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0 Department of Plant and Soil Sciences, French Hall, University of Massachusetts, Amherst, Massachusetts 01003 USA
Received for publication January 19, 1999. Accepted for publication June 22, 1999.
ABSTRACT
Many higher plants have shoot apical meristems that possess discrete cell layers, only one of which normally gives rise to gametes following the transition from vegetative meristem to floral meristem. Consequently, when mutations occur in the meristems of sexually reproducing plants, they may or may not have an evolutionary impact, depending on the apical layer in which they reside. In order to determine whether developmentally sequestered mutations could be released by herbivory (i.e., meristem destruction), a characterized genetic mosaic was subjected to simulated herbivory. Many plants develop two shoot meristems in the leaf axils of some nodes, here referred to as the primary and secondary axillary meristems. Destruction of the terminal and primary axillary meristems led to the outgrowth of secondary axillary meristems. Seed derived from secondary axillary meristems was not always descended from the second apical cell layer of the terminal shoot meristem as is expected for terminal and primary shoot meristems. Vegetative and reproductive analysis indicated that secondary meristems did not maintain the same order of cell layers present in the terminal shoot meristem. In secondary meristems reproductively sequestered cell layers possessing mutant cells can be repositioned into gamete-forming cell layers, thereby adding mutant genes into the gene pool. Herbivores feeding on shoot tips may influence plant evolution by causing the outgrowth of secondary axillary meristems.
Key Words: cell fate • herbivory • mutational loading • Nicotiana • periclinal chimeras • plant evolution • Solanaceae
It has been hypothesized that all long-lived plants may eventually become complex genetic mosaics because somatic cells in shoot apical meristems can spontaneously generate mutant cell lineages over time (Klekowski, 1988
; Gill et al., 1995
). It is possible for mutations to be passed on to offspring when vegetative meristems in genetic mosaics convert to reproductive meristems. It is not possible for plants possessing a mixture of normal and mutant cells to be sexually perpetuated as mosaics because gametes are single cells, and all cells of individual offspring would either possess the mutation or would not (Marcotrigiano, 1997
).
Any understanding of the evolutionary significance of genetically mosaic meristems is dependent upon knowledge of the development of meristems and the origin of gametes. In the angiosperms, and some gymnosperms, independent cell lineages develop in shoot meristems. When observed histologically the lineages appear as discrete cell layers. This stratification is the consequence of the orientation of cell division, which is almost always anticlinal (perpendicular to the surface) in the outer cell layers of the meristem. The layers in which cell divisions are anticlinal are called the "tunica" layers, while subtending cells not displaying these restricted divisions, and making up the bulk of the meristem, are termed the "corpus." Hence, tunica-corpus meristems are those that appear stratified.
In almost all dicotyledonous plants, there are three apical cell layers in shoot meristems. The layers are generally designated L1 (outermost apical cell layer), L2 (middle layer), and L3 (innermost layer). Within each cell layer, there are cells called "shoot apical initials." Initials are neither genetically nor developmentally unique but are fortuitously located at the terminus of the dome-like meristem where they generate the daughter cells for that layer. On occasion, they can be positionally and functionally replaced by other cells within the layer (Stewart and Dermen, 1970
; Marcotrigiano, 1997
) or much more rarely from cells of another layer (Sagawa and Mehlquist, 1957
; Pohlheim and Kaufhold, 1985
; Marcotrigiano, 1997
).
If a mutation occurs in a shoot apical initial, its daughter cells can eventually populate an entire apical cell layer. The layer can remain developmentally independent from adjacent layers. This condition results in what is known as a "periclinal chimera," a specific type of genetic mosaic in which one or more entire apical cell layers are genetically distinct from adjacent layer(s). The majority of genetic mosaics in plants with stratified shoot apices eventually may become either periclinal chimeras or nonchimeral following stochastic processes (Klekowski, Kazarinova-Fukshansky, and Mohr, 1985
).
Axillary buds begin their development in the leaf axils of immature leaves on the main shoot. In many species more than one bud can develop in a node. Multiple axillary buds appear frequently in woody plants (Romberger, 1963
; Halle, Oldeman, and Tomlinson, 1978
) and have been documented in herbaceous plants as well (Seltman and Kim, 1964
; Tian and Marcotrigiano, 1994
).
