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Development and Morphogenesis |
Department of Biology, Bellarmine University, 2001 Newburg Road, Louisville, Kentucky 40205 USA
Received for publication January 4, 2001. Accepted for publication April 3, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: apical initials • chimeras • Cupressaceae • gymnosperms • meristems • shoot apex
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Szymkowiak and Sussex, 1996
). In gymnosperms, lineage analysis of variegated patterns have permitted an inspection of the internal dynamics of stem meristem organization not possible by conventional morphological descriptions of cell packets and zonations. Stewart and Derman (1970)
identified white sectors in Juniperus expansa nana that arose by an insertion of a white mutant tunica cell into the green corpus region to form mostly one-third white merigonal, or sectorial, corpus chimeras. They concluded that one to three apical initials reside at the summit of the stem. In another juniper, J. davurica ‘expansa variegata,’ Ruth, Klekowski, and Stein (1985)
found most sectorial shoots became completely white, and they concluded this result came from competition between albino and green regions in the corpus.
Several subtle assumptions are embedded in these two studies on juniper chimeras that need to be inspected more closely. First, the sectorial fraction is interpreted as the reciprocal of the number of apical initials. For example, a one-third albino sector indicates three apical initials are present at the summit of the meristem. This assumption was initially explored by Satina, Blakeslee, and Avery (1949)
for polyploid cytochimeras in stems and later was applied gratuitously by others to the more complex case of variegated leaf patterns along shoots (Derman, 1960
; Stewart and Derman, 1970
; Ruth, Klekowski, and Stein, 1985
). The second assumption is that apical initials are solely proliferative cells (Newman, 1956
; Esau, 1977
) and that by necessity some initial cells passively must be the ultimate source of all cells. However, it is also possible to interpret these apical initials as centers of control that regulate rates of growth as well as cell division and to some extent the developmental fate of cells (Korn, 1993
). Consequently, apical initials can be given equivocal interpretations, and which interpretation is selected usually depends upon the perspective of the investigator. Finally, the assumption that related taxa have different apical organizations based on the difference in sector length as measured in number of nodes and sector fate in the two junipers cited above is also gratuitous. Chimeric behavior in six members of the family Cupressaceae was found here to express interesting differences from those of the junipers cited above, differences that are related to how analysis is carried out more than to actual variations in apical organization. Also, from the data found in this study it will be proposed that a single apical cell is present, one that both is the proliferative fount of all cells as well as the control over this proliferation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Frequency of initiation of sectorial chimeras was determined by counting the number of leaf pairs on green decussate stems beginning at the base of a branch until either a white sectorial leaf was encountered or the tip of the branch was reached. The length of a sector, again, was determined by counting leaf pairs until the stem became completely white, and the sector fraction was based on divisions or multiples of one-fourth because four leaves surround a stem in the decussate condition.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1.7 mm), adult scale leaves and each node is taken as a pair of opposite leaves. Some species have flattened sprays (Cupressocyparis, Calocedrus, Thuja, and Cameocyparis), while others have square shoots (Juniperus sabina and J. davurica; Fig. 1A, B). Green-yellow shoot chimeras appear only in young regions of branches as older regions drop their leaves, enlarge in girth and become woody. The first parameter inspected was the frequencies of initiation of sectorial chimeras, and these values ranged from 0.021 to 0.040 initiation/node (Table 1, column A). These frequencies are not significantly different from one another according to a null hypothesis 
2 test (2 = 8.6, df = 5, P > 0.1).
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10% of the initial sectored shoots, completely white shoots never revert back to green.
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Sector fraction was also scored in branches by determining the size of the original sector at the site of its inception, it ranged from 1/16 to 1/1 white (Table 1, columns F–J). These values are only approximations in many cases, particularly when sectors extended over half the width of a leaf; this problem of determining sector fraction will be reexamined in the Discussion. The majority of sectors were 1/8 and 1/4 in all species examined with the 1/16 and 1/1 sectors less common (Figs. 4 and 5). The one exception of fraction size is in the juvenile sprays of J. davurica (Fig. 1B). These shoots have long (9 mm), needle-like leaves with either decussate or tricussate phyllotaxy. In the tricussate state, sector fractions were more 1/6 and 1/12 types, namely a fraction of the inverse of the three leaves at a node.
