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Myosin-Powered Membrane Compartment Drives Cytoplasmic Streaming, Cell Expansion and Plant Development.

Peremyslov VV, Cole RA, Fowler JE, Dolja VV - PLoS ONE (2015)

Bottom Line: Furthermore, the extents of this reduction were similar for each of these compartments suggesting that MyoB compartment plays primary role in cytosol dynamics.Using gene knockout analysis in Arabidopsis thaliana, it is demonstrated that inactivation of MyoB1-4 results in reduced velocity of mitochondria implying slower cytoplasmic streaming.It is also shown that myosins XI and MyoB receptors genetically interact to contribute to cell expansion, plant growth, morphogenesis and proper onset of flowering.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331, United States of America.

ABSTRACT
Using genetic approaches, particle image velocimetry and an inert tracer of cytoplasmic streaming, we have made a mechanistic connection between the motor proteins (myosins XI), cargo transported by these motors (distinct endomembrane compartment defined by membrane-anchored MyoB receptors) and the process of cytoplasmic streaming in plant cells. It is shown that the MyoB compartment in Nicotiana benthamiana is highly dynamic moving with the mean velocity of ~3 μm/sec. In contrast, Golgi, mitochondria, peroxisomes, carrier vesicles and a cytosol flow tracer share distinct velocity profile with mean velocities of 0.6-1.5 μm/sec. Dominant negative inhibition of the myosins XI or MyoB receptors using overexpression of the N. benthamiana myosin cargo-binding domain or MyoB myosin-binding domain, respectively, resulted in velocity reduction for not only the MyoB compartment, but also each of the tested organelles, vesicles and cytoplasmic streaming. Furthermore, the extents of this reduction were similar for each of these compartments suggesting that MyoB compartment plays primary role in cytosol dynamics. Using gene knockout analysis in Arabidopsis thaliana, it is demonstrated that inactivation of MyoB1-4 results in reduced velocity of mitochondria implying slower cytoplasmic streaming. It is also shown that myosins XI and MyoB receptors genetically interact to contribute to cell expansion, plant growth, morphogenesis and proper onset of flowering. These results support a model according to which myosin-dependent, MyoB receptor-mediated transport of a specialized membrane compartment that is conserved in all land plants drives cytoplasmic streaming that carries organelles and vesicles and facilitates cell growth and plant development.

No MeSH data available.


Related in: MedlinePlus

Velocity distribution profiles for organelles, VAMP721 vesicles, mCherry- μNS inclusion bodies, and MyoB1-GFP vesicle-like bodies in the presence of GUS (see legend to Fig 1).Distributions were plotted as % of objects exhibiting velocity range that falls in each bin of 0.5 μm/sec width.
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pone.0139331.g002: Velocity distribution profiles for organelles, VAMP721 vesicles, mCherry- μNS inclusion bodies, and MyoB1-GFP vesicle-like bodies in the presence of GUS (see legend to Fig 1).Distributions were plotted as % of objects exhibiting velocity range that falls in each bin of 0.5 μm/sec width.

Mentions: A comparative analysis of the velocity distribution profiles (Fig 2) was even more telling. The three organelles, VAMP721 vesicles and mCherry-μNS bodies showed very similar motility patterns, with the majority of them (~80%) moving at ~0.5–1.5 μm/sec or being nearly immobile. In contrast, only a minority (19%) of MyoB1-GFP compartment exhibited movement within this velocity range, whereas ~80% of MyoB1-GFP bodies moved at 2–9 μm/sec (Fig 2). The differences between the motility pattern of the MyoB1-GFP compartment on one hand, and those of the organelles or inert bodies on the other, provide further support for distinct transport mechanisms involved. It seems reasonable to propose that the relatively low mean velocities of organelles, VAMP721 vesicles and inert particles are determined by the fraction of time they move with the localized cytosol flows versus staying within relatively immobile cytosol outside the flow routes.


