Advertisement

Science China Life Sciences

, Volume 62, Issue 4, pp 453–466 | Cite as

Plant Morphogenesis 123: a renaissance in modern botany?

  • Shu-Nong BaiEmail author
Review
  • 23 Downloads

Abstract

Plants are a group of multicellular organisms crucial for the biosphere on the Earth. In the 17th century, the founding fathers of modern botany viewed the bud as the basic unit undergoing the plant life cycle. However, for many understandable reasons, the dominant conceptual framework evolved away from the “bud-centered” viewpoint to a “plant-centered” viewpoint that treated the whole plant, consisting of numerous buds, as a unit and considered the entire plant to be the functional equivalent of an animal individual. While this “plant-centered” viewpoint is convenient and great progress has been made using this conceptual framework, some fundamental problems remain logically unsolvable. Previously, I have proposed a new conceptual framework for interpretation of plant morphogenesis, called Plant Morphogenesis 123, which revives a “bud-centered” viewpoint. The perspective of Plant Morphogenesis 123 allows us to address new questions regarding to the mechanisms of plant morphogenesis that are important, and technically accessible, but previously neglected under the “plant-centered” conceptual framework. In addition to describing these questions, I address a more fundamental question for further discussion: why do people study plants?

Keywords

Plant Morphogenesis 123 bud-centered viewpoint developmental unit life cycle renaissance 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

I would like to sincerely thank Prof. Manyuan Long (Chicago University) for inviting me to write this article. This invitation gave me the opportunity to propose some new questions about plant morphogenesis which I feel are worthy of investigation.