A sector type here called harlequin is seen as a row of white leaves bordering a row of green leaves and was found five times in Cupressocyparis (Fig. 6). Each mature leaf in a decussate shoot is wider than one-fourth of the stem and overlaps with leaves in adjacent rows, a row of leaves different in color from leaves in an adjacent row creates a zigzag pattern. Other kinds of sectors are rarely (<5% of sectors) found, often of a confounding nature, as in the double sector, also in Cupressocyparis, in which a green sector passes transversely through the stem and is separated by two white sectors (Fig. 7).
The fate of sectorial axillary branches of the original sectorial shoot was the final parameter inspected. Branches were only scored if the size of the sector was between one-fourth and three-fourths, that is, when an axillary branch begins with sizable amounts of both white and green stem tissue. The fate of these sectorial branches in all six species was conversion to either completely green or completely white status, following a 1 : 1 ratio (Figs. 8 and 9: Table 1, columns B, C).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, as well as Juniperus squatama by Derman (1960)
. This type of chimera has not been reported in other gymnosperms, suggesting a peculiar dynamics in the shoot apex of this family. Anatomically, the construction of the stem apex in the Cupressaceae expresses little variation among the genera examined and manifests the Coniferophyta type of shoot with a single-celled layer of tunica over the corpus (Johnson, 1951
). Newman (1956)
proposed that in gymnosperms several apical cells residing at the summit of the tunica serve as the fount for all other cells of the apical meristem mostly by anticlinal divisions and infrequently by periclinal divisions, a view similar to those of Douliot (1890)
, Johnson (1951)
, Hejnowicz (1956)
, and Pillai (1963)
. Such apical cells were later termed apical initials by Esau (1977)
in apical meristems of both gymnosperms and angiosperms.
Hejnowicz (1956)
first explained the sectors in juniper as arising from periclinal divisions in an albino tunica layer. Later Derman (1960)
named this phenomenon cell displacement when he encountered it in privet and juniper, and this feature was further verified by Stewart and Derman (1970)
and Ruth, Klekowski, and Stein (1985)
in other species of juniper. The epidermis of nonsectorial chimerical shoots in the six species examined here appear to be L1 chimeras as a green leaf has an epidermis with colorless plastids in guard cells.
Sectoral chimeras supposedly reveal the number of apical initials at the summit of the shoot apex. For example, Stewart and Derman (1970)
found seven of nine white sectors in Juniperus expansa nana were one-third a fraction they interpreted as indicating three apical initials were present. Similarly, Ruth, Klekowski, and Stein (1985)
interpreted the many one-third chimeras in J. davurica ‘expansa-variegata’ as coming from three apical initials in the tunica.
In the six decussate forms examined here, 1/4 and 1/8 sectors constitute 111/147, or 76% of the sectors, and this line of reasoning suggests there are four or eight apical initials. But 1/1 (5%) and 1/16 (1%) patterns were also found, leading to the conclusion that the shoot apex has from 1 to 16, but mostly 4 or 8, apical initials following numbers of the 2n series. In the tricussate, juvenile state of J. davurica, the sectorial fractions followed the 1/6, 1/12, and 1/18 series suggesting the range of apical cells is from 6 to 18.
An alternative to the idea of the sector fraction equaling the reciprocal of the number of apical initials is that leaf arrangement plays some role in determining sector width. As leaves and not stems are visible, sector identification is based mainly on leaves. Perhaps a few albino mutant cells along the flank of the apex are the source of a leaf buttress that enlarges disproportionately to become greater than the neighboring apical flank region and form the leaf blade with a large mutant sector. This idea that leaf development alters sector size is supported by the harlequin chimera (Fig. 6). Here, leaves in adjacent rows and with a different phenotype laterally overlap in a zigzag fashion because a leaf in a decussate condition can occupy more than one-fourth of the stem circumference. Hence, as leaves overlap laterally, sectors also overlap. Clearly, sector fractions of shoots are, at least in part, determined by leaf growth and not necessarily entirely by the number of apical initials.
