SCIENCE CHINA Life Sciences, Volume 62 , Issue 4 : 453-466(2019) https://doi.org/10.1007/s11427-018-9457-1

Plant Morphogenesis 123: a renaissance in modern botany?

More info
  • ReceivedOct 5, 2018
  • AcceptedOct 25, 2018
  • PublishedFeb 21, 2019


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?


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.

Interest statement

The author(s) declare that they have no conflict of interest.


[1] Andrés F., Coupland G.. The genetic basis of flowering responses to seasonal cues. Nat Rev Genet, 2012, 13: 627-639 CrossRef PubMed Google 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), S119123. Google Scholar

[4] Bai, S.N., and Xu, Z.H. (2013). Unisexual cucumber flowers, sex and sex differentiation. Int Rev Cell Mol Biol 304, 155. Google Scholar

[5] Bai S.. The concept of the sexual reproduction cycle and its evolutionary significance. Front Plant Sci, 2015, 6: 11 CrossRef PubMed Google 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, 73116. 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.. Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol, 2010, 341: 95-113 CrossRef PubMed Google 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. A gene expression profiling of early rice stamen development that reveals inhibition of photosynthetic genes by OsMADS58. Mol Plant, 2015, 8: 1069-1089 CrossRef PubMed Google Scholar

[15] Chiang G.C.K., Barua D., Kramer E.M., Amasino R.M., Donohue K.. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA, 2009, 106: 11661-11666 CrossRef PubMed ADS Google Scholar

[16] Coen E.. Goethe and the ABC model of flower development. C R Acad Sci III, 2001, 324: 523-530 CrossRef ADS Google Scholar

[17] Crawford B.C.W., Sewell J., Golembeski G., Roshan C., Long J.A., Yanofsky M.F.. Genetic control of distal stem cell fate within root and embryonic meristems. Science, 2015, 347: 655-659 CrossRef PubMed ADS Google 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., Dennis E.S.. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA, 2011, 108: 6680-6685 CrossRef PubMed ADS Google Scholar

[20] Dkhar J., Pareek A.. What determines a leaf’s shape?. EvoDevo, 2014, 5: 47 CrossRef PubMed Google Scholar

[21] Druege U., Franken P., Hajirezaei M.R.. Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci, 2016, 7: 381 CrossRef PubMed Google Scholar

[22] Efroni I., Eshed Y., Lifschitz E.. Morphogenesis of simple and compound leaves: a critical review. Plant Cell, 2010, 22: 1019-1032 CrossRef PubMed Google Scholar

[23] Fahn, A. (1982). Plant Anatomy, 3rd ed. (Oxford: Pergamon Press). Google Scholar

[24] Freeling M.. A conceptual framework for maize leaf development. Dev Biol, 1992, 153: 44-58 CrossRef Google Scholar

[25] Garner W.W., Allard H.A.. Photoperiodism, the response of the plant to relative length of day and night. Science, 1922, 55: 582-583 CrossRef PubMed ADS Google 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.. Plants: novel developmental processes. Science, 1988, 240: 1460-1467 CrossRef ADS Google 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., Langdale J.A.. Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Curr Biol, 2009, 19: 461-471 CrossRef PubMed Google Scholar

[31] Haughn G.W., Schultz E.A., Martinez-Zapater J.M.. The regulation of flowering in Arabidopsis thaliana: meristems, morphogenesis, and mutants. Can J Bot, 1995, 73: 959-981 CrossRef Google Scholar

[32] Higashiyama T., Yang W.C.. Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol, 2017, 173: 112-121 CrossRef PubMed Google Scholar

[33] Hohe A., Rensing S.A., Mildner M., Lang D., Reski R.. Day length and temperature strongly influence sexual reproduction and expression of a novel MADS-box gene in the moss Physcomitrella patens. Plant biol, 2002, 4: 595-602 CrossRef Google Scholar

[34] Huang, W., Han, Z., Liu, S., Xu, X., and Li, B. (1999). Effects of point-daub 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., Wessel G.. Versatile germline genes. Science, 2010, 329: 640-641 CrossRef PubMed Google Scholar

[36] Kaplan D.R.. The science of plant morphology: definition, history, and role in modern biology. Am J Bot, 2001, 88: 1711-1741 CrossRef Google Scholar

[37] Kelliher T., Walbot V.. Hypoxia triggers meiotic fate acquisition in maize. Science, 2012, 337: 345-348 CrossRef PubMed ADS Google Scholar

[38] Kenrick P., Strullu-Derrien C.. The origin and early evolution of roots. Plant Physiol, 2014, 166: 570-580 CrossRef PubMed Google Scholar

[39] Kofuji R., Hasebe M.. Eight types of stem cells in the life cycle of the moss Physcomitrella patens. Curr Opin Plant Biol, 2014, 17: 13-21 CrossRef PubMed Google Scholar

[40] Kofuji R., Yagita Y., Murata T., Hasebe M.. Antheridial development in the moss Physcomitrella patens: implications for understanding stem cells in mosses. Phil Trans R Soc B, 2018, 373: 20160494 CrossRef PubMed Google Scholar

