A chromosome-level genome of black rockfish, Sebastes schlegelii, provides insights into the evolution of live birth.
ATAC-seq
astacin metalloproteinase
evolution
rockfish genome
viviparity
zona pellucida
Journal
Molecular ecology resources
ISSN: 1755-0998
Titre abrégé: Mol Ecol Resour
Pays: England
ID NLM: 101465604
Informations de publication
Date de publication:
Sep 2019
Sep 2019
Historique:
received:
20
03
2019
revised:
29
04
2019
accepted:
06
05
2019
pubmed:
12
5
2019
medline:
18
1
2020
entrez:
12
5
2019
Statut:
ppublish
Résumé
The black rockfish (Sebastes schlegelii) is a teleost in which eggs are fertilized internally and retained in the maternal reproductive system, where they undergo development until live birth (viviparity). In the present study, we report a chromosome-level black rockfish genome assembly. High-throughput transcriptome analysis (RNA-seq and ATAC-seq) coupled with in situ hybridization (ISH) and immunofluorescence reveal several candidate genes for maternal preparation, sperm storage and release, and hatching. We propose that zona pellucida (ZP) proteins retain sperm at the oocyte envelope, while genes in two distinct astacin metalloproteinase subfamilies serve to release sperm from the ZP and free the embryo from chorion at prehatching stage. We present a model of black rockfish reproduction, and propose that the rockfish ovarian wall has a similar function to the uterus of mammals. Together, these genomic data reveal unprecedented insights into the evolution of an unusual teleost life history strategy, and provide a sound foundation for studying viviparity in nonmammalian vertebrates and an invaluable resource for rockfish ecological and evolutionary research.
Identifiants
pubmed: 31077549
doi: 10.1111/1755-0998.13034
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1309-1321Subventions
Organisme : Research Funds for Central Universities
ID : 201822026
Organisme : National Key R&D Program of China
ID : 2018YFD0900101
Organisme : National Key R&D Program of China
ID : 2018YFD0901205
Organisme : National Key R&D Program of China
ID : 2018YFD0900301
Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Ahn, H., Shin, S. C., Kim, B. M., Kang, S., Kim, J. H., Ahn, I., … Park, H. (2017). Draft genome of the Antarctic dragonfish, Parachaenichthys charcoti. Gigascience, 6, 1-6.https://doi.org/10.1093/gigascience/gix060
Albertin, C. B., Simakov, O., Mitros, T., Wang, Z. Y., Pungor, J. R., Edsinger-Gonzales, E., … Rokhsar, D. S. (2015). The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature, 524, 220. https://doi.org/10.1038/nature14668
Avise, J. (2013). Evolutionary perspectives on pregnancy. New York, NY: Columbia University Press.
Bao, W., Kojima, K. K., & Kohany, O. (2015). Repbase update, a database of repetitive elements in eukaryotic genomes. Mobile DNA, 6, 11. https://doi.org/10.1186/s13100-015-0041-9
Birney, M., & Clamp, R. (2004). Durbin, GeneWise and genomewise. Genome Research, 14, 988-995. https://doi.org/10.1101/gr.1865504
Blackburn, D. G. (1999). Viviparity and oviparity: evolution and reproductive strategies. In E. Knobil, M. K. Skinner, & J. D. Neill (Eds.), Encyclopedia of reproduction (Vol. 4, pp. 994-1003). San Diego, CA: Academic Press.