In all six species examined here the majority, 143/162, or 88%, of the original sectorial branches eventually became completely white. Ruth, Klekowski, and Stein (1985)
also found the "majority of sectors shifted over to white branches," however they made no distinction between original sectorial and axillary sectorial branches. The explanation offered by Ruth, Klekowski, and Stein (1985)
for the preponderance of a white fate for branches was cell selection, with the white state more favorable than the green. A simple test to detect the presence of selection is the comparison of the frequency of the completely white state in original chimeric shoots with that in their sectorial auxiliary branches. Cell selection, if present, should occur in both types of sectorial branches regardless of the origin of the chimera, and the frequencies of the completely white state should be the same in both cases. It is important to emphasize that this examination did not include all sectorial axillary branches of the original sectorial shoots but only those that began with at least a one-fourth albino or green sector in order to give selection a chance to operate. Selection, if present, could be expressed by favoring one type of sector over the other. Although 88% of the original sectorial shoots became completely white, only 48% (97/200) of the axillary sectorial branches became completely white. This dramatic difference in the fate of different types of shoots in all six species excludes selection as an explanation of white dominance. It can be explained more simply by the origin of the chimeras in these two types of shoots. A chimera in an original shoot comes from one mutant corpus cell arising in an established shoot beneath the single apical cell by cell displacement. A chimera in an axillary shoot comes from many founder cells in the parental stem and these cells can be different in color. One of these founder cells is beneath the single tunica apical initial of a new branch by chance alone, and it will determine the eventual color of the axillary branch.
Additional support of the one apical cell idea is the occurrence of what are called 1/16, 1/8, l/4, l/2, and 1/1 sectors. By the hypothesis that apical cell number is the inverse of sector size, there would be from 1 to 16 apical cells at different times during shoot development. This large number of apical cell number makes little sense because it would require a complex explanation for maintaining their number, types, and positions. However, had the previous authors on various Juniperus spp. examined more shoots, the full range of sector sizes would have been revealed, and the inverse rule would have been seen as untenable. A second problem with the interpretation of these fractions is that they are likely to be approximations, perhaps simplifying a complex fraction, e.g., 4/13 to one with a smaller denominator, such as 1/3, begs the inverse rule. Third, the initial fraction usually shifts to larger ones with more nodes added until the sector takes over the stem. Ruth, Klekowski, and Stein (1985)
selected the fraction existing over the most nodes as characteristic of that chimera but since they also invoked selection, the prolonged fraction cannot be used simultaneously as evidence for both the number of initials and the effect of selection. Curiously, when the stem apex is taken as having one apical initial and no cell selection among chimeras, two points suggested here, specific sectorial fractions have no developmental significance. It is expected that sectors gradually increase in size as a stem grows in length, but transitions of specific fractions are unlikely given the variability of size and shape of cells at the apex (Figs. 12 and 13).
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With one apical cell in a shoot apex, sectors also arise, but through a more complex growth pattern (Figs. 12 and 13). One basic fact about stem apices is that they remain dome-shaped during cell proliferation. Consider a block of cells constrained at the base by attachment to a laterally stretchable substratum in the way an apex is attached to a mature stem. If all block cells grow at the same rate, the block will increase in size but remain constant in shape (which is similar to how callus grows) and the apex balloons out. If cells at the center of the constrained base of the block grow faster than those laterally and above it the block will tear at the top and sides as the bottom expands. If cells at the top of the block grow faster than those at the attached base, the block will become elevated and the top will become dome-shaped (Korn, 1993
). It can be concluded that cells at the summit of the stem grow the fastest and cells sequentially more distal to the apex grow progressively slower. It is not correct to say that cells at the summit become the apical initials because the implication is that location is the cause and status is the effect. It is more meaningful to state that the apical initials and their recent derivatives create the summit by growing faster than other cells. This point contradicts the generally accepted position that cells at the summit grow slower than those at the base, which was demonstrated by rates of cell division and incorporation of radioactive precursor to DNA synthesis (Nougarède, 1967
; Lyndon, 1990
). If a distinction is made between a dome, from summit to base, and the tissue immediately below the dome that forms leaf initials, then growth is faster at the summit than at the base of the dome and independent of that for the tissues below the base. Logically, if the single apical cell has the fastest growth and is not replaced by prior descendent cells, then this apical cell is the control center of growth and therefore of development of the apex, which makes this apical cell comparable to the apical cell in cryptogams that is both the fount of proliferation and the site of control (Korn, 1993
).