The axillary meristems become growing shoots when they are released from apical dominance either naturally or by the death or removal of the terminal shoot. The axillary shoots, in turn, have a terminal shoot meristem and also develop axillary meristems. This progressive development provides an ever-growing pool of shoot meristems, typical of a branched plant.
Axillary meristems are derived from the terminal shoot meristem, from tissue that is never incorporated into leaf primordia nor differentiates into other tissues (Wardlaw, 1965
). Axillary meristems become independent via a detachment, which in some species is delimited by several files of elongated cells that establish the "shell zone" (Garrison, 1949
; Sussex, 1955
; Remphery and Steeves, 1984). Studies of both genetically homogenous plants (e.g., Garrison, 1955
) and periclinal chimeras (e.g., Tian and Marcotrigiano, 1994
) indicate that the cell layers of axillary meristems are in a direct lineage with the terminal meristem. Therefore, in the case of periclinal chimeras, the shoot apices of primary axillary buds have the same order of genetically different cell layers as the terminal bud from which they are descended, and axillary shoots of periclinal chimeras are normally exact copies of the original periclinal chimera.
The variegation pattern of leaves on variegated plastid chimeras has been used to deduce the genetic makeup of the shoot meristem cell layers since leaf cell layers acquire their specific arrangement from the shoot meristem layers that give rise to them (Stewart and Burk, 1970
; Poethig, 1984
). Therefore, specific leaf variegation patterns are indicative of specific arrangement of cell layers in the shoot meristem. By studying periclinal plastid chimeras, it is known that L1 gives rise to the leaf epidermis (Poethig, 1984
). Although most epidermal cells do not express chlorophyll, the guard cells that surround stomata contain green plastids on plants with genetically green epidermis (Burk, Stewart, and Dermen, 1964
). L2 generates the palisade parenchyma and the lower spongy parenchyma as well as all of the spongy parenchyma of the leaf margin. L3 generates the upper and middle layers of the spongy parenchyma but makes no contribution to the leaf margin. Of most relevance to evolution are breeding studies, which indicate that, with few exceptions (e.g., Klekowski, Lowenfeld, and Klekowski, 1996
), the gametes are descended from L2 derivatives in flowering plants, and especially in dicots (Kirk and Tilney-Bassett, 1978
). Therefore, shoot apical cells that have undergone spontaneous mutations have a genetic consequence for the next generation only if they reside in L2 of the shoot meristem. Mutations in other layers would remain sequestered.
Shoot apical meristems are frequently destroyed by other organisms. In particular there are classes of insects and insect-related pests that feed on the meristematic regions of plants (Johnson and Lyon, 1976
; Coulson and Witter, 1984
). Tip moths, borers, and twig girdlers can destroy so many buds that they alter the architecture of a plant. When herbivores remove or kill the terminal bud, one or more lower buds develops into an elongated shoot (Crawley, 1983
).
To determine whether herbivore damage can change the apical cell layer responsible for seed production in plants, a model variegated genetic mosaic was subjected to two simulated herbivore treatments. Using a variegated plant allowed for rapid phenotypic analysis to determine the proportion of seedlings derived from specific shoot apical cell layers. The eradication of terminal and primary axillary buds led to the outgrowth of secondary axillary buds, in which the fidelity of apical cell layer organization was highly compromised. It was demonstrated that seed could arise from apical cell layers that are genetically distinct and developmentally isolated from adjacent cell layers in certain types of genetic mosaics. The end result was the recovery of seed progeny possessing genes that were developmentally isolated in the cell layers of the shoot meristem that would not normally generate gametes. It is proposed that herbivory can release developmentally sequestered mutations in plants.
