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Anatomy and Morphology |
Section of Plant Biology, Division of Biological Sciences, University of California, Davis, California 95616 USA; Centro de Investigaciones Biológicas del Noroeste (CIBNOR), La Paz, Baja California Sur, Apartado Postal 128, México 23000
Received for publication August 2, 2001. Accepted for publication January 3, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Arabidopsis • Brassicaceae • cortex • development • root apical meristem • vascular tissue
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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consisted of five types in the seed plants. Schüepp (1926)
had nine types that covered both spore bearing plants and seed plants. Another German anatomist, von Guttenberg (1960)
, simplified the classification scheme by lumping all RAMs within two types—open and closed. Popham (1966)
used a system that consisted of eight types, based mostly on Janczewski's work. We chose von Guttenberg's system of open and closed because it was the simplest. He considered that root tissues and root cap either shared common initials (open) or had distinct initials (closed).
In closed organization all cell files of a tissue can be traced to a histogen (Hanstein, 1870
) or tier of initial cells. In roots with closed organization, the dermatogen, periblem, and plerome histogens derive the three primary meristems: protoderm (epidermis), ground meristem (cortex), and procambium (vascular cylinder) (Esau, 1953
; Rost, 1994
). The calyptrogen histogen was identified and named by Janczewski (1874)
and it derives the epidermis or is combined with the dermatogen to derive the epidermis and root cap.
There are a number of definitions for the term "initial." Clowes (1950)
states that cells are called initials because of their position within the meristem and not because of any special properties. Barlow (1996)
has suggested that there are two types of initials; structural initials, which are the cells to which all cell files in a root can be traced, and functional initials that in practice will give rise to cells in a lineage. Seago and Heimsch (1969)
define initials as cells at the most apical position of a tissue(s) or cell file. Further, when initials divide, one derivative remains meristematic and the other becomes part of the root body. Finally, Esau (1953)
defined an initial as "a cell that remains within the meristem indefinitely by combining self-perpetuation with addition of cells to the plant body" (p. 90). The definition used by Esau (1953)
is the most flexible one and it will be used in this paper.
Arabidopsis thaliana has closed root apical organization (Dolan et al., 1993
; Baum and Rost, 1996
; Kidner et al., 2000
). Baum and Rost (1996)
reported on the developmental behavior of the dermatogen/calyptrogen histogen (initial tier) and the early development of the root cap and epidermis. Using 1- and 2-wk-old sand-grown plants, it was shown that the cells within this histogen (consisting of the central columella initials and the peripheral root cap/protoderm initials) divided in a sequence resulting in a root cap whose three-dimensional structure resembled interconnected cones of decreasing size toward the inside. A transverse section taken at the level of the initial tier showed that the peripheral root cap cells (also called "lateral root cap cells") are in a spiral pattern. The sequential pattern of divisions creating a spiraling-cone root cap is a post-embryonic event, commencing later than 1 wk post-germination. The epidermis is created one cell at a time in sequence by a T division of the root cap/protoderm initial. The resulting protoderm initial cell divided anticlinally to form the first protoderm cell and the regenerated root cap/protoderm initial. Each protoderm cell divided again forming packets of up to 16 epidermal cells.
The periblem histogen tier that derives the cortex appears to be the most variable and dynamic tier. Unlike the other histogens, the names of cells associated with this tier are confusing. Von Guttenberg (1960)
calls the cells of the periblem "Verbindungszellen," which Esau (1965)
translated in a general way as meaning central or connecting cells. According to von Guttenberg (1960)
, the cells on the periphery of the "Verbindungszellen" are connecting cells, and he calls the cell in the very middle "the central cell." In Guttenberg's model, the single central cell gives rise to the connecting cells and columella initials in root meristems older than 48 h. Clowes (1961)
suggests Guttenberg's model is an adaptation of the apical cell theory used to describe the meristems of ferns and other lower vascular plants. The use of the term "central cells" is further confused by Clowes (1981)
when he uses the term in a different way to describe "the central cells of the columella." This terminology is further complicated by the use of the term "quiescent center" by Dolan et al. (1993)
. This tier of initials may be quiescent during early root development as suggested by Fujie et al. (1993)
, but later in development these cells do divide as we will show.
