, ovaries, and androgenic glands using second-generation sequencing. In total, 24,007 genes were identified and 9,199 differentially expressed genes (DEGs) were identified by pairwise comparison. There were 272 differentially expressed transcription factors (TFs); 107, 152, and 13 differentially expressed TFs were identified in the testes, ovaries, and androgenic glands by three pairwise comparisons, respectively. GO and KEGG analyses of the TFs and DEGs involved in the MAPK signaling and transcriptional regulation pathways and play key roles in the cell cycle of the testes, whereas involved in the thyroid hormone signaling pathway and neuroactive ligand–receptor interaction play important roles in the ovary. We determined the existence of networks comprising important TFs related to sex development in adult M. rosenbergii gonads. The key TFs were Piwi (expressed only in the testes and ovaries) and Argonaute 3 (expressed only in the ovaries), which might be involved in the regulation of testes and ovary development.
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Data availability
All data generated in this study were deposited in the Gene Expression Omnibus (GEO) with the accession code GSE171823.
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References
Aflalo ED, Raju DVSN, Bommi NA, Verghese JT, Samraj TYC, Hulata G, Ovadia O, Sagi A (2012) Toward a sustainable production of genetically improved all-male prawn (Macrobrachium rosenbergii): evaluation of production traits and obtaining neo-females in three Indian strains. Aquaculture 338–341:197–207. https://doi.org/10.1016/j.aquaculture.2012.01.025
Aflalo ED, Hoang TTT, Nguyen VH, Lam Q, Nguyen DM, Trinh QS, Raviv S, Sagi A (2006) A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 256:468–478. https://doi.org/10.1016/j.aquaculture.2006.01.035
Al-Kurdi B (2017) Hierarchical transcriptional profile of urothelial cells development and differentiation. Differentiation 95:10–20. https://doi.org/10.1016/j.diff.2016.10.001
Amterat Abu Abayed F, Manor R, Aflalo ED, Sagi A (2019) Screening for Dmrt genes from embryo to mature Macrobrachium rosenbergii prawns. Gen Comp Endocrinol 282:113205. https://doi.org/10.1016/j.ygcen.2019.06.009
Bernabé BP, Woodruff T, Broadbelt LJ, Shea LD (2020) Ligands, receptors, and transcription factors that mediate inter-cellular and intra-cellular communication during ovarian follicle development. Reprod Sci 27(2):690–703. https://doi.org/10.1007/s43032-019-00075-8
Bhargava M, Lei J, Mariash CN, Ingbar DH (2007) Thyroid hormone rapidly stimulates alveolar Na, K-ATPase by activation of phosphatidylinositol 3-kinase. Curr Opin Endocrinol Diabetes Obes 14(5):416–420. https://doi.org/10.1097/med.0b013e3282f02ae8
Bonni A (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science 286(5443):1358–1362. https://doi.org/10.1126/science.286.5443.1358
Bothun AM, Woods DC (2019) Dynamics of WNT signaling components in the human ovary from development to adulthood. Histochem Cell Biol 151(2):115–123. https://doi.org/10.1007/s00418-018-1729-y
Casarini L, Crépieux P (2019) Molecular mechanisms of action of FSH. Front Endocrinol (lausanne) 10:305. https://doi.org/10.3389/fendo.2019.00305
Chen X, Xizeng M, Jiaju H, Yang D, Jianmin W, Shan D, Lei K, Ge G, Chuan-Yun L, Liping W (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39(2):W316–W322. https://doi.org/10.1093/nar/gkr483
Cioffi MDB, Kejnovsky E, Marquioni V, Poltronieri J, Molina WF, Diniz D (2012) The key role of repeated DNAs in sex chromosome evolution in two fish species with ZW sex chromosome system. Mol Cytogenet 5(1):28. https://doi.org/10.1186/1755-8166-5-28
