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First published online January 4, 2008; 10.1104/pp.107.113647 Plant Physiology 146:1098-1108 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Myosin XI-K Is Required for Rapid Trafficking of Golgi Stacks, Peroxisomes, and Mitochondria in Leaf Cells of Nicotiana benthamiana1,[W],[OA]Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon 97331 (D.A., A.I.P., V.V.P., V.V.D.); and National Center for Biotechnology Information, National Institutes of Health, Bethesda, Maryland 20894 (K.S.M., E.V.K.)
A prominent feature of plant cells is the rapid, incessant movement of the organelles traditionally defined as cytoplasmic streaming and attributed to actomyosin motility. We sequenced six complete Nicotiana benthamiana cDNAs that encode class XI and class VIII myosins. Phylogenetic analysis indicates that these two classes of myosins diverged prior to the radiation of green algae and land plants from a common ancestor and that the common ancestor of land plants likely possessed at least seven myosins. We further report here that movement of Golgi stacks, mitochondria, and peroxisomes in the leaf cells of N. benthamiana is mediated mainly by myosin XI-K. Suppression of myosin XI-K function using dominant negative inhibition or RNA interference dramatically reduced movement of each of these organelles. When similar approaches were used to inhibit functions of myosin XI-2 or XI-F, only moderate to marginal effects were observed. Organelle trafficking was virtually unaffected in response to inhibition of each of the three class VIII myosins. Interestingly, none of the tested six myosins appears to be involved in light-induced movements of chloroplasts. Taken together, these data strongly suggest that myosin XI-K has a major role in trafficking of Golgi stacks, mitochondria, and peroxisomes, whereas myosins XI-2 and XI-F might perform accessory functions in this process. In addition, our analysis of thousands of individual organelles revealed independent movement patterns for Golgi stacks, mitochondria, and peroxisomes, indicating that the notion of coordinated cytoplasmic streaming is not generally applicable to higher plants.
Membrane-bounded organelles are essential for the function of any eukaryotic cell. Their inheritance and position within the cell are tightly regulated throughout the cell cycle (Pruyne et al., 2004  ; Weisman, 2006). The required translocations of organelles generally depend on cytoskeletal motility systems (Vale, 2003; Boldogh and Pon, 2006). Although plant cells are less motile than animal cells, they exhibit extensive intracellular dynamics that involve repositioning of the nucleus, reshaping of the vacuole, and rapid trafficking of the Golgi stacks, mitochondria, and peroxisomes (Shimmen and Yokota, 2004; Wada and Suetsugu, 2004; Matheson et al., 2006). This trafficking was originally characterized in filamentous algae where the continuous directional flow of cytoplasm is believed to carry the organelles along the cell wall-associated files of chloroplasts (Shimmen and Yokota, 1994). High velocity organelle movement in angiosperms is also traditionally attributed to such directional flow, known as cytoplasmic streaming (Shimmen and Yokota, 2004; Shimmen, 2007). Although the functional significance of organelle motility in nondividing cells is not understood, its occurrence throughout the plant kingdom suggests an important physiological role. In addition, chloroplasts are engaged in much slower light-induced movements (Wada et al., 2003). It was found that destabilization of actin microfilaments by drugs abolishes organelle trafficking and inheritance, as well as chloroplast and nucleus repositioning (Boevink et al., 1998; Nebenfuhr et al., 1999; Mano et al., 2002; Hoffmann and Nebenfuhr, 2004; Sheahan et al., 2004; Kim et al., 2005; Hanton et al., 2006).
The actomyosin motility system also has been implicated in translocation of plant viruses and protein targeting to plasmodesmata (Boevink and Oparka, 2005
Myosins are conserved molecular motors of eukaryotes (Vale, 2003
Similarly to other myosins, class V and class XI myosins possess an N-terminal head or motor domain that hydrolyzes ATP and binds actin microfilaments (Vale, 2003
The genome of the reference plant Arabidopsis (Arabidopsis thaliana) encodes 13 class XI and four class VIII myosins (Reddy and Day, 2001 Using overexpression of dominant negative myosin mutants and RNA interference (RNAi), we show that the class XI myosin XI-K plays a major role in the movement of Golgi stacks, mitochondria, and peroxisomes in the leaf cells. Our analyses of organelle trafficking patterns suggest a revision of the general notion of continuous cytoplasmic streaming in higher plants.