Boehlert, G. W., Kusakari, M., Shimizu, M., & Yamada, J. (1986). Energetics during embryonic development in kurosoi, Sebastes schlegelii Hilgendorf. Journal of Experimental Marine Biology and Ecology, 101, 239-256. https://doi.org/10.1016/0022-0981(86)90266-2
Brunori, M., Giuffrè, A., Nienhaus, K., Nienhaus, G. U., Scandurra, F. M., & Vallone, B. (2005). Neuroglobin, nitric oxide, and oxygen: Functional pathways and conformational changes. Proceedings of the National Academy of Sciences of the United States of America, 102, 8483-8488. https://doi.org/10.1073/pnas.0408766102
Burmester, T., Weich, B., Reinhardt, S., & Hankeln, T. (2000). A vertebrate globin expressed in the brain. Nature, 407, 520. https://doi.org/10.1038/35035093
Burton, J. N., Adey, A., Patwardhan, R. P., Qiu, R., Kitzman, J. O., & Shendure, J. (2013). Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nature Biotechnology, 31, 1119-1125. https://doi.org/10.1038/nbt.2727
Candemir, E., Kollert, L., Weißflog, L., Geis, M., Müller, A., Post, A. M., … Freudenberg, F. (2016). Interaction of NOS1AP with the NOS-I PDZ domain: Implications for schizophrenia-related alterations in dendritic morphology. European Neuropsychopharmacology, 26, 741-755. https://doi.org/10.1016/j.euroneuro.2016.01.008
Chen, C.-Y., Chan, C.-H., Chen, C.-M., Tsai, Y.-S., Tsai, T.-Y., Wu Lee, Y.-H., & You, L.-R. (2016). Targeted inactivation of murine Ddx3x: Essential roles of Ddx3x in placentation and embryogenesis. Human Molecular Genetics, 25, 2905-2922.
Dantas, B., Ribeiro, T., Assis, V., Furtado, F., Assis, K., Alves, J., … Braga, V. (2014). Vasorelaxation induced by a new naphthoquinone-oxime is mediated by NO-sGC-cGMP pathway. Molecules, 19, 9773-9785. https://doi.org/10.3390/molecules19079773
de Vries, S., Naarmann-de Vries, I. S., Urlaub, H., Lue, H., Bernhagen, J., Ostareck, D. H., & Ostareck-Lederer, A. (2013). Identification of DDX6 as a cellular modulator of VEGF expression under hypoxia. Journal of Biological Chemistry, 288, 5818-5827.
Durand, N. C., Shamim, M. S., Machol, I., Rao, S. S., Huntley, M. H., Lander, E. S., & Aiden, E. L. (2016). Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems, 3, 95-98. https://doi.org/10.1016/j.cels.2016.07.002
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797. https://doi.org/10.1093/nar/gkh340
Elsik, C. G., Mackey, A. J., Reese, J. T., Milshina, N. V., Roos, D. S., & Weinstock, G. M. (2007). Creating a honey bee consensus gene set. Genome Biology, 8, R13.
Fukuda, M. N., Sato, T., Nakayama, J., Klier, G., Mikami, M., Aoki, D., & Nozawa, S. (1995). Trophinin and tastin, a novel cell adhesion molecule complex with potential involvement in embryo implantation. Genes & Development, 9, 1199-1210. https://doi.org/10.1101/gad.9.10.1199
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., … Zeng, Q. (2011). Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnology, 29, 644-652.
Harris, R. S. (2007). Improved pairwise alignment of genomic DNA. PhD thesis, Pennsylvania State University.
Haynes, J. L. (1995). Standardized classification of poeciliid development for life-history studies. Copeia, 1995(1), 147-154. https://doi.org/10.2307/1446809
Helmstetter, J., Papadopulos, A. S., Igea, J., Van Dooren, T. J., Leroi, A. M., & Savolainen, V. (2016). Viviparity stimulates diversification in an order of fish. Nature Communications, 7, 11271.https://doi.org/10.1038/ncomms11271
Ho, D. H. (2014). Transgenerational epigenetics: The role of maternal effects in cardiovascular development. Integrative and Comparative Biology, 54, 43-51. https://doi.org/10.1093/icb/icu031
Kawaguchi, M., Nakagawa, M., Noda, T., Yoshizaki, N., Hiroi, J., Nishida, M., … Yasumasu, S. (2008). Hatching enzyme of the ovoviviparous black rockfish Sebastes schlegelii-environmental adaptation of the hatching enzyme and evolutionary aspects of formation of the pseudogene. The FEBS Journal, 275, 2884-2898.
Kawaguchi, M., Tomita, K., Sano, K., & Kaneko, T. (2015). Molecular events in adaptive evolution of the hatching strategy of ovoviviparous fishes. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 324, 41-50.