Diniz D, Laudicina A, Cioffi MB, Bertollo LA (2008) Microdissection and whole chromosome painting. Improving sex chromosome analysis in Triportheus (Teleostei, Characiformes). Cytogenet Genome Res 122(2):163–168. https://doi.org/10.1159/000163094
Dumesic DA, Meldrum DR, Katz-Jaffe MG, Krisher RL, Schoolcraft WB (2015) Oocyte environment: follicular fluid and cumulus cells are critical for oocyte health. Fertil Steril 103(2):303–316. https://doi.org/10.1016/j.fertnstert.2014.11.015
Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7(10):e1002195. https://doi.org/10.1371/journal.pcbi.1002195
Edson MA, Nagaraja AK, Matzuk MM (2009) The mammalian ovary from genesis to revelation. Endocr Rev 30(6):624–712. https://doi.org/10.1210/er.2009-0012
Fan R, Kim YS, Wu J, Chen R, Zeuschner D, Mildner K, Adachi K, Wu G, Galatidou S, Li J, Sch?ler HR, Leidel SA, & Bedzhov I, (2020) Wnt/beta-catenin/Esrrb signalling controls the tissue-scale reorganization and maintenance of the pluripotent lineage during murine embryonic diapause. Nat Commun 11(1):5499. https://doi.org/10.1038/s41467-020-19353-0
Folli C, Mangiarotti L, Folloni S, Alfieri B, Gobbo M, Berni R, Rivetti C (2008) Specificity of the TraA-DNA interaction in the regulation of the pPD1-encoded sex pheromone response in Enterococcus faecalis. J Mol Biol 380(5):932–945. https://doi.org/10.1016/j.jmb.2008.05.058
Fontana J, Martínková S, Petr J, Žalmanová T, Trnka J (2020) Metabolic cooperation in the ovarian follicle. Physiol Res 69(1):33–48. https://doi.org/10.33549/physiolres.934233
Galindo-Torres P, Ventura-López C, Llera-Herrera R, Ibarra AM (2019) A natural antisense transcript of the fem-1 gene was found expressed in female gonads during the characterization, expression profile, and cellular localization of the fem-1 gene in Pacific white shrimp Penaeus vannamei. Gene 706:19–31. https://doi.org/10.1016/j.gene.2019.04.066
Ge C, Ye J, Weber C, Sun W, Zhang H, Zhou Y, Cai C, Qian G, Capel B (2018) The histone demethylase KDM6B regulates temperature-dependent sex determination in a turtle species. Science 360(6389):645–648. https://doi.org/10.1126/science.aap8328
Hurlin PJ, Huang J (2006) The MAX-interacting transcription factor network. Semin Cancer Biol 16(4):265–274. https://doi.org/10.1016/j.semcancer.2006.07.009
Izawa M (1993) Molecular cloning and sequencing of rat Max cDNA: castration-induced expression of the 2 kb transcript in male accessory sex organs of rats. Biochim Biophys Acta 1216(3):492–494. https://doi.org/10.1016/0167-4781(93)90021-5
Jiang J, Yuan X, Qiu Q, Huang G, Jiang Q, Fu P, Zhang Y, Jia Y, Yang X, Jiang H (2019) Comparative transcriptome analysis of gonads for the identification of sex-related genes in giant freshwater prawns (Macrobrachium rosenbergii) using RNA sequencing. Genes (basel) 10(12):1035. https://doi.org/10.3390/genes10121035
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(10):e76840. https://doi.org/10.1371/journal.pone.0076840
Joseph SR, Pálfy M, Hilbert L, Kumar M, Karschau J, Zaburdaev V, Shevchenko A, Vastenhouw NL (2017) Competition between histone and transcription factor binding regulates the onset of transcription in zebrafish embryos. Elife 6:e23326. https://doi.org/10.7554/eLife.23326
Jung H, Yoon BH, Kim WJ, Kim DW, Hurwood DA, Lyons RE, Salin KR, Kim HS, Baek I, Chand V, Mather PB (2016) Optimizing hybrid de novo transcriptome assembly and extending genomic resources for giant freshwater prawns (Macrobrachium rosenbergii): the identification of genes and markers associated with reproduction. Int J Mol Sci 17(5):690. https://doi.org/10.3390/ijms17050690
Katsuma S, Kiuchi T, Kawamoto M, Fujimoto T, Sahara K (2018) Unique sex determination system in the silkworm, Bombyx mori: current status and beyond. Proc JpnAcad Ser B Phys Biol Sci 94(5):205–216. https://doi.org/10.2183/pjab.94.014