Isolation of Myosin cDNAs from N. benthamiana and Phylogenetic Analysis of Plant and Algal Myosins
To enable the analysis of organelle movement in N. benthamiana, a system that provides convenient assays for transient protein expression, RNAi, and organelle tracking, the nucleotide sequences of six distinct myosin cDNAs were determined. These sequences complement the current, increasingly representative set of plant and algal myosin sequences that includes the full repertoire of genes from four complete flowering plant genomes (Arabidopsis, rice [Oryza sativa], poplar [Populus spp.], and grapevine [Vitis vinifera]), two genomes of unicellular green algae (Chlamydomonas reinhardtii and Ostreococcus lucimarinus), and several other myosins from various plants (Supplemental Table S1). To ascertain the phylogenetic affinities of each of the sequenced N. benthamiana myosins and to elucidate salient features of myosin evolution in green plants and algae, we performed a detailed phylogenetic analysis. A maximum-likelihood tree of class VIII, XI, and XIII myosins was constructed using three sequences from myosin class V as an outgroup (see Supplemental Fig. S1 for corresponding multiple alignment). The topology of the resulting tree shown in Figure 1A
is generally compatible with the conclusions of a recent study of myosin evolution (Foth et al., 2006
The amended data set analyzed here provided for a better resolution of the scenario of myosin evolution in land plants. We found that class VIII myosins split into two distinct lineages [VIII(A) and VIII(B)], whereas class XI myosins split into five lineages [XI(I), XI(G), XI(F), XI(K), and XI(J); the designations for the clades are taken from representatives from Arabidopsis]. Each of these clades is strongly supported by bootstrap analysis, and all except VIII(B) include both dicot and monocot species. Conceivably, the basal position of one of the rice myosins reflects accelerated evolution, and this myosin actually might belong in group VIII(B). Thus, at least seven lineages of class XI and VIII myosins appear to have been represented already in the common ancestor of Magnoliophyta, implying their early functional specialization. Duplication of myosin genes during plant evolution seems to have been quite prolific, in contrast to the near lack of such duplications in the currently available algal genomes. In addition to the duplications that occurred prior to the divergence of monocots and dicots, each of these branches has many lineage-specific paralogs (Fig. 1A).
Phylogenetic analysis informed classification of N. benthamiana myosins that belong to five out of the seven identified groups. These myosins were designated with the letters or digits previously assigned to the most closely related Arabidopsis myosins (Reddy and Day, 2001
Because the attachment of the cargo such as organelle is mediated by myosin tails, overexpression of headless tails is expected to interfere with the tail-binding capacity of the organelles and inhibit their transport. Alternatively, free tails might interact with the heads of corresponding myosins, thus reducing the motor activity (Krementsov et al., 2004
The Golgi stacks and peroxisomes were simultaneously visualized in the leaf epidermal cells using transient expression of the Golgi-targeted yellow fluorescent protein (YFP) and the peroxisome-targeted mCherry (Fig. 3A , top row, green and magenta, respectively). The patterns, velocities, and displacement rate of at least 400 individual organelles in the presence of each coexpressed myosin tail were determined using Volocity software. It should be emphasized that over 99% of the cells in the infiltrated areas expressed both organelle markers. This result strongly suggested that the vast majority of these cells also coexpressed the myosin tails as appropriate for each experimental variant (see "Materials and Methods" for details).
It was found that the tails of myosins XI-2, XI-F, VIII-1, VIII-2, or VIII-B did not significantly affect the Golgi trafficking patterns, mean velocity (Fig. 3, A and B; Supplemental Movies S1 and S2), or displacement rate (Supplemental Table S2). In contrast, overexpression of myosin XI-K tail nearly halted Golgi trafficking (Fig. 3A, column XI-K; Supplemental Movie S1), resulting in an approximately 10-fold reduction of the mean velocity (Fig. 3B) and displacement rate (Supplemental Table S2). It should be mentioned that the residual low velocity was largely due to oscillations rather than processive movement of organelles (Fig. 3A, bottom row; Supplemental Movie S1). The mean distance traveled by Golgi stacks over the observation period in the presence of myosin XI-K tails was only approximately 0.6 µm compared to approximately 30 µm for the control (Supplemental Table S2). Such dramatic reduction in organelle trafficking was observed in virtually all cells in the infiltrated leaf area supporting the uniformity of the myosin tail expression levels among individual cells.
