Cytoplasmic streaming in plants

By Andres Hernandez Maduro

Though seemingly docile on the outside, plants, like all other multicellular organisms, are in constant dynamic turmoil on the inside.

Under the microscope, you might notice that live plant cells are never quite motionless in place; their outer membrane fluctuates and vibrates, organelles swim around in the cytoplasm, and the very cytosol itself moves as if pulled along by an internal breeze.¹ Occasionally, this might even look like a slow-moving vortex. Such motion can be linked to the plant cytoskeletal system, which is tasked with the structural support and transport of molecular structures around the cell. Modular protein filaments in the system link from one location to another, while protein motors carry important cellular cargo (including organelles) along those filaments.¹ It is these mechanisms that allow organelles like chloroplasts and mitochondria to gently glide around a plant cell – a phenomenon referred to as cytoplasmic streaming, or cyclosis.

The common theory behind cytoplasmic streaming is that it evolved to optimise environmental conditions for organelle function. If a chloroplast is moved from one end of a cell to the other, for example, it would then be positioned to receive as much sunlight as possible throughout the day. Since changes in temperature, light intensity and pH are known to alter the rate of fluid flow in plant cells,² this theory is most probably correct.

It should be noted that cytoplasmic streaming is more common in larger eukaryotic species, including higher plants, macroalgae, fungi and even nematodes and flies.² All these species require streaming to efficiently transport nutrients and mineral ions around their cells. However, there is increasing evidence that streaming also has roles in both cell-cell signaling and organelle communication (more on this later).

Although they are technically not plants, one type of model organism used to explore cytoplasmic streaming is the characean algae family. Displaying some of the most organised and rapid streaming routes in any organism (reaching speeds of up to 100 micrometers per second), these algae are heavily studied for their large size and morphology, traits that facilitate the identification of such streaming mechanisms.³

Incidentally, characean branch cells were also the first specimens that scientists used to observe the streaming process with light microscopy in the 1960s.² Their findings soon revealed long ‘ropes’ with pointed ends circumventing the cells – similar to the actin-myosin complexes in animal muscle cells. With further investigations, we have since learned that this comparison was no coincidence. It is now well-established that the eukaryotic cytoskeleton is made of the very same fibres used for muscle contraction in animals.

In characean thallus cells, pH has been found to be regulated by cytoplasmic streaming.² This means that crucial pathways in photosynthetic carbon fixation are dependent on regulated streaming. Recent research further demonstrated that the long-distance communication between photosynthesising chloroplasts was induced by background light.³ Since this type of communication is mediated by cytoplasmic streaming, the researchers involved concluded that cytoplasmic streams were affected by differences in light intensity – perhaps demonstrating an inherent circadian clock in plant and algae cells.

Additionally, some plant biologists believe that the process is involved in the interdependent communication between different organelles in plant cells; between mitochondria and chloroplasts, in particular.⁴ A team of researchers from Kyoto University and the Center for Sustainable Resource Science, Japan, recently tested this idea.

Using confocal laser-scanning microscopy (CLSM), the team studied how the movement of mitochondria in isolated Arabidopsis thaliana (i.e., thale cress) mesophyll cells was affected when in the presence of active chloroplasts.⁵ Images showed two types of mitochondrial movement: wiggling, where they moved slowly but stayed mostly in place; and the directional motion in cytoplasmic streaming, where cytoskeletal F-actin filaments translated them more rapidly and for longer distances around the cell.

Interestingly, degrading the F-actin filaments showed that the mitochondria could still migrate without directional motion by only wiggling (though it was far slower than before). Furthermore, association with chloroplasts appeared to further stimulate mitochondrial wiggling, thereby leading the team to propose that they might also inhibit F-actin-dependent motion across the cell. Both this and the mechanisms behind mitochondrial wiggling are unclear (though the latter is thought to probably occur due to simple random Brownian motion⁵).

But why is this research so significant to cytoplasmic streaming? It does admittedly seem somewhat uneventful, after all. However, investigation here may unveil exciting implications – starting with the metabolic regulation of plant cells.

One possibility for mitochondrial wiggling is that it occurs due to the metabolite exchange between mitochondria and chloroplasts. This would involve key metabolites present in both organelles – such as malate/oxaloacetate shuttling, photorespiration and lipid trafficking.⁶ As this slows down directional motion (and hence cytoplasmic streaming), this would indicate that organelle movement around the cell is regulated intracellularly – not just to react to changes in environmental conditions, but also to communicate between organelles.

With further research on the tethering molecules involved in mitochondrion-chloroplast association, the physiological importance of mitochondrial movement in plants will be better understood. Eventually, this could produce methods in metabolic engineering to manipulate crop physiology and health more effectively. Combined with current advances in cell imaging and microscopy techniques, future research on the cells of model organisms like A. thaliana and characean algae should further expedite industrial advances in both agriculture and natural conservation.

References:

1. Woodhouse FG. & Goldstein RE. Cytoplasmic streaming in plant cells emerges naturally by microfilament self-organization. Biophysics and Computational Biology 2013;110(35). Retrieved from https://doi.org/10.1073/pnas.1302736110

• Beilby MJ. Multi-Scale Characean Experimental System: From Electrophysiology of Membrane Transporters to Cell-to-Cell Connectivity, Cytoplasmic Streaming and Auxin Metabolism. Frontiers in Plant Science 2016. Retrieved from https://doi.org/10.3389/fpls.2016.01052

• Bulychev AA. Cyclosis-mediated intercellular transmission of photosynthetic metabolites in Chara revealed with chlorophyll microfluorometry. Protoplasma 2019;256(3):815-826. Retrieved from https://doi.org/10.1007/s00709-018-01344-0

• Bulychev AA. & Komarova AV. Photoinduction of cyclosis-mediated interactions between distant chloroplasts. Biochim Biophys Acta 2015;1847(4-5):379-389. Retrieved from 4. https://doi.org/10.1016/j.bbabio.2015.01.004

• Oikawa K, et al. Mitochondrial movement during its association with chloroplasts in Arabidopsis thaliana. Commun Biol 2021;4:292. Retrieved from https://doi.org/10.1038/s42003-021-01833-8

• Selinski J, Scheibe R. Malate valves: old shuttles with new perspectives. Plant Biol 2019;21:21-30. Retrieved from https://dx.doi.org/10.1111%2Fplb.12869