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Department of Plant Biology, Ohio State University, 1735 Neil Avenue, Columbus, Ohio 43210
Received for publication August 28, 1998. Accepted for publication November 24, 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Arabidopsis • asymmetric division • Brassicaceae • differentiation • division site • guard cell • meristemoid • stomate
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Horvitz and Herskowitz, 1992
; Sachs and Novoplansky, 1993
; Sylvester, Smith, and Freeling, 1996
; Larkin et al., 1997
; Croxdale, 1998
).
Stomatal development and differentiation have been described (reviewed in Palevitz, 1981
; Sack, 1987
; Larkin et al., 1997
), but there are few cytological studies of the development of the kidney-shaped stomata of dicotyledons (e.g., Landré, 1972
; Galatis and Mitrakos, 1979,
1980
; Galatis et al., 1982
). Moreover with the emergence of Arabidopsis as a valuable genetic system for identifying genes involved in cell patterning and development and with the identification of several stomatal mutants in Arabidopsis, it is important to identify key ultrastructural events and stages leading to the formation and differentiation of wild-type stomata (Yang and Sack, 1995
; Larkin et al., 1997
; Schiefelbein, Masucci, and Wang, 1997
; Geisler, Yang, and Sack, 1998
).
Ultrastructural data in the literature on Arabidopsis stomata are confined to a few images of mature cells (Hippe-Sanwald, 1993
; Lascève, Leymarie, and Vavasseur, 1997
). Aspects of the distribution and timing of stomatal formation in Arabidopsis are known (Pyke, Marrison and Leech, 1991
; Telfer and Poethig, 1994
; Berger et al., 1998
), but only preliminary cytological data have been published on precursor cells and on stomatal development in this plant (Yang and Sack, 1995
; Serna and Fenoll, 1997
). Here we describe, using light and electron microscopy, the types of divisions of stomatal precursor cells and the major morphologically detectible stages that characterize stomatal development in Arabidopsis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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150 µmol · m-2 · s-1 and a room temperature of 23°C. Unless otherwise noted, all observations were derived from examination of the first pair of leaves, which are subopposite.
Microscopy
Differential interference contrast microscopy was used to examine hand-cut sections of fresh leaves. Possible division patterns from fixed tissues were reconstructed as in Paliwal (1967)
and Landré (1972)
using leaves from 3- to 21-d-old seedlings that were cleared according to Geisler, Yang, and Sack (1998)
. Cleared material was also used to calculate cell size, which was estimated by tracing the paradermal outline of cells of different stages from a bright-field videomicroscope image onto an acetate overlay on a video monitor. The outlines were digitally scanned and areas were determined for 60 cells of each stage using NIH image analysis software.
For transmission electron microscopy, leaf pieces from 5- to 15-d-old seedlings were fixed in 3% (v/v) glutaraldehyde in 75 mmol/L phosphate buffer at 4°C for 6–8 h. The tissue was then rinsed, postfixed in 2% (w/v) osmium tetroxide for at least 3 h, dehydrated in an acetone series, and embedded in Spurr's epoxy resin. Thin sections cut with a diamond knife were stained with aqueous uranyl acetate and lead acetate and examined at 60 kV with a CM-12 Phillips electron microscope.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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. The SM also can divide asymmetrically one or more times before becoming a GMC. With respect to timing, Arabidopsis stomata develop in a mosaic fashion, and several stages can often be seen side by side (Figs. 2–3).
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). One way that this pattern appears to arise is from meristemoids that divide twice (D2, Fig. 1); thus, these D2 complexes are produced by a total of three asymmetric divisions including that of the MMC.
Meristemoid formation and cytology
The earliest cytological event detected in stomatal precursor cell formation was the polarization of cytoplasm in the meristemoid mother cell. Prior to the asymmetric division of the MMC, the nucleus and most of the cytoplasm become located on one side of the cell near the apparent division site, the future location of cell plate fusion with the parent wall (Fig. 4). The division site in MMCs appeared marked by a weak preprophase band of microtubules (PPB) consisting of a single layer (Figs. 4–6). The cell wall at the division site has the same thickness as elsewhere in the cell.
MMCs were found in regions devoid of stomata as well as in cells next to stomata. Asymmetric divisions of the latter type of MMC produced satellite meristemoids. These divisions are oriented such that the satellite meristemoid (and the GMC it produces) is placed away from the already existing stomate (Figs. 1,7).