To investigate the contribution of the tail subdomains to the observed inhibition of Golgi trafficking, GTDs that possess no IQ and coiled-coil regions were expressed (Fig. 1B). Once again, overexpression of the XI-K GTD interfered with Golgi trafficking and reduced the mean velocity by approximately 10-fold, whereas GTDs of the other five tested myosins had only moderate effects (Fig. 3, A and B; Supplemental Movies S1 and S3; data not shown). This result indicated that the XI-K tail-mediated suppression of Golgi trafficking did not require IQ or coiled-coil motifs and was likely dependent on interference with cargo binding rather than tail-mediated inhibition of the motor domain given that the latter tail activity was shown to require the coiled-coil region (Li et al., 2006 To determine the statistical significance of the observed differences in organelle velocity, a general linear model analysis followed by Scheffe's multiple comparison test was performed. This approach was chosen given the varying number of replicates between the treatments. The logarithmic transformation was done prior to the analysis to achieve homoscedascity of the variances for each treatment. This transformation also reduced the positive skewness of the data and thus approached normality. In addition to the mean values, the medians were also determined to obtain a central measurement that is not significantly affected by the skewness (Supplemental Table S3). This analysis confirmed that the decrease in the Golgi velocity in the presence of the entire tails or GTDs of myosin XI-K was statistically significant (Supplemental Table S3; Scheffe's group D). Analyses of the peroxisome motility in the same leaf cells revealed that overexpression of myosin XI-K tails reduced mean velocity of the peroxisomes 15-fold compared to that in the empty vector control (Fig. 3B) and virtually arrested trafficking of this organelle. The effects of myosin XI-2 and XI-F tails were significant but less dramatic; an approximately 3-fold reduction of the peroxisomes' mean velocity was observed (Fig. 3, A and B; Supplemental Movie S1; Supplemental Table S3). The GFP reporter-tagged mitochondria were examined in separate experiments that revealed a drastic reduction of mitochondrial trafficking by myosin XI-K tails. None of the other myosin XI or VIII tails had a significant effect on trafficking of this organelle (Fig. 4 ; Supplemental Movie S4). Taken together, these experiments suggested that, in leaf cells of N. benthamiana, myosin XI-K is required for trafficking of Golgi stacks, peroxisomes, and mitochondria, and, in addition, myosins XI-2 and XI-F functionally contribute to the trafficking of peroxisomes.
The analyses of individual organelle motility in control samples showed that the directions of translocation were apparently random with no dominant pattern for each of the three organelles (Figs. 2A and 3A, columns EV). The predominant translocation mode was saltatory rather than continuous. The velocity range was very broad, with some organelles being nearly immobile over the observation period and others moving large distances (Supplemental Movies S1 and S4), resulting in high SDs of the velocity values (Supplemental Table S2). Furthermore, we found that the mean velocities for the Golgi stacks and peroxisomes in the same set of leaf cells differed more than 2-fold under certain treatments (Fig. 3B; Supplemental Table S2). These results indicated that individual Golgi stacks, peroxisomes, and mitochondria move independent of each other rather than passively following the current of cytoplasmic streaming.
Systemic and local RNAi were used to confirm a major role of myosin XI-K in organelle motility by an independent approach. The systemic RNAi assays were performed in GFP-transgenic plants to monitor the overall efficiency of RNAi by disappearance of green fluorescence (Fig. 5A ). Because the Golgi stacks were tagged with the YFP reporter and the nucleotide sequence of the YFP gene differs from that of the GFP transgene, GFP silencing eliminated GFP fluorescence but did not compromise analyses of Golgi trafficking (Fig. 5B). The RNAi experiments with myosins XI-2, XI-F, and XI-K were performed by using the corresponding inverted repeat constructs whose efficiency was confirmed in separate experiments (Supplemental Fig. S2). The analyses of Golgi stacks and peroxisome trafficking showed that abrogation of myosin XI-K expression resulted in major reduction of the translocation distances (Fig. 5B; Supplemental Movie S5) and velocity (Fig. 5D; Supplemental Table S2) for both organelles. In contrast, RNAi of the myosin XI-2 or XI-F had only a moderate effect on the trafficking of these organelles.
