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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

Growth phenotypes of the synthetic quintuple mutant Arabidopsis lines xi-k xi-1 myob1-3 and xi-k xi-2 myob1-3 compared to Columbia and parental lines myob1-3, xi-k xi-1 and xi-k xi-2.Red asterisks, same as in Fig 3. (A) Mean plant heights and standard deviations. (B) Mean leaf rosette spans and standard deviations.
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pone.0139331.g004: Growth phenotypes of the synthetic quintuple mutant Arabidopsis lines xi-k xi-1 myob1-3 and xi-k xi-2 myob1-3 compared to Columbia and parental lines myob1-3, xi-k xi-1 and xi-k xi-2.Red asterisks, same as in Fig 3. (A) Mean plant heights and standard deviations. (B) Mean leaf rosette spans and standard deviations.

Mentions: The growth phenotypes of the s5KO mutants were characterized under short day conditions (10/14 hrs light/dark) to favor vegetative growth over transition to flowering. The growth parameters of each s5KO line were measured and statistically evaluated against the three corresponding control plant lines. Analysis of the plant heights demonstrated that whereas myob1 myob2 myob3 and xi-k xi-1 lines exhibited only modest (~3% and ~10%, respectively) height reduction relative to the wild type Columbia line, the heights of the xi-k xi-1 myob1 myob2 myob3 plants were reduced by 35% (Fig 4A). The differences between the mean plant height of the latter line compared to each of the three control lines were highly statistically significant (p<0.001). An analogous analysis of the xi-k xi-2 myob1 myob2 myob3 s5KO line showed even more severe, 40% height reduction (Fig 4A; p<0.001 relative to each of the three control lines).


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

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

Growth phenotypes of the synthetic quintuple mutant Arabidopsis lines xi-k xi-1 myob1-3 and xi-k xi-2 myob1-3 compared to Columbia and parental lines myob1-3, xi-k xi-1 and xi-k xi-2.Red asterisks, same as in Fig 3. (A) Mean plant heights and standard deviations. (B) Mean leaf rosette spans and standard deviations.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0139331.g004: Growth phenotypes of the synthetic quintuple mutant Arabidopsis lines xi-k xi-1 myob1-3 and xi-k xi-2 myob1-3 compared to Columbia and parental lines myob1-3, xi-k xi-1 and xi-k xi-2.Red asterisks, same as in Fig 3. (A) Mean plant heights and standard deviations. (B) Mean leaf rosette spans and standard deviations.
Mentions: The growth phenotypes of the s5KO mutants were characterized under short day conditions (10/14 hrs light/dark) to favor vegetative growth over transition to flowering. The growth parameters of each s5KO line were measured and statistically evaluated against the three corresponding control plant lines. Analysis of the plant heights demonstrated that whereas myob1 myob2 myob3 and xi-k xi-1 lines exhibited only modest (~3% and ~10%, respectively) height reduction relative to the wild type Columbia line, the heights of the xi-k xi-1 myob1 myob2 myob3 plants were reduced by 35% (Fig 4A). The differences between the mean plant height of the latter line compared to each of the three control lines were highly statistically significant (p<0.001). An analogous analysis of the xi-k xi-2 myob1 myob2 myob3 s5KO line showed even more severe, 40% height reduction (Fig 4A; p<0.001 relative to each of the three control lines).

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