in

Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius

  • 1.

    Stocker, T. F. et al. Climate change 2013: The physical science basis. (Cambridge University Press Cambridge, 2013).

  • 2.

    Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).

  • 3.

    Richardson, A. J. & Schoeman, D. S. Sea animals are more vulnerable to warming than are land ones. Nature 569, 50–51 (2019).

  • 4.

    Pecorino, D., Lamare, M. D., Barker, M. F. & Byrne, M. How does embryonic and larval thermal tolerance contribute to the distribution of the sea urchin Centrostephanus rodgersii (Diadematidae) in New Zealand? J. Exp. Mar. Biol. Ecol. 445, 120–128 (2013).

    • Article
    • Google Scholar
  • 5.

    Shama, L. N. S. et al. Transgenerational effects persist down the maternal line in marine sticklebacks: gene expression matches physiology in a warming ocean. Evol. Appl. 9, 1096–1111 (2016).

  • 6.

    Liu, W., Huang, X., Lin, J. & He, M. Seawater acidification and elevated temperature affect gene expression patterns of the pearl oyster Pinctada fucata. PLoS One 7, e33679 (2012).

  • 7.

    Ross, P. M., Parker, L. & Byrne, M. Transgenerational responses of molluscs and echinoderms to changing ocean conditions. ICES J. Mar. Sci. J. Cons. 73, 537–549 (2016).

    • Article
    • Google Scholar
  • 8.

    Salinas, S. & Munch, S. B. Thermal legacies: transgenerational effects of temperature on growth in a vertebrate: thermal transgenerational plasticity. Ecol. Lett. 15, 159–163 (2012).

    • Article
    • Google Scholar
  • 9.

    Chirgwin, E., Marshall, D. J., Sgrò, C. M. & Monro, K. How does parental environment influence the potential for adaptation to global change? Proc. R. Soc. B Biol. Sci. 285, 20181374 (2018).

    • Article
    • Google Scholar
  • 10.

    Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180174 (2019).

    • Article
    • Google Scholar
  • 11.

    Byrne, M., Selvakumaraswamy, P., Ho, M. A., Woolsey, E. & Nguyen, H. D. Sea urchin development in a global change hotspot, potential for southerly migration of thermotolerant propagules. Deep Sea Res. Part II Top. Stud. Oceanogr. 58, 712–719 (2011).

  • 12.

    Wong, J. M., Johnson, K. M., Kelly, M. W. & Hofmann, G. E. Transcriptomics reveal transgenerational effects in purple sea urchin embryos: adult acclimation to upwelling conditions alters the response of their progeny to differential p CO2 levels. Mol. Ecol. 27, 1120–1137 (2018).

  • 13.

    Veilleux, H. D. et al. Molecular processes of transgenerational acclimation to a warming ocean. Nat. Clim. Change 5, 1074–1078 (2015).

  • 14.

    Rahman, S., Tsuchiya, M. & Uehara, T. Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla. Biologia (Bratisl.) 64, 768–775 (2009).

    • Article
    • Google Scholar
  • 15.

    Zhao, C. et al. Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius. Ecotoxicol. Environ. Saf. 151, 212–219 (2018).

  • 16.

    Otim, O., Amore, G., Minokawa, T., McClay, D. R. & Davidson, E. H. SpHnf6, a transcription factor that executes multiple functions in sea urchin embryogenesis. Dev. Biol. 273, 226–243 (2004).

  • 17.

    Bonaventura, R., Poma, V., Russo, R., Zito, F. & Matranga, V. Effects of UV-B radiation on development and hsp70 expression in sea urchin cleavage embryos. Mar. Biol. 149, 79–86 (2006).

  • 18.

    Suckling, C. C. et al. Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures. J. Anim. Ecol. 84, 773–784 (2015).

    • Article
    • Google Scholar
  • 19.

    Runcie, D. E. et al. Genetics of gene expression responses to temperature stress in a sea urchin gene network: temperature stress in a gene network. Mol. Ecol 21, 4547–4562 (2012).

  • 20.