Baum and Rost (1998)
identified two components of the periblem. The central cells (quiescent center cells in the terminology of Dolan et al. [1993]
) they called "central ground meristem initial cells," and the peripheral part was called "ground meristem initials." Several other terms have also been used to describe the periblem initial tier. Zhu, Lucas, and Rost (1998)
attempted to clarify this abundance of terms and make their function more readily identifiable by calling the central part the "central cortex initials" and the peripheral part "cortex initials." We intended to continue using these terms to be consistent but reviewers and the cell ablation observations of van den Berg et al. (1997)
suggest that this tier of initials might have multiple functions. Consequently, in this paper we will call the central cortex initials "the central initials" (CTI).
The cells of the periblem histogen have been shown to become mitotically active after germination in Helianthus annuus and Anoda triangularis (von Guttenberg, 1960
), Malva sylvestris (Byrne and Heimsch, 1970
), in the Convolvulaceae (Seago and Heimsch, 1969
; Seago, 1971
), and in other species in the Asteraceae (Armstrong and Heimsch, 1976
). This histogen has been shown to have one, two, or more layers associated with it that may arise as a subsequent step to the meristem enlarging (Clowes, 1950
; Popham, 1966
; Byrne and Heimsch, 1968
). These cells are apparently not quiescent.
The plerome histogen, which derives the vascular cylinder, is the least described of all the histogens. Esau (1943)
and Williams (1947)
describe the pattern of tissues within the primary meristem, the procambium, but there is little published on earlier events outside of the work of Peterson (1967)
who studied tissue development in roots of white mustard (Sinapis alba). The processes involved in primary xylem and phloem differentiation have been documented (Esau, 1969
; Barnett, 1981
).
The objectives of this study are to characterize the developmental organization of the initial tiers for the cortex and vascular cylinder over a 4-wk period and to investigate whether spiral cell division patterns occur as they do in the development of the root cap. In addition, the patterns of vascular development within the apex will be characterized. These results will be discussed in the context of earlier studies on root apical organization.
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MATERIAL AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Pots were submerged in water and roots were gently extracted and cut from the shoot. Agar-grown plants of a different ecotype, Col-2, were also analyzed to verify the apical organization patterns. These plants were grown under conditions described in other studies (Dubrovsky et al., 2000
).
Tissue pieces were fixed overnight in 1.5% glutaraldehyde and 0.3% paraformaldehyde in 25 m mol Pipes buffer. The fixed tissue was rinsed three times for 15 min in buffer, post-fixed in 1% osmium tetroxide for 30 min (or without postfixation), dehydrated in a graded ethanol series (15 min per step), and then embedded in Historesin (Leica, Chicago, Illinois, USA). Plastic blocks were mounted on wooden dowels (with Duco cement) and sectioned on a Reichert-Jung 2050 Supercut microtome (Cambridge Instruments GmbH, Nussloch, Germany). Sections 1.5–2 µm thick were mounted on gelatin-coated (subbed) slides. Sections were stained with either 0.05% toluidine blue O for 30 s or by PAS reaction (periodic acid, 40°C, 20 min; Schiff reagent at room temperature for 60 min, modified from O'Brien and McCully, 1981
) and counter-stained with 1.0% fast green (room temperature, 90 s) and toluidine blue O (0.05% room temperature, 30 s).
Sections were viewed and photographed using an Olympus Vanox AHBT photomicroscope and a Scanarray-2 image analysis system (Galai Production, Haemek, Israel). Viewed images were captured and printed directly from the microscope using a CCD Sony XC-75 video camera module (Sony, Los Angeles, California, USA). This procedure facilitated the examination of hundreds of serial sections without using traditional photography. Sections were later photographed with Kodak Technical Pan 2415 film (Kodak, Rochester, New York, USA).
To facilitate a lineage analysis of the cortex tissues, printouts of serial sections were arranged in consecutive order and aligned in the same orientation. The cell files were traced and periclinal divisions marked. To study the xylem, phloem, pericycle, and vascular parenchyma tissues, the respective tissues were traced from the consecutively arranged printouts. Once traced, the tissues of interest were color-coded and the respective cell files analyzed. The periclinal divisions and cell numbers in transverse sections were then noted.
