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The cellular parameters of leaf development in tobacco: a clonal analysis

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Abstract

The cellular parameters of leaf development in tobacco (Nicotiana tabacum L.) have been characterized using clonal analysis, an approach that provides unequivocal evidence of cell lineage. Our results indicate that the tobacco leaf arises from a group of around 100 cells in the shoot apical meristem. Each of these cells contributes to a unique longitudinal section of the axis and transverse section of the lamina. This pattern of cell lincage indicates that primordial cells contribute more or less equally to the growth of the axis, in contrast to the more traditional view of leaf development in which the leaf is pictured as arising from a group of apical initials. Clones induced prior to the initiation of the lamina demonstrate that the subepidermal layer of the lamina arises from at least six files of cells. Submarginal cells usually divide with their spindles parallel to the margin, and therefore contribute relatively little to the transverse expansion of the lamina. During the expansion of the lamina the orientation and frequency of cell division are highly regulated, as is the duration of meristematic growth. Initially, cell division is polarized so as to produce lineages that are at an oblique angle to the midrib; later cell division is in alternating perpendicular planes. The distribution of clones generated by irradiation at various stages of development indicates that cell division ceases at the tip of the leaf when the leaf is about one tenth its final size, and then ceases in progressively more basal regions of the lamina. Variation in the mutation frequency within the lamina reflects variation in the frequency of mitosis. Prior to the mergence of the leaf the frequency of mutation is maximal near the tip of the leaf and extremely low at its base; after emergence, the frequency of mutation increases at the base of the leaf. In any given region of the lamina the frequency of mutation is highest in interveinal regions, and is relatively low near the margin. Thus, both the orientation and frequency of cell division at the leaf margin indicate that this region plays a minor role in the growth of the lamina.

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Abbreviations

MF:

mutation frequency

References

  • Avery, G.S. (1933) Structure and development of the tobacco leaf. Am. J. Bot. 20, 565–592

    Google Scholar 

  • Bensink, J. (1971) On the morphogenesis of leaves in relation to light and temperature. Meded. Landbouwhogeschool Wageningen 71, No. 15

    Google Scholar 

  • Bryant, P.J. (1970) Cell lineage relationships in the imaginal wing disc of Drosophila melanogaster. Dev. Biol. 22, 389–441

    Google Scholar 

  • Coe, E.H. (1978) The aleurone tissue of maize as a genetic tool. In: Maize breeding and genetics, pp. 447–459, Walden, D.B., ed. Wiley-Interscience, New York

    Google Scholar 

  • Coe, E.H. Neuffer, M.G. (1978) Embryo cells and their destinies in the corn plant. In: The clonal basis of development, pp. 113–129, Subtelny, S., Sussex, I., eds. Academic Press, New York

    Google Scholar 

  • Deshayes, A. (1973) Mise en évidence d'une corrélation entre la fréquence de variations somatiques sur feuilles et l'état physiologique d'un mutant chlorophyllien monogénique chez Nicotiana tabacum var. Samsun. Mutat. Res. 17, 323–334

    Google Scholar 

  • Deshayes, A., Dulieu H. (1974) Étude des variations somatiques de deux mutants chlorophylliens de Nicotiana tabacum L., leur nature génétique et les facteurs les favorisent. In: Polyploids and induced mutations in plant breeding, pp. 85–99. International Atomic Energy Agency, Vienna

    Google Scholar 

  • Dewey, W.C., Furman S.C., Miller, H.H. (1970) Comparison of lethality and chromosomal damage induced by X-rays in synchronized chinese hamster cells in vitro. Radiat. Res. 43, 561–581

    Google Scholar 

  • Dubuc-Lebreux, M.A., Sattler, R. (1980) Développement des organes foliacés chez Nicotiana tabacum et le problème des méristèmes marginaux. Phytomorphology 30, 17–32

    Google Scholar 

  • Dulieu, H. (1968) Emploi des chimères chlorophylliennes pour l'étude de l'ontogénie foliare. Bull. Sci. Bourgogne 25, 1–60

    Google Scholar 

  • Dulieu, H. (1970) Les mutations somatiques induites et l'ontogénie de la pousse feuillee. Ann. Amelior. Plant. 20, 27–44

    Google Scholar 

  • Dulieu, H. (1975) Somatic variations on a yellow mutant in Nicotiana tabacum L. (a1 +/a1 a2 +/a2). I. Non-reciprocal genetic events occurring in leaf cells. Mutat. Res. 25, 289–304