References

  1. Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13, 627–639.CrossRefGoogle Scholar
  2. Arber, A.R. (1950). The Natural Philosophy of Plant Form (Cambridge England: Cambridge University Press).Google Scholar
  3. Bai, S.N., and Xu, Z.H. (2012). Bird–nest puzzle: can the study of unisexual flowers such as cucumber solve the problem of plant sex determination? Protoplasma 249(Suppl 2), S119–123.Google Scholar
  4. Bai, S.N., and Xu, Z.H. (2013). Unisexual cucumber flowers, sex and sex differentiation. Int Rev Cell Mol Biol 304, 1–55.CrossRefGoogle Scholar
  5. Bai, S. (2015). The concept of the sexual reproduction cycle and its evolutionary significance. Front Plant Sci 6, 11.CrossRefGoogle Scholar
  6. Bai, S.N. (2016). Make a new cloth for a grown body: from plant developmental unit to plant developmental program. Annu Rev New Biol, 73–116.Google Scholar
  7. Bai, S.N. (2017). Reconsideration of plant morphological traits: from a structure–based perspective to a function–based evolutionary perspective. Front Plant Sci 8, 345.Google Scholar
  8. Bai, S.N. (2019). A Reconsideration of Sex: Heterogametogenesis, Sex Differentiation, and Sexual Behavior, from the Perspective of the Sexual Reproduction Cycle. In Regulation of Plant Development, H. Ma, and Z.H. Xu, ed. (in Press).Google Scholar
  9. Barton, M.K. (2010). Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341, 95–113.CrossRefGoogle Scholar
  10. Bernier, G., Kinet, J.M., and Sachs, R.M. (1981). The Physiology of Flowering (Boca Raton: CRC Press).Google Scholar
  11. Bower, F.O. (1935). Primitive Land Plants, Also Known as the Archegoniatae (London: Macmillan).Google Scholar
  12. Buchanan, B.B., Gruissem, W., and Jones, R.L. (2015). Biochemistry & Molecular Biology of Plants, 2nd ed. (Chichester, West Sussex Hoboken, NJ: John Wiley & Sons Inc.).Google Scholar
  13. Campbell, N.A., and Reece, J.B. (2005). Biology, 7th ed. (San Francisco, CA: Pearson Benjamin Cummings).Google Scholar
  14. Chen, R., Shen, L.P., Wang, D.H., Wang, F.G., Zeng, H.Y., Chen, Z.S., Peng, Y.B., Lin, Y.N., Tang, X., Deng, M.H., et al. (2015). A gene expression profiling of early rice stamen development that reveals inhibition of photosynthetic genes by OsMADS58. Mol Plant 8, 1069–1089.CrossRefGoogle Scholar
  15. Chiang, G.C.K., Barua, D., Kramer, E.M., Amasino, R.M., and Donohue, K. (2009). Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106, 11661–11666.CrossRefGoogle Scholar
  16. Coen, E. (2001). Goethe and the ABC model of flower development. C R Acad Sci III 324, 523–530.CrossRefGoogle Scholar
  17. Crawford, B.C.W., Sewell, J., Golembeski, G., Roshan, C., Long, J.A., and Yanofsky, M.F. (2015). Genetic control of distal stem cell fate within root and embryonic meristems. Science 347, 655–659.CrossRefGoogle Scholar
  18. Cutter, E.G., and Wardlaw, C.W. (1966). Trends in Plant Morphogenesis: Essays Presented to C. W. Wardlaw on His Sixty–fifth Birthday (London: Longmans).Google Scholar
  19. Deng, W., Ying, H., Helliwell, C.A., Taylor, J.M., Peacock, W.J., and Dennis, E.S. (2011). FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108, 6680–6685.CrossRefGoogle Scholar
  20. Dkhar, J., and Pareek, A. (2014). What determines a leaf’s shape? EvoDevo 5, 47.CrossRefGoogle Scholar
  21. Druege, U., Franken, P., and Hajirezaei, M.R. (2016). Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci 7, 381.CrossRefGoogle Scholar
  22. Efroni, I., Eshed, Y., and Lifschitz, E. (2010). Morphogenesis of simple and compound leaves: a critical review. Plant Cell 22, 1019–1032.CrossRefGoogle Scholar
  23. Fahn, A. (1982). Plant Anatomy, 3rd ed. (Oxford: Pergamon Press).Google Scholar
  24. Freeling, M. (1992). A conceptual framework for maize leaf development. Dev Biol 153, 44–58.CrossRefGoogle Scholar
  25. Garner, W.W., and Allard, H.A. (1922). Photoperiodism, the response of the plant to relative length of day and night. Science 55, 582–583.CrossRefGoogle Scholar
  26. Gifford, E.M., and Foster, A.S. (1989). Morphology and Evolution of Vascular Plants, 3rd ed. (New York: W.H. Freeman and Co.).Google Scholar
  27. Gilbert, S.F. (2010). Developmental Biology, 9th ed. (Sunderland, MA: Sinauer Associates).Google Scholar
  28. Goldberg, R.B. (1988). Plants: novel developmental processes. Science 240, 1460–1467.CrossRefGoogle Scholar
  29. Halevy, A.H. (1985). CRC Handbook of Flowering (Boca Raton: CRC Press).Google Scholar
  30. Harrison, C.J., Roeder, A.H.K., Meyerowitz, E.M., and Langdale, J.A. (2009). Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr Biol 19, 461–471.CrossRefGoogle Scholar
  31. Haughn, G.W., Schultz, E.A., and Martinez–Zapater, J.M. (1995). The regulation of flowering in Arabidopsis thaliana: meristems, morphogenesis, and mutants. Can J Bot 73, 959–981.CrossRefGoogle Scholar
  32. Higashiyama, T., and Yang, W.C. (2017). Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol 173, 112–121.CrossRefGoogle Scholar
  33. Hohe, A., Rensing, S.A., Mildner, M., Lang, D., and Reski, R. (2002). Day length and temperature strongly influence sexual reproduction and expression of a novel MADS–box gene in the moss Physcomitrella patens. Plant biol 4, 595–602.CrossRefGoogle Scholar
  34. Huang, W., Han, Z., Liu, S., Xu, X., and Li, B. (1999). Effects of pointdaub with 6–BA ointment on bud breaking, shoot growth, and the shaping of young apple trees. Rev China Agri Sci Tech, 72–75.Google Scholar
  35. Juliano, C., and Wessel, G. (2010). Versatile germline genes. Science 329, 640–641.CrossRefGoogle Scholar
  36. Kaplan, D.R. (2001). The science of plant morphology: definition, history, and role in modern biology. Am J Bot 88, 1711–1741.CrossRefGoogle Scholar
