Skip to main content
Log in

Developmental stability in plants: Symmetries, stress and epigenesis

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Plant developmental stability has received little attention in the past three or four decades. Here we review differences in plant and animal development, and discuss the advantages of using plants as experimental subjects in exploring developmental stability. We argue that any type of developmental invariant may be used to assess developmental stability and review the use of fluctuating asymmetry in studies of plant developmental stability. We also examine the use of deviations from translatory, radial, and self-symmetry as measures of developmental instability. The role of nonlinear dynamics and epigenesis in the production of the phenotype is also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aono, M. & T. L. Kunii, 1984. Botanical tree image generation. Institution of Electrical and Electronics Engineers Computer Graphics and Applications 4: 10–34.

    Article  Google Scholar 

  • Burton, R. S., 1987. Differentiation and integration of the genome in populations ofTigriopus californicus. Evolution 41: 504–513.

    Article  Google Scholar 

  • Burton, R. S., 1990a. Hybrid breakdown in physiological response: a mechanistic approach. Evolution 44: 1806–1813.

    Article  Google Scholar 

  • Burton, R. S., 1990b. Hybrid breakdown in developmental time in the copepodTigriopus californicus. Evolution 44: 1814–1822.

    Article  Google Scholar 

  • Bush, R. M., P. E. Smouse & F. T. Ledig, 1987. The fitness consequences of multiple-locus heterozygosity: the relationship between heterozygosity and growth rate in pitch pine (Pinus rigida Mill.) Evolution 41: 787–798.

    Article  Google Scholar 

  • Byrd, D. W., 1992. Biochemical assessment of the hybrid zone formed byArtemisia tridentata tridentata andArtemisia tridentata vaseyana using an automated gas chromatography-data system and statistical methods. Master's thesis. Wayne State University, Detroit, Michigan.

    Google Scholar 

  • Clarke, G. M. & J. A. McKenzie, 1987. Developmental stability of insecticide resistant phenotypes in blowfly; a result of canalizing natural selection. Nature 325: 345–346.

    Article  CAS  Google Scholar 

  • Clarke, G. M., 1992. Fluctuating asymmetry: a technique for measuring developmental stress of genetic and environmental origin. Acta Zool. Fennica 191: 31–35.

    Google Scholar 

  • Clarke, G. M., B. P. Oldroyd & P. Hunt, 1992. The genetic basis of developmental stability inApis mellifera: heterozygosity versus genic balance. Evolution 46: 753–762.

    Article  Google Scholar 

  • Cocho, G. & J. L. Rius, 1989. Discreet aspects of morphogenesis and gene dynamics, pp. 177–190 in Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems, edited by B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Cullis, C. A., 1977. Molecular aspects of the environmental induction of heritable changes in flax. Heredity 38: 129–154.

    Google Scholar 

  • Cullis, C. A., 1983. Environmentally induced DNA changes in plants. CRC Critical Reviews in Plant Sciences 1: 117–129.

    CAS  Google Scholar 

  • Cullis, C. A., 1986. Phenotypic consequences of environmentally induced changes in plant DNA. Trends in Genetics 2: 307–309.

    Article  CAS  Google Scholar 

  • Cullis, C. A., 1987. The generation of somatic and heritable variation in response to stress. American Naturalist 130: S62-S73.

    Article  Google Scholar 

  • Davies, P. C. W., 1989. The physics of complex organization, pp. 101–111 in Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems, edited by B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Davis, T. A., 1962. The non-inheritance of asymmetry inCocos nucifera. J. Genet. 58: 42–50.

    Google Scholar 

  • Davis, T. A., 1962. Asymmetry and yield in coconut. Experientia 18: 321–322.

    Article  Google Scholar 

  • Davis, T. A., 1963. The dependence of yield on asymmetry in coconut palms. J. Genet. 58: 186–215.

    Google Scholar 

  • Desbiez, M. O., M. Tort & M. Thellier, 1991. Control of a symmetry-breaking process in the course of the morphogenesis of plantlets ofBidens pilosa L. Planta 184: 397–402.