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9 µm. Older meristemoids that appear to be premitotic display a polar distribution of cell contents with a vacuole at one end, and the nucleus and a preponderance of cytoplasm at the other end (meristemoid "b" in Figs. 2 and 9 ). Relatively few meristemoids were found at this stage in fixed and sectioned material. In several polarized meristemoids, a weak preprophase band of microtubules (PPB) appeared to be present in the form of a mostly single layer of aggregated cortical microtubules on both sides of the nucleus (Figs. 9–11). This band was located in a position that would predict the formation of a smaller triangular cell and a larger sister cell. No cell wall thickenings were detected at the apparent division site.
The large vacuole eventually becomes allocated to the larger daughter cell of the asymmetric division of the meristemoid. In some divisions, there was not a great disparity in the sizes of the two daughter cells (e.g., Fig. 12). Even in these cases, there usually was a difference in the shape and in the extent of vacuolation of the two daughter cells, the triangular cell, presumably the regenerated meristemoid, being less vacuolated.
It is likely that the positions of some of the asymmetric divisions of meristemoids are spatially regulated. The two meristemoids shown in Fig. 2 appear to be part of what might have become anisocytic stomatal complexes. Meristemoid "a" is surrounded by three vacuolated cells whose outer walls (away from the meristemoid) are almost continuous, a pattern consistent with the possibility that the meristemoid arose from the division of a single MMC and then divided twice (a D2 meristemoid, see Fig. 1). If so, then the larger cell products from the two asymmetric divisions of the meristemoid were placed to the outside of the cell lineage. An earlier stage of such a polar placement may be shown in meristemoid "b" in Fig. 2. If this meristemoid were also part of an anisocytic complex, then the polarity of its probable second division would have been positioned such that the vacuole would be to the outside; a subsequent division would thus have positioned the larger cell product, the neighbor cell, to the outside, producing an anisocytic stomatal cell complex and thus surrounding the future stomate with three neighbor cells produced from the same MMC (see Fig. 1). However, not all stomatal complexes are anisocytic, e.g., some complexes contain four cells (Fig. 2, top left). It is difficult to reconstruct a likely history of divisions from cell wall patterns in some stomatal complexes.
Guard mother cell development and division
After the meristemoid has finished dividing, it converts into a guard mother cell, the final stomatal precursor (Fig. 1). Young GMCs can be distinguished morphologically from meristemoids by their increased accumulation of starch in plastids, by their larger vacuoles, and by their more rounded shape (compare Fig. 13 with Figs. 3, 7, 14). Mature guard mother cells that are oval in shape are about twice the paradermal area of meristemoids and have a mean area of 74.3 ± 2.0 µm2 with mean lengths and maximal widths of 11.4 ± 0.2 and 9.4 ± 0.2 µm, respectively.
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0.2–0.4 µm thick and 2.7–3.4 µm long. The rest of the cell wall is typically 0.05–0.09 µm thick. Some thickenings span cell junctions or corners (Fig. 15, lower left), and other thickenings are entirely located between cell corners (Fig. 15, upper right). In GMCs that are somewhat elongated, these thickenings are usually perpendicular to the long axis as seen in paradermal section (Figs. 14–15), and this position at the ends of the cell is often maintained during GMC expansion. Prior to and during early wall thickening, microtubules, often as a single cortical layer, are present on opposite sides of the GMC, either under new, developing thickenings (Fig. 14) or in locations where presumably the thickenings subsequently arise. Cortical microtubules are less frequent elsewhere in the GMC at these stages. During GMC expansion the wall thickenings increase in width (Figs. 14–15), a widening accompanied by the formation of a PPB with several layers of microtubules located opposite the thickenings (Figs. 15–17).
During GMC telophase, the reforming nuclei and the cell plate are aligned at right angles to the wall thickenings (Fig. 18). Both early and late cell plates are sometimes slightly curved or zigzag-shaped. The cell plate fuses with the wall thickenings and frequently bisects them (Figs. 19–20). The wall thickenings are still evident in developing stomata (Figs. 20–23). Thus, the wall thickenings mark the location where the cell plate will fuse with the parent cell wall. This division site is placed such that cytokinesis is symmetrical and produces two guard cells of equal size and fate.
