IEDA
Project Information
Antarctic Fish and MicroRNA Control of Development and Physiology
Short Title:
IcemiR
Start Date:
2016-09-01
End Date:
2019-08-31
Description/Abstract
microRNAs (miRNAs) are key post-transcriptional regulators of gene expression that modulate development and physiology in temperate animals. Although miRNAs act by binding to messenger RNAs (mRNAs), a process that is strongly sensitive to temperature, miRNAs have yet not been studied in Antarctic animals, including Notothenioid fish, which dominate the Southern Ocean. This project will compare miRNA regulation in 1) Antarctic vs. temperate fish to learn the roles of miRNA regulation in adaptation to constant cold; and in 2) bottom-dwelling, dense-boned, red-blooded Nototheniods vs. high buoyancy, osteopenic, white-blooded icefish to understand miRNA regulation in specialized organs after the evolution of the loss of hemoglobin genes and red blood cells, the origin of enlarged heart and vasculature, and the evolution of increased buoyancy, which arose by decreased bone mineralization and increased lipid deposition. Aim 1 is to test the hypothesis that Antarctic fish evolved miRNA-related genome specializations in response to constant cold. The project will compare four Antarctic Notothenioid species to two temperate Notothenioids and two temperate laboratory species to test the hypotheses that (a) Antarctic fish evolved miRNA genome repertoires by loss of ancestral genes and/or gain of new genes, (b) express miRNAs that are involved in cold tolerance, and (c) respond to temperature change by changing miRNA gene expression. Aim 2 is to test the hypothesis that the evolution of icefish from red-blooded bottom-dwelling ancestors was accompanied by an altered miRNA genomic repertoire, sequence, and/or expression. The project will test the hypotheses that (a) miRNAs in icefish evolved in sequence and/or in expression in icefish specializations, including head kidney (origin of red blood cells); heart (changes in vascular system), cranium and pectoral girdle (reduced bone mineral density); and skeletal muscle (lipid deposition), and (b) miRNAs that evolved in icefish specializations had ancestral functions related to their derived roles in icefish, as determined by functional tests of zebrafish orthologs of icefish miRNAs in developing zebrafish. The program will isolate, sequence, and determine the expression of miRNAs and mRNAs using high-throughput transcriptomics and novel software. Results will show how the microRNA system evolves in vertebrate animals pushed to physiological extremes and provide insights into the prospects of key species in the most rapidly warming part of the globe.
Personnel
Person Role
Postlethwait, John Investigator and contact
Desvignes, Thomas Co-Investigator
Funding
Antarctic Organisms and Ecosystems Award # 1543383
AMD - DIF Record(s)
Deployment
Deployment Type
Postlethwait general deployment
Data Management Plan
None in the Database
Product Level:
0 (raw data)
Publications
  1. Le François N. R., Sheehan, E., Desvignes, T., Belzile, C., Postlethwait, J. H., Detrich, H. W., III. (2017) Characterization and Husbandry of Wild Broodstock of the Blackfin Icefish Chaenocephalus aceratus (Lönnberg 1906) from the Palmer Archipelago (Southern Ocean) for Breeding Purposes. Polar Biol. 40, 2499-2516. (doi:10.1007/s00300-017-2161-9)
  2. Berthelot, C., Clarke, J., Desvignes, T., Detrich, H. W., III, Flicek, P., Peck, L. S., Peters, M. J., Postlethwait, J. H., & Clark, M. S. (2018) Global Analysis of Protein Cold Adaptation in Antarctic Fish: An Important Role for Methionine? Genome Biol. Evol., evy262. (doi:10.1093/gbe/evy262)
  3. Bista, I., McCarthy, S. A., Wood, J., Ning, Z., Detrich III, H. W., … Desvignes, T. (2020). The genome sequence of the channel bull blenny, Cottoperca gobio (Günther, 1861). Wellcome Open Research, 5, 148. (doi:10.12688/wellcomeopenres.16012.1)
