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The Tangled1 Gene Is Required for Spatial Control of Cytoskeletal Arrays Associated with Cell Division during Maize Leaf DevelopmentAnn L. Clearya and Laurie G. Smithba Plant Cell Biology Group, Research School of Biological Sciences, Australian National University, GPO Box 475, ACT 2601, Canberra, Australia b Department of Biology, Coker Hall CB 3280, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3280 Correspondence to: Laurie G. Smith, at the Department of Biology 0116, 9500 Gilman Drive, University of California at San Diego, La Jolla, CA 92093-0116., lsmith{at}biomail.ucsd.edu (E-mail), 619-534-7108 (fax).
The cytoskeleton plays a major role in the spatial regulation of plant cell division and morphogenesis. Arrays of microtubules and actin filaments present in the cell cortex during prophase mark sites to which phragmoplasts and associated cell plates are guided during cytokinesis. During interphase, cortical microtubules are believed to influence the orientation of cell expansion by guiding the pattern in which cell wall material is laid down. Little is known about the mechanisms that regulate these cytoskeleton-dependent processes critical for plant development. Previous work showed that the Tangled1 (Tan1) gene of maize is required for spatial regulation of cytokinesis during maize leaf development but not for leaf morphogenesis. Here, we examine the cytoskeletal arrays associated with cell division and morphogenesis during the development of tan1 and wild-type leaves. Our analysis leads to the conclusion that Tan1 is required both for the positioning of cytoskeletal arrays that establish planes of cell division during prophase and for spatial guidance of expanding phragmoplasts toward preestablished cortical division sites during cytokinesis. Observations on the organization of interphase cortical microtubules suggest that regional influences may play a role in coordinating cell expansion patterns among groups of cells during leaf morphogenesis.
The cellular architecture of plant tissues is defined by a network of cell walls, which determine the shape, size, and position of each cell. It is well known that the formation and initial positioning of cell walls, as well as their patterns of expansion during organ growth, are influenced by the cytoskeleton. Cell walls are initiated through the action of a phragmoplast composed of microtubules (MTs) and actin filaments, which guide the deposition of vesicles containing cell wall material to the growing cell plate (
A variety of observations has established that during cytokinesis, the phragmoplast is actively guided to the former PPB site (
Cytoskeletal filaments, particularly MTs, have also been implicated in the control of cell shape via their influence on the pattern of cell wall deposition. Although the organization of interphase cortical MTs is related in a predictable way to cell shape and the pattern of cell expansion, very little is known about how their arrangement is controlled (reviewed in
One approach to tackling unsolved problems concerning the cytoskeletal basis of cell division and morphogenesis is isolating and analyzing mutants that are affected in these processes. In recent years, this approach has begun to yield new information regarding genes and molecules required for spatial regulation of cell division and morphogenesis during plant development (e.g.,
Observations on the effects of this mutation on cell division have raised many questions regarding the cytoskeletal basis of the tan1 mutant phenotype. For example, are division planes established during prophase as marked by the formation of PPBs and ADZs? If so, do these arrays form in orientations that predict the abnormal planes of cell division found in developing mutant leaves, or are they oriented normally, implying that the division defects are due to events occurring at later stages of the cell cycle? Previous work with tan1 has also shown that despite the fact that cells in all tissue layers divide in abnormal orientations throughout the development of mutant leaves, these leaves acquire normal shapes ( To address these questions, we undertook an investigation of cytoskeletal organization in developing tan1 leaves compared with their wild-type siblings. The results of this analysis show that the Tan1 gene is required for the normal positioning of cytoskeletal arrays associated with cell division at all stages of the cell cycle but not for their formation. Analysis of interphase cortical MTs suggests that mutant leaves are of normal shape in part because of regional control of MT organization during interphase.
