Genomic conservation of erythropoietic microRNAs (erythromiRs) in white-blooded Antarctic icefish

Desvignes, T., Detrich, H.W., Postlethwait, J.H.
Marine genomics   30: 27-34 (Journal)
Registered Authors
Desvignes, Thomas, Detrich, H. William, Postlethwait, John H.
Channichthyidae, Hematopoiesis, Notothenioidei, miRNA, mirc144
MeSH Terms
  • Animals
  • Antarctic Regions
  • Evolution, Molecular
  • Gene Expression Regulation*
  • Genome*
  • Hemoglobins/genetics
  • Kidney/metabolism
  • Male
  • MicroRNAs/genetics*
  • MicroRNAs/metabolism
  • Perciformes/genetics*
  • Perciformes/metabolism
  • Species Specificity
  • Transcriptome
27189439 Full text @ Mar. Genomics
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.
Genes / Markers
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Engineered Foreign Genes