    Article  Google Scholar 

  • Duke, S. O., R. N. Paul, Jr. & S. M. Lee, 1988. Terpenoids fromArtemisia as potential pesticides. ACS Symposium Series 380: 318–334.

    Article  CAS  Google Scholar 

  • Eanes, W. F., 1984. Viability interactions,in vivo activity and the G6PD polymorphism inDrosophila melanogaster. Genetics 106: 95–107.

    CAS  PubMed  Google Scholar 

  • Eanes, W. F., 1987. Allozymes and fitness: Evolution of a problem. TREE 2: 44–48.

    Google Scholar 

  • Eilbeck, J. C., 1989. Pattern formation and pattern selection in reaction-diffusion systems, pp. 31–41 in Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems, edited by B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Emlen, J. M., D. C. Freeman & J. H. Graham. Nonlinear growth dynamics and the origin of fluctuating asymmetry (Genetica, this volume).

  • Fahn, A., 1974. Plant Anatomy. Pergamon Press, New York.

    Google Scholar 

  • Gilbert, S. F., 1991. Developmental Biology. Third Edition. Sinauer Associates, Inc., Sunderland, Mass.

    Google Scholar 

  • Goodwin, B. C., 1989. Evolution and the generative order, pp. 89–100 in Theoretical Biology, Epigenetic and Evolutionary Order from Complex Systems, edited by B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Goss, R. J., 1966. Hypertrophy versus hyperplasia. Science 153: 1615–1620.

    CAS  PubMed  Google Scholar 

  • Graham, J. H., 1992. Genomic coadaptation and developmental stability in hybrid zones. Acta Zool. Fennica 191: 121–131.

    Google Scholar 

  • Grahm, J. H., D. C. Freeman & J. M. Emlen, 1993a. Antisymmetry, directional asymmetry and chaotic morphogenesis. (Genetica, this volume).

  • Graham, J. H., D. C. Freeman & J. M. Emlen, 1993b. Developmental stability: a sensitive indicator of populations under stress. In Environmental risk assessment, ASTM STP 1179, Wayne G. Landis, Jane S. Hughes, and Michael A. Lewis, Eds. American Society for Testing and Materials, Philadelphia pp. 136–158.

    Google Scholar 

  • Graham, J. H., D. C. Freeman & E. D. McArthur. Selection and dispersal in narrow hybrid zones between two subspecies of big sagebrush (Artemisia tridentata ssp.tridentata andA. t. ssp.vaseyana). Submitted to the American Journal of Botany.

  • Hecks, B., Z. Hejnowicz & A. Sievers, 1992. Spontaneous oscillations of extracellular electrical potentials measured onLepidium sativum L. roots. Plant, Cell and Environment 15: 115–121.

    Article  Google Scholar 

  • Huberman, B. A., 1989. The adaptation of complex systems, pp. 124–133 in: Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Hughes, M. B. & J. C. Lucchesi, 1977. Genetic rescue of a lethal ‘null’ activity allele of 6 phosphogluconate dehydrogenase fromDrosophila melanogaster. Science 196: 1114–1115.

    CAS  PubMed  Google Scholar 

  • Jaffe, L. F., 1980. Control of plant development by steady ionic currents. In: Plant Membrane Transport: Current Conceptual Issues. Editors: W. Spanswick, J. Lucas and J. Dainty. pp. 381–388. Biomedical Press/Elsevier, North-Holland.

    Google Scholar 

  • Jaffe, L. F. & R. Nuccitelli, 1977. Electrical controls of development. Annual Review of Biophysics and Bioengineering 6: 445–476.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, D. R. & W. Hagemann, 1991. The relationship of cell and organism in vascular plants. Are cells the building blocks of plant form? Bioscience 41: 693–703.

    Article  Google Scholar 

  • Kauffman, S. A., 1989. Origins of order in evolution: self-organization and selection, pp. 67–88 in: Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Kelsey, R. G., 1984. Foliage biomass and crude terpenoid productivity of big sagebrush. Symposium on the biology ofArtemisia andChrysothamus; Department of Agriculture, Forest Service, Intermountain Research Station. General Technical Report INT-200: 375–388.