MATERIALS AND METHODS
Definitions
An axillary bud develops in a leaf axil and begins as a shoot apical meristem. In Nicotiana, a primary axillary bud is that axillary bud which is the first to develop in a given leaf axil. Secondary axillary buds are formed in the same leaf axil and in the same file as the primary bud. They form on the petiole side of the primary bud, farther away from the leaf petiole-stem junction (Fig. 1; Seltman and Kim, 1964
). Secondary axillary buds develop chronologically later than primary buds (Tian and Marcotrigiano, 1994
). Histological evidence supporting the above have been presented elsewhere (Seltman and Kim, 1964
; Tian and Marcotrigiano, 1994
).
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Treatments
A control and two treatments were employed. There were two whole-plant replications for the control plants and treated plants but the data of concern were the individual seed capsules of each plant. Controls were allowed to grow until the terminal shoot apex had flowered and seed were mature. Two treatments consisted of different levels of simulated herbivory. In treatment 1, the terminal shoot tip was manually destroyed to eliminate the terminal bud and the most dominant primary axillary shoot was allowed to grow and flower. In treatment two, the terminal bud and all primary axillary buds were manually destroyed and the most dominant secondary axillary shoot was allowed to grow and flower. Observations were made to verify that axillary, not adventitious buds, were generated.
Plants were grown in a greenhouse under 16-h or longer days to promote flowering. They were allowed to self-pollinate without manual assistance. All capsules from the inflorescence were collected individually as they ripened, and all seed from a capsule was planted in a flat in a growth room. Because the seed in Nicotiana are so small and numerous, the number of seed per capsule was estimated by counting and weighing two samples of 100 seed for each inflorescence. These seed samples were then sown to acquire a germination percentage so that data could be adjusted to account for seed that were inviable. There was a concern that a rare green seedling germinating in a milieu of dying white seedlings might go unnoticed or die and critical data would be lost. To test this, three seeds of Nicotiana tabacum, a related but phenotypically distinguishable green species, were sown along with the seed from each capsule of the mosaic N. sylvestris plant. The phenotype of seedlings derived from mosaic shoots was evaluated 10 d after the seed had germinated, when the surviving green seedlings had initiated their first true leaves. Seedling phenotype was used to determine from which apical cell layer eggs were ultimately derived. Lethal white seedlings were derived from L2 and all green seedlings (with the exception of the three N. tabacum seeds added) from either L1 or L3.
RESULTS
Characterization of plant material
The plant used was confirmed to be a Green-White-Green (G-W-G) periclinal chimera (L1-L2-L3, respectively). Verification that the L1 was green was based upon the observation of green chloroplasts in the guard cells. Additional support for a green L1 was the very rare appearance of green mesophyll patches on the otherwise white leaf edge, a trait caused by atypical periclinal divisions of L1 into L2 along the leaf margin (Fig. 20 in Marcotrigiano, 1997
). L2 and L3 verification was based upon leaf variegation pattern and the seedling phenotype of self-pollinated populations (Burk, Stewart, and Dermen, 1964
). Reciprocal crosses between wild-type N. sylvestris and the G-W-G chimera indicated that the chlorotic trait was inherited cytoplasmically (Table 1). Therefore, the egg genotype (descendent of L2) determined whether seedlings would be white or green, as the relevant organelles (plastids) are maternally inherited in Nicotiana (Burk, Stewart, and Dermen 1964
; Wildman, Lu-Liao, and Wong-Staal, 1973
).
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) indicated that, unlike adventitious buds, secondary axillary buds grow out quickly following the removal of primary bud and develop in the nodal area prior to the removal of the primary bud. As observed in this experiment (Fig. 1) and as summarized by Esau (1977)
, the midvein of each prophyll of axillary buds is perpendicular to the stem axis of the main shoot (Fig. 1) whereas the first leaves of adventitious shoots are oriented randomly (Tian and Marcotrigiano, 1994
). All shoots generated on treated plants in the experiment were derived from axillary buds.