Figure 1 is a schematic drawing of a root. The dashed line A marks the root cap/root body junction, D marks the relative meristem height (Rost and Baum, 1988
), while B and C mark intermediate levels within the meristem. To calculate the number of cells within the meristem, a mean length for all tissue-specific cell types was determined. Cell lengths were measured from median longitudinal sections from at least three roots, and at least 35 cells per cell type were used to calculate a mean value. Because the number of tissue specific cell files is not constant throughout the length of the meristem, it was divided up into segments, e.g., meristem segment AB, BC, and CD (Fig. 1). Transverse sections from levels A, B, C, and D were taken for the purpose of determining the number of tissue-specific cell files. As an example, to calculate the number of epidermal cells within the meristem segment CD, transverse sections were taken at levels C and D and the average number of epidermal cells was calculated using the respective sections. The number of epidermal cells in the meristem segment CD = (d/l)(x); where d = the length of the segment CD, l = the average length of an epidermal cell, and x = the average number of epidermal cell files within the meristem segment CD. The total number of tissue-specific cells per meristem segment was calculated, and then the values were summed to give the total number of cells per meristem. Unless otherwise indicated, the analysis was done on sand-grown WS plants.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In 3-wk-old roots, there are three layers of immature cortex (ground meristem) the outer, middle, and inner (endodermis) layers. To produce the outer cortex layer, the OCI divides anticlinally. The middle and inner cortex layers arise from the ICI. The sequence of divisions that give rise to the middle and inner ground meristem layers is as follows: (1) the ICI divides anticlinally, creating a new ICI located distally and a proximal derivative cell (Fig. 6E); (2) the proximal cell divides periclinally, forming the respective layers (Figs. 4 and 6E). It is not uncommon for the proximal cell to first divide anticlinally one or more times before dividing periclinally. Similar developmental patterns were observed in in vitro-grown Arabidopsis 8-d-old plants of the Col-2 ecotype.
By 3 wk the appearance of the CTIs has changed. Some of the CTIs have divided forming a partial two-tiered CTI (Fig. 4). The "zigzag" appearance of the distal transverse walls has become more pronounced, and there are now small and large CTIs with some longer in the axial direction (Figs. 4 and 6D).
In 4- and 5-wk-old roots, the once-distinct row of CTI cells becomes relatively disorganized (Fig. 5). At this stage, they are highly vacuolated and they appear to be continuous with the columella root cap cell files (Fig. 5). These observations show that the RAM has closed organization from 1–2 wk and changes to open from 3–4 wk.
Ground meristem and its initials in transverse view
In a root less than 1 wk old, there are eight or nine cortical and endodermal cells in the meristem (Fig. 7). These cells originate from eight CIs that form a ring around 5–8 CTIs (Fig. 8). The number of CIs varies as the root ages; in 1- to 3-wk-old roots there are 5–12 CIs and in 4- and 5-wk-old roots there are 8–10 CIs.
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Phloem
Phloem sectors contain prospective protophloem sieve tube members (STMs). Surrounding the STMs are three or four cells, all of which, including the STM (asterisks, Fig. 7), originate from the same procambium initial. This initial first divides transversely, followed by two longitudinal anticlinal divisions of the derivative cell that create three cells aligned next to each other and adjacent to the pericycle (asterisks in Fig. 17). In longitudinal sections made perpendicular to the diarch xylem pattern (in the plane of the phloem), a protophloem cell file can be traced down to its initial (Fig. 19). In this example (Fig. 19), the derivatives of initial cells divided anticlinally once and periclinally twice. At a later stage, the middle cell of the three will divide periclinally forming the protophloem STM (Fig. 17). Protophloem STMs are always situated between two adjacent pericycle cells (Fig. 17). Identification of other STMs is not possible because detection of a nacreous wall is difficult and all the cells surrounding the protophloem STM appear vacuolated and cytoplasm can still be detected in cells on either side of the STM (data not shown). When viewed in sections, mature protophloem shows characteristic features such as the absence of cytoplasm and dark nacreous cell walls. Protophloem maturation occurred between 200 and 275 µm from the root cap/root body junction in 1–4-wk-old roots (Baum, 1996
).
At the level where the most distal mature STM is located (asterisk in Fig. 19) there are 12–18 pericycle cells. As the root meristem ages from 1 to 3 wk old, the number of pericycle cells at this level increases and then decreases in 4-wk-old root meristems. New pericycle cell files are produced as a result of longitudinal anticlinal divisions of existing pericycle cells located in the basal half of the meristem. Not all newly formed pericycle cell files are continuous, i.e., some files only extend 10–20 µm.