Mitochondrial trafficking was analyzed using local RNAi whose efficiency and specificity was confirmed by quantitative PCR analyses (Supplemental Fig. S2). As shown in Figure 5, C and D, and Supplemental Movie S6, motility of mitochondria was slightly reduced by RNAi of myosins XI-2 and XI-F but virtually abolished by RNAi of myosin XI-K. Statistical analyses confirmed that the results for myosin XI-K RNAi were significantly different from those for two other myosins (Supplemental Table S3). Collectively, the RNAi experiments supported the principal role of myosin XI-K in the rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in the leaf cells of N. benthamiana.
The leading role of myosin XI-K in trafficking of the three distinct organelles prompted the question if this same myosin is required for the light-induced relocation of chloroplasts. Drug treatments were used to confirm that the movements of N. benthamiana chloroplasts in response to changing light depended on the integrity of actin microfilaments rather than microtubules (data not shown). The potential role of each of the six available N. benthamiana myosins in both bright-light avoidance movement and blue-light attraction movement of chloroplasts was assayed using overexpression of the cognate myosin tails. Surprisingly, none of the tested myosin tails had any detectable effect on chloroplast relocation under either bright or blue light illumination (Fig. 6 ). This result indicated that the light-regulated chloroplast translocations require distinct myosin motors that are yet to be identified and also confirmed the specificity of myosin XI-K function in trafficking of Golgi stacks, mitochondria, and peroxisomes.
Membrane-bounded organelles are a defining feature of the eukaryotic cell. Among those, mitochondria are universally present in eukaryotes (Embley and Martin, 2006 ); their arrival at the evolutionary scene via endosymbiosis, undoubtedly, was a major event in eukaryotic evolution and might have triggered the entire process of eukaryogenesis (Martin and Koonin, 2006). The endomembrane secretion pathway that includes the ER, the Golgi complex, and specialized derivatives, such as peroxisomes, is another pan-eukaryotic feature (Lee et al., 2004; Scheckman, 2005; Gabaldon et al., 2006; Hanton et al., 2006). The morphology, distribution, and inheritance of the membrane-bounded organelles are dependent on the cytoskeleton that provides the infrastructure of the eukaryotic cell and carries molecular motors that are responsible for the physical translocation of the organelles (Vale, 2003; Pruyne et al., 2004). Comparative functional genomics using diverse models, such as yeast, vertebrates, and plants, is gradually progressing toward a unifying picture of the eukaryotic cell dynamics defined by the interactions between the organelles and the cytoskeleton.
The actomyosin system is, arguably, the most ancient of the cytoskeletal motility systems of the eukaryotes (Vale, 2003 We used N. benthamiana (family Solanaceae) to identify the myosin that is largely responsible for the continuous trafficking of the Golgi stacks, mitochondria, and peroxisomes, and to investigate translocation patterns of these organelles. First, we isolated six class XI and class VIII myosins from N. benthamiana and expressed the cognate cargo-binding tails in plants that possessed fluorophore-tagged organelles. This dominant negative approach was used to interfere with the myosins' ability to bind and transport their respective cargoes. Surprisingly, it was found that the tails of one and the same myosin, XI-K, dramatically reduced processive movement and mean velocity of each of the three studied organelles. Substantially less pronounced, albeit statistically significant effects of other myosin tails can be explained by the incomplete specificity of the approach (i.e. potential cross reactivity of myosins in the dominant-negative test) or by the certain contributions of these myosins to organelle trafficking. The latter possibility appears very likely in the case of the N. benthamiana myosins XI-2 and XI-F that might play a supportive role in peroxisome trafficking as suggested by substantial reduction in peroxisome velocity upon expression of the corresponding GTDs. To validate the results obtained using overexpression of the truncated myosins, we employed transient RNAi to knock down N. benthamiana myosins. As expected, RNAi for myosin XI-K, but not those for any of the other myosins, inhibited substantially trafficking of Golgi stacks, mitochondria, and peroxisomes. These results support the principal role of myosin XI-K in the organelle translocation in this plant species.