Myosin-Powered Membrane Compartment Drives Cytoplasmic Streaming, Cell Expansion and Plant Development.

Peremyslov VV, Cole RA, Fowler JE, Dolja VV - PLoS ONE (2015)

Velocity distribution profiles for organelles, VAMP721 vesicles, mCherry- μNS inclusion bodies, and MyoB1-GFP vesicle-like bodies in the presence of GUS (see legend to Fig 1).Distributions were plotted as % of objects exhibiting velocity range that falls in each bin of 0.5 μm/sec width.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4591342&req=5

pone.0139331.g002: Velocity distribution profiles for organelles, VAMP721 vesicles, mCherry- μNS inclusion bodies, and MyoB1-GFP vesicle-like bodies in the presence of GUS (see legend to Fig 1).Distributions were plotted as % of objects exhibiting velocity range that falls in each bin of 0.5 μm/sec width.
Mentions: A comparative analysis of the velocity distribution profiles (Fig 2) was even more telling. The three organelles, VAMP721 vesicles and mCherry-μNS bodies showed very similar motility patterns, with the majority of them (~80%) moving at ~0.5–1.5 μm/sec or being nearly immobile. In contrast, only a minority (19%) of MyoB1-GFP compartment exhibited movement within this velocity range, whereas ~80% of MyoB1-GFP bodies moved at 2–9 μm/sec (Fig 2). The differences between the motility pattern of the MyoB1-GFP compartment on one hand, and those of the organelles or inert bodies on the other, provide further support for distinct transport mechanisms involved. It seems reasonable to propose that the relatively low mean velocities of organelles, VAMP721 vesicles and inert particles are determined by the fraction of time they move with the localized cytosol flows versus staying within relatively immobile cytosol outside the flow routes.

Bottom Line: Furthermore, the extents of this reduction were similar for each of these compartments suggesting that MyoB compartment plays primary role in cytosol dynamics.Using gene knockout analysis in Arabidopsis thaliana, it is demonstrated that inactivation of MyoB1-4 results in reduced velocity of mitochondria implying slower cytoplasmic streaming.It is also shown that myosins XI and MyoB receptors genetically interact to contribute to cell expansion, plant growth, morphogenesis and proper onset of flowering.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR 97331, United States of America.

ABSTRACT
Using genetic approaches, particle image velocimetry and an inert tracer of cytoplasmic streaming, we have made a mechanistic connection between the motor proteins (myosins XI), cargo transported by these motors (distinct endomembrane compartment defined by membrane-anchored MyoB receptors) and the process of cytoplasmic streaming in plant cells. It is shown that the MyoB compartment in Nicotiana benthamiana is highly dynamic moving with the mean velocity of ~3 μm/sec. In contrast, Golgi, mitochondria, peroxisomes, carrier vesicles and a cytosol flow tracer share distinct velocity profile with mean velocities of 0.6-1.5 μm/sec. Dominant negative inhibition of the myosins XI or MyoB receptors using overexpression of the N. benthamiana myosin cargo-binding domain or MyoB myosin-binding domain, respectively, resulted in velocity reduction for not only the MyoB compartment, but also each of the tested organelles, vesicles and cytoplasmic streaming. Furthermore, the extents of this reduction were similar for each of these compartments suggesting that MyoB compartment plays primary role in cytosol dynamics. Using gene knockout analysis in Arabidopsis thaliana, it is demonstrated that inactivation of MyoB1-4 results in reduced velocity of mitochondria implying slower cytoplasmic streaming. It is also shown that myosins XI and MyoB receptors genetically interact to contribute to cell expansion, plant growth, morphogenesis and proper onset of flowering. These results support a model according to which myosin-dependent, MyoB receptor-mediated transport of a specialized membrane compartment that is conserved in all land plants drives cytoplasmic streaming that carries organelles and vesicles and facilitates cell growth and plant development.

No MeSH data available.


Related in: MedlinePlus