How the cytoplasm separates from the yolk

May 09, 2019

The segregation of yolk from the surrounding cytoplasm in the very early fish embryo is a key process for the development of the fish larva. To identify its underlying mechanisms, biologists at the Institute of Science and Technology Austria (IST Austria) teamed up with their colleagues from theoretical physics. The discovery: Actin dynamics in the bulk of the cell drive phase segregation in zebrafish oocytes.

A single-cell fish egg evolves into a multi-cell embryo in less than two hours after fertilization. Within these two hours, the cytoplasm, which will later form the animal body, must separate completely from the yolk, which the larva is going to feed on. Previously, cell biologists had proposed that local expansion of the cell surface at one pole of the egg mediates this segregation. However, direct evidence supporting this model was lacking.

Joined forces: lab experiments and physical theory

To understand the physical basis of this segregation process, Shayan Shamipour, PhD student in the research group of developmental biologist Carl-Philipp Heisenberg, teamed up with the research group of theoretical physicist Edouard Hannezo. Based on the combined expertise of these two groups, the authors, also including a third professor of IST Austria, Björn Hof, reveal that the forces exerted at the cell surface are dispensable for this process--as opposed to previous models. Instead, they discovered that combined pulling and pushing forces within the embryo facilitate the segregation of cytoplasm from the yolk granules. Importantly, the theory developed to describe this process can be applied to any segregation due to the forces exerted from an active fluid and could thus also be used to examine potential similar processes in mammalian/human embryos.

Size matters

But how are these concerted pulling and pushing movements generated? In the bulk of the cell, far away from the cell surface, filaments of actin and myosin--proteins also involved in muscle cell contraction--form a dense mesh. Polymerization and contraction of this mesh trigger actin flows towards the animal pole of the egg, the hemisphere that is going to differentiate into the later embryo. Via passive frictional forces, these actin flows drag along cytoplasm. The bigger yolk granules, in contrast, are not dragged along by actin since their friction with actin is much lower. Instead, they are actively pushed, or rather squeezed, towards the opposite vegetal pole of the egg by comet-like actin structures--particular actin structures whose function had not been reported in developmental processes before. The combination of these pulling and pushing forces ensures a robust segregation of the cytoplasm and yolk granules within the developing embryo.

Bringing darkness into the light

By examining deeper parts of the cell more closely, the multi-disciplinary team has revealed that animal pole expansion at the cell surface, as previously proposed, is not essential for the yolk-cytoplasm segregation. "The actin structures at the cell surface appear very bright and are therefore quite easy to study. Maybe that's why scientists have so far simply missed to look more deeply into the much darker bulk area, which makes up most of the cell," says Shayan Shamipour, lead author of the study. Refined image processing allowed the IST Austria researchers to take a closer look at the developments in fish eggs during the moments right after fertilization. But, as Shamipour adds, another key to success was something else: "To catch the very first moments of egg development, we had to be really fast: Whenever one of our fish had started to release its eggs into the water, I would press start on my stop watch and my colleagues would see me sprint from the fish facility to the microscopy room to observe and record the process."

Curiosity-driven teamwork at its best

According to the cell biologist with a background in physics, Shamipour had been suspicious of the prevailing surface-based explanation for a while: "The embryo follows a big goal: It has to divide from one into thousands of cells in a very short amount of time. It was thus evident that the proposed surface mechanism alone could not accomplish this segregation and that the embryo would have to come up with some other mechanisms to accelerate the process." It is this curiosity-driven attitude of the young scientist paired with the interdisciplinary research culture of the Heisenberg and Hannezo groups--a mode of scientific work IST Austria particularly fosters--that enabled Shamipour to identify and analyze central cell processes that could be relevant in many other settings and organisms.
-end-
This project has received funding from the European Union (European Research Council Advanced Grant) and from the Austrian Science Fund (FWF).

IST Austria

The Institute of Science and Technology (IST Austria) is a PhD-granting research institution located in Klosterneuburg, 18 km from the center of Vienna, Austria. Inaugurated in 2009, the Institute is dedicated to basic research in the natural and mathematical sciences. IST Austria employs professors on a tenure-track system, postdoctoral fellows, and doctoral students. While dedicated to the principle of curiosity-driven research, the Institute owns the rights to all scientific discoveries and is committed to promote their use. The first president of IST Austria is Thomas A. Henzinger, a leading computer scientist and former professor at the University of California in Berkeley, USA, and the EPFL in Lausanne, Switzerland. The graduate school of IST Austria offers fully-funded PhD positions to highly qualified candidates with a bachelor's or master's degree in biology, neuroscience, mathematics, computer science, physics, and related areas. http://www.ist.ac.at

Animal welfare

Understanding cell biological processes is only possible by studying real cells, in this case of zebrafish. No other methods can serve as alternatives. The animals were raised, kept and treated according to the strict regulations of Austrian law.

Institute of Science and Technology Austria

Related Fish Articles from Brightsurf:

Fish banks
Society will require more food in the coming years to feed a growing population, and seafood will likely make up a significant portion of it.

More than 'just a fish' story
For recreational fishing enthusiasts, the thrill of snagging their next catch comes with discovering what's hooked on the end of the line.

Fish evolution in action: Land fish forced to adapt after leap out of water
Many blennies - a remarkable family of fishes - evolved from an aquatic 'jack of all trades' to a 'master of one' upon the invasion of land, a new study led by UNSW scientists has shown.

How fish got onto land, and stayed there
Research on blennies, a family of fish that have repeatedly left the sea for land, suggests that being a 'jack of all trades' allows species to make the dramatic transition onto land but adapting into a 'master of one' allows them to stay there.

Fish feed foresight
As the world increasingly turns to aqua farming to feed its growing population, there's no better time than now to design an aquaculture system that is sustainable and efficient.

Robo-turtles in fish farms reduce fish stress
Robotic turtles used for salmon farm surveillance could help prevent fish escapes.

Heatwaves risky for fish
A world-first study using sophisticated genetic analysis techniques have found that some fish are better than others at coping with heatwaves.

A new use for museum fish specimens
This paper suggests using museum specimens to estimate the length-weight relationships of fish that are hard to find alive in their natural environment.

Reef fish caring for their young are taken advantage of by other fish
Among birds, the practice of laying eggs in other birds' nests is surprisingly common.

Anemones are friends to fish
Any port in a storm, any anemone for a small fish trying to avoid being a predator's dinner.

Read More: Fish News and Fish Current Events
Brightsurf.com is a participant in the Amazon Services LLC Associates Program, an affiliate advertising program designed to provide a means for sites to earn advertising fees by advertising and linking to Amazon.com.