Analysis of Cell Division Orientations in tan1-py1 Leaf Primordia
To do this, we used a whole-mount technique to visualize recently formed epidermal cell walls in leaf primordia that were ~1 cm long. At this stage, wild-type leaves are ~1% of their final length, most cells are rectangular, little cellular differentiation is apparent, as evidenced by the absence of guard mother cells and trichomes, and cells are dividing in both transverse and longitudinal orientations throughout the leaf (
In wild-type primordia, approximately two-thirds of new cell walls identified by this method are oriented transversely relative to the mother cell's long axis (at an angle of 76 to 90°), and the remaining one-third are oriented longitudinally (0 to 15°) (Figure 2A and Figure 2C). By comparison, previous analysis of new cell wall orientations in wild-type 1-cm leaf primordia by using scanning electron microscopy (SEM) showed approximately equal proportions of transverse and longitudinal divisions (
In tan-py1 leaf primordia, a similar spectrum of new cell wall orientations can be observed by using the acriflavine staining method compared with that found previously in tan-Mu1 primordia by using SEM (Figure 1 and Figure 2B). However, the frequency of transverse divisions observed in tan1-py1 primordia (~25%) is lower than that observed previously for tan1-Mu1 (~50%;
In summary, the results of the present analysis using acriflavine staining to examine the effects of tan-py1 on cell division orientations are broadly similar to those obtained in the previous analysis of tan-Mu1 by using SEM; however, they paint a somewhat different picture when the frequencies are considered. The previous analysis showed that the frequency of transverse divisions in tan-Mu1 primordia was almost unchanged compared with that of the wild type, whereas the frequency of longitudinal divisions was reduced from almost 50% in the wild type to <5% in mutants. This result was interpreted to suggest that the Tan1 gene product may be selectively required for longitudinal cell divisions (
Analysis of MT Arrays Associated with Cell Division in Wild-Type and tan1 Leaf Primordia
As shown in Figure 4A% of PPBs in wild-type leaf primordia are transverse (oriented 76 to 90° relative to the cell's long axis), whereas 22% are longitudinal (oriented 0 to 15° relative to the long axis). These frequencies are in close agreement with those obtained for newly formed cell walls by using the acriflavine method (Figure 2C). Only 2% of wild-type PPBs were found at oblique angles (16 to 75°), and only 2% were found in an asymmetrical position (outside of the middle third of the cell). Thus, the vast majority of PPBs in wild-type leaf primordia are symmetrically positioned and are either transversely or longitudinally oriented. As illustrated in Figure 4B% of wild-type spindles are transversely oriented (i.e., the spindle axis is parallel to the long axis of the cell), whereas 10% are longitudinally oriented. Unexpectedly, the majority of spindles (57% altogether) are obliquely oriented, indicating that the spindles rotate during mitosis in wild-type cells and that their orientations are not constrained by any prior definition of the division site, as indicated by the PPB. Analysis of phragmoplast orientations (Figure 4C) indicates that phragmoplasts are repositioned during cytokinesis to "correct" for the oblique spindles: although oblique early phragmoplasts are often seen in wild-type cells (e.g., Figure 3A, arrow labeled with a circle), the vast majority of late phragmoplasts (those whose edges are within 2 µm of the parental wall at both ends) are either transversely (73%) or longitudinally (24%) oriented. Thus, as would be expected, the distribution of late phragmoplast orientations (Figure 4C) closely matches that of PPBs (Figure 4A) as well as that of new cell walls (Figure 2C). In tan1 leaf primordia, cells with PPBs, spindles, and phragmoplasts were seen at approximately the same frequency as in wild-type primordia on a per cell basis as well as at similar relative frequencies. These arrays were seen at a variety of orientations relative to the long axis of the dividing cell, but they always appeared structurally normal (Figure 3B to D). Virtually all PPBs in mutant cells are straight, and 90% are positioned symmetrically (within the middle third of the cell). Thus, asymmetrically placed PPBs are found more frequently than they are in wild-type cells (10 versus 2%) but are still a small minority. As might be expected from the very low frequency of longitudinal divisions within this population of cells, a 10-fold decrease in the proportion of longitudinal PPBs was observed (2%) when compared with the wild type (22%). As illustrated in Figure 3B to D and Figure 4A, the vast majority of PPBs formed by mutant cells are transverse or slightly oblique (80% at a 76 to 90° angle; 12% at a 61 to 75° angle relative to the long axis). Notably, PPBs predicting the abnormally shaped and oriented new cell walls found in this population of cells were not observed. The abnormal orientations of new cell walls seen in mutant cells appear to result mainly from events that occur during mitosis and cytokinesis. Spindle orientations in mutant cells are highly variable, indicating that spindle rotation occurs during mitosis in mutant cells as it does in wild-type cells (Figure 3B and Figure 4B). By the end of the cell cycle, only 28% of late phragmoplasts are transverse (Figure 4C). Thus, unlike the situation in wild-type cells, in which the orientations of late phragmoplasts closely match those of PPBs, a substantial proportion of mutant phragmoplasts fail to return to the transverse orientations occupied by most PPBs. As seen earlier in the analysis of new cell wall orientations (Figure 2B), many of the late phragmoplasts seen in mutant cells are curved (see arrows marked with asterisks in Figure 3C and Figure 3D). Indeed, the majority of late phragmoplasts in the 0 to 15° class are curved and form at a steeply oblique angle relative to the cell's long axis. Thus, the distribution of late phragmoplast orientations and shapes seen in mutant cells (Figure 4C) corresponds closely to that shown in Figure 2C for new cell walls in this population of cells.