Analysis of progeny from axillary buds
The control plants (i.e., plants with undamaged terminal shoots) of the self-pollinated G-W-G N. sylvestris chimera produced a total of 172 capsules containing over 305 000 germinable seeds. All seedlings were white indicating they were derived from L2 (Table 2). The primary axillary shoots produced 91 capsules containing 128 402 germinable seed, all of which were white (Table 2). These seedlings germinated to the cotyledonary stage, quickly became chlorotic, and died. The phenotype of the primary axillary shoots was identical in the control plants and was typical of a stable periclinal chimera (Figs. 2–4). In sharp contrast, secondary axillary shoots yielded capsules with L2 and non-L2 derived progeny (Table 2). One shoot (Fig. 6) produced 77 473 germinating seed, of which only 16 765 were of L2 origin with the remaining 60 708 being descended from L1 or L3. Upon flowering, the other secondary axillary shoot (Fig. 5) was a weak white shoot with only one capsule setting seed, all of which were white.
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DISCUSSION
Biological evidence to support the concept proposed
Most mosaic plants, although genetically mosaic, are phenotypically homogeneous since most mutations are recessive. Since plants possess multicellular apices and most higher plants possess stratified shoot apices (Klekowski, 1988
), the spontaneous mutation of one apical cell would be unlikely to result in a homogeneously mutant shoot apical meristem. Rather, individual mosaic apices would develop where mutant cell types are confined to a single apical cell layer. Since some genes are expressed only in certain cell layers (e.g., Pereau-Leroy, 1974
; Fleming et al., 1993
), even dominant mutations may not be expressed if they are sequestered in a cell layer where they are not developmentally expressed. For example, there are horticultural varieties of prickleless ("thornless") blackberries that are periclinal chimeras possessing a genetically prickleless epidermis (L1) surrounding a core of genetically prickled cells (McPheeters and Skirvin, 1983
). Yet, they do not develop prickles since the genes that initiate the developmental pathway to prickles are expressed in only the epidermal cells. If shoots emerge from an inner tissue layer (e.g., L2 or L3 adventitious shoots derived from root cuttings), their epidermis is genetically prickled and prickles develop. Even if, hypothetically, a spontaneously occurring dominant trichome (i.e., epidermal hair) mutation that conferred the production of an insect toxin arose, it would be effective only if it was present in cells of L1, the cell layer responsible for the epidermis. Since gametes are derived from L2 in most higher plants, this mutation would be beneficial only to the individual plant and possibly its vegetative offspring, not to its sexual offspring. If this mutation occurred in the L2, it would not be expressed in the shoot of the original plant, and this plant would be at no selective advantage with regard to surviving predation. If the plant survived by chance alone, some offspring could inherit the trait. It is clear that meristem anatomy can developmentally isolate mutant cell lineages from gamete-producing cells and future generations. Therefore, in sexually reproducing populations, it is not the fact that genetic mosaics exist that is important, rather it is the fate of the gametes of genetic mosaics, as presented by this study, that should concern us.
Stratified shoot apices and "gene escape"
Within the plant kingdom, there is variability in the organization of cells in shoot apices. Lower plants, such as ferns, do not have stratified apices. Instead, they possess a single initial cell at the terminus of the meristem (e.g., Steeves, 1963
). In the gymnosperms, apical organization varies between families. In the Cupressaceae, a one-layered tunica with a subtending corpus is common and layer invasions from L1 to L2 appear quite frequently as evidenced by the foliage phenotype of periclinal chloroplast chimeras (Pohlheim, 1971a, b
). Periclinal chimeras are common in monocots (Marcotrigiano, 1997
), but variability in the contribution of apical cell layers to defined leaf areas is greater than in dicots. Progeny analysis of monocot periclinal chimeras has received little attention.
