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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

Mean flowering time and standard deviations for 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.Black asterisk indicates marginally statistically significant difference (p = 0.05) between the xi-k xi-2 myob1-3 and a corresponding xi-k xi-2 control (the difference between this s5KO and Columbia or myob1-3 controls was highly significant at p<0.001).
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pone.0139331.g006: Mean flowering time and standard deviations for 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.Black asterisk indicates marginally statistically significant difference (p = 0.05) between the xi-k xi-2 myob1-3 and a corresponding xi-k xi-2 control (the difference between this s5KO and Columbia or myob1-3 controls was highly significant at p<0.001).

Mentions: A significant decrease in the growth of the s5KO lines (Figs 4 and 5) prompted investigation of their developmental rate, of which onset of flowering is one of the key characteristics. As shown in Fig 6, inactivation of MyoB1-3 did not significantly affect flowering time compared to Columbia (p>0.05). On the other hand, inactivation of the myosins XI-K and XI-1 or XI-K and XI-2 did delay the flowering onset by 10 and 6 days, respectively, relative to Columbia (Fig 6; p<0.001 for xi-k xi-1 and p<0.01 for xi-k xi-2). The simultaneous inactivation of the three MyoB receptors and either of the myosin XI pairs further exacerbated this delay. The most significant effect was observed for the xi-k xi-2 myob1 myob2 myob3 s5KO line that flowered 15 days later than Columbia, 14 days later than myob1-3 3KO, and 9 days later than xi-k xi-2 2KO controls (Fig 4). It should be noted, however, that although the difference in flowering time between this s5KO and Columbia or MyoB 3KO controls was very significant (p<0.001), the statistical analysis pointed to only marginal significance of the difference with myosin 2KO (p = 0.05).


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

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

Mean flowering time and standard deviations for 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.Black asterisk indicates marginally statistically significant difference (p = 0.05) between the xi-k xi-2 myob1-3 and a corresponding xi-k xi-2 control (the difference between this s5KO and Columbia or myob1-3 controls was highly significant at p<0.001).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0139331.g006: Mean flowering time and standard deviations for 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.Black asterisk indicates marginally statistically significant difference (p = 0.05) between the xi-k xi-2 myob1-3 and a corresponding xi-k xi-2 control (the difference between this s5KO and Columbia or myob1-3 controls was highly significant at p<0.001).
Mentions: A significant decrease in the growth of the s5KO lines (Figs 4 and 5) prompted investigation of their developmental rate, of which onset of flowering is one of the key characteristics. As shown in Fig 6, inactivation of MyoB1-3 did not significantly affect flowering time compared to Columbia (p>0.05). On the other hand, inactivation of the myosins XI-K and XI-1 or XI-K and XI-2 did delay the flowering onset by 10 and 6 days, respectively, relative to Columbia (Fig 6; p<0.001 for xi-k xi-1 and p<0.01 for xi-k xi-2). The simultaneous inactivation of the three MyoB receptors and either of the myosin XI pairs further exacerbated this delay. The most significant effect was observed for the xi-k xi-2 myob1 myob2 myob3 s5KO line that flowered 15 days later than Columbia, 14 days later than myob1-3 3KO, and 9 days later than xi-k xi-2 2KO controls (Fig 4). It should be noted, however, that although the difference in flowering time between this s5KO and Columbia or MyoB 3KO controls was very significant (p<0.001), the statistical analysis pointed to only marginal significance of the difference with myosin 2KO (p = 0.05).

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