    Google Scholar 

  • Dulieu, H. (1975) Somatic variations on a yellow mutant in Nicotiana tabacum L. (a1 +/a1 a2 +/a2). II. Reciprocal genetic events occurring in leaf cells. Mutat. Res. 28, 69–77

    Google Scholar 

  • Dulieu, H., Dalebroux, M.A. (1976) Composantes de variabilité et interactions fonctionnelles aux loci a1 +/a1 et a2 +/a2 de Nicotiana tabacum L. Ann. Amelior. Plant. 26, 569–577

    Google Scholar 

  • Evans, D.A., Paddock, E.F. (1977) X-ray induced increase of mitotic crossovers in Nicotiana tabacum. Environ. Exp. Bot. 17, 99–106

    Google Scholar 

  • Evans, H.J., Scott, D. (1964) Influence of DNA synthesis on the production of chromatid aberrations by X-rays and maleic hydrazide in Vicia faba. Genetics 49, 17–38

    Google Scholar 

  • Fuchs, C. (1966) Observations sur l'extension en largeur du limbe foliaire du Lupinus albus L. C.R. Acad. Sci. Ser. D 263, 1212–1215

    Google Scholar 

  • Fuchs, C. (1975) Ontogenèse foliare et acquisition de la forme chez le Tropaeolum peregrinum L. I. Les premiers stades de l'ontogenèse du lobe médian. Ann. Sci. Nat. Bot. Biol. Veg. 16, 321–390

    Google Scholar 

  • Fuchs, C. (1976) Ontogenèse foliare et acquisition de la forme chez le Tropeolum peregrinum L. II. Le développement du lobe après la formation de lobules. Ann. Sci. Nat. Bot. Biol. Veg. 17, 121–158

    Google Scholar 

  • Garcia-Bellido, A. (1975) Genetic control of wing disc development in Drosophila. In: Cell Patterning, Ciba Foundation Symp. Vol. 29, pp. 161–182. Elsevier, New York

    Google Scholar 

  • Green, P.B. (1984) Shifts in plant cell axiality: histogenetic influence on cellulose orientation in the succulent, Graptopetalum. Dev. Biol. 103, 18–27

    Google Scholar 

  • Green, P.B., Brooks, K.E. (1978) Stem formation from a succulent leaf: its bearing on theories of axiation. Am. J. Bot. 65, 13–26

    Google Scholar 

  • Green, P.B., Lang, J.M. (1981) Toward a biophysical theory of organogenesis: birefringence observations on regenerating leaves in the succulent Graptopetalum paraguayense E. Walther. Planta 151, 413–426

    Google Scholar 

  • Green, P.B., Poethig, R.S. (1982) Biophysics of the extension and initiation of plant organs. In: Developmental order: Its origin and regulation, pp. 485–509, Subtelny S., Green, P.B., eds. A.R. Liss, New York

    Google Scholar 

  • Gudkov, I.N., Grodzinsky, D.M. (1982) Cell radiosensitivity variation in synchronously dividing root meristems of Pisum sativum L. and Zea mays L. during the mitotic cycle. Int. J. Radiat. Biol. 41, 401–409

    Google Scholar 

  • Haber, A.H. (1962) Nonessentiality of concurrent cell divisions for degree of polarization of leaf growth. I. Studies with radiation induced mitotic inhibition. Am. J. Bot. 49, 583–589

    Google Scholar 

  • Haber, A.H., Foard, D.E. (1963) Nonessentiallity of concurrent cell divisions for degree of polarization of leaf growth. II. Evidence from untreated plants and chemically induced changes in the degree of polarization. Am. J. Bot. 50, 937–944

    Google Scholar 

  • Hardham, A.R., Green, P.B., Lang, J.M. (1980) Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense. Planta 149, 181–195

    Google Scholar 

  • Jeune, B. (1972) Observations et expérimentation sur les feuilles juveniles du Paulownia tomentosa. Bull. Soc. Bot. France 119, 215–230

    Google Scholar 

  • Jeune, B. (1982) Morphogénèse des feuilles et stipules de Castanea sativa Miller. Bull. Mus. Natn. Hist. Nat., Paris, Sect. B, Adansonia 4, 85–101

    Google Scholar 

  • Johri, M.M., Coe, E.H. (1983) Clonal analysis of corn plant development. I. The development of the tassel and ear shoot. Dev. Biol. 97, 154–172