The adaptive significance of the evolution of stratified apices in the most dominant group of vascular plants, the angiosperms, has not been resolved (e.g., Klekowski, Kazarinova-Fukshansky, and Mohr, 1985
). Mathematical models indicate that the primary consequence of the stratified shoot apex is an increase in the retention of mutations in somatic tissues when compared to stochastic apices (Klekowski, Kazarinova-Fukshansky, and Mohr, 1985
). Yet, the retention in stratified apices of mutations that might otherwise be lost in stochastic apices does not insure that these mutations have an evolutionary consequence. Mutations may be sequestered from the gene pool, since gametes are almost always derived from a single apical cell layer and apices in higher plants are multilayered. For example, when an unstable mutation in the W locus of peach (Prunus persica) was analyzed, it was noted that reversions of the W locus that occurred in L1 were not seed transmissible except in very rare cases where cell layer displacements occurred and cells from L1 were displaced into L2 during flower development (Chaparro et al., 1995
). In morning glory (Ipomoea purpurea), it has been demonstrated that color mutations, not expressed in the epidermis of periclinal chimeras, can be transmitted through progeny because gametes are derived from subepidermal layers (Inagaki, Histomi, and Ida, 1996
). In Nicotiana, the terminal shoot apex of the main shoot of a periclinal chimera possessing a phenotypically marked and genetically unique L2 was self-pollinated and over 50 000 seed sown (Marcotrigiano and Bernatzky, 1995
). All seedlings were derived from L2, indicating that L1 and L3 derivatives played no role in contributing to the genetic makeup of offspring. Similarly, the control plants of the G-W-G N. sylvestris chimera (Tables 1, 2) produced L2-derived seedlings as did the shoots derived from primary axillary buds. Yet, secondary axillary buds yielded capsules with L2, or a mixture of L2 and non-L2 derived progeny. "Layer invasions," as depicted in Fig. 7, appear to be common in secondary buds.
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). In contrast, the shoots derived from secondary axillary buds displayed an irregular and unpredictable pattern of variegation. This phenomenon has been previously noted in the secondary axillary buds in interspecific graft chimeras (Tian and Marcotrigiano, 1994
). In the G-W-G Nicotiana sylvestris, unstable cell lineages in secondary axillary buds are reported here for the first time in intraspecific chimeras.
Secondary shoot phenotype displayed gross changes in composition when compared to control and primary shoots. No single capsule from the complex mosaic produced both white and green seedlings. Twenty percent of the capsules produced all white seedlings, while 80% produced all green seedlings. Interpreting the cause of such large changes in plant phenotype and the absence of intracapsule mixed seedling populations is assisted by the literature on clonal analysis. In clonal analysis, radiation induced chromosome damage is used to create phenotypically marked cells whose descendants form a clone. Since radiation can be applied either early or late in the development of an organ, it is possible to trace cell lineage at both times. Clonal analysis (Poethig, 1987
) supports the concept that extreme changes in leaf variegation pattern (Figs. 5–6) are caused by events that occur early in the development of an organ at a time when fewer cells exist, while small changes in phenotype would indicate that cell division was nearly ceasing at the time of the event. This supports the fact that the displacement of cell layers in secondary axillary buds occurred early in development, not within individual floral meristems, a possible explanation for the absence of mixed seedling populations in individual capsules. In a previous study, we determined that secondary axillary buds are smaller than primary buds and histological evidence indicates they contain fewer cells (Tian and Marcotrigiano, 1994
). It is feasible that early cell layer displacements between layers occurred in the shoot apices of the smaller secondary axillary buds. Since these buds possess relatively fewer cells, this led to major novel sectors that produce floral meristems with sectors of "green" L2 as depicted in Fig. 7. Alternatively, the order of cell layers in the leaf axil where secondary axillary buds originate may not be conserved to the extent that it is in the region where primary buds originate. In either case, the continuity of cell lineage was not maintained from terminal apex of the main shoot to the apex of the growing secondary bud. The result is that secondary meristems, while still possessing stratified apices, may not maintain the lineage of the shoot apical pattern of the main shoot. Therefore, as the inflorescence branches, it develops floral meristems with sectors of "green" in L2. These sectors are ultimately descended from either the L1 or L3 of the main shoot.
Whitham and Slobodchikoff (1981)
realized that genetic mosaics could have an impact on the evolution of plants in that they could make mutations unavailable to the gene pool. They correctly concluded that the development of adventitious buds arising de novo on genetically mosaic plants would allow mutations not normally expressed in gametes to be incorporated in the gene pool. Adventitious buds generally develop following the destruction of most, if not all, preformed axillary buds. In eucalypts, for example, coppice or adventitious shoots are developed following the destruction of much of the tree by wild fire (Steinbauer, Clarke, and Paterson, 1998
).