Analysis of Actin Arrays Associated with Cell Division in Wild-Type and tan1 Leaf Primordia Examination of actin arrays in each of three wild-type and three mutant leaf primordia revealed no differences in actin organization at any stage of the cell cycle. Figure 5 illustrates cells at various stages of the cell cycle that are double labeled for MTs (Figure 5A, Figure 5C, Figure 5E, Figure 5G, and Figure 5I) and actin (Figure 5B, Figure 5D, Figure 5F, Figure 5H, and Figure 5J). Both mutant and wild-type cells have all classes of F-actin typically found during interphase: randomly oriented cortical actin filaments, longitudinal subcortical actin bundles, and actin bundles found within transvacuolar cytoplasmic strands and associated with the periphery of the nucleus (Figure 5B). As cells approached mitosis (early preprophase), cortical actin filaments became more uniformly oriented in the transverse direction before the formation of actin bands (data not shown).
Examination of cortical actin in 120 preprophase–prophase cells from wild-type and mutant leaves combined revealed three distinct arrangements of actin. Previous work has established that as prophase proceeds, MT PPBs become progressively narrower ( Actin filaments and MTs are coaligned in wide bands during the initial stage (stage I) of PPB formation (arrows marked I in Figure 5A and Figure 5B). At this stage, the width of the actin PPB usually exceeds that of the MT PPB (19.0 ± 9.5 µm for MT PPBs versus 22.9 ± 9.3 µm for actin PPBs). The high variability in band width during this stage reflects the wide range of values within which MT PPBs narrow while intact actin PPBs are retained. During stage II, MT PPBs are consistently narrower than at stage I (14.2 ± 4.3 µm), and the density of actin diminishes in the central area of the band (arrows marked II in Figure 5A and Figure 5B). This area, a putative early ADZ, is generally narrower than the corresponding MT PPB (10.7 ± 3.8 µm). Parallel actin filaments, which are remnants of the former band, flank the ADZ and extend past the edges of the MT PPB. In some cases, the width of the remnant band is equivalent to the stage I actin band; however, in others, the parallel filaments extend over larger areas of the cell cortex and are indistinguishable from non-PPB cortical actin filaments. During stage III of PPB development, both the MT PPB (8.2 ± 3.1 µm) and ADZ (5.8 ± 3.0 µm) are even narrower, with the ADZ again being consistently narrower than the MT PPB (arrows marked III in Figure 5A to D). A pair of thick actin cables frequently delineate the edges of the ADZ from the persistent cortical F-actin (see Figure 5D), which in some cases is still arranged in parallel arrays; however, in other instances, it is faintly stained and randomly organized. Several clear examples were observed in which the stage III actin arrangement persisted after the disappearance of the MT PPB (e.g., leftmost cell in Figure 5C and Figure 5D). Although ADZs were clearly and consistently observed in both wild-type and tan1 mutant cells during prophase, they were not consistently observed during mitosis and cytokinesis in either wild-type or mutant cells. Those ADZs that were observed demonstrate that wild-type cells can maintain ADZs in both transverse (Figure 5E and Figure 5F) and longitudinal (Figure 5G and Figure 5H) orientations and in the transverse orientation in the mutant (Figure 5I and Figure 5J). However, the low frequency at which ADZs were identified during mitosis and cytokinesis meant that little information could be obtained concerning the maintenance or orientation of division sites at these stages of the cell cycle. In summary, this analysis demonstrates that actin bands and ADZs are present during prophase in both tan1 mutant and wild-type cells. Furthermore, in tan1 cells, they have the same temporal and spatial relationship to MT PPBs observed in wild-type cells, that is, they appear to undergo the same maturation process during prophase, and they always coincide with MT PPBs. Thus, we conclude that actin PPBs and ADZs are affected by the tan1 mutation in the same way as the PPB of MTs: they are present and structurally normal but form mainly in transverse orientations instead of forming both transversely and longitudinally.