These apical cells in the dome, as defined by Stewart and Derman (1970)
, are then located at the exact center point of the apical curvature, that is, at the intersection between the longitudinal axis and the center of two-dimensional curvature of the dome. Combining the idea that one apical initial is present, based on chimeric sector conversion to white branches, and that this apical initial (ai) cell is the fastest growing cell in the apical dome, based on the shape of apex, the dynamics of apical growth can be described. First, an original apical initial cell (ai) over time becomes a lineage of single apical initials residing in the tunica layer that produce tunica cells (tc) by anticlinal divisions (ai 
ai + tc, tc tc + tc) (Fig. 14). Occasionally an apical initial divides periclinally to form a new ai cell in the tunica and a sister corpus (sc) cell, namely, ai ai + sc. This sister corpus cell becomes an apparent initial cell (aic) in the corpus and forms a lineage of aic cells contiguous with the tunica ai cell as well as forming sister corpus cells (cc), (sc aic, aic aic + cc, cc cc + cc). Several corpus cell packets, or vegetative clones, from an aci cell will surround the aci cells in an asymmetric fashion. A mutant aci cell lineage forms mutant cell packets, and the first mutant packet to reach the base of the apex generates a mutant sector (Fig. 13). The size of this sector varies depending upon the shape of the first mutant packet but generally is expected to be about one-fourth the circumference based on the number of cells around the apical initial. This fraction can change dramatically depending on how sector cells are incorporated into a leaf buttress. It is the oldest mutant cell packet that will become a sector of less than one-half and when the next mutant packet arrives at the base of the apex and lateral to the first packet, together they will form about a one-half mutant sector. Finally, when the fourth mutant packet reaches the base of the apex the shoot becomes completely mutant. The theoretical fractions of one-fourth, one-half are not expected because of size and shape variations of cells and so of their descendent packets. In general, chimeric sectors can occur in apices with a single initial cell. This pattern of cell packets viewed from above is comparable to that described in fern apices (Bierhorst, 1977
) except that three-dimensional fern packets become piece-of-pie shaped while those in conifers are more quadrilateral.
Single apical cells not only form chimeric sectors but sectors that persist for long periods of time and over many nodes. In the model presented here, growth is greater at the summit than at the base of the domed apex, but it could be the greatest below the dome where leaf initiation occurs. During each plastochron the nodal region immediately beneath the dome region rapidly elongates, while a small amount of tissue at the base of the dome is enlisted as another nodal region (Figs. 14–16). Repetition of basal domed tissue becoming nodal material consumes relatively little of the dome. Any chimeric sector at the base of the apex can then be telescoped out into a sectorial segment many nodes in length. Soma and Ball (1963)
found that during the time that carbon particles placed on the stem apex of Lupinus alba moved down along the flanks, 9–11 new leaves formed, indicating the apex grows slower than the latest nodal region. In sunflower, Jegla and Sussex (1989)
found that each of four rows of meristematic cells in the shoot apex give rise to 14 nodes. Klekowski and Kazarova-Fukshansky (1984)
claim that organs with apical cells like those found in mosses and ferns cannot form persistent chimeras. But, as shown here, a single apical cell forms an asymmetric array of derivatives and when it mutates, the different sizes of the derivatives can at least lead to long sectors.
Steward and Derman (1970)
found sectors in juniper ranging from 27 to 104 nodes in length and claimed that the longest sectors are evidence of stable three-celled group of initials. Ruth, Klekowski, and Stein (1985)
found an upper limit of 20 nodes, which they interpreted as the results of impermanence of initials and cell selection. Maximum sector length in this study is also 25 nodes but is explained by chimeric sectors in the apex gradually telescoped out by nodal elongation. In general, evidence offered here refutes cell selection as well as multiplicity and impermanence of cell initials. What is impermanent is the aci cell lineage in the corpus as it is replaced when a periclinal division of the ai cell initiates a new sc cell or aci cell lineage. A permanent single apical cell lineage in the tunica coupled with occasional cell displacement into the corpus is the simplest explanation of all the pertinent data.
