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Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish.
Mar Genomics. 2016 Dec; 30:27-34.MG

Abstract

White-blooded Antarctic crocodile icefish are the only vertebrates known to lack functional hemoglobin genes and red blood cells throughout their lives. We do not yet know, however, whether extinction of hemoglobin genes preceded loss of red blood cells or vice versa, nor whether erythropoiesis regulators disappeared along with hemoglobin genes in this erythrocyte-null clade. Several microRNAs, which we here call erythromiRs, are expressed primarily in developing red blood cells in zebrafish, mouse, and humans. Abrogating some erythromiRs, like mir144 and mir451a, leads to profound anemia, demonstrating a functional role in erythropoiesis. Here, we tested two not mutually exclusive hypotheses: 1) that the loss of one or more erythromiR genes extinguished the erythropoietic program of icefish and/or led to the loss of globin gene expression through pseudogenization; and 2) that some erythromiR genes were secondarily lost after the loss of functional hemoglobin and red blood cells in icefish. We explored small RNA transcriptomes generated from the hematopoietic kidney marrow of four Antarctic notothenioids: two red-blooded species (bullhead notothen Notothenia coriiceps and emerald notothen Trematomus bernacchii) and two white-blooded icefish (blackfin icefish Chaenocephalus aceratus and hooknose icefish Chionodraco hamatus). The N. coriiceps genome assembly anchored analyses. Results showed that, like the two red-blooded species, the blackfin icefish genome possessed and the marrow expressed all known erythromiRs. This result indicates that loss of hemoglobin and red blood cells in icefish was not caused by loss of known erythromiR genes. Furthermore, expression of only one erythromiR, mir96, appears to have been lost after the loss of red blood cells and hemoglobin-expression was not detected in the erythropoietic organ of hooknose icefish but was present in blackfin icefish. All other erythromiRs investigated, including mir144 and mir451a, were expressed by all four species and thus are present in the genomes of at least the two white-blooded icefish. Our results rule out the hypothesis that genomic loss of any known erythromiRs extinguished erythropoiesis in icefish, and suggest that after the loss of red blood cells, few erythromiRs experienced secondary loss. Results suggest that functions independent of erythropoiesis maintained erythromiRs, thereby highlighting the evolutionary resilience of miRNA genes in vertebrate genomes.

Authors+Show Affiliations

Institute of Neuroscience, University of Oregon, Eugene, OR, 97403, USA. Electronic address: desvignes@uoneuro.uoregon.edu.Department of Marine and Environmental Sciences, Northeastern University Marine Science Center, Nahant, MA, 01908, USA. Electronic address: iceman@neu.edu.Institute of Neuroscience, University of Oregon, Eugene, OR, 97403, USA. Electronic address: jpostle@uoneuro.uoregon.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

27189439

Citation

Desvignes, Thomas, et al. "Genomic Conservation of Erythropoietic microRNAs (erythromiRs) in White-blooded Antarctic Icefish." Marine Genomics, vol. 30, 2016, pp. 27-34.
Desvignes T, Detrich HW, Postlethwait JH. Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish. Mar Genomics. 2016;30:27-34.
Desvignes, T., Detrich, H. W., & Postlethwait, J. H. (2016). Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish. Marine Genomics, 30, 27-34. https://doi.org/10.1016/j.margen.2016.04.013
Desvignes T, Detrich HW, Postlethwait JH. Genomic Conservation of Erythropoietic microRNAs (erythromiRs) in White-blooded Antarctic Icefish. Mar Genomics. 2016;30:27-34. PubMed PMID: 27189439.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish. AU - Desvignes,Thomas, AU - Detrich,H William,3rd AU - Postlethwait,John H, Y1 - 2016/05/14/ PY - 2016/02/06/received PY - 2016/04/27/revised PY - 2016/04/27/accepted PY - 2016/5/18/pubmed PY - 2017/5/11/medline PY - 2016/5/19/entrez KW - Channichthyidae KW - Hematopoiesis KW - Notothenioidei KW - miRNA KW - mirc144 SP - 27 EP - 34 JF - Marine genomics JO - Mar Genomics VL - 30 N2 - White-blooded Antarctic crocodile icefish are the only vertebrates known to lack functional hemoglobin genes and red blood cells throughout their lives. We do not yet know, however, whether extinction of hemoglobin genes preceded loss of red blood cells or vice versa, nor whether erythropoiesis regulators disappeared along with hemoglobin genes in this erythrocyte-null clade. Several microRNAs, which we here call erythromiRs, are expressed primarily in developing red blood cells in zebrafish, mouse, and humans. Abrogating some erythromiRs, like mir144 and mir451a, leads to profound anemia, demonstrating a functional role in erythropoiesis. Here, we tested two not mutually exclusive hypotheses: 1) that the loss of one or more erythromiR genes extinguished the erythropoietic program of icefish and/or led to the loss of globin gene expression through pseudogenization; and 2) that some erythromiR genes were secondarily lost after the loss of functional hemoglobin and red blood cells in icefish. We explored small RNA transcriptomes generated from the hematopoietic kidney marrow of four Antarctic notothenioids: two red-blooded species (bullhead notothen Notothenia coriiceps and emerald notothen Trematomus bernacchii) and two white-blooded icefish (blackfin icefish Chaenocephalus aceratus and hooknose icefish Chionodraco hamatus). The N. coriiceps genome assembly anchored analyses. Results showed that, like the two red-blooded species, the blackfin icefish genome possessed and the marrow expressed all known erythromiRs. This result indicates that loss of hemoglobin and red blood cells in icefish was not caused by loss of known erythromiR genes. Furthermore, expression of only one erythromiR, mir96, appears to have been lost after the loss of red blood cells and hemoglobin-expression was not detected in the erythropoietic organ of hooknose icefish but was present in blackfin icefish. All other erythromiRs investigated, including mir144 and mir451a, were expressed by all four species and thus are present in the genomes of at least the two white-blooded icefish. Our results rule out the hypothesis that genomic loss of any known erythromiRs extinguished erythropoiesis in icefish, and suggest that after the loss of red blood cells, few erythromiRs experienced secondary loss. Results suggest that functions independent of erythropoiesis maintained erythromiRs, thereby highlighting the evolutionary resilience of miRNA genes in vertebrate genomes. SN - 1876-7478 UR - https://www.unboundmedicine.com/medline/citation/27189439/Genomic_conservation_of_erythropoietic_microRNAs__erythromiRs__in_white_blooded_Antarctic_icefish_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1874-7787(16)30037-X DB - PRIME DP - Unbound Medicine ER -