Kawaguchi, M., Yasumasu, S., Hiroi, J., Naruse, K., Inoue, M., & Iuchi, I. (2006). Evolution of teleostean hatching enzyme genes and their paralogous genes. Development Genes & Evolution, 216, 769-784. https://doi.org/10.1007/s00427-006-0104-5
Kent, W. J. (2002). BLAT-The BLAST-like alignment tool. Genome Research, 12, 656-664. https://doi.org/10.1101/gr.229202
Koren, S., Walenz, B. P., Berlin, K., Miller, J. R., Bergman, N. H., & Phillippy, A. M. (2017). Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research, 27, 722-736.
Kotov, A. A., Akulenko, N. V., Kibanov, M. V., & Olenina, L. V. (2014). Olenina, DEAD-Box RNA helicases in animal gametogenesis. Molecular Biology, 48, 16-28. https://doi.org/10.1134/S0026893314010063
Kusakari, M. (1991). Mariculture of kurosoi, Sebastes schlegelii. Environmental Biology of Fishes, 30, 245-251. https://doi.org/10.1007/BF02296892
Langfelder, P., & Horvath, S. (2008). WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559. https://doi.org/10.1186/1471-2105-9-559
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9, 357-359. https://doi.org/10.1038/nmeth.1923
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25. https://doi.org/10.1186/gb-2009-10-3-r25
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Li, J., Zhou, W., Wang, Y., & Niu, C. (2018). The dual role of cGMP in oocyte maturation of zebrafish. Biochemical and Biophysical Research Communications, 499, 998-1003. https://doi.org/10.1016/j.bbrc.2018.04.037
Lin, Q., Fan, S., Zhang, Y., Xu, M., Zhang, H., Yang, Y., … Venkatesh, B. (2016). The seahorse genome and the evolution of its specialized morphology. Nature, 540, 395-399. https://doi.org/10.1038/nature20595
Litscher, S., & Wassarman, P. M., editors (2018). Chapter Eight: The Fish Egg's Zona Pellucida. Extracellular matrix and egg coats (Vol. 130, pp. 295). Amsterdam, The Netherlands: Elsevier.
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550. https://doi.org/10.1186/s13059-014-0550-8
Lundin, V. F., Srayko, M., Hyman, A. A., & Leroux, M. R. (2008). Efficient chaperone-mediated tubulin biogenesis is essential for cell division and cell migration in C. elegans. Developmental Biology, 313, 320-334. https://doi.org/10.1016/j.ydbio.2007.10.022
Mori, H., Nakagawa, M., Soyano, K., & Koya, Y. (2003). Annual reproductive cycle of black rockfish Sebastes schlegelii in captivity. Fisheries Science, 69, 910-923. https://doi.org/10.1046/j.1444-2906.2003.00707.x
Nie, G., Li, Y., He, H., Findlay, J. K., & Salamonsen, L. A. (2006). Salamonsen, HtrA3, a serine protease possessing an IGF-binding domain, is selectively expressed at the maternal-fetal interface during placentation in the mouse. Placenta, 27, 491-501. https://doi.org/10.1016/j.placenta.2005.03.009
Omoto, N., Koya, Y., Chin, B., Yamashita, Y., Nakagawa, M., & Noda, T. (2010). Gonadal sex differentiation and effect of rearing temperature on sex ratio in black rockfish (Sebastes schlegelii). Ichthyological Research, 57, 133-138. https://doi.org/10.1007/s10228-009-0137-7
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017). Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, 14, 417-419. https://doi.org/10.1038/nmeth.4197
Pesce, M., Bolognesi, A., Bocedi, P., Ascenzi, S., Dewilde, L., Moens, T., & Hankeln, T. (2002). Burmester, Neuroglobin and cytoglobin: Fresh blood for the vertebrate globin family. EMBO Reports, 3, 1146-1151. https://doi.org/10.1093/embo-reports/kvf248
Price, M. N., Dehal, P. S., & Arkin, A. P. (2009). FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Molecular Biology and Evolution, 26, 1641-1650. https://doi.org/10.1093/molbev/msp077
Schartl, M., Walter, R. B., Shen, Y., Garcia, T., Catchen, J., Amores, A., … Warren, W. C. (2013). The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nature Genetics, 45, 567. https://doi.org/10.1038/ng.2604