  • Kelsey, R. G., J. R. Stephens & F. Sharizadeh, 1982. The chemical constituents of sagebrush foliage and their isolation. Journal of Range Management 35: 617–622.

    CAS  Google Scholar 

  • Kieser, J. A., 1993. Developmental instability, evolution and the theory of acquisition. Genetica: Special Issue.

  • Kigel, J., I. Konsens & M. Ofir, 1991. Branching, flowering and pod-set patterns in snap-bean (Phaseolus vulgaris L.) as affected by temperature. Can. J. Plant Sci. 71: 1233–1242.

    Google Scholar 

  • Kojima, K., T. Mukai, H. Suemoto, N. Sueoka & H. Ono, 1955. Studies on the right- and left-handedness of spikelets in Einkorn wheats. VI. Polygenic analysis in a species cross. Proc. Japan Acad. 31: 228–233.

    Google Scholar 

  • Konsens, I., M. Ofir & J. Kigel, 1991. The effect of temperature on the production and abscission of flowers and pods in snap-bean (Phaseolus vulgaris L.). Ann. Bot. 67: 391–399.

    Google Scholar 

  • Lara-Ochoa, F., 1989. Membrane Phase Transitions, pp. 147–161 in: Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1983. Developmental stability and enzyme heterozygosity in rainbow trout. Nature 301: 71–72.

    Article  CAS  PubMed  Google Scholar 

  • Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1984. Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Amer. Nat. 124: 540–551.

    Article  Google Scholar 

  • Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1985. Developmental instability as an indicator of reduced genetic variation in hatchery trout. Trans. Amer. Fish. Soc. 114: 230–235.

    Article  Google Scholar 

  • Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1992. Genetic, environmental and developmental causes of meristic variation in rainbow trout. Acta Zool. Fennica 191: 79–95.

    Google Scholar 

  • Lerner, I. M., 1954. Genetic Homeostasis. John Wiley & Sons, Inc., New York.

    Google Scholar 

  • Lindenmayer, A., 1968. Mathematical models for cellular interaction in development, Parts I and II. J. Theoret. Biol. 18: 280–315.

    Article  CAS  Google Scholar 

  • Ludwig, J. A. & J. F. Reynolds, 1988. Statistical ecology. John Wiley and Sons. New York. 337 p.

    Google Scholar 

  • Markow, T. A. & J. P. Ricker, 1991. Developmental stability in hybrids between the sibling species pairDrosophila melanogaster andDrosophila simulans. Genetica 84: 115–121.

    Article  CAS  PubMed  Google Scholar 

  • Mather, K., 1953. Genetical control of stability in development. Heredity 7: 297–336.

    Google Scholar 

  • McKenzie, J. & K. O'Farrell, 1993. Modification of developmental instability and fitness: Malathion-resistance in the Australian blowflyLucilia cuprina. Genetica: Special Issue.

  • Meinhardt, H., 1982. Models of Biological Patterns Formation. Academic, New York.

    Google Scholar 

  • Minzoni, A. A. & F. Alonso-deFlorida, 1989. Time and Space Scales in Neurophysiology, pp. 191–197 in: Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Mitchison, G. J., 1977. Phyllotaxis and the fibonacci series. Science 196: 270–275.

    PubMed  Google Scholar 

  • Mitchison, G. J., 1980. A model for vein formation in higher plants. Proc. R. Soc. Lond. B 207: 79–109.

    Article  Google Scholar 

  • Palmer, A. R. & C. Strobeck, 1992. Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool. Fennica 191: 57–72.

    Google Scholar 

  • Palmer, A. R. & C. Strobeck, 1986. Fluctuating asymmetry: measurement, analysis, patterns. Ann. Rev. Ecol. System. 17: 391–421.

    Article  Google Scholar 

  • Paxman, G. J., 1956. Differentiation and stability in the development ofNicotiana rustica. Ann. Bot. 20: 331–347.