Analysis of Interphase Cortical MT Arrays in Wild-Type and tan1 Leaf Primordia
It is well established that interphase cortical microtubules generally are aligned perpendicular to the major axis of cell expansion (reviewed in A representative image of cortical microtubules in a wild-type leaf primordium is shown in Figure 6A. Although there is variation in the degree and orientation of alignment observed, cortical MTs of most interphase cells are predominantly transversely aligned. Occasionally, cortical MTs are aligned predominantly parallel to the long axis of the cell (Figure 6A, arrow). It is likely that such cells either recently completed a longitudinal division or were about to divide longitudinally at the time of fixation, because they are most often seen in areas in which surrounding cells are at various stages of the longitudinal division process. In some cells, little or no alignment of interphase cortical MTs could be discerned.
Images of cortical MT arrays in two different areas of tan1 mutant leaf primordia are shown in Figure 6B and Figure 6C, illustrating considerable variation in the orientations of long cell axes and in the arrangements of interphase cortical MTs. Alignment of cortical MTs was observed within most cells; for many, the orientation of alignment is perpendicular to the cell's long axis (e.g., Figure 6B, upper right quadrant). Interphase cortical MTs generally are not coaligned across cell fields of the size shown in Figure 6B and Figure 6C. However, a striking degree of coalignment typically is observed across boundaries at which shifts in cell orientation occur. For example, cortical MTs in the cells indicated with arrowheads in Figure 6B and Figure 6C are better aligned with the MTs of neighboring cells than they are with the indicated cell's own transverse axis. Not all cells follow this rule: MTs in some cells are neither coaligned with MTs of neighboring cells nor transverse to the cell's long axis. In view of the observed combination of transversely aligned, regionally coaligned, and sometimes unpredictably arranged interphase cortical MTs, it seems remarkable that when mutant cells enter prophase, PPBs are virtually always oriented transversely (Figure 4A). Notably, this occurs even in areas in which the interphase cortical MTs are all oriented differently (e.g., Figure 6B, cell marked with large arrow). These observations suggest that there may be some regional influence on interphase cortical MT orientations, which helps to guide normal morphogenesis in mutant leaves but apparently has no impact on the choice of division plane in cells preparing to divide.