At the level where the most distal mature STM is located there are 20–60 vascular parenchyma cells in transverse sections. Two- to 4-wk-old root meristems had a greater number of vascular parenchyma cells than 1-wk-old root meristems. The number of vascular parenchyma cells increased along the root meristem from the root cap/root body junction up to a distance of 25 µm (in the proximal direction) in 1-wk-old roots and up to 35–45 µm in older roots. The position at which the most distal mature protophloem STM is located corresponds to the point at which rapid cell elongation begins (asterisk in Fig. 19) indicating the proximal border of the meristem for this tissue (Rost and Baum, 1988
) in the root. Comparison of the total number of cells in the meristem (when the proximal border was judged by the above-mentioned criterion) showed that with age, the number of cells in the meristem increased from 1 to 3 wk and then decreased (Fig. 20).
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The pericycle opposite the xylem poles divides at angles relative to the diarch pattern (single arrows in Fig. 24). This extends the pericycle away from the xylem poles and creates new cells that eventually will complete the vascular cambium (Fig. 24). At this developmental stage, the number of pericycle cell divisions is greater around the area of the xylem poles than between the xylem and phloem. The result of these divisions is a continuous cylinder of vascular cambium (arrowheads in Fig. 24).
The pericycle continues dividing periclinally to form the phellogen (double arrows in Fig. 24). The epidermis and cortex are gradually stretched and break away from the expanding root. Figure 25 is a cross section through the base of a 4-wk-old root showing a developed vascular cambium (arrowheads in Fig. 25) and phellogen. The vascular cambium produces secondary xylem to the inside and secondary phloem to the outside. The secondary xylem is made up of vessels with interspersed parenchyma cells.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIAL AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, extending Janczewski's (1874)
classification of root apices, characterized root meristems into six groups and two subgroups based on the lineage of tissues from initial cells. The classification scheme of von Guttenberg (1960)
is the simplest with two types, open and closed. In closed organization, all cell files can be traced to a histogen or tier of initial cells. The initial cells (Hanstein, 1870
; Janczewski, 1874
) divide to form the various tissues of the root body and cap. Arabidopsis thaliana roots have closed apical organization (Dolan et al., 1993
; Baum and Rost, 1996
, 1998
; Kidner et al., 2000
); the plerome, periblem, and dermatogen/calyptrogen histogens eventually produce the vascular, cortex, and epidermis/root cap tissues, respectively.
Baum and Rost (1996)
reported that the dermatogen/calyptrogen histogen (they refer to the columella initials surrounded by a ring of root cap/protoderm initials) divided in specific sequences to produce a root cap composed of interconnected cones. If viewed in transverse section at the level of the histogen, the cells of the peripheral root cap formed a spiral pattern in sand-grown roots older than 2 wk.
The RAM in A. thaliana is a dynamic structure that goes through specific developmental stages, starting with distinct tiers of initials (closed organization) that go through a series of changes and ending with a disordered array of vacuolated cells (open organization). The size of the RAM first increases and then decreases over 1–4 wk post germination. Changes in RAM cell number followed the same pattern. Nonsteady-state growth of Arabidopsis roots during the first 14 d post-germination is due to changes in meristem cell number (Beemster and Baskin, 1998
). Zhu, Lucas, and Rost (1998)
observed that the number and frequency of plasmodesmata decrease in cell walls of the RAM as the root ages indicating that RAM cells stop dividing and communicating with each other as the root reaches its determinate length. After 3 wk of growth post-germination, the middle cortex layer is produced via a helical arrangement of periclinal divisions. The location of specific maturation events associated with xylem and phloem tissues all changes as the root ages (Baum, 1996
).
The periblem is not quiescent
Popham (1966)
identified roots with closed organization and a one-layered periblem as type III and closed meristems with a two-layered periblem as type IIIA. Arabidopsis thaliana has a type III organization up to 1 wk and then becomes type IIIA but with a partial two-layered periblem. The change from one layer of ground meristem initials (cortex initials) to two layers of initials (the outer cortex and inner cortex initials) preceded the change from two layers of ground meristem cells to three and in some instances four layers of adjacent ground meristem cells.
The change in periblem architecture has also been observed in Helianthus annuus and Anoda triangularis (von Guttenberg, 1960
), Malva sylvestris (Byrne and Heimsch, 1970
), Ipomoea purpurea (Seago, 1971
), and some members of the Asteraceae (Armstrong and Heimsch, 1976
). In H. annuus and M. sylvestris, the CTI (our terminology) of the periblem are relatively quiescent during an initial stage of growth, but subsequent to this stage, the CTI are reported to begin dividing transversely, contributing to the columella root cap (von Guttenberg, 1960
). Von Guttenberg (1960)
called the dividing CTI a secondary columella and defined the RAM in which they were observed as exhibiting an "open" architecture. These same roots exhibited a "closed" architecture at a mature embryo stage. Even in the "open" architecture of Guttenberg, the cell files of the cortex can still be traced to a histogen and as such conform to the characteristics that by definition classify this meristem as closed (Popham, 1966
; Rost, 1994
). Even though in A. thaliana the lineage of columella root cap cells can be traced to the periblem in older roots, no mitotic figures were observed within the CTI to suggest an actual lineage to columella root cap cells. Seago (1971)
also did not observe transverse divisions in the periblem of I. purpurea though the CTI appeared to be located at the proximal end of columella cell files.