    Google Scholar 

  • Pearson, J. E. & W. Horsthemke, 1989. Turing instabilities with nearly equal diffusion coefficients. J. Chem. Phys. 90: 1588–1599.

    Article  CAS  Google Scholar 

  • Prusinkiewicz, P. & J. Hanan, 1985. Lindenmayer systems, fractals, and plants. In: Lecture Notes in Biomathematics. Managing Editor: S. Levin. Springer-Verlag, New York.

    Google Scholar 

  • Richards, F. J., 1951. The geometry of phyllotaxis and its origin. Symp. Soc. Exp. Biol. 2: 217–245.

    Google Scholar 

  • Roy, S. K., 1963. The variation of organs of individual plants. J. Genet. 58: 147–176.

    Article  Google Scholar 

  • Sachs, T., 1975. The control of the differentiation of vascular networks. Ann. Bot. 39: 197–204.

    Google Scholar 

  • Sakai, K. & Y. Shimamoto, 1965. Developmental instability in leaves and flowers ofNicotiana tabacum. Genetics 51: 801–813.

    PubMed  CAS  Google Scholar 

  • Saunders, P. T. & C. Kubal, 1989. Bifurcations and the epigenetic landscape, pp. 16–30 in: Theoretical Biology; Epigenetic and Evolutionary Order From Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Savageau, M. A., 1989. Are there rules governing patterns of gene regulation?, pp. 42–66 in: Theoretical Biology; Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Schroeder, M., 1991. Fractals, Chaos, Power Laws; Minutes from an Infinite Paradise. W. H. Freeman and Co., New York.

    Google Scholar 

  • Souda, M., K. Toko, K. Hayashi, T. Fujiyoshi, S. Ezaki & K. Yamafuji, 1990. Relationship between growth and electric oscillations in bean roots. Plant Physiology 93: 432–436.

    Google Scholar 

  • Strauss, S. H., 1987. Heterozygosity and developmental stability under inbreeding and crossbreeding inPinus attentuata. Evolution 41: 331–339.

    Article  Google Scholar 

  • Sueoka, N. & T. Mukai, 1956. Studies on the right- and left-handedness of spikelets in Einkorn wheats. VII. The c-value of the species ofTriticum andAegilops. Proc. Japan Acad. 32: 191–196.

    Google Scholar 

  • Tatsum, J., A. Yamauchi & Y. Kono, 1989. Fractal analysis of plant root systems. Annals of Botany 64: 499–503.

    Google Scholar 

  • Thom, R. An inventory of Waddingtonian concepts. 1989, pp. 1–7 in: Theoretical Biology; Epigenetic and Evolutionary Order From Complex Systems. Editors: B. Goodwin and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

  • Timofeeff-Ressovsky, N. V., 1934. Uber der einfluss des genotypischen milieus und der aussenhebedigunen auf die realisation des genotypes. Genmutation vti beiDrosophila funebris. Nachr. Acad. Wiss. Gottingen II. Math-Phys. Kl. Fg. 6: 53–106.

    Google Scholar 

  • Toko, K., S. Iiyama, C. Tanaka, K. Hayashi, Keiko Yamafuji & Kaoru Yamafuji, 1987. Relation of growth process to spatial patterns or electrical and enzyme activity in bean roots. Biophysical Chemistry 27: 39–58.

    Article  CAS  PubMed  Google Scholar 

  • Toko, K., M. Souda, T. Matsumo & K. Yamafuji, 1990. Oscillations of electrical potential along a root of a higher plant. Biophysical Journal 57: 269–279.

    Article  PubMed  Google Scholar 

  • Tornheim, K., 1986. Fructose-2, 6-biphosphate and glycolytic oscillation in skeletal-muscle extract. Federation Proceedings 45: 1840.

    Google Scholar 

  • Trewavas, A., 1991. How do plant growth substances work? II. Plant, Cell and Environment 14: 1–12.

