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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?

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

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?


Acknowledgment

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.


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  • 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

    Internode

    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

    Plastochron shortening

    Phyllotaxis

    Change in phyllotaxis

    Bernier et al., 1981.

  • Table 2   Definition or description of sex in authorized resources

    Types

    Years

    Definition or description

    Authors

    Resource

    Encyclopedia

    2017

    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

    https://www.britannica.com/science/sex#toc29374

    2017

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

    http://en.wikipedia.org/wiki/Sex

    Textbooks

    2005

    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.

    2000

    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.

    Monograph

    1982

    —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

    1983

    —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

    2014

    Sex is defined by the occurrence of meiosis.

    Beukeboom and Perrin

    The Evolution of SexDetermination

    Reviewarticles

    2002

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

    Cavalier-Smith

    Origins of the machinery of recombination and sex

    2013

    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.

     

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