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The pore develops from the ventral wall. Early on, microtubules are abundant along the length of the ventral wall. Portions of the middle lamella between the two ventral walls become electron lucent. Then a lens-shaped thickening develops at the mid-length of the ventral wall (Figs. 21–22) where the pore eventually forms. Anticlinally oriented cortical microtubules are concentrated around the growing pore thickening. The middle lamella at the pore site becomes electron dense (Fig. 22). The pore is created by a separation at the middle lamella that appears to involve the stretching of electron dense material (Fig. 23). In the mature stomate, the surface of the pore is somewhat undulate, often in a complementary fashion on opposite sides of the pore as if these ribs and grooves might fit together upon full closure (Fig. 24). Pore opening results in the attainment of the typical kidney- or bean-shaped guard cell (Fig. 25). Parts of the separating pore wall can sometimes be seen as strands connecting the two sides of the pore (arrowhead in Fig. 26).
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Various cytoplasmic changes accompany stomatal maturation. Starch accumulation increases strongly after the pore opens (Figs. 23–25). Vacuole enlargement occurs prior to and during pore formation (Figs. 21–24). In mature (functional) stomata, large vacuoles are located at both ends of the guard cell, and the nucleus is usually located opposite the pore and closer to the inner paradermal wall (towards the substomatal cavity) of the guard cell (Figs. 24–27).
Mature stomata are on average 22.2 ± 0.2 µm wide and 15.6 ± 0.2 µm long. The mean paradermal area of mature stomata 243.8 ± 3.9 µm2 (including the pore), is three times larger than the GMC and about six times larger than the meristemoid.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Importance of asymmetric divisions
Arabidopsis meristemoids form in an asymmetric division, and meristemoids themselves divide asymmetrically. These divisions are asymmetric in cell fate and also usually in cell size. Premitotic meristemoids also display an asymmetric distribution of the nucleus, cytoplasm, vacuoles, and PPB. Similar polarities have been found in meristemoids in the Fabaceae and in the formation of stomatal subsidiary cells in monocots (Galatis and Mitrakos, 1979
; Galatis et al., 1982
; Cho and Wick, 1989
; Kennard and Cleary, 1997
). These premitotic polarities probably function in positioning the future cell wall and in distributing cell contents asymmetrically upon division.
However, some stomatal meristemoid divisions in Vigna are reported to be equal in the distribution of vacuoles and in the size of the daughter cells (Fig. 28 in Galatis and Mitrakos, 1979
). And there are many examples in non-plant systems of asymmetric divisions producing daughter cells of different fate but with the same size (e.g., Horvitz and Herskowitz, 1992
). But in Arabidopsis most meristemoid divisions were cytologically polar and unequal in the size of the products. Even in those few cases where the sizes were almost equal, there were still differences in vacuole distribution and in the shape of the daughter cells. The key event in all asymmetric divisions may be the unequal distribution of molecular determinants specifying cell fate (e.g., Rhyu, Jan, and Jan, 1994
). It remains to be determined whether the cytoplasmic polarities found in Arabidopsis meristemoids are necessary for the allocation of cell fate determinants.
A similar issue concerns the importance of the preprophase band of microtubules in stomatal formation. McClinton and Sung (1997)
found that stomata are present in the fass (tonneau) mutant of Arabidopsis, which does not form a PPB. Assuming that PPBs were also absent from stomatal precursors, then either these asymmetric divisions can occur without PPBs or stomatal formation can bypass asymmetric divisions.
The PPBs found in asymmetric divisions of wild-type Arabidopsis stomatal precursor cells seem weaker than in the symmetric division of the GMC, whereas in legumes no such difference was reported (Galatis et al., 1982
). This difference in Arabidopsis might result from the period of maximal microtubule accumulation being relatively short, from a fixation protocol that could be sub-optimal for microtubules, or it could be representative for Arabidopsis. While PPBs have previously been described in Arabidopsis, to our knowledge this has only been at the light microscope level (e.g., McClinton and Sung, 1997
).
Asymmetric divisions and formation of stomatal complex
It is likely that the asymmetric divisions that produce the anisocytic stomatal complex in Arabidopsis meristemoids are positionally regulated. The anisocytic stomatal complex consists of three neighbor cells of which one is much smaller than the other two. This type of complex is representative for the Brassicaceae and is found in Arabidopsis (Figs. 1–3; Metcalfe and Chalk 1950
; Paliwal, 1967
; Pant and Kidwai, 1967
; Landré, 1972
; Telfer and Poethig, 1994
; Yang and Sack, 1995
; Serna and Fenoll, 1997
). Analysis of the arrangement of cell walls suggests that anisocytic complexes can be formed by two divisions of the meristemoid (Fig. 1, D2) and that the premitotic polarity and division site for the second division are positioned so that the larger cell product is placed to the outside (Fig. 2).