  37. Kelliher, T., and Walbot, V. (2012). Hypoxia triggers meiotic fate acquisition in maize. Science 337, 345–348.CrossRefGoogle Scholar
  38. Kenrick, P., and Strullu–Derrien, C. (2014). The origin and early evolution of roots. Plant Physiol 166, 570–580.CrossRefGoogle Scholar
  39. Kofuji, R., and Hasebe, M. (2014). Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol 17, 13–21.CrossRefGoogle Scholar
  40. Kofuji, R., Yagita, Y., Murata, T., and Hasebe, M. (2018). Antheridial development in the moss Physcomitrella patens: implications for understanding stem cells in mosses. Phil Trans R Soc B 373, 20160494.CrossRefGoogle Scholar
  41. Koornneef, M., Hanhart, C.J., and van der Veen, J.H. (1991). A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229, 57–66.CrossRefGoogle Scholar
  42. Lebon, G., Wojnarowiez, G., Holzapfel, B., Fontaine, F., Vaillant–Gaveau, N., and Clément, C. (2008). Sugars and flowering in the grapevine (Vitis vinifera L.). J Exp Bot 59, 2565–2578.CrossRefGoogle Scholar
  43. Ledford, H. (2018). The lost art of looking at plants. Nature 553, 396–398.CrossRefGoogle Scholar
  44. Li, T., Huang, W., and Meng, Z. (1996). Study on the mechanisms of flower bud induction in apple tree. Acta Phytophysiol Sin 22, 251–257.Google Scholar
  45. Mattsson, J., Sung, Z.R., and Berleth, T. (1999). Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979–2991.Google Scholar
  46. Navarro, C., Cruz–Oró, E., and Prat, S. (2015). Conserved function of FLOWERING LOCUS T (FT) homologues as signals for storage organ differentiation. Curr Opin Plant Biol 23, 45–53.CrossRefGoogle Scholar
  47. Niwa, M., Endo, M., and Araki, T. (2013). Florigen is involved in axillary bud development at multiple stages in Arabidopsis. Plant Signal Behav 8, e27167.CrossRefGoogle Scholar
  48. Pin, P.A., and Nilsson, O. (2012). The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ 35, 1742–1755.CrossRefGoogle Scholar
  49. Poethig, R.S. (2010). The past, present, and future of vegetative phase change. Plant Physiol 154, 541–544.CrossRefGoogle Scholar
  50. Poethig, R.S. (2013). Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105, 125–152.CrossRefGoogle Scholar
  51. Prusinkiewicz, P., and Lindenmayer, A. (1990). The Algorithmic Beauty of Plants (New York: Springer–Verlag).CrossRefGoogle Scholar
  52. Prusinkiewicz, P., and Runions, A. (2012). Computational models of plant development and form. New Phytol 193, 549–569.CrossRefGoogle Scholar
  53. Raven, J.A., and Edwards, D. (2001). Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52, 381–401.CrossRefGoogle Scholar
  54. Schiavone, F.M., and Racusen, R.H. (1991). Regeneration of the root pole in surgically transected carrot embryos occurs by position–dependent, proximodistal replacement of missing tissues. Development 113, 1305–1313.Google Scholar
  55. Sena, G., Wang, X., Liu, H.Y., Hofhuis, H., and Birnbaum, K.D. (2009). Organ regeneration does not require a functional stem cell niche in plants. Nature 457, 1150–1153.CrossRefGoogle Scholar
  56. Shimamura, M. (2016). Marchantia polymorpha: taxonomy, phylogeny and morphology of a model system. Plant Cell Physiol 57, 230–256.CrossRefGoogle Scholar
  57. Smith, A.M. (2010). Plant biology (New York: Garland Science).Google Scholar
  58. Steeves, T.A., and Sussex, I.M. (1989). Patterns in Plant Development, 2nd ed. (Cambridge England; New York: Cambridge University Press).CrossRefGoogle Scholar
  59. Strasburger, E., Denffer, D.V., Bell, P.R., and Coombe, D. (1976). Strasburger’s Textbook of Botany, New English ed. (London; New York: Longman).Google Scholar
  60. Stuessy, T.F., Mayer, V., and Horandl, E. (2003). Deep Morphology Toward a Renaissance of Morphology in Plant Systematics (Vienna: A. R. G., Gantner Verlag).Google Scholar
  61. Tromas, A., and Perrot–Rechenmann, C. (2010). Recent progress in auxin biology. Comptes Rendus Biol 333, 297–306.CrossRefGoogle Scholar
  62. Tsukaya, H. (2014). Comparative leaf development in angiosperms. Curr Opin Plant Biol 17, 103–109.CrossRefGoogle Scholar
  63. Vernoux, T., and Benfey, P.N. (2005). Signals that regulate stem cell activity during plant development. Curr Opin Genets Dev 15, 388–394.CrossRefGoogle Scholar
  64. Waddington, C.H. (1966). Principles of Development and Differentiation (New York: Macmillan).Google Scholar
  65. Waites, R., and Hudson, A. (1995). Phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143–2154.Google Scholar
  66. Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F., Alonso–Blanco, C., Coupland, G., and Albani, M.C. (2009). PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423–427.CrossRefGoogle Scholar
  67. Wang, X. (2017). The Dawn Angiosperms: Uncovering the Origin of Flowering Plants (New York: Springer Berlin Heidelberg).Google Scholar
  68. Wardlaw, C.W. (1956). The floral meristem as a reaction system. Nature 178, 394–408.CrossRefGoogle Scholar
  69. Wareing, P.F. (1959). Problems of juvenility and flowering in trees. J Linnean Soc London Bot 56, 282–289.CrossRefGoogle Scholar
  70. White, J. (1979). The plant as a metapopulation. Annu Rev Ecol Syst 10, 109–145.CrossRefGoogle Scholar
  71. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., and Poethig, R. S. (2009). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750–759.CrossRefGoogle Scholar
  72. Wu, G., and Poethig, R.S. (2006). Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133, 3539–3547.CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Life SciencesPeking UniversityBeijingChina

Personalised recommendations