[41] Koornneef M., Hanhart C.J., van der Veen J.H.. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet, 1991, 229: 57-66 CrossRef Google Scholar

[42] Lebon G., Wojnarowiez G., Holzapfel B., Fontaine F., Vaillant-Gaveau N., Clément C.. Sugars and flowering in the grapevine (Vitis vinifera L.). J Exp Bot, 2008, 59: 2565-2578 CrossRef PubMed Google Scholar

[43] Ledford H.. The lost art of looking at plants. Nature, 2018, 553: 396-398 CrossRef PubMed ADS Google 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., Prat S.. Conserved function of FLOWERING LOCUS T (FT) homologues as signals for storage organ differentiation. Curr Opin Plant Biol, 2015, 23: 45-53 CrossRef PubMed Google Scholar

[47] Niwa M., Endo M., Araki T.. Florigen is involved in axillary bud development at multiple stages in Arabidopsis. Plant Signal Behav, 2013, 8: e27167 CrossRef PubMed Google Scholar

[48] Pin P.A., Nilsson O.. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ, 2012, 35: 1742-1755 CrossRef PubMed Google Scholar

[49] Poethig R.S.. The past, present, and future of vegetative phase change. Plant Physiol, 2010, 154: 541-544 CrossRef PubMed Google Scholar

[50] Poethig, R.S. (2013). Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105, 125-152. Google Scholar

[51] Prusinkiewicz, P., and Lindenmayer, A. (1990). The Algorithmic Beauty of Plants (New York: Springer-Verlag). Google Scholar

[52] Prusinkiewicz P., Runions A.. Computational models of plant development and form. New Phytol, 2012, 193: 549-569 CrossRef PubMed Google Scholar

[53] Raven J.A., Edwards D.. Roots: evolutionary origins and biogeochemical significance. J Exp Bot, 2001, 52: 381-401 CrossRef Google 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., Birnbaum K.D.. Organ regeneration does not require a functional stem cell niche in plants. Nature, 2009, 457: 1150-1153 CrossRef PubMed ADS Google Scholar

[56] Shimamura M.. Marchantia polymorpha: taxonomy, phylogeny and morphology of a model system. Plant Cell Physiol, 2016, 57: 230-256 CrossRef PubMed Google 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). Google 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., Perrot-Rechenmann C.. Recent progress in auxin biology. Comptes Rendus Biol, 2010, 333: 297-306 CrossRef PubMed Google Scholar

[62] Tsukaya H.. Comparative leaf development in angiosperms. Curr Opin Plant Biol, 2014, 17: 103-109 CrossRef PubMed Google Scholar

[63] Vernoux T., Benfey P.N.. Signals that regulate stem cell activity during plant development. Curr Opin Genets Dev, 2005, 15: 388-394 CrossRef PubMed Google 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., Albani M.C.. PEP1 regulates perennial flowering in Arabis alpina. Nature, 2009, 459: 423-427 CrossRef PubMed ADS Google 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. Google Scholar

[69] Wareing P.F.. Problems of juvenility and flowering in trees. J Linnean Soc London Bot, 1959, 56: 282-289 CrossRef Google Scholar

[70] White J.. The plant as a metapopulation. Annu Rev Ecol Syst, 1979, 10: 109-145 CrossRef Google Scholar

[71] Wu G., Park M.Y., Conway S.R., Wang J.W., Weigel D., Poethig R.S.. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 2009, 138: 750-759 CrossRef PubMed Google Scholar

[72] Wu G., Poethig R.S.. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development, 2006, 133: 3539-3547 CrossRef PubMed Google Scholar

  • Figure 1

    A diagram of the modified cell cycle called “sexual reproduction cycle (SRC)”. The three rounded rectangles containing yellow ovals represent diploid cells. The red dashed line and arrows represent one diploid cells become two (a cell cycle). Dark red dashed curve represents a process, in which three biologic events, i.e., meiosis, fertilization and heterogametogenesis, integrated, and inserted into the cell cycle represented by two rounded rectangles (blue and red, respectively) and an oval (light green). Through the SRC, a diploid eukaryote can autonomously increase genetic variations and increase adaptability to the unpredictably changed environment. Reprinted from Bai, 2016 by permission of Science Press.

  • Figure 2

    Comparison of morphogenetic strategies of animals, fungi, and plants within the framework of the SRC. Yellow background indicates the diploid phase and blue background indicates the haploid phase. In the intervals between zygote and diploid germ cells, the interpolation of multicellular structures occurs in animals (red) and plants (green), whereas none are present in fungi (pink). In the intervals between meiotically produced cells and gametogenic cells, the interpolation of multicellular structures occurs in fungi and plants but not in animals. Reprinted from Bai, 2015.

  • Figure 3

    A diagram of the PM123 theory. Two multicellular structures are interpolated into the two intervals (green framed for the diploid and light green framed for haploid) during the SRC (the “1” of the PM123). Represented in diploid phase, two themes (the “2” of the PM123) underlie the morphogenesis of the multicellular structures: structure building, the “axial tree” (AT) derived neo-modularization (NM), and two driving forces for sequential changes of organ types, including photoautotroph and stress response. Three sequential steps (the “3” of the PM123) are elaborated in the upper frame. Reprinted from Bai, 2019.

