Evolutionary suppression of erythropoiesis via the modulation of TGF-β signalling in an Antarctic icefish.
The Antarctic icefish, a family (Channichthyidae) of teleosts within the perciform suborder Notothenioidei, are the only known vertebrates without oxygen-transporting haemoglobins and that are largely devoid of circulating erythrocytes. To elucidate the evo-devo mechanisms underpinning the suppressed erythropoiesis in the icefish, we conducted comparative studies on the transcriptomes and microRNAomes of the primary haematopoietic tissues between an icefish (Chionodraco hamatus) and two red-blooded notothenioids (Trematomus bernacchii and Gymnodraco acuticeps). We identified substantial remodelling of the haematopoietic programs in the icefish through which erythropoiesis is selectively suppressed. Experimental verification showed that erythropoietic suppression in the icefish may be attributable to the upregulation of TGF-β signalling, which coincides with reductions in multiple transcription factors essential for erythropoiesis and the upregulation of hundreds of microRNAs, the majority (> 80%) of which potentially target erythropoiesis regulating factors. Of the six microRNAs selected for verification, three miRNAs (miR-152, miR-1388 and miR-16b) demonstrated suppressive functions on GATA1 and ALAS2, which are two factors important for erythroid differentiation, resulting in reduced numbers of erythroids in microinjected zebra fish embryos. Codon substitution analyses of the genes of the TGF-β superfamily revealed signs of positive selection in TGF-β1 and endoglin in the lineages leading to Antarctic notothenioids. Both genes are previously known to function in erythropoietic suppression. These findings implied a general trend of erythropoietic suppression in the cold-adapted notothenioid lineages through evolutionary modulation of the multi-functional TGF-β signalling pathway. This trend is more pronounced in the haemoglobin-less icefish, which may pre-emptively hinder the otherwise defective erythroids from production.
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.|Collaborative Innovation Center for Distant-water Fisheries, Shanghai, 201306, China.
Qianghua
Q
Xu
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Chang
C
Cai
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Xingxing
X
Hu
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Yun
Y
Liu
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Yanan
Y
Guo
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Peng
P
Hu
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Zuozhou
Z
Chen
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Sihua
S
Peng
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Dongsheng
D
Zhang
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Shouwen
S
Jiang
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Zhichao
Z
Wu
Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Jiulin
J
Chan
Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai, 201306, China.
Liangbiao
L
Chen
D000818:Animals; D000864:Antarctic Regions; D005075:Biological Evolution; D004920:Erythropoiesis; D035683:MicroRNAs / Q000235:genetics; D010473:Perciformes / Q000235:genetics*; D010802:Phylogeny; D012641:Selection, Genetic; D017423:Sequence Analysis, RNA; D015398:Signal Transduction; D055411:TGF-beta Superfamily Proteins / Q000235:genetics; D059467:Transcriptome; D016212:Transforming Growth Factor beta / Q000235:genetics*
D035683:MicroRNAs; D055411:TGF-beta Superfamily Proteins; D016212:Transforming Growth Factor beta
Antarctic icefish; TGF-β signalling; erythropoiesis; microRNAome; transcriptome comparison