Within 1 or 2 d after germination, the four CTI (Scheres et al., 1994
) divided periclinally in relation to the root tip and then during subsequent growth further divided both anticlinally and periclinally. Dolan et al. (1993)
reported in A. thaliana (Columbia ecotype, grown on agar) that there were four CTI and that these cells comprised the quiescent center (QC). Our results bring into question the nature of the QC in this instance. In H. annuus (which has open apical organization post-germination), Clowes (1981)
reported that the CTI modulate in and out of the QC depending on mitotic activity of the columella initials. Our results demonstrate that these cells do divide initially after germination and apparently continue to divide during subsequent root growth until the primary root reaches its final length.
Van den Berg et al. (1997)
concluded from ablating QC cells of Arabidopsis that the function of the QC in Arabidopsis is to inhibit differentiation of initials that are in direct contact with the QC cells. When a QC cell is ablated, the columella initial that is in contact with the ablated cell begins to differentiate as a columella root cap cell. A cortex initial in contact with the ablated QC cell stops dividing anticlinally and divides periclinally. The patterns of cell development observed by van den Berg et al. (1997)
are similar to that observed in root meristems as they age from 1 to 4 wk. Results from both of these studies suggest that in Arabidopsis, as the root meristem ages, the inhibitory effect of the QC cells on differentiation of neighboring cells is ameliorated over time. This reduction of inhibition by the QC cells may account for the patterns of root architecture that we observed in Arabidopsis roots over time and also in other species for the formation of a secondary columella.
The ground meristem is changeable
In sand-grown A. thaliana (WS ecotype) plants older than 1 wk, as well as in agar-grown 8-d-old plants, Col-2 ecotype (data not shown), the endodermis divided periclinally to form a middle layer of cortex. The first endodermal cells to divide were always adjacent to the protoxylem elements before spreading to neighboring endodermal cell files. The division event progressed distally until reaching a point 1–3 cells proximal to the vascular initials (plerome). Williams (1947)
concluded from his observations of 179 species of angiosperms that the endodermis acts like a "cambium" by dividing to create additional layers of cortex. Heimsch (1960)
observed that in soil-grown and cultured excised tomato root apices, the cortex also increased in diameter due to periclinal divisions of the endodermis.
In 3-wk-old A. thaliana roots, the continued production of middle cortex and endodermal cell files is the result of a series of sequential divisions of cells and initials. Based on three-dimensional reconstructions of the CTI (periblem histogen) from serial transverse sections of 3-wk-old roots, we observed a helical pattern of periclinal divisions creating the middle cortex and endodermal cell files. This pattern of divisions is similar to the arrangement of root cap/protoderm (RCP) initials reported by Baum and Rost (1996)
. In the columella + RCP initial tier (dermatogen/calyptrogen histogen), the RCP initials first divided periclinally and then transversely, creating a spiral arrangement of peripheral root cap cells, as seen in transverse section. In the cortex, there is only one complete gyre of formative periclinal divisions; therefore, only two layers of cortex cells are produced. Based on the sequential pattern of divisions found in A. thaliana, we would predict that in larger roots having a similar organization, a spiral pattern of cortex cells should be observed near the CTI tier. This pattern is observed in transverse sections of root tips taken near the histogens (see Fig. 1, middle section on the right, in Heimsch [1960
]; and Fig. 14 in Seago [1973
]).
The formation of the middle cortex layer by the periclinal divisions of the endodermis is initiated in endodermal cells situated a small distance basal from the CI. SCARECROW (SCR) is a regulator of longitudinal divisions that establishes the two layers of cortex in Arabidopsis roots (Di Laurenzio et al., 1996
). Two of the postulated functions of SHORTROOT (SHR) are as a transcriptional activator of SCR and as a specifier of cell fate for the endodermis (Nakajima et al., 2001)
. The SHR protein has been observed to be localized in the nucleus of most endodermal cells situated within the meristem. In roots older than 1–2 wk, we speculate that there must exist other factors, working with or without SCR and SHR, whose function is to induce the endodermis to divide in a helical pattern, thereby giving rise to the middle cortex layer.