  • Figure 4

    (Color online) A summary of the evolution of conceptual frameworks on plant morphogenesis. Main information adopted from Arber (1950). Additional references: Bai, 2016; Coen, 2001. The abbreviations “R, St, L, F, Fr, Se” used in “Anatomic description” refer to “root, stem, leaf, flower, fruit, seed”, respectively.

  • Figure 5

    An axial tree. Open circle, terminal node; filled circle, branching point; dashed arrow, apex; solid arrow, internode. Modified from Prusinkiewicz and Lindenmayer, 1990.

  • Figure 6

    Diagram of key events and their possible relationships evolved during the axial growth in diploid multicellular structures.

  • Figure 7

    Different levels of elaboration around the core processes in the life cycles of the three plant phyla. The sexual reproduction cycle from one zygote to the next generation’s zygotes through meiosis and fertilization is the backbone of the lifecycle for all three land plant groups, Bryophyta, Pteridophyta, and Spermatophyta. Green arrows show the differentiation of various organ types in diploid phase, and light green for organs in haploid phase. Dark red arrowheads indicate unlimited tip growth activity. cot., cotyledons; j. leaf, juvenile leaf (e.g., rosette leaves in Arabidopsis); a. leaf, adult leaf (e.g., cauline leaves in Arabidopsis). Reprinted from Bai, 2017.

  • Figure 8

    Comparison of the SRC derived “Double-Ring” strategies of morphogenesis in three land plant groups. Symbols and abbreviations: gray circle, heterogametogenesis; pink circle, real sex differentiation; brown circle, pseudo sex differentiation; Cap, capsule; Tip, growth tip; JL, juvenile leaf; AL, adult leaf; Sp, sporangium; SAM, shoot apical meristem; Cot, cotyledon; Mi, microsporangium; Ma, macrosporangium; Se, seed; RL, rosette leaf; CL, cauline leaf; S, sepal; P, petal; C, carpel; O, ovule.

  • Figure 9

    A diagram of three key concepts of sex, sex differentiation and sexual behavior from the perspective of SRC. Reprinted from Bai, 2019.

  • Table 1   The flowering syndrome

    Relevant traits to flowering

    Morphological changes


    Increased internode elongation

    Shape of SAM

    Broadening and doming of the SAM

    Shape of leaf

    Changing in leaf shape: petiole and lamina

    Axillary buds

    Precocious initiation of axillary buds

    Leaf growth

    Change in leaf growth rate


    Plastochron shortening


    Change in phyllotaxis

    Bernier et al., 1981.

  • Table 2   Definition or description of sex in authorized resources



    Definition or description





    Sex, the sum of features by which members of species can be divided into two groups—male and female—that complement each other reproductively.

    N.J. Berrill



    Organisms of many species are specialized into male and female varieties, each known as a sex.




    Sexual reproduction is the creation of offspring by the fusion of haploid gametes to form a zygote, which is diploid.

    Campbell and Reece

    Biology 7th ed.


    It should be noted that sex and reproduction are two distinct and separable processes. Reproduction involves the creation of new individuals; sex involves the combining of genes from two different individuals into new arrangements.

    S. F. Gilbert

    Developmental Biology 6th ed.



    —Sex is a composite process in the course of which genomes are diversified by a type of nuclear division called meiosis, and by type of nuclear fusion called syngamy, or fertilization.

    Sex and reproduction are quite distinct processes: sex is a change in the state of cells or individuals, whilst reproduction is a change in their number.

    G. Bell

    The Masterpiece of Nature: The evolution and geneticsof sexuality


    —Fisher, 1930: No practical biologist interested in sexual reproduction would be led to work out the detailed consequences experience by organism having three or more sexes, yet what else should he do if he wishes to understand why the sexes are, in fact, always two?

    —Sex is defined as gender, male or female.

    Sex development refers collectively to the various molecular, genetic, and physiological processes that produce a male or a female from a zygote of a given genotype and parents in a given environment.

    J. Bull

    Evolution of Sex Determining Mechanisms


    Sex is defined by the occurrence of meiosis.

    Beukeboom and Perrin

    The Evolution of SexDetermination



    True sex—syngamy, nuclear fusion and meiosis—is found only in eukaryotes.


    Origins of the machinery of recombination and sex


    The core features of sexual reproduction involve: (i) ploidy changes from diploid to haploid to diploid states, (ii) the production of haploid mating partners or gametes from the diploid state via meiosis which recombines the two parental genomes to produce novel genotypes and halves the ploidy and (iii) cell-cell recognition between the mating partners or gametes followed by cell-cell fusion to generate the diploid zygote and complete the cycle.

    Heitman et al.


Copyright 2020 Science China Press Co., Ltd. 《中国科学》杂志社有限责任公司 版权所有

京ICP备17057255号       京公网安备11010102003388号