But meristemoids appear to divide a variable number of times, and many stomatal complexes are not anisocytic (this study; Landré, 1972
; Galatis and Mitrakos, 1979
; Yang and Sack, 1995
; Serna and Fenoll, 1997
). Berger et al. (1998)
also found evidence for a variable number of divisions leading up to stomatal formation in Arabidopsis hypocotyls. Given this variability, a more direct description of meristemoid behavior and stomatal patterning will require studying the same cells through time, e.g., using dental resin replicas (Sachs and Novoplansky, 1993
).
Meristemoid and guard mother cell markers
Stage-specific markers for different precursor cells are valuable for the cytological, molecular, and genetic analysis of stomatal development and patterning. Meristemoids are distinguishable as small, mostly triangular cells. Newly formed meristemoids are densely cytoplasmic with a central nucleus. In premitotic meristemoids (and MMCs), the nucleus, cytoplasm, vacuoles, and PPB are distributed asymmetrically. Guard mother cells are larger, more rounded, and contain more starch than meristemoids, and GMCs also have wall thickenings at opposite ends of the cell.
Although GMCs originate from meristemoids, no cytological events accompanying this conversion were identified. Cells starting to convert to GMCs may express genes involved in the specification and differentiation of the GMC. If so, these "pre-GMCs" might look like newly formed meristemoids, but not premitotic meristemoids.
Wall thickenings mark the GMC division site
Arabidopsis guard mother cells have specialized wall thickenings at both ends that are later intercepted by the fusion of the cell plate. Thus, these thickenings are a morphological manifestation of the division site in addition to the spatially-associated PPB (Galatis et al., 1982
; Mineyuki and Gunning, 1990
).
Such thickenings have also been found in GMCs in 20 members of the Fabaceae (Galatis and Mitrakos, 1979
; Galatis et al., 1982
), but have not been described in GMCs from other families. There has been no systematic study to determine which taxa have GMCs with thickenings, but they appear to be absent from mosses, ferns and grasses (Galatis, 1982
; Sack and Paolillo, 1985
; Apostolakos, Panteris, and Galatis, 1997
). These thickenings are also absent from stomatal meristemoids in Arabidopsis and in legumes (this study; Galatis and Mitrakos, 1979
; Galatis et al., 1982
). Although Packard and Stack (1976)
reported the presence of wall thickenings near the PPB in root cells of Allium undergoing symmetric divisions, thickenings were not unequivocally illustrated in their report and, if present, are not as thick or as specialized as in GMCs. To our knowledge, clear division site wall thickenings have not been described in any cell type except guard mother cells, suggesting that they are a unique feature of GMCs in some dicots.
The function of these wall thickenings is not known. The division site is thought to contain unknown factors that are responsible for guiding the edges of the cell plate to the correct site of insertion and fusion at the parent cell wall, and other factors that promote the maturation of the new cell wall (Mineyuki and Gunning, 1990
). Although the GMC wall thickenings predict where subsequent cell plate fusion will occur, so do PPBs in all cell types in which they occur. PPBs are also present in Arabidopsis and legume GMCs (Galatis and Mitrakos, 1979
; Galatis et al., 1982
). Thus, the GMC wall thickenings may play no direct role in the insertion of the cell plate.
Galatis et al. (1982)
suggested that these thickenings set up mechanical forces that promote the splitting of the stomatal pore during development. This possibility is supported by the observation that after pore opening, the end wall thickenings often cease to be distinguishable in legumes and in Arabidopsis. Another hypothesis is that the end wall thickenings act earlier in stomatal differentiation by retarding the local expansion of the GMC; this could promote the elongation of the young GMC and the attainment of an oval shape. If so, this would be one more example, along with the initiation of starch accumulation and vacuole enlargement, of stomatal differentiation actually beginning during the guard mother cell phase.
Stomatal differentiation
The events involved in the development and differentiation of the Arabidopsis stomate are comparable to those described using electron microscopy for other genera with kidney-shaped guard cells (e.g., Landré, 1972
; Galatis and Mitrakos, 1980
; Sack, 1987
).