    Article  CAS  Google Scholar 

  • Turing, A. M., 1952. The chemical basis of morphogenesis. Philos. Trans. Roy. Soc. London B 327: 37–72.

    Google Scholar 

  • Van Valen, L., 1962. A study of fluctuating asymmetry. Evolution 16: 125–142.

    Article  Google Scholar 

  • Vastano, J. A., J. E. Pearson, W. Horsthemke & H. L. Swinney, 1987. Chemical pattern formation with equal diffusion coefficients. Physics Letters A. 1234: 320–324.

    Article  Google Scholar 

  • Waddington, C. H., 1957. The strategy of genes. Allen & Unwin London.

    Google Scholar 

  • Ward, J. M. & K. B. Armitage, 1981. Circannual rhythms of food consumption, body mass and metabolism in yellow-bellied marmots (Marmota flaviventris). Comp. Biochem. Physiol. 69[A]: 621–626.

    Article  Google Scholar 

  • Watkinson, A. R. & J. White, 1986. Some life-history consequences of modular construction in plants. Phil. Trans. R. Soc. London B 313: 31–51.

    Google Scholar 

  • Wegner, T. & M. Peterson, 1991. The Waite Group's Fractal Creations. Waite Group Press. Mill Valley, CA. 315 p.

    Google Scholar 

  • Weisenseel, M. H., A. Dorn & L. F. Jaffe, 1979. Natural H+ currents traverse growing roots and root hairs of barley (Hordeum vulgare L.). Plant Physiology 64: 512–518.

    CAS  PubMed  Google Scholar 

  • Weisenseel, M. H. & R. M. Kicherer, 1981. Ionic currents as control mechanism in cytomorphogenesis. In: Cell Biology Monographs, Vol. 8. Editor: O. Kiermayer. pp. 379–399. Springer-Verlag, Berlin.

    Google Scholar 

  • West, B. J. & A. L. Goldberger, 1987. Physiology in fractal dimensions. Am. Scientist 75: 354–365.

    Google Scholar 

  • West, B. J. & M. F. Shlesinger, 1989. On the ubiquity of 1/f noise. Inter. J. Mod. Phys. B 3(6): 795–819.

    Article  Google Scholar 

  • West, B. J., 1990. Physiology in fractal dimensions: error tolerance. Ann. Biomed. Eng. 18: 135–149.

    Article  CAS  PubMed  Google Scholar 

  • West, B. J. & M. Shlesinger, 1990. The noise in natural phenomena. Am. Sci. 78: 40–45.

    Google Scholar 

  • Zakharov, V. M., 1989. Future prospects for populations phenogenetics. Sov. Sci. Rev. F. Physiol. Gen. Biol. 4: 1–79.

    Google Scholar 

  • Zakharov, V. M., E. Pankakoske, B. I. Sheftel, A. Peltonen & I. Hanski, 1991. Developmental stability and population dynamics in the common shrewSorex araneus. Am. Nat. 138: 797–810.

    Article  Google Scholar 

  • Zakharov, V. M., 1990. Analysis of fluctuating asymmetry as a method of biomonitoring at the population level. pp 187–198 In. Krivolutsky (ed). Bioindications of chemical and radioactive pollution. Mir Publishers Moscow/CRC Press Boca Raton.

    Google Scholar 

  • Zakharov, V. M., 1992. Population phenogenetics: Analysis of developmental stability in natural populations. In V. M. Zakharov & J. H. Graham. Developmental stability in natural populations. Acta Zool. Fennica 19: 7–30.

    Google Scholar 

  • Zeeman, C., 1989. A new concept of stability, pp. 8–15 in: Theoretical Biology. Epigenetic and Evolutionary Order from Complex Systems. Editors: B. Goodwin, and P. Saunders. Edinburgh University Press, Edinburgh.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Freeman, D.C., Graham, J.H. & Emlen, J.M. Developmental stability in plants: Symmetries, stress and epigenesis. Genetica 89, 97–119 (1993). https://doi.org/10.1007/BF02424508

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02424508

Key words

Navigation