Kuris AM, Raanan Z, Sagi A, Cohen D (1987) Morphotypic differentiation of male Malaysian giant prawns, Macrobrachium rosenbergii. J Crustac Biol 7(2):219–237. https://doi.org/10.2307/1542358
Leelatanawit R, Klinbunga S, Aoki T, Hirono I, Valyasevi R, Menasveta P (2008) Suppression subtractive hybridization (SSH) for isolation and characterization of genes related to testicular development in the giant tiger shrimp Penaeus monodon. BMB Rep 41(11):796–802. https://doi.org/10.5483/bmbrep.2008.41.11.796
Lee T-H, Naitoh N, Yamazaki F (2004) Chromosome studies on the mitten crabs Eriocheir japonica and E. sinensis. Fisheries Sci 70:211–214. https://doi.org/10.1111/j.1444-2906.2003.00793.x
Lee TI, Young RA (2013) Transcriptional regulation and its misregulation in disease. Cell 152:1237–1251. https://doi.org/10.1016/j.cell.2013.02.014
Levy T, Rosen O, Manor R, Dotan S, Azulay D, Abramov A, Sklarz MY, Chalifa-Caspi V, Baruch K, Shechter A, Sagi A (2019) Production of WW males lacking the masculine Z chromosome and mining the Macrobrachium rosenbergii genome for sex-chromosomes. Sci Rep 9(1):12408. https://doi.org/10.1038/s41598-019-47509-6
Levy T, Rosen O, Eilam B, Azulay D, Aflalo ED, Manor R, Shechter A, Sagi A (2016) A single injection of hypertrophied androgenic gland cells produces all-female aquaculture. Mar Biotechnol (NY) 18(5):554–563. https://doi.org/10.1007/s10126-016-9717-5
Li S, Li F, Wen R, Xiang J (2012) Identification and characterization of the sex-determiner transformer-2 homologue in Chinese shrimp. Fenneropenaeus Chinensis Sex Dev 6(5):267–278. https://doi.org/10.1159/000341377
Mathers TC, Hammond RL, Jenner RA, Hänfling B, Atkins J, Gómez A (2015) Transition in sexual system and sex chromosome evolution in the tadpole shrimp Triops cancriformis. Heredity 115(1):37–46. https://doi.org/10.1038/hdy.2015.10
Matson C, Zarkower D (2012) Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Rev Genet 13:163–174. https://doi.org/10.1038/nrg3161
Morohashi K, Mizusaki H, Sugiyama N, Katoh-Fukui Y (2004) Sex differentiation of the gonads and regulation of gene expression. Nihon Rinsho 62(2):255–261
Ohkusu-Tsukada K, Tominaga N, Udono H, Yui K (2004) Regulation of the maintenance of peripheral T-cell anergy by TAB1-mediated p38 alpha activation. Mol Cell Biol 24(16):6957–6966. https://doi.org/10.1128/MCB.24.16.6957-6966.2004
Pasookhush P, Hindmarch C, Sithigorngul P, Longyant S, Bendena WG, Chaivisuthangkura P (2019) Transcriptomic analysis of Macrobrachium rosenbergii (giant fresh water prawn) post-larvae in response to M. rosenbergii nodavirus (MrNV) infection: de novo assembly and functional annotation. BMC Genomics 20(1):762. https://doi.org/10.1186/s12864-019-6102-6
Patnaik BB, Wang TH, Kang SW, Hwang HJ, Park SY, Park EB, Chung JM, Song DK, Kim C, Kim S, Lee JS, Han YS, Park HS, Lee YS (2016) Sequencing, de novo assembly, and annotation of the transcriptome of the endangered freshwater pearl bivalve, Cristaria plicata, provides novel insights into functional genes and marker discovery. PLoS ONE 11(2):e0148622. https://doi.org/10.1371/journal.pone.0148622
Rai N, Singh AK, Singh SK, Gaurishankar B, Kamble SC, Mishra P, Kotiya D, Barik S, Atri N, Gautam V (2020) Recent technological advancements in stem cell research for targeted therapeutics. Drug DelivTransl Res 10(4):1147–1169. https://doi.org/10.1007/s13346-020-00766-9
Shibuya H, Yamaguchi K, Shirakabe K, Tonegawa A, Gotoh Y, Ueno N, Irie K, Nishida E, Matsumoto K (1996) TAB1: an activator of the TAK1 MAPKKK in TGF-beta signal transduction. Science (new York) 272(5265):1179–1182. https://doi.org/10.1126/science.272.5265.1179
