Golden pompano genome and embryo transcriptome shed light on regulation of minor ZGA gene on heart and vascular development

Whole-genome duplication (WGD) event affects embryo development in teleosts1-3. Although minor zygotic genome activation (ZGA) contributes to further activation of the genome in the mouse4, the cardio- and vascular-linked functions of the genes in the WGD shaping minor ZGA in marine fish are largely unknown. Here, we present a de novo chromosome level-assembly of a marine fish golden pompano and mass transcriptome analyses from 19 embryo development stages to explore how the WGD (Ts3R) contributed to minor-ZGA. Subgenome comparative analyses showed that karyotypes-retained genes are crucial for retaining embryo development stability. Remarkably, we identified one group of specific highly expressed hub-genes within minor ZGA which is essential for the major ZGA. Of which, we discovered a function unknown gene XingHuo (designated as XH) belonging to medium fractionated subgenome locates in key node of specific expression network. For the first time, we report that loss of its homolog ZfXH decreases the subsequent ZGA activation, causes pericardial oedema, body axis bending, caudal fin defects, thinner intersegmental vessels (ISVs), and disruption of the honeycomb structure in the caudal vein plexus (CVPs) in zebrafish. Furthermore, loss of ZfXH downregulates the heart- and vascular-associated landmark gene network (including keystone gene Ptprb, Hand2, Tie2, Hey2, and S1pr1, etc.) via a hitherto unreported ZfXH-Nucleolin-Ptprb pathway. This suggests that XH may function similarly in golden pompano development. We also found that silencing of HARBI1, the human homolog of XH, does suppress the angiogenesis of the cancer cells, indicating its potential as an anti-cancer therapeutic target. Our findings provide new insights into cardio- and vascular-linked functions of the genes in the WGD shaping minor ZGA of marine fish during embryo development.