In a previous study, it was shown that tan1 causes cells to divide in abnormal orientations throughout maize leaf development (Figure 1;
Analysis of cytoskeletal arrays associated with cell division in wild-type leaf primordia led us to infer the sequence of events depicted in Figure 7A. As expected from a large body of previous work showing that MT PPBs accurately predict planes of cell division in a wide variety of plant cells (reviewed in
Although this high frequency of oblique spindles was unexpected, it was not surprising in view of earlier reports of spindle rotation followed by compensatory movements of the phragmoplast to position the cell plate at the site previously occupied by the PPB (e.g.,
The corresponding sequence of events inferred from analysis of cytoskeletal arrays in tan1 mutant leaf primordia is shown in Figure 7B. During prophase, all cytoskeletal arrays observed in wild-type cells were also formed in mutant cells and appeared to be structurally normal: wide, early PPBs containing MTs and actin filaments, and late, narrow PPBs of MTs coinciding with ADZs. Thus, with respect to all pro-phase events that we were able to evaluate, division planes appeared to be established normally in mutant cells but formed mostly in transverse orientations. Therefore, the Tan1 gene is apparently not required for division plane establishment per se but is required for the establishment of longitudinal division planes. One proposal to explain how cells choose a division plane is that they seek the shortest path that will halve the volume of the cell ( As illustrated in Figure 7B, our results clearly show that most of the abnormally oriented divisions in mutant cells can be attributed to the frequent failure of phragmoplasts and associated cell plates to attach at cortical sites previously occupied by PPBs. During mitosis, approximately half of the spindles rotate to become oblique; by the end of cytokinesis, the majority of cells have non-transverse phragmoplasts in the variety of orientations and conformations illustrated, which are similar to those seen for new cell walls in mutant primordia. Thus, we conclude that Tan1 is also required during cytokinesis for guidance of phragmoplasts and new cell walls to previously established division sites. Because non-transverse phragmoplasts outnumber oblique spindles, some of these phragmoplasts must arise in cells that had transverse spindles at mitosis, suggesting that aberrantly oriented divisions are not due exclusively to a failure to correct for spindle rotation. Indeed, using time-lapse video microscopy to watch living cells undergoing division, we observed a mutant cell in which the cell plate arose in a transverse orientation and drifted radically during cytokinesis to form an oblique, curved cell wall similar to the one illustrated in the lower right corner of Figure 7B (H.J. Passas and L.G. Smith, unpublished observations). Our observations suggest that the requirement for Tan1 to achieve proper phragmoplast guidance applies not only to cells dividing longitudinally but to all dividing cells in the leaf primordium. It may be that many mutant cells divide transversely simply because this is a common outcome for an elongated cell that establishes a transverse division plane at prophase, even in the absence of phragmoplast guidance during cytokinesis. Because ADZs could not be identified consistently during mitosis and cytokinesis in either wild-type or mutant cells, we were unable to determine whether mispositioning of phragmoplasts during cytokinesis results from a failure to maintain the division site throughout the cell cycle or a failure of the phragmoplast to interact with it appropriately.
Our analysis of the cytoskeletal basis of the tan1 mutant phenotype shows that this mutation disrupts the spatial regulation of cytokinesis differently than do the tonneau (ton) mutations of Arabidopsis. Examination of MT arrays in ton embryos showed that they lack PPBs altogether, which probably accounts for the abnormally shaped cells found in these embryos ( Similarly, Tan1 is required for the establishment of longitudinal division planes and also for guidance of phragmoplasts to cortical division sites. Although our analysis did not reveal differences in actin organization between mutant and wild-type cells, the similarities between the effects of cytochalasins and the effects of the tan1 mutation lead us to speculate that the Tan1 gene product may be involved in the mechanism by which actin influences the positioning of new cell walls. It is hoped that ongoing molecular analysis of the Tan1 gene will elucidate further the role of this gene in the spatial regulation of cytokinesis. Finally, to explore the problem of how tan1 leaves can acquire normal overall shapes despite the abnormal division behavior of their constituent cells, we also investigated how the tan1 mutation affects arrangements of interphase cortical MTs during primordial stages of leaf development. As expected on the basis of their rectangular shapes, most interphase cells in wild-type leaf primordia have predominantly transverse cortical MTs. In mutant leaf primordia, we found a variety of cortical MT arrangements, and no rule could be devised that would allow us to predict or explain the arrangement in every cell. Nevertheless, where cells with nonaligned long axes are juxtaposed, cortical MTs tend to be coaligned across cell boundaries rather than having arrangements related to individual cell shapes.
