Abstract
In zebrafish embryos, the maternally supplied pool of ATP is insufficient to power even the earliest of developmental events (0–3 hpf) such as oocyte-to-embryo transition (OET). The embryos generate an additional pulse (2.5 h long) of ATP (1.25–4 hpf) to achieve the embryonic ATP homeostasis. We demonstrate that the additional pulse of ATP is needed for successful execution of OET. The maternally supplied yolk lipids play a crucial role in maintaining the embryonic ATP homeostasis. In this paper, we identify the source and trafficking routes of free fatty acids (FFAs) that feed the mitochondria for synthesis of ATP. Interestingly, neither the maternally supplied pool of yolk-FFA nor the yolk-FACoA (fatty acyl coenzyme A) is used for ATP homeostasis during 0–5 hpf in zebrafish embryos. With the help of lipidomics, we explore the link between lipid droplet (LD)-mediated lipolysis and ATP homeostasis in zebrafish embryos. Until 5 hpf, the embryonic LDs undergo extensive lipolysis that generates FFAs. We demonstrate that these newly synthesized FFAs from LDs are involved in the maintenance of embryonic ATP homeostasis, rather than the FFAs/FACoA present in the yolk. Thus, the LDs are vital embryonic organelles that maintain the ATP homeostasis during early developmental stages (0–5 hpf) in zebrafish embryos. Our study highlights the important roles carried on by the LDs during the early development of the zebrafish embryos.
Highlights
The precision of embryonic development into an adult depends on the underlying biochemical reaction network
We propose two distinct sources of free fatty acids (FFAs) that might fulfil the needs of embryonic ATP synthesis: (i) the maternally stored FFAs in the yolk and (ii) the FFA generated by breakdown of other neutral lipids (NLs) in lipid droplet (LD) via lipolysis
We examined the fluorescence image of live zebrafish embryos stained with lipophilic dye, Nile red (NR) [29]
Summary
The precision of embryonic development into an adult depends on the underlying biochemical reaction network. Various literature reports have established that oxidation of yolk free fatty acids (FFAs) in pythons [3], reptiles [2] and birds [4,5,6] fulfil the ATP needs of these lecithotrophic embryos These studies are performed at later developmental stages such as hatching (20 –59 days post-fertilization for different organisms). We propose two distinct sources of FFAs that might fulfil the needs of embryonic ATP synthesis: (i) the maternally stored FFAs in the yolk and (ii) the FFA generated by breakdown of other NLs in LDs via lipolysis (figure 1a, route 1). Morpholino-based proteomic manipulation takes 1 – 3 days to show a desirable phenotype in zebrafish embryos [27,28] Such manipulations cannot be used for functional knockdown of a class of gene family during early stages of embryonic development. This highlights an important function of LDs in zebrafish early development
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