    Clark, M. S. et al. Molecular mechanisms underpinning transgenerational plasticity in the green sea urchin Psammechinus miliaris. Sci. Rep. 9, 952 (2019).

  • 21.

    Franks, R. R., Hough-Evans, B. R., Britten, R. J. & Davidson, E. H. Direct introduction of cloned DNA into the sea urchin zygote nucleus, and fate of injected. DNA. Dev. Camb. Engl. 102, 287–299 (1988).

    • CAS
    • Google Scholar
  • 22.

    Stumpp, M. et al. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl. Acad. Sci. U. S. A. 109, 18192–18197 (2012).

  • 23.

    Burke, R. D., Moller, D. J., Krupke, O. A. & Taylor, V. J. Sea urchin neural development and the metazoan paradigm of neurogenesis: Embryonic Neurogenesis. genesis 52, 208–221 (2014).

    • Article
    • Google Scholar
  • 24.

    Byrne, M. et al. Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios. Proc. R. Soc. B Biol. Sci. 276, 1883–1888 (2009).

    • Article
    • Google Scholar
  • 25.

    Dinsmore, J. H. & Sloboda, R. D. Calcium and calmodulin-dependent phosphorylation of a 62 kd protein induces microtubule depolymerization in sea urchin mitotic apparatuses. Cell 53, 769–780 (1988).

  • 26.

    Cox, R. L., Mariano, T., Heck, D. E., Laskin, J. D. & Stegeman, J. J. Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 130, 479–491 (2001).

  • 27.

    Farach-Carson, M. C. A calcium-binding, asparagine-linked oligosaccharide is involved in skeleton formation in the sea urchin embryo. J. Cell Biol. 109, 1289–1299 (1989).

  • 28.

    Haley, S. A. & Wessel, G. M. The cortical granule serine protease CGSP1 of the sea urchin, Strongylocentrotus purpuratus, is autocatalytic and contains a low-density lipoprotein receptor-like Domain. Dev. Biol. 211, 1–10 (1999).

  • 29.

    Strader, M. E., Wong, J. M., Kozal, L. C., Leach, T. S. & Hofmann, G. E. Parental environments alter DNA methylation in offspring of the purple sea urchin, Strongylocentrotus purpuratus. J. Exp. Mar. Biol. Ecol. 517, 54–64 (2019).

    • Article
    • Google Scholar
  • 30.

    Tavaria, M., Gabriele, T., Kola, I. & Anderson, R. L. A hitchhiker’s guide to the human Hsp70 family. Cell Stress Chaperones 1, 23–28 (1996).

  • 31.

    Morano, K. A. New tricks for an old dog: the evolving world of Hsp70. Ann. N. Y. Acad. Sci. 1113, 1–14 (2007).

  • 32.

    Sconzo, G. et al. Activation by Heat Shock of hsp70 Gene Transcription in Sea Urchin Embryos. Biochem. Biophys. Res. Commun. 217, 1032–1038 (1995).

  • 33.

    Zhang, L. et al. Effects of long-term elevated temperature on covering, sheltering and righting behaviors of the sea urchin Strongylocentrotus intermedius. PeerJ 5, e3122 (2017).

    • Article
    • Google Scholar
  • 34.

    Agatsuma, Y. Strongylocentrotus intermedius. in Sea Urchins: Biology and Ecology (ed. John Miller Lawrence) vol. 38 437–447 (Elsevier, 2013).

  • 35.

    Wang, Z. & Chang, Y. Studies on hatching of Japanese sea urchin Strongylocentrotus intermedius. J. Fish. Sci. China 4, 60–67 (1997).

    • Google Scholar
  • 36.

    Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).

  • 37.

    Pertea, G. et al. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651–652 (2003).

  • 38.

    Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    • Article
    • Google Scholar
  • 39.

    Gotz, S. et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36, 3420–3435 (2008).

  • 40.

    Kanehisa, M. et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36, D480–484 (2008).

  • 41.

    Anders, S. & Huber, W. Differential expression of RNA-Seq data at the gene level – the DESeq package (2012).


  • Source: Ecology - nature.com

    Climate knowledge for everyone

    Susan Solomon earns Killian Award, MIT’s highest faculty honor