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461(7261):267–271. https://doi.org/10.1038/nature08298
Salvadori S, Deiana AM, Deidda F, Lobina C, Mulas A, Coluccia E (2018) XX/XY sex chromosome system and chromosome markers in the snake eel Ophisurus serpens (Anguilliformes: Ophichtidae). Mar Biol Res 14(2):158–164. https://doi.org/10.1080/17451000.2017.1406665
Suwansa-Ard S, Thongbuakaew T, Wang T, Zhao M, Elizur A, Hanna PJ, Sretarugsa P, Cummins SF, Sobhon P (2015) In silico neuropeptidome of female Macrobrachium rosenbergii based on transcriptome and peptide mining of eyestalk, central nervous system and ovary. PLoS ONE 10(5):e0123848. https://doi.org/10.1371/journal.pone.0123848
Suzuki MG, Imanishi S, Dohmae N, Nishimura T, Shimada T, Matsumoto S (2008) Establishment of a novel in vivo sex-specific splicing assay system to identify a trans-acting factor that negatively regulates splicing of Bombyx mori dsx female exons. Mol Cell Biol 28(1):333–343. https://doi.org/10.1128/MCB.01528-07
Tomer V, Rivka M, Eliahu AD, Simy W, Ohad R, Amir S (2012) Timing sexual differentiation: full functional sex reversal achieved through silencing of a single insulin-like gene in the prawn, Macrobrachium rosenbergii. Bio Reprod 86(3):90–1–6. https://doi.org/10.1095/biolreprod.111.097261
Tsoi M, Morin M, Rico C, Johnson RL, Paquet M, Gévry N, Boerboom D (2019) Lats1 and Lats2 are required for ovarian granulosa cell fate maintenance. FASEB J 33(10):10819–10832. https://doi.org/10.1096/fj.201900609R
Ventura T, Manor R, Aflalo ED, Weil S, Raviv S, Glazer L, Sagi A (2009) Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 150(3):1278–1286. https://doi.org/10.1210/en.2008-0906
Wei Q, Fedail JS, Kong L, Zheng K, Meng C, Fadlalla MB, Shi F (2018) Thyroid hormones alter estrous cyclicity and antioxidative status in the ovaries of rats. Anim Sci J 89(3):513–526. https://doi.org/10.1111/asj.12950
Yang G, Lu Z, Qin Z, Zhao L, Pan G, Shen H, Zhang M, Liang R, Lin L, Zhang K (2020) Insight into the regulatory relationships between the insulin-like androgenic gland hormone gene and the insulin-like androgenic gland hormone-binding protein gene in giant freshwater prawns (Macrobrachium rosenbergii). Int J Mol Sci 21(12):4207. https://doi.org/10.3390/ijms21124207
Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C, Matsuda Y, Takamatsu N, Shiba T, Ito M (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 105(7):2469–2474. https://doi.org/10.1073/pnas.0712244105
Zhang HM, Liu T, Liu CJ, Song S, Zhang X, Liu W, Jia H, Xue Y, Guo AY (2015) AnimalTFDB 2.0: a resource for expression, prediction and functional study of animal transcription factors. Nucleic Acids Res 43(Database issue):D76-81. https://doi.org/10.1093/nar/gku887
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This work was supported by the Zhejiang Provincial Natural Science Foundation under Grant number LY21C190001.
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Jindong Ren: methodology, samples collection, data analysis, writing original draft, funding acquisition, project administration. Rong Na: writing—review and editing. Honglin Chen: methodology. Bao Lou: project administration, supervision. Baolong Niu: methodology, supervision.
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Ren, J., Na, R., Chen, H. et al. RNA sequencing and functional analysis of adult gonadal tissue to identify candidate key genes in Macrobrachium rosenbergii sex development. Aquacult Int 29, 2805–2821 (2021). https://doi.org/10.1007/s10499-021-00780-9
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DOI: https://doi.org/10.1007/s10499-021-00780-9