  4. Kelley, J. L., Desvignes, T., McGowan, K. L., Perez, M., Rodriguez, L. A., Brown, A. P., … Tobler, M. (2020). microRNA expression variation as a potential molecular mechanism contributing to adaptation to hydrogen sulphide. Journal of Evolutionary Biology, 34(6), 977–988. (doi:10.1111/jeb.13727)
  5. Desvignes, T., Batzel, P., Sydes, J., Eames, B. F., & Postlethwait, J. H. (2019). miRNA analysis with Prost! reveals evolutionary conservation of organ-enriched expression and post-transcriptional modifications in three-spined stickleback and zebrafish. Scientific Reports, 9(1). (doi:10.1038/s41598-019-40361-8)
  6. Damsgaard, C., Lauridsen, H., Funder, A. M., Thomsen, J. S., Desvignes, T., Crossley, D. A., … Bayley, M. (2019). Retinal oxygen supply shaped the functional evolution of the vertebrate eye. eLife, 8. (doi:10.7554/elife.52153)
  7. Ashique, A. M., Atake, O. J., Ovens, K., Guo, R., Pratt, I. V., Detrich, H. W., … Eames, B. F. (2021). Bone microstructure and bone mineral density are not systemically different in Antarctic icefishes and related Antarctic notothenioids. Journal of Anatomy. (doi:10.1111/joa.13537)
  8. Le François, N. R., Desvignes, T., Sheehan, E., Belzile, C., Savoie, A., Beirão, J., … Detrich, W. H. (2020). Toward controlled breeding of the blackfin icefish Chaenocephalus aceratus (Lönnberg 1906): determination of spermatozoa concentration and evaluation of short- and long-term preservation of semen. Polar Biology, 43(10), 1583–1593. (doi:10.1007/s00300-020-02729-9)
  9. Desvignes, T., Sydes, J., Montfort, J., Bobe, J., & Postlethwait, J. H. (2021). Evolution after Whole-Genome Duplication: Teleost MicroRNAs. Molecular Biology and Evolution, 38(8), 3308–3331. (doi:10.1093/molbev/msab105)
  10. Desvignes, T., Postlethwait, J.H. & Konstantinidis, P. (2020) Biogeography of the Antarctic dragonfishes Acanthodraco dewitti and Psilodraco breviceps with re-description of Acanthodraco dewitti larvae (Notothenioidei: Bathydraconidae). Polar Biol 43, 565–572. (doi:10.1007/s00300-020-02661-y)
  11. Desvignes T, Le François NR, Goetz LC, Smith SS, Shusdock KA, Parker SK, Postlethwait JH, Detrich HW 3rd. (2019) Intergeneric hybrids inform reproductive isolating barriers in the Antarctic icefish radiation. Sci Rep. 9:5989. PMID:30979924. doi: 10.1038/s41598-019-42354-z. (doi:10.1038/s41598-019-42354-z.)
  12. Desvignes, T., Le François, N. R., Goetz, L. C., Smith, S. S., Shusdock, K. A., Parker, S. K., Postlethwait, J. H., & Detrich, H. W., III. (2019) Intergeneric Hybrids Inform Reproductive Isolating Barriers in the Antarctic Icefish Radiation. Sci. Rep. 9, 5989. (doi:10.1038/s41598-019-42354-z)
  13. Cytrynbaum EG, Small CM, Kwon RY, Hung B, Kent D, Yan YL, Knope ML, Bremiller RA, Desvignes T, Kimmel CB. (2019) Developmental tuning of mineralization drives morphological diversity of gill cover bones in sculpins and their relatives. Evol Let. 3(4):374-391. PMID:31388447. doi: 10.1002/evl3.128. (doi:10.1002/evl3.128. )
  14. Desvignes T, Batzel P, Sydes J, Eames BF, Postlethwait JH. (2019) miRNA analysis with Prost! reveals evolutionary conservation of organ-enriched expression and post-transcriptional modifications in three-spined stickleback and zebrafish. Sci Rep. 9:3913. PMID:30850632. doi: 10.1038/s41598-019-40361-8. (doi:10.1038/s41598-019-40361-8.)
  15. Kim BM, Amores A, Kang S, Ahn DH, Kim JH, Kim IC, Lee JH, Lee SG, Lee H, Lee J, Kim HW, Desvignes T, Batzel P, Sydes J, Titus T, Wilson CA, Catchen JM, Warren WC, Schartl M, Detrich HW 3rd, Postlethwait JH, Park H. (2019) Antarctic blackfin icefish genome reveals adaptations to extreme environments. Nat Ecol Evol. 3(3):469-478. PMID:30804520. doi: 10.1038/s41559-019-0812-7. (doi:10.1038/s41559-019-0812-7.)
  16. Voskoboinikova O, Detrich HW III, Albertson RC, Postlethwait JH, Ghigliotti L, Pisano E. (2017) Evolution Reshaped Life for the Water Column: The Skeleton of the Antarctic Silverfish Pleuragramma antarctica Boulenger, 1902. In The Antarctic Silverfish: a Keystone Species in a Changing Ecosystem.