Schultz, J., Copley, R. R., Doerks, T., Ponting, C. P., & Bork, P. (2000). SMART: A web-based tool for the study of genetically mobile domains. Nucleic Acids Research, 28, 231-234. https://doi.org/10.1093/nar/28.1.231
Servant, N., Varoquaux, N., Lajoie, B. R., Viara, E., Chen, C.-J., Vert, J.-P., … Barillot, E. (2015). HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Genome Biology, 16, 259. https://doi.org/10.1186/s13059-015-0831-x
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212. https://doi.org/10.1093/bioinformatics/btv351
Singh, H., Endo, Y., & Nie, G. (2011). Decidual HtrA3 negatively regulates trophoblast invasion during human placentation. Human Reproduction, 26, 748-757. https://doi.org/10.1093/humrep/der019
Sladek, S. M., Magness, R. R., & Conrad, K. P. (1997). Nitric oxide and pregnancy. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 272, R441-R463. https://doi.org/10.1152/ajpregu.1997.272.2.R441
Stanke, M., & Waack, S. (2003). Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics, 19, ii215-ii225. https://doi.org/10.1093/bioinformatics/btg1080
Suzuki, N., Zara, J., Sato, T., Ong, E., Bakhiet, N., Oshima, R. G., … Fukuda, M. N. (1998). A cytoplasmic protein, bystin, interacts with trophinin, tastin, and cytokeratin and may be involved in trophinin-mediated cell adhesion between trophoblast and endometrial epithelial cells. Proceedings of the National Academy of Sciences of the United States of America, 95, 5027-5032. https://doi.org/10.1073/pnas.95.9.5027
Szklarczyk, D., Morris, J. H., Cook, H., Kuhn, M., Wyder, S., Simonovic, M., … Bork, P. (2017). The STRING database in 2017: Quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Research, 45, D362-D368.
Thibault, R. E., & Schultz, R. J. (1978). Reproductive adaptations among viviparous fishes (Cyprinodontiformes: Poeciliidae). Evolution, 32, 320-333. https://doi.org/10.1111/j.1558-5646.1978.tb00648.x
Tropea, T., Wareing, M., Greenwood, S. L., Feelisch, M., Sibley, C. P., & Cottrell, E. C. (2018). Nitrite mediated vasorelaxation in human chorionic plate vessels is enhanced by hypoxia and dependent on the NO-sGC-cGMP pathway. Nitric Oxide, 80, 82-88. https://doi.org/10.1016/j.niox.2018.08.009
Tsvilovskyy, V. V., Zholos, A. V., Aberle, T., Philipp, S. E., Dietrich, A., Zhu, M. X., … Flockerzi, V. (2009). Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology, 137, 1415-1424. https://doi.org/10.1053/j.gastro.2009.06.046
Walker, B. J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., … Earl, A. M. (2014). Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE, 9, e112963. https://doi.org/10.1371/journal.pone.0112963
Wootton, R. J., & Smith, C. (2014). Chapter 9: Parental care. Reproductive biology of teleost fishes (pp. 252-279). Chichester, UK: John Wiley & Sons Ltd.
Wourms, J. P. (1981). Viviparity: The maternal-fetal relationship in fishes. American Zoologist, 21, 473-515. https://doi.org/10.1093/icb/21.2.473
Wu, J., Huang, B. O., Chen, H. E., Yin, Q., Liu, Y., Xiang, Y., … Xie, W. (2016). The landscape of accessible chromatin in mammalian preimplantation embryos. Nature, 534, 652-657. https://doi.org/10.1038/nature18606
Wu, T., Cheng, Y., Liu, Z., Tao, W., Zheng, S., & Wang, D. (2018). Bioinformatic analyses of zona pellucida genes in vertebrates and their expression in Nile tilapia. Fish Physiology and Biochemistry, 44, 435-449. https://doi.org/10.1007/s10695-017-0434-4
Xu, Z., & Wang, H. (2007). LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research, 35, W265-W268. https://doi.org/10.1093/nar/gkm286
Zhang, Y., Liu, T., Meyer, C. A., Eeckhoute, J., Johnson, D. S., Bernstein, B. E., … Liu, X. S. (2008). Model-based analysis of ChIP-Seq (MACS). Genome Biology, 9, R137. https://doi.org/10.1186/gb-2008-9-9-r137