    Google Scholar 

  • Maksymowych, R. (1963) Cell division and cell elongation in leaf development of Xanthium pensylvanicum. Am. J. Bot. 50, 891–901

    Google Scholar 

  • Maksymowych, R., Erickson, R.O. (1960) Development of the lamina in Xanthium italicum represented by the plastochron index. Am. J. Bot. 47, 451–459

    Google Scholar 

  • Mericle, L.W., Mericle, R.P. (1969) Induced somatic mutations for interpreting floral development and inflorescence aging. In: Induced mutations in plants, pp. 591–601. International Atomic Energy Agency, Vienna

    Google Scholar 

  • Poethig, R.S. (1984a) Cellular parameters of leaf morphogenesis in maize and tobacco. In: Contemporary problems in plant anatomy, pp. 235–259, White, R.A., Dickison, W.C., eds. Academic Press, New York

    Google Scholar 

  • Poethig, R.S. (1984b) Patterns and problems in angiosperm leaf morphogenesis. In: Pattern formation, pp. 413–432, Malacinski, G.M. Bryant, S.V., eds. MacMillan, New York

    Google Scholar 

  • Poethig, R.S., Sussex, I.M. (1985) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165, 158–169

    Google Scholar 

  • Sachs, T. (1969) Regeneration experiments on the determination of the form of leaves. Israel. J. Bot. 18, 21–30

    Google Scholar 

  • Sand, S.A. (1957) Phenotypic variability and the influence of temperature on somatic instability in cultures derived from hybrids between Nicotiana langsdorffii and N. sanderae. Genetics 42, 685–703

    Google Scholar 

  • Scott, D., Evans, H.J. (1967) X-ray induced chromosome aberrations in Vicia faba: changes in response during the cell cycle. Mutat. Res. 4, 579–599

    Google Scholar 

  • Sax, K. (1940) An analysis of X-ray induced chromosomal aberrations in Tradescantia. Genetics 25, 41–68

    Google Scholar 

  • Sinnott, E.W. (1960) Plant morphogenesis. McGraw-Hill, New York

    Google Scholar 

  • Snow, M. and Snow, R. (1933) Experiments on phyllotaxis. II. The effect of displacing a primordium. Phil. Trans. R. Soc. London Ser. B 222, 353–400

    Google Scholar 

  • Sparrow, A.H. (1951) Radiation sensitivity of cells during mitotic and meiotic cycles with emphasis on possible cytochemical changes. Ann. N.Y. Acad. Sci. 51, 1508–1540

    Google Scholar 

  • St. Amand, W. (1956) Mitotic inhibition and chromosome breakage induced in grasshopper neuroblasts by X-irradiation at known mitotic stages. Radiat. Res. 5, 65–78

    Google Scholar 

  • Stadler, L.J. (1930) Some genetic effects of X-rays in plants. J. Hered. 21, 3–19

    Google Scholar 

  • Stein, O.L., Steffensen, D.M. (1959) The activity of X-rayed apical meristems: a genetic and morphogenetic analysis in Zea mays. Z. Vererbungsl. 90, 483–502

    Google Scholar 

  • Steffensen, D.M. (1968) A reconstruction of cell development in the shoot apex of maize. Am. J. Bot. 55, 354–369

    Google Scholar 

  • Stewart, R.N., Burk, L.G. (1970) Independence of tissues derived from apical layers in ontogeny of the tobacco leaf and ovary. Am. J. Bot. 57, 1010–1016

    Google Scholar 

  • Thomasson, M. (1970) Quelques observations sur la répartition de zones de croissance de la feuille du Jasminum nudiflorum Lindl. Candollea 25, 297–340

    Google Scholar 

  • von Papen, R. (1935) Beiträge zur Kenntnis des Wachstums der Blattspreite. Bot. Arch. 37, 159–206

    Google Scholar 

  • Wolff, S. (1968) Chromosomal aberrations and the cell cycle. Radiat. Res. 33, 609–619

    Google Scholar 

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Author notes

  1. R. S. Poethig

    Present address: Department of Biology, Leidy Laboratories/G7, University of Pennsylvania, 19104, Philadelphia, PA, USA

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  1. Department of Biology, Yale University, 06511, New Haven, CT, USA

    R. S. Poethig & I. M. Sussex

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Poethig, R.S., Sussex, I.M. The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165, 170–184 (1985). https://doi.org/10.1007/BF00395039

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