  17. Le François N, Desvignes T, Sheehan E, Belzile C, Savoie A, Beirão J, Postlethwait J, Detrich HD, (Submitted) Toward controlled breeding of blackfin icefish Chaenocephalus aceratus: spermatozoa concentration and evaluation of short- and long-term preservation of semen. Polar Biology.
  18. Amores A, Wilson CA, Allard CAH, Detrich HW III, Postlethwait JH. (2017) Cold fusion: Massive karyotype evolution in the Antarctic bullhead notothen Notothenia coriiceps. G3. 7: 2195-2207. doi: 10.1534/g3.117.040063. (doi:10.1534/g3.117.040063.)
  19. Postlethwait JH, Yan YL, Desvignes T, Allard C, Titus T, Le François NR, Detrich HW 3rd. (2016) Embryogenesis and early skeletogenesis in the Antarctic bullhead notothen, Notothenia coriiceps. Dev Dyn. 245(11):1066-1080. PMID:27507212. doi: 10.1002/dvdy.24437. (doi:10.1002/dvdy.24437. )
  20. Desvignes T, Detrich HW III, Postlethwait JH. (2016) Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish. Mar Genomics. 30:27-34. PMID:27189439. doi: 10.1016/j.margen.2016.04.013. (doi:10.1016/j.margen.2016.04.013. )
  21. Desvignes T, Batzel P, Berezikov E, Eilbeck K, Eppig JT, McAndrews MS, Singer A, Postlethwait JH. (2015) miRNA nomenclature: A view incorporating genetic origins, biosynthetic pathways, and sequence variants. Trends Genet. 31(11):613-626. PMID:26453491. doi: 10.1016/j.tig.2015.09.002. (doi:10.1016/j.tig.2015.09.002. )
  22. Damsgaard C, Lauridsen H, Funder AMD, Thomsen JS, Desvignes T, Crossley II DA, Møller PR, Huong DTT, Phuong NT, Detrich HW 3rd, Brüel A, Wilkens H, Warrant E, Wang T, Nyengaard JR, Berenbrink M, Bayley M. (In Press) Retinal oxygen supply shaped the functional evolution of the vertebrate eye. eLife. 2019 Dec 10;8. pii: e52153. doi: 10.7554/eLife.52153. (doi:10.7554/eLife.52153.)
  23. Desvignes T, Loher P, Eilbeck K, Ma J, Urgese G, Fromm B, Sydes J, Aparicio-Puerta E, Barrera V, Espin R, Thibord F, Bofill De Ros X, Londin E, Telonis AG, Ficarra E, Friedlander MR, Postlethwait J, Rigoutsos I, Hackenberg M, Vlachos I, Halushka M, Pantano L. (2019) Unification of miRNA and isomiR research: the mirGFF3 format and the miRTOP API. Bioinform. doi:0.1093/bioinformatics/btz675. doi: 10.1093/bioinformatics/btz675. (doi:10.1093/bioinformatics/btz675.)
  24. Kraberger, S., Austin, C., Farkas, K., Desvignes, T., Postlethwait, J. H., Fontenele, R. S., … Varsani, A. (2022). Discovery of novel fish papillomaviruses: From the Antarctic to the commercial fish market. Virology, 565, 65–72. (doi:10.1016/j.virol.2021.10.007)
  25. Cardona, E., Guyomar, C., Desvignes, T., Montfort, J., Guendouz, S., Postlethwait, J. H., … Bobe, J. (2021). Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout. BMC Biology, 19(1). (doi:10.1186/s12915-021-01163-5)
  26. Auvinet, J., Graça, P., Dettai, A., Amores, A., Postlethwait, J. H., Detrich, H. W., … Higuet, D. (2020). Multiple independent chromosomal fusions accompanied the radiation of the Antarctic teleost genus Trematomus (Notothenioidei:Nototheniidae). BMC Evolutionary Biology, 20(1). (doi:10.1186/s12862-020-1600-3)
  27. Cytrynbaum, E. G., Small, C. M., Kwon, R. Y., Hung, B., Kent, D., Yan, Y., … Kimmel, C. B. (2019). Developmental tuning of mineralization drives morphological diversity of gill cover bones in sculpins and their relatives. Evolution Letters, 3(4), 374–391. (doi:10.1002/evl3.128)
  28. Hotaling, S., Borowiec, M.L., Lins, L.S.F., Desvignes, T., Kelley, J.L. (2021) The biogeographic history of eelpouts and related fishes: Linking phylogeny, environmental change, and patterns of dispersal in a globally distributed fish group. Molecular Phylogenetics and Evolution (doi:10.1016/j.ympev.2021.107211)
Platforms and Instruments

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