None of the tested tails of myosins XI or VIII interfered with the light-induced chloroplast movements. Because it has been shown previously (Paves and Truve, 2007
A comparison of the results described here with the results of analogous experiments in Arabidopsis that are reported in the accompanying article (Peremyslov et al., 2008
The functions of plant myosins XI-K and XI-2 in the transport of Golgi stacks and peroxisomes is reminiscent of yeast class V myosin Myo2p that is responsible for mechanical translocation and segregation of these organelles during cell division (Pruyne et al., 2004
The concept of cytoplasmic streaming defined as a coordinated flow of the cytosol that carries smaller organelles has become a staple of biology textbooks (Buchanan et al., 2000
Our results do not rule out more uniform patterns of organelle movement in certain parts of the cell or certain cell types. Indeed, the flow of the peroxisomes in a predominant direction was seen in parts of elongated cells such as the cells of vascular epidermis or root hairs (Peremyslov et al., 2008
Although rapid organelle trafficking appears to be characteristic of all green plants, its exact functional significance remains unclear. In our experiments, immobilized mitochondria and peroxisomes were frequently seen in close association with the chloroplasts (not shown). Observations of frequent encounters between these organelles and chloroplasts also have been reported by others (Logan and Leaver, 2000
Isolation and Sequencing of Myosin cDNAs of Nicotiana benthamiana and Bioinformatics Analyses
A conserved region in myosin mRNA was amplified using degenerate primers as described (Bezanilla et al., 2003
All binary expression vectors were transformed to Agrobacterium tumefaciens strain C58 GV2260, and the resulting bacteria were used for the N. benthamiana leaf infiltrations at 0.2 to 0.5 OD600 (Prokhnevsky et al., 2005
Confocal laser scanning microscopy was performed using a Zeiss LSM 510 META microscope fitted with the following configurations of excitation and emission filters, respectively: 488 nm and 508 nm for GFP, 513 nm and 527 nm for YFP, and 587 nm and 610 nm for mCherry. For time-lapse experiments, the consecutive images were taken at 2-s intervals. Confocal movie clips (25 frames) were analyzed using the Volocity 3.7.0 Classification software (Improvision, Image Processing and Vision Company; http://www.improvision.com/products/volocity/) using the setting recommended in the software manual for all measurements. All organelles present in each clip were analyzed and two-dimensional movement was recorded. The mean track velocity (micrometers per second) was calculated for a minimum of 10 movie clips; over 400 individual organelles were recorded using three to four leaves from different plants per each treatment (Supplemental Table S2). It should be emphasized that clips were obtained for dozens of individual cells picked at random to avoid any bias.
The inverted repeat constructs harboring N. benthamiana myosin sequences (nts 3,146–3,375 in the myosin XI-2 open reading frame, 3,143–3,370 for myosin XI-F, and 3,153–3,357 for myosin XI-K) were generated in pRTL2-based plasmid (Johansen and Carrington, 2001 The quantitative PCR was done using Reverse-iT first-strand synthesis kit (ABgene), 500 µg of the leaf RNA with anchored oligo(dT), and Absolute QPCR SYBR Green mix (ABgene) in the Rotor-Gene 3000 machine (Corbett Life Sciences). The results were analyzed by the software provided by the manufacturer; primer sequences are available upon request. Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers DQ875135 (XI-2), DQ875136 (XI-F), DQ875137 (XI-K), DQ875138 (VIII-1), DQ875139 (VIII-2), and DQ875140 (VIII-B).
The following materials are available in the online version of this article.
We are grateful to Jim Carrington, John Fowler, and Todd Mockler for useful discussions and critical reading of the manuscript, and to Amit Gal-On for kindly providing lab space to D.A. We thank David Baulcombe, Chris Hawes, David Logan, Shoji Mano, and Roger Tsien for providing plasmids and transgenic plant lines. The authors acknowledge the Confocal Microscopy Facility of the Oregon State University Center for Genome Research and Biocomputing. Received November 27, 2007; accepted December 24, 2007; published January 4, 2008.
1 This work was supported in part by the National Institutes of Health (grant no. GM053190 to V.V.D.) and by the Vaadia/U.S.-Israel Binational Agricultural Research and Development Fund (postdoctoral fellowship award no. F1–354–2004 to D.A.). 
2 These authors contributed equally to the article. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Valerian V. Dolja (doljav{at}science.oregonstate.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.113647 * Corresponding author; e-mail doljav{at}science.oregonstate.edu.
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