Phytomers, collet and founder cells: a "universal" plant embryonic body plan from a developmental, molecular, and evolutionary perspective

Abstract

This article presents a novel perspective on plant embryogenesis, fundamentally differentiating it from the animal embryo model upon which plant models have long been based to discern the genetic and molecular mechanisms. We propose a plant embryonic body plan that aligns developmental and evolutionary insights across all five embryophyte groups (bryophytes, lycophytes, monilophytes, gymnosperms, and angiosperms). This conceptual model is grounded in a Reprogramming Potential (RP) involving an activation (RP1+) -suppression (RP1-) switch (RP1+/RP1-), which integrates embryonic development in a stepwise manner across diverse embryophytes. We further explore the evolutionary trajectory of this body plan, tracing the gradual assembly of the embryophyte genetic toolkit from bryophytes to angiosperms. Key developmental processes, such as the emergence of shoot and root meristems, vascular tissues, and seeds, are also examined within an evo-devo framework. Plant phenotypic plasticity, fundamental to their adaptation and survival, is manifested in two key hallmarks: (A) the iterative, modular growth of shoot and root units, and (B) their remarkable regenerative potential. While traditionally viewed as separate phenomena, we propose a novel, integrative model that connects these hallmarks within the context of plant embryogenesis. Our "proposed universal plant embryonic body plan" reconciles the genetic and molecular mechanisms of Arabidopsis thaliana embryogenesis with the contrasting developmental patterns observed in monocots. This unified model also integrates the concept of root founder cells and collet (shoot-root junction) into an embryonic framework facilitating the study of gene regulatory networks that underpin root evolution and its architecture.

Keywords: GRN; development; embryo - evolution; embryophytes; model.

Figure 1

A comparative developmental profile of embryonic (orange line) and post-embryonic development (purple line) in a plant (mustard plant) and a mammal(mouse). The figure captures the fundamental difference between plant and animal embryogenesis. The organs are iteratively produced post-embryonically in plants by the shoot and root meristems, whereas the organs are formed (organogenesis) during embryogenesis in animals. The green vertical double-ended arrow indicates indeterminate growth. Embryonic phase in plants establishes the embryonic body plan (zoomed image) with shoot (SAM)/root (RAM) meristems and embryonic organs (cotyledon, hypocotyl).

Figure 2

The developing root system during embryonic to seedling transition in different plant species. PR, primary root; AR, anchor root; Hy, Hypocotyl; HR, hypocotyl root; NR, nodal root (embryonic crown root); SR, seminal root; LR, lateral root; BR, basal root; SN, scutellar node; CN, coleoptilar node; SI, sub-crown internode; M, mesocotyl; C, coleoptile; CT, cotyledon; SAM, shoot apical meristem; RAM, root apical meristem; MZ, meristematic zone; TZ, transition zone; DZ, differentiation zone. Adapted from (Salvi, 2017).

Figure 3

Developmental map of Arabidopsis and monocot embryo development and post-embryonic development with reference to the two hallmarks (iterative, regenerative) Upper panel: Step 1 - zygote to two-cell stage; Step 2 - hypophyseal cell specification (32-cell stage); Step 3 – the collet-hypocotyl partitioning separating the phytomer from the radicle; Step 4 – phytomer bilateral symmetry; Lower panel: RP1+ - embryonic potential; RP1- - suppressed embryonic potential; RP2+ - activation of the root program; RP2- - suppressed shoot-borne root program (in the collet region); RP3+ - activation of the shoot-borne root program; RP3- - suppression of lateral root program (pericycle cell fate); RP4 – suppressed nodal root program; RP5 – activated lateral root program. T, totipotency; R, re-generative potential; (+) activated; (-) suppressed; SB, shoot-borne; L, lateral. While the upper panel of image 3 illustrates the Arabidopsis (dicot) pattern, the lower panel depicts a simplified monocot representation. Specifically, the lateral positioning of shoot and root meristems in monocots, relative to surrounding embryonic and maternal tissues, can be understood within our framework. Step 1, establishing polarity, is evident in the initial asymmetric division. Step 2, tissue specification, accounts for the differentiation leading to the distinct positioning of these meristems. Step 3, organogenesis, reflects the subsequent development of these lateral meristems within the monocot embryo’s unique architecture. Finally, regarding Step 4, the “universally conserved” aspect refers to the establishment of the basic body plan, not the precise form of cotyledon symmetry. Monocots, while lacking symmetrical cotyledons, still undergo a defined phase of embryo maturation and growth, aligning with the core concept of Step 4.

Figure 4

Hypothetical Evo-Devo map of embryo development and post-embryonic development with reference to the two hallmarks (iterative, regenerative) in seed plants (e.g., Arabidopsis) and the corresponding stages in bryophytes, lycophytes and monilophytes. Upper panel: Step 1 - zygote to two-cell stage; Step 2 - hypophyseal cell specification (32-cell stage); Step 3 – the collet-hypocotyl partitioning separating the phytomer from the radicle; Step 4 – phytomer bilateral symmetry; Lower panel: RP1+ - embryonic potential; RP1- - repressed embryonic potential; RP2+ - activation of the root program; RP2- - repressed shoot-borne root program; RP3+ - activation of the shoot-borne root program; RP3- - suppression of lateral root program (pericycle cell fate); RP4 – suppressed nodal root program; RP5 – activated lateral root program. T, totipotency; R, re-generative potential; (+) activated; (-) suppressed; SB, shoot-borne; L, lateral; LP, Lycophyte/monilophyte (Pteridophyte); B, Bryophyte.