In this report, I offer an additional mechanism by which sequestered mutant cell lineages can "escape" from a non-gamete-forming cell layer in a periclinal chimera and eventually develop into gametes. It is not necessary for all axillary buds to be destroyed and for de novo adventitious shoot formation to occur to induce the dissociation of a genetic mosaic. Rather, in plants that produce multiple axillary buds, the secondary buds may be inherently unstable with regard to maintenance of cell lineage from the terminal shoot meristem. Herbivores may influence plant evolution by causing the outgrowth of secondary buds where previously sequestered mutant cells can enter gamete-forming cell layers allowing mutations to enter the gene pool.
FOOTNOTES
1 The author thanks Dr. Edward J. Klekowski Jr. for the stimulating conversations and constructive reviews of earlier drafts of this manuscript; and Polly Ryan, Carrie Lapaire, Paul Risi, Johanna Hyde, and Susan Dorais for technical assistance. 
LITERATURE CITED
Burk, L. G., R. N. Stewart, and H. Dermen. 1964 Histogenesis and genetics of a plastid-controlled chlorophyll variegation in tobacco. American Journal of Botany 51: 713–724. [CrossRef][ISI]
Chaparro, J. X., D. J. Werner, R. W. Whetten, and D. M. O'Malley. 1995 Characterization of a unstable anthocyanin phenotype and estimation of somatic mutation rates in peach. Journal of Heredity 86: 186–193.
Coulson, R. N., and J. A. Witter. 1984 Forest entomology—ecology and management. John Wiley & Sons, New York, New York, USA.
Crawley, M. J. 1983 Herbivory—the dynamics of animal-plant interactions. University of California Press, Berkeley, California, USA.
Esau, K. 1977 Anatomy of seed plants. John Wiley and Sons, New York, New York, USA.
Fleming, A. J., T. Mandel, I. Roth, and C. Kuhlemeier. 1993 The patterns of gene expression in tomato shoot apical meristems. Plant Cell 5: 297–309. [Abstract]
Garrison, R. 1949 Origin and development of axillary buds: Syringa vulgaris L. American Journal of Botany 36: 205–213. [CrossRef][ISI]
———. 1955 Studies in the development of axillary buds. American Journal of Botany 42: 257–266. [CrossRef][ISI]
Gill, D. E., L. Chao, S. L. Perkins, and J. B. Wolf. 1995 Genetic mosaicism in plants and clonal animals. Annual Review of Ecology and Systematics 26: 423–444. [ISI]
Halle, F., R. A. A. Oldeman, and P. B. Tomlinson. 1978 Tropical trees and forests—an architectural analysis. Springer-Verlag, New York, NY.
Hartmann, H. T., D. E. Kester, R. T. Davies, Jr., and R. L. Geneve. 1997 Plant propagation: principles and practices. Prentice Hall, Upper Saddle River, NJ.
Inagaki, Y., Y. Hisatomi, and S. Ida. 1996 Somatic mutations caused by excision of the transposable element, Tpn1, from the DFR gene for pigmentation in sub-epidermal layer of periclinally chimeric flowers of Japanese morning glory and their transmission to their progeny. Theoretical and Applied Genetics 92: 499–504. [CrossRef][ISI]
Johnson, W. T., and H. H. Lyon. 1976 Insects that feed on trees and shrubs. Comstock Publishing Associates/Cornell University Press, Ithaca, New York, USA.
Kirk, J. T. O., and R. A. E. Tilney-Bassett. 1978 The plastids—their chemistry, structure, growth and inheritance. Elsevier/North Holland Biomedical Press, Amsterdam.
Klekowski, E. J., Jr. 1988 Mutation, developmental selection, and plant evolution. Columbia University Press, New York, New York, USA.
———, N. Kazarinova-Fukshansky, and H. Mohr. 1985 Shoot apical meristems and mutation: stratified meristems and angiosperm evolution. American Journal of Botany 72: 1788–1800. [CrossRef][ISI]
———, R. Lowenfeld, and E. H. Klekowski. 1996 Mangrove genetics. IV. Postzygotic mutations fixed as periclinal chimeras. International Journal of Plant Science 157: 398–405. [CrossRef]
Marcotrigiano, M. 1997 Chimeras and variegation: patterns of deceit. HortScience 32: 773–784.