The fractional size and nodal length of sectors were taken by others as the primary clues as to the organization of the shoot apex (Stewart and Derman, 1970
; Ruth, Klekowski, and Stein, 1985
). However, when a single apical cell status and infrequent cell displacement are assumed, sectorial features carry little developmental meaning about the shoot apex. Some of the sectors are informative in other developmental respects. The harlequin sector indicates how a nodal region expands into leaf width. Numerous double sectors are split single sectors rather than two independent sectors because the expected frequency of two sector initiations (0.04 x 0.04, or 0.0016) is less than the reciprocal of the number of nodes examined. How a sector splits remains unclear but could be from an irregular outline of a cell packet in an apex that is part of a chimera. Sectors limited to a small fraction of a leaf are also not easily explained but are probably related to Poethig's (1987)
apparent cell number (ACN), that is, the number of cells in one organ (stem) contributing to a new organ (leaf).
This study agrees with those of Stewart and Derman (1970)
and Ruth, Klekowski, and Stein (1985)
that the infrequent reversion of original sectorial stems back to completely green is probably due to insertion of a white tunic cell into the green corpus, not at the summit but along the flanks, that is, by a cell displacement along a flank. Since such a reversion is rare, its cause is of little developmental significance. A general feature of all species examined is that no completely white shoot ever formed a green shoot, much less a green sector. The absence of this feature is expected since white sectors appear by cell displacement and green sectors arising in a white region can only come about by either (a) reverse chloroplast mutation or (b) reverse cell displacement in which a corpus cell becomes inserted into the tunica, both of which are possible but extremely unlikely.
The question of the number of apical initials in higher plants has been raised repeatedly over the past century. Clearly there is one apical cell in moss and fern stems, based on cell lineages of discernable apical cells but the data for seed plants is less convincing. Douliot (1890)
proposed a single apical cell for gymnosperms and about three apical cells for angiosperms, based solely on cell appearances at the summit of apices, but morphological description can be highly subjective and so such observations prove little. In angiosperms, Naylor and Johnson (1937)
interpreted the origin of a peculiar adventitious shoot in Saintpaulia as coming from a single cell. Sparrow, Sparrow, and Schairer (1960)
, using Saintpaulia, and Moh (1961)
, using coffee, also argue in favor of a single apical cell because x-ray-induced mutants were not expressed first as chimeras. In contrast, Jegla and Sussex (1989)
, using sunflower, Irish and Sussex (1992)
, using Arabidopsis, and Furner and Pumfrey (1992)
, also using Arabidopsis, found x-rays do produce chimeras. These chimeras lasted over a number of nodes, either at the beginning of development for several leaves or later to include both leaves and the inflorescence, features expected of a shoot apex growing slowly at the base and more rapidly in the basipetal nodal region. Also, Korn (1993)
found target analysis for sunflower stem inactivation followed one-hit kinetics, suggesting a single apical initial. But morphological description is highly subjective and x-ray data can come from tissue damage followed by complex reorganization pathways (Langenauer and Davis, 1973
).
Chimeras from cell insertion, on the other hand, have the advantages over both morphological description and x-ray data because both cell lineages are identifiable and no damage is involved. Chimeras of plastid differences in the nonphotosynthetic stem apex also minimize any role of selection that could alter developmental pathways. Also, chimeras formed by cell displacement do not experience delayed phenotypic expression as from high energy radiation due to somatic segregation (Poethig, 1987
). This immediate expression of a mutant state leads to a single continuous chimera rather than one with a sister wild-type segment, a feature complicating analysis.