Several previous studies have described instances in which neighboring cells have MT arrays that are coaligned (
Plant Material
Analysis of Cell Division Orientations
Midplane optical sections from at least 10 fields of view were collected from dispersed areas for each of three wild-type and three mutant individuals. To analyze cell division orientations, we examined images to identify all walls that were stained less intensely than the walls they adjoined at both ends, indicating a lower content of cellulose. More than 1000 recently formed cell walls were analyzed in each data set (wild type and mutant). A line was drawn joining the two end points of each new wall, and a second line was drawn corresponding to the long axis of the mother cell or its best approximation. For each cell wall analyzed, the angle between these two lines was measured to obtain the data plotted in Figure 2C. The Fisher-Behrens test for comparison of two populations with unequal variances (
Labeling and Analysis of Microtubules and Nuclei (DNA) Images of microtubules and DNA were collected on the Zeiss laser scanning confocal system by using a 63x oil immersion objective. Fluorochromes were excited successively using either the 488-nm (FITC) or 568-nm (PI) lines from an ArKr laser. Each emission wavelength passed through a double dichroic mirror (FT 488 / 568) and was selected for imaging using the dichroic mirror DCLP 560. FITC images were collected using emission filter BP 515-540, and PI images were collected using emission filter LP590. Surface and midplane optical sections for each fluorochrome were collected for at least 15 fields of view representing dispersed areas of four mutant and four wild-type leaf primordia. This collection of images was used to reconstruct in each field of view the shape, nuclear position, and microtubule (MT) array present in every cell containing a preprophase band (PPB), spindle, or phragmoplast.
More than 1000 such dividing cells from each data set (wild type and mutant) were analyzed. For each dividing cell, we drew a reference line down the middle to represent the long axis or its best approximation. A second line was drawn to represent the orientation of the MT array; this line was parallel to PPBs and phragmoplasts and perpendicular to the spindle axes. For phragmoplasts that were curved or were elongated such that only their edges contained MTs, a straight line was drawn through the two ends of the phragmoplast to assign its orientation. For each MT array, the angle between the two lines was determined to obtain the angles plotted in Figure 4. A distinction was made between early phragmoplasts (>2 µm from the parent cell wall at one or both ends) and late phragmoplasts (<2 µm from the parental wall at both ends). Because late phragmoplasts were considered to be a better indicator of the final position of the cell plate, data for this category only were included in Figure 4C. The Fisher-Behrens test for comparison of two populations with unequal variances (
Double Labeling of F-Actin and MTs
The fixed, digested, detergent-extracted leaf segments were incubated overnight at room temperature in a mixture of B512 anti– Double labeling of MTs and actin was observed using a 63x NA oil immersion objective on a Bio-Rad MRC-600 confocal laser scanning system fitted with an ArKr laser and coupled to a Zeiss Axiovert microscope. Surface and midplane optical sections of FITC-labeled MTs (excitation at 488 nm; BHS filter block) and Texas Red–labeled actin (excitation at 568 nm; YHS filter block) were recorded successively for each field of view (filter blocks; BioRad). In general, the best MT labeling was found near the edges of the tissue segments, whereas the best actin labeling was found toward the center. However, sufficient overlap between MT and actin staining was obtained to allow analysis of both images in >100 cells (wild type and mutant combined) containing a PPB, spindle, or phragmoplast.
We gratefully acknowledge financial support for this work from the National Institutes of Health (Grant No. R01-GM53137 to L.G.S.) and from a U.S. Department of Agriculture/National Science Foundation/Department of Energy Interagency grant to the Cytonet Group, which supported our collaboration. We thank the Maize Genetics Cooperation Stock Center for seeds; Kim Gallagher, Jocelyn Malamy, and Erik Vollbrecht for advice and help with the acriflavine staining procedure; Susan Whitfield for help with preparing figures; Tony Perdue for help with confocal microscopy; Margaret Sammut for technical assistance with the MT/actin labeling; and Dawn Franklin for help with the data analysis. We are grateful for stimulating and helpful discussions with Adrienne Hardham, Brian Gunning, Paul Green, and Richard Cyr, and thank John Fowler, Brian Gunning, and Kim Gallagher for helpful comments on the manuscript. Received March 30, 1998; accepted September 8, 1998.
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ABSTRACT
INTRODUCTION
75° to the long axis of the parent cell. In mutant cells, the frequencies of new cell walls at all angles are significantly different from those in wild-type cells (P < 0.05). Error bars indicate standard errors. For the wild type, n = 1807; for tan1, n = 1167. Bar in (A) = 20 µm for (A) and (B).
-tubulin antibody (Sigma) and Texas Red–conjugated phalloidin (Molecular Probes, Inc., Eugene, OR). To prepare this staining solution, we evaporated methanol from the appropriate volume of a 6.6 µM Texas Red–phalloidin methanol stock solution. The precipitated Texas Red–phalloidin was then redissolved to a final concentration of 0.66 µM in anti–