Reconsideration of Plant Morphological Traits: From a Structure-Based Perspective to a Function-Based Evolutionary Perspective

Abstract

This opinion article proposes a novel alignment of traits in plant morphogenesis from a function-based evolutionary perspective. As a member species of the ecosystem on Earth, we human beings view our neighbor organisms from our own sensing system. We tend to distinguish forms and structures (i.e., "morphological traits") mainly through vision. Traditionally, a plant was considered to be consisted of three parts, i.e., the shoot, the leaves, and the root. Based on such a "structure-based perspective," evolutionary analyses or comparisons across species were made on particular parts or their derived structures. So far no conceptual framework has been established to incorporate the morphological traits of all three land plant phyta, i.e., bryophyta, pteridophyta and spermatophyta, for evolutionary developmental analysis. Using the tenets of the recently proposed concept of sexual reproduction cycle, the major morphological traits of land plants can be aligned into five categories from a function-based evolutionary perspective. From this perspective, and the resulting alignment, a new conceptual framework emerges, called "Plant Morphogenesis 123." This framework views a plant as a colony of integrated plant developmental units that are each produced via one life cycle. This view provided an alternative perspective for evolutionary developmental investigation in plants.

Keywords: function-based evolutionary perspective; morphological traits; plant developmental unit; plant morphogenesis 123; sexual reproduction cycle.

FIGURE 1

Different levels of elaboration around the core processes in the life cycles of the three plant phyla. The sexual reproduction cycle (Bai, 2015a) 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). This figure was revised from Figure 1.9 in Bai and Xu (2013).

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 (2015a).

FIGURE 3

Comparison of SRC-derived developmental modes in animals and plants. (A) Represents a cell cycle, i.e., one diploid cell becomes two cells through mitosis; (B) Represents the SRC (sexual reproduction cycle, Bai, 2015a). Two arrows (orange and gray) between M (meiosis) and F (fertilization) represent heterogametogenesis. (C) Represents the “dichotomous mode” for animal development. Orange and gray lines represent female and male soma and germlines, respectively, and orange and gray Gs represent female and male gametogenesis, respectively. (D) Represents the “double-ring mode” of plant development. On the SRC backbone, the green dashed ring on the left represents diploid multicellular structures composed of various types of organs; the light green ring on the right represents haploid multicellular structures composed of various types of organs. This figure was modified from Figure 16 in Bai (2016).

FIGURE 4

Comparison of developmental units in plants and animals required for life-cycle completion. While plant growth tip generated from a zygote (pink circle) can produce numerous lateral organs and branches, only seven organ types in Arabidopsis are present in a complete the life cycle (A). The half circles along the dashed orange arrow represent organ primordia. By comparison, the basic structure required for Drosophila to complete its life cycle is the embryo, elaborated from a zygote to larva. Embryogenesis is represented by an orange-lined yellow triangle (B). Unlike animal individuals, which contain limited types and numbers of organs in a determined pattern, the functionally equivalent structure in plants is the imaginal unit shown in (A), referred to as a “developmental unit,” rather than the whole plant. According to this perspective, the structural equivalent of an animal embryo would be the process represented as the yellow area in (A). Orange dashed lines in the yellow region indicate that the process is relatively open but ultimately limited. (B) Was modified from Figures 2–6 in Wolpert et al. (2007) edited Principles of Development. This figure was modified from Figure 6 in Bai (1999).