Traditionally, the shoot apex has been described statically as an ensemble of zones and dynamically as passing through a series of geometric changes during each plastochron cycle. This elaborate description begs the conclusion of a complex set of apical initials in each layer of the meristem. Superficially, chimeral sectoring only strengthens this perspective on the apex by assuming sector fraction relates to number of cell initials. The single apical cell as proposed here directly conflicts with the notion of a meristem as a complex integration of cells of different types. However, if zones are viewed as not proper to the meristem but as representing the acropetally advancing fronts of tissue differentiation, if more emphasis is placed on the impermanence of sectors rather than their fractional presence, and if growth is understood as regulated by a simple, apical site of control, then an apical cell interpretation becomes more acceptable. In general, the sectoring data from six species in the Cupressaceae examined here clearly support the idea of a single apical cell in the tunica layer in the shoot apex in this family, yet caution should be doubly exercised. First, the argument for a single apical initial is based on the conclusion that no selection is present that, in turn, is based on a 1 : 1 ratio of green to white axillary shoots. It would be desirable to find other evidence for a single apical cell. And second, if one apical cell is found to characterized this family, similar kinds of evidence should be sought in other gymnosperms and in angiosperms as well.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Coombes A. J. 1992 Trees. Houghton Mifflin, Boston, Massachusetts, USA
Derman H. 1960 The nature of plant sports. American Horticulture Magazine 39: 123-173
Douliot H. 1890 Recherches sur la croissance terminale de la tige des Phanérogames. Annales des Sciences, Séries VII, Botanique 11: 283-350
Esau K. 1977 Anatomy of seed plants. Holt, Rinehart and Winston, New York, New York, USA
Furner I. J. J. E. Pumfrey 1992 Cell fate of the shoot apical meristem of Arabidopsis thaliana. Development 115: 755-764[Abstract]
Hejnowicz Z. 1956 The first periclinal chimera among gymnosperms. Acta Societatis Botanicorum Poloniae 25: 181-202
Irish V. F. I. M. Sussex 1992 A fate map of the Arabidopsis embryonic shoot apical meristem. Development 115: 745-753[Abstract]
Jegla D. E. I. M. Sussex 1989 Cell lineage patterns in the shoot meristem of the sunflower embryo in the dry seed. Developmental Biology 131: 215-225[CrossRef][ISI][Medline]
Johnson M. A. 1951 The shoot apex in gymnosperms. Phytomorphology 1: 188-203
Klekowski E. J., Jr. N. Kazarova-Fukshansky 1984 Shoot apical meristems and mutation: fixation of selectively neutral genotypes. American Journal of Botany 71: 22-71[CrossRef][ISI]
Korn R. 1993 Apical cells as meristems. Acta Biotheoretica 41: 175-189[CrossRef][ISI]
Langenauer H. D. E. L. Davis 1973 Helianthus annus response to acute radiation. I. Damage and recovery in the vegetative apex and effects on development. Botanical Gazette 134: 301-316[CrossRef][ISI]
Lyndon R. F. 1990 Plant development. Unwin Hyman, London, UK
Moh C. C. 1961 Does a coffee plant develop from one initial cell in the shoot apex of an embryo?. Radiation Botany 1: 97-99
Naylor E. H. B. Johnson 1937 A histological study of vegetative reproduction in Saintpaulia ionantha. American Journal of Botany 24: 673-678[CrossRef][ISI]
Newman I. V. 1956 A review of shoot apical meristems of gymnosperms, with comments on apical biology and taxonomy, and a statement of some fundamental concepts. Journal of the Linnean Society of New South Wales 86: 9-59
Nougarède A. 1967 Experimental cytology of the shoot apical cells during vegetative growth and flowering. International Review of Cytology 21: 203-351[Medline]
Pillai S. K. 1963 Structure and seasonal study of the shoot apex of some Cupressus species. New Phytologist 62: 335-341[CrossRef]
Poethig R. S. 1987 Clonal analysis of cell lineage patterns in plant development. American Journal of Botany 74: 581-594[CrossRef][ISI]
Poethig R. S. 1998 Clonal analysis of leaf development in cotton. American Journal of Botany 85: 315-321[Abstract]
Ruth J. J. Klekowski O. Stein 1985 Impermanent initials of the shoot apex and diplontic selection in a juniper chimera. American Journal of Botany 72: 1127-1135[CrossRef][ISI]
Satina S. A. F. Blakeslee A. G. Avery 1949 Demonstration of three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. American Journal of Botany 27: 895-905[CrossRef]
Soma K. E. Ball 1963 Studies on the surface growth of the shoot apex of Lupinus albus. Brookhaven Symposium on Biology 16: 13-45
Sparrow A. H. R. C. Sparrow L. A. Schairer 1960 The use of X rays to induce somatic mutations in Saintpaulia. African Violet 13: 32-37
Stewart R. N. H. Derman 1970 Determination of number and mitotic activity of shoot apical initial cells by analysis of mericlinal chimeras. American Journal of Botany 57: 816-826[CrossRef][ISI]
Szymkowiak E. J. I. M. Sussex 1996 What chimeras can tell us about plant development. Annual Review of Plant Physiology and Plant Molecular Biology 47: 351-376[CrossRef][ISI]
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