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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

Size analysis of the leaf mesophyll and leaf midvein epidermal cells 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 indicate highly statistically significant differences (p<0.001) between each of the quintuple mutant line on one hand, and each of the corresponding control lines. (A) Mean diameters and standard deviations of the leaf mesophyll cells. (B) Mean lengths and standard deviations of the epidermal cells. (C and D) Representative images of the mesophyll and epidermal cells, respectively, of the Columbia and xi-k xi-2 myob1-3 plant lines. Note apparently normal cell morphology in the quintuple mutant lines.
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pone.0139331.g003: Size analysis of the leaf mesophyll and leaf midvein epidermal cells 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 indicate highly statistically significant differences (p<0.001) between each of the quintuple mutant line on one hand, and each of the corresponding control lines. (A) Mean diameters and standard deviations of the leaf mesophyll cells. (B) Mean lengths and standard deviations of the epidermal cells. (C and D) Representative images of the mesophyll and epidermal cells, respectively, of the Columbia and xi-k xi-2 myob1-3 plant lines. Note apparently normal cell morphology in the quintuple mutant lines.

Mentions: To investigate the potential contributions of the myosin-MyoB compartment to cell growth, we measured the sizes of three cell types (leaf mesophyll, leaf midrib epidermis, and root hairs) in the s5KO lines and compared those to the control lines Columbia-0, myob1 myob2 myob3, xi-k xi-1 and xi-k xi-2. The mean mesophyll cell diameters in all these controls were not significantly different from each other (Fig 3A; p>0.05). On the other hand, this diameter in the xi-k xi-1 myob1 myob2 myob3 s5KO was 13% smaller than that of Columbia (p<0.001 for pairwise comparisons with each of the three corresponding controls). The xi-k xi-2 myob1 myob2 myob3 s5KO line exhibited an even stronger diameter reduction, by 25% relative to Columbia (Fig 3A; p<0.001 for all controls). The overall cell morphology was apparently normal in these s5KO mutants (Fig 3C).


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

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

Size analysis of the leaf mesophyll and leaf midvein epidermal cells 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 indicate highly statistically significant differences (p<0.001) between each of the quintuple mutant line on one hand, and each of the corresponding control lines. (A) Mean diameters and standard deviations of the leaf mesophyll cells. (B) Mean lengths and standard deviations of the epidermal cells. (C and D) Representative images of the mesophyll and epidermal cells, respectively, of the Columbia and xi-k xi-2 myob1-3 plant lines. Note apparently normal cell morphology in the quintuple mutant lines.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0139331.g003: Size analysis of the leaf mesophyll and leaf midvein epidermal cells 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 indicate highly statistically significant differences (p<0.001) between each of the quintuple mutant line on one hand, and each of the corresponding control lines. (A) Mean diameters and standard deviations of the leaf mesophyll cells. (B) Mean lengths and standard deviations of the epidermal cells. (C and D) Representative images of the mesophyll and epidermal cells, respectively, of the Columbia and xi-k xi-2 myob1-3 plant lines. Note apparently normal cell morphology in the quintuple mutant lines.
Mentions: To investigate the potential contributions of the myosin-MyoB compartment to cell growth, we measured the sizes of three cell types (leaf mesophyll, leaf midrib epidermis, and root hairs) in the s5KO lines and compared those to the control lines Columbia-0, myob1 myob2 myob3, xi-k xi-1 and xi-k xi-2. The mean mesophyll cell diameters in all these controls were not significantly different from each other (Fig 3A; p>0.05). On the other hand, this diameter in the xi-k xi-1 myob1 myob2 myob3 s5KO was 13% smaller than that of Columbia (p<0.001 for pairwise comparisons with each of the three corresponding controls). The xi-k xi-2 myob1 myob2 myob3 s5KO line exhibited an even stronger diameter reduction, by 25% relative to Columbia (Fig 3A; p<0.001 for all controls). The overall cell morphology was apparently normal in these s5KO mutants (Fig 3C).

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