———, and R. Bernatzky. 1995 Arrangement of cells layers in the shoot apical meristems of periclinal chimeras influences cell fate. Plant Journal 7: 193–202.
McPheeters, K., and R. M. Skirvin. 1983 Histogenic layer manipulation in chimeral thornless evergreen trailing blackberry. Euphytica 32: 351–360. [CrossRef][ISI]
Pereau-Leroy, P. 1974 Genetic interactions between the tissues of carnation petals as periclinal chimeras. Radiation Botany 14: 109–116. [CrossRef][ISI]
Poethig, R. S. 1984 Patterns and problems in angiosperm leaf morphogenesis. In G. M. Malacinski and S. V. Bryant [eds.], Pattern formation: a primer in developmental biology, 413–432, MacMillan, New York, New York, USA.
———. 1987 Clonal analysis of cell lineage patterns in plant development. American Journal of Botany 74: 581–594. [CrossRef][ISI]
Pohlheim, F. 1971a Untersuchungen zur Sprossvariation der Cupressaceae. 1. Nachweis immerspaltender Periklinalchimären. Flora 160: 264–293. [ISI]
———. 1971b Untersuchungen zur Sproßvariation der Cupressaceae. 3. Quantitative Auswertung des Scheckungmusters immerspaltender Periklinalchimaren. Flora 160: 360–372. [ISI]
———, and M. Kaufhold. 1985 On the formation of variegation patterns in Filipendula ulmaria ‘Aureo-Variegata’ through changes in the plane of cell division in the epidermisses of young leaves. Flora 177: 167–174. [ISI]
Remphrey, W. R., and T. A. Steeves. 1984 Shoot ontogeny in Arctostaphylos uva-ursi (bearberry): origin and early development of lateral vegetative and floral buds. Canadian Journal of Botany 62: 1933–1939.
Romberger, J. A. 1963 Meristems, growth, and development in woody plants. Technical Bulletin Number 1293, United States Department of Agriculture, Beltsville, MD.
Sagawa, Y., and G. A. L. Mehlquist. 1957 The mechanism responsible for some x-ray induced changes in flower color of the carnation, Dianthus caryophyllus. American Journal of Botany 44: 397–403.
Seltmann, H., and C. S. Kim. 1964 Anatomy of the leaf axil of Nicotiana tabacum L. Tobacco Science: 8: 86–92.
Steeves, T. A. 1963 Morphogenetic studies of Osmunda cinnamonea L.: The shoot apex. Journal of the Indian Botanical Society 42A: 225–236.
Steinbauer, M. J., A. R. Clarke, and S. C. Paterson. 1998 Changes in eucalypt architecture and the foraging behavior and development of Amorbus obscuricornis (Hemiptera: Coreidae). Bulletin of Entomological Research 88: 641–651. [ISI]
Stewart, R. N., and L. G. Burk. 1970 Independence of tissues derived from apical layers in ontogeny of the tobacco leaf and ovary. American Journal of Botany 57: 1010–1016. [CrossRef][ISI]
———, and H. Dermen. 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]
Sussex, I. 1955 Morphogenesis in Solanum tuberosum L.: apical structure and developmental patterns of the juvenile shoot. Phytomorphology 55: 253–273.
Tian, H-c., and M. Marcotrigiano. 1994 Cell-layer interactions influence the number and position of lateral shoot meristems in Nicotiana. Developmental Biology 162: 579–589.
Wardlaw, C. W. 1965 The organization of the shoot apex. In W. Ruhland [ed.], Handbuch der Pflanzenphysiolgie, vol. 15, 969–1076. Springer, Berlin, Germany.
Whitham, T. G., and C. N. Slobodchikoff. 1981 Evolution of individuals, plant-herbivore interactions, and mosaics of genetic variability: the adaptive significance of somatic mutations in plants. Oecologia 49: 287–292. [CrossRef][ISI]
Wildman, S. G., C. Lu-Liao, and F. Wong-Staal. 1973 Maternal inheritance, cytology and macromolecular composition of defective chloroplasts in a variegated mutant of Nicotiana tabacum. Planta 113: 293–312.
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