Plerome and the vascular cylinder
The vascular initial (VI) tier (plerome) is the most basal of the histogens and is composed of one layer of cells. Mähönen et al. (2000)
suggest that the development of the vascular cylinder in Arabidopsis roots is a function of a WOODEN LEG (WOL) gene product that may control the asymmetric division of the VI initials. The basic patterns and development sequences observed in A. thaliana in the current study are similar to those reported in white mustard (Peterson, 1967
), also in the Brassicaceae. Earlier studies in other plants have reported the spatial pattern of vascular tissue differentiation within the procambium and stele but not the cell lineage to the VI tier (Esau, 1943
, 1969
). All the initials of the VI tier are tissue specific except for those in a lineage to the STMs. The pattern of mature tissues can be recognized within 15 µm basipetal to the VI tier. The division sequence of the VI and proximally located procambium cells follows a predictable pattern, i.e., the pericycle initials only divide anticlinally; the xylem initials divide anticlinally, with one or two subsequent periclinal divisions; and the vascular parenchyma initials divide periclinally and anticlinally. As the root ages, the number of VI in the RAM remain somewhat constant.
Establishment of secondary meristems and features of secondary growth in soil-grown plants described in this work were similar to those found in agar-grown plants (Dolan and Roberts, 1995
). The presence and then absence of arabinogalactan protein epitopes on cell surfaces of secondary vascular tissue represents events associated with biochemical differentiation. Antibodies against these epitopes (e.g., named JIM 13 and JIM 14) have been shown to transiently label specific secondary xylem and phloem cell types but not the cambial initials from which they arose, indicating that they label specific derivative cells of a formative division (Dolan and Roberts, 1995
).
Is RAM determinacy a common developmental theme in roots?
The anatomy of the RAM exhibits characteristics of being determinate; that is, the arrangement of initials becomes disorganized (open apical organization) and vacuolated, the number of plasmodesmata decreases (Zhu, Lucas, and Rost, 1998
), and the maturation of xylem and phloem tissues modulates acropetally as the primary root stops growing (Baum, 1996
). These characteristics are associated with root determinacy, which is the final developmental stage of root growth. Hamblin and Hamblin (1985)
concluded from field growth experiments that the 13 legume species studied exhibited a high degree of genetic determinance for maximum root length. In Pisum, primary root growth rate first increased followed by a deceleration phase terminating in arrest (Gladish and Rost, 1993
). Changes in growth temperature affected the primary root growth kinetics, causing the root to reach its determinate length at different times. Gunning (1978)
showed that the primary root of Azolla was determinate, and Clowes (1958)
reported that lateral roots of the aquatic plants Pistia and Eichhornia were determinate. The roots of some species within the Cactaceae have been shown to be determinate (Dubrovsky, 1997
). In those species, meristematic cells within the RAM cycle 2–5 times before differentiating into vacuolated cells.
Arabidopsis thaliana exhibits closed organization with three initial tiers producing the procambium, ground meristem, and protoderm/root cap, respectively. The pattern of cells within the histogen tiers that is established in the embryo changed during post-embryonic growth. Earlier studies by Seago (1971)
, Byrne and Heimsch (1970)
, and von Guttenberg (1960)
have documented changes within the arrangement of cells that make up the periblem but these authors described their findings in the context of two-dimensional sections of the meristem. The present study attempts to construct a three-dimensional model of the meristem that includes its changing nature through time. The RAM is a dynamic structure whose internal arrangement of cells changes as it ages from 1 to 4 wk old, from closed apical organization to open when the primary root reaches its determinate length. During the course of its development, two spiral motifs were observed—the sequential cell division pattern of the root cap/protoderm initials (Baum and Rost, 1996
) and the helical arrangement of periclinal divisions that produce the middle cortex and endodermis in 3-wk-old plants.
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FOOTNOTES |
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4 Present address: Instituto de Biotecnología, Universidad Nacional Autónoma de México., Apartado Postal 510-3, Cuernavaca, Morelos, 62250, México
5 Author for reprint requests (tlrost{at}ucdavis.edu
)
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Clowes F. A. L. 1950 Root apical meristems of Fagus sylvatica. New Phytologist 49: 248-268[CrossRef]
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