The cell biological mechanisms controlling the attainment of the complex architecture of mature stomata are unknown. Although the developmental relationship between the cytoskeleton and the shaping of GMCs and guard cells has not yet been described at a light microscope level in Arabidopsis as it has for other genera (e.g., Marc, Mineyuki, and Palevitz, 1989
; Apostolakos, Panteris, and Galatis, 1997
), Arabidopsis stomata do contain a characteristic radial microtubule array that emanates from the cell cortex at developing and mature stomatal pores (L. Zhao and J. Nadeau, Ohio State University, unpublished data; Wasteneys, Willingale-Theune, and Menzel, 1997
). But fundamental questions remain about stomatal differentiation, such as how the pore site thickens in a coordinated fashion across two cells, how pore separation is localized and initiated (the only anticlinal walls in the epidermis that do so), how the complex distribution of wall thickenings throughout the guard cell is programmed, and what controls the distinct distribution of cell components (central nucleus, polar vacuoles). A comparable ignorance characterizes the possible role of these and other features, such as guard cell wall layering, in stomatal functioning.
Clearly, stomatal development involves an intricate series of events, some of which are variable, such as the number of asymmetric divisions, and others which are invariant, especially those related to guard cell differentiation. These data on stomatal development will provide a foundation for the analysis of the phenotypes of various stomatal mutants in Arabidopsis that affect stomatal patterning, guard mother cell cytokinesis, stomatal differentiation, and stomatal function and signal transduction (Armstrong et al., 1995
; Yang and Sack, 1995
; Larkin et al., 1997
). A coordinated cytological and molecular analysis of stomatal development and functioning should provide major new opportunities for understanding the mechanisms underlying these processes in an important and fascinating cell type.
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FOOTNOTES |
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2 Author for correspondence (sack.1{at}osu.edu)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Armstrong, F., J. Leung, A. Grabov, J. Brearley, J. Giraudat, and M. R. Blatt. 1995 Sensitivity to abscisic acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase. Proceedings of the National Academy Sciences, USA 92: 9520–9524.
Berger, F., P. Linstead, L. Dolan, and J. Haseloff. 1998 Stomata patterning on the hypocotyl of Arabidopsis thaliana is controlled by genes involved in the control of root epidermis patterning. Developmental Biology 194: 236–234.
Cho, S.-O., and S. M. Wick. 1989 Microtubule orientation during stomatal differentiation in grasses. Journal of Cell Science 92: 581–594.
Croxdale J. 1998 Stomatal patterning in monocotyledons: Tradescantia as a model system. Journal of Experimental Botany 49: 279–292.[Abstract]
Galatis, B. 1982 The organization of microtubules in guard cell mother cells of Zea mays. Canadian Journal of Botany 60: 1148–1166.
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Packard, M. J., and S. M. Stack. 1976 The preprophase band: possible involvement in the formation of the cell wall. Journal of Cell Science 22: 403–411.[Abstract]
Palevitz, B. A. 1981 The structure and development of stomatal cells. In P. G. Jarvis and T. A. Mansfield [eds.], Stomatal physiology, 1–23. Cambridge University Press, Cambridge.
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———, and D. J. Paolillo. 1985 Incomplete cytokinesis in the stomata of Funaria. American Journal of Botany 72: 1325 1333.
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A. Majewska-Sawka, A. Munster, and M. I. Rodriguez-Garcia Guard cell wall: immunocytochemical detection of polysaccharide components J. Exp. Bot., May 1, 2002; 53(371): 1067 - 1079. [Abstract] [Full Text] [PDF]
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R. G. Atkinson, R. Schroder, I. C. Hallett, D. Cohen, and E. A. MacRae Overexpression of Polygalacturonase in Transgenic Apple Trees Leads to a Range of Novel Phenotypes Involving Changes in Cell Adhesion Plant Physiology, May 1, 2002; 129(1): 122 - 133. [Abstract] [Full Text] [PDF]
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 B. Menand, T. Desnos, L. Nussaume, F. Berger, D. Bouchez, C. Meyer, and C. Robaglia Expression and disruption of the Arabidopsis TOR (target of rapamycin) gene PNAS, April 30, 2002; 99(9): 6422 - 6427. [Abstract] [Full Text] [PDF]
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M. Geisler, J. Nadeau, and F. D. Sack Oriented Asymmetric Divisions That Generate the Stomatal Spacing Pattern in Arabidopsis Are Disrupted by the too many mouths Mutation PLANT CELL, November 1, 2000; 12(11): 2075 - 2086. [Abstract] [Full Text]
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U. Menke, N. Renault, and B. Mueller-Roeber StGCPRP, a Potato Gene Strongly Expressed in Stomatal Guard Cells, Defines a Novel Type of Repetitive Proline-Rich Proteins Plant Physiology, March 1, 2000; 122(3): 677 - 686. [Abstract] [Full Text] [PDF]
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