Dynamical Patterning Modules, Biogeneric Materials, and the Evolution of Multicellular Plants

Abstract

Comparative analyses of developmental processes across a broad spectrum of organisms are required to fully understand the mechanisms responsible for the major evolutionary transitions among eukaryotic photosynthetic lineages (defined here as the polyphyletic algae and the monophyletic land plants). The concepts of dynamical patterning modules (DPMs) and biogeneric materials provide a framework for studying developmental processes in the context of such comparative analyses. In the context of multicellularity, DPMs are defined as sets of conserved gene products and molecular networks, in conjunction with the physical morphogenetic and patterning processes they mobilize. A biogeneric material is defined as mesoscale matter with predictable morphogenetic capabilities that arise from complex cellular conglomerates. Using these concepts, we outline some of the main events and transitions in plant evolution, and describe the DPMs and biogeneric properties associated with and responsible for these transitions. We identify four primary DPMs that played critical roles in the evolution of multicellularity (i.e., the DPMs responsible for cell-to-cell adhesion, identifying the future cell wall, cell differentiation, and cell polarity). Three important conclusions emerge from a broad phyletic comparison: (1) DPMs have been achieved in different ways, even within the same clade (e.g., phycoplastic cell division in the Chlorophyta and phragmoplastic cell division in the Streptophyta), (2) DPMs had their origins in the co-option of molecular species present in the unicellular ancestors of multicellular plants, and (3) symplastic transport mediated by intercellular connections, particularly plasmodesmata, was critical for the evolution of complex multicellularity in plants.

Keywords: algal evolution; convergent evolution; dynamical patterning modules; plant evolution; plasmodesmata.

FIGURE 1

The occurrence of multicellularity shown on a highly redacted and unrooted phylogenetic diagram of the major groups of photosynthetic eukaryotes. Although some groups are entirely unicellular or multicellular (e.g., prasinophytes and the land plants, respectively), most contain a mixture of body plans such as the unicellular and colonial body plans (e.g., diatoms), or a mixture of the unicellular, colonial, and multicellular body plans (e.g., brown algae). In general, early-divergent persistent lineages are dominated by unicellular species (e.g., prasinophytes in the green algal clade), whereas later-divergent lineages contain a mixture of body plans (e.g., chlorophytes and charophytes). Species-rich, late-divergent persistent lineages tend to be exclusively multicellular (e.g., the land plants and metazoans).

FIGURE 2

The different adhesives utilized by the cell-to-cell adhesive (ADH) dynamic patterning module among some of the major multicellular lineages.

FIGURE 3

Schematic of the land plant phragmoplast (A,B: longitudinal and transverse views, respectively). AAC, apical actin cluster; AC, actin cable; AAEP, actin/ABPA endocytoic patches; CC, condensed chromatin; CW, cell wall; EE, endocytotic elements; FCWC, future cell wall components; GA, Golgi apparatus; ML, middle lamella; MT, microtubule; PH, phragmoplast; PM, plasma membrane; SE, post-Golgi sorting endosome; TGN, trans-Golgi network; VC, vesicle cluster.

FIGURE 4

Paired dynamic patterning modules (indicated by arrows) that participate in the evolution of multicellularity. The acquisition of each of these modules is required for the evolution of multicellularity. These modules operate in pairs for organisms with cell walls because cell-to-cell adhesion is related to the location of a new cell wall and because intercellular communication operates in tandem with cell polarity. ADH, the capacity for cell-to-cell adhesion. DIF, the establishment of intercellular communication and cellular differentiation, FCW, the future cell wall module (establishes the location and orientation of the new cell wall), POL, the capacity for polar (preferential) intercellular transport. (Adapted from Hernández-Hernández et al., 2012.)

FIGURE 5

A morphospace for the four major plant body plans shown in bold (unicellular, siphonous/coenocytic, colonial, and multicellular) resulting from the intersection of five developmental processes: (1) whether cytokinesis and karyokinesis are synchronous, (2) whether cells remain aggregated after they divide, (3) whether symplastic continuity or some other form of intercellular communication is maintained among neighboring cells, and (4) whether individual cells continue to grow indefinitely in size. Note that the siphonous/coenocytic body plan may evolve from a unicellular or a multicellular progenitor. The lower panels deal with the plane of cell division (depicted by small cubes and arrows shown to the right) to yield unbranched and branched filaments, pseudoparenchyma, and parenchyma (found in the plants) and the localization of cellular division. The operation of the four DPMs reviewed in the article is summarized in Figure 7. (Adapted from Niklas, 2000, 2014).

FIGURE 6

Schematics of the diversity of intercellular communication among adjoining (A) land plant and (B–D) animal cells. Each of these cell-to-cell linkages participates in the establishment of cell polarity as well as physiological communication among adjoining cells. Thus, each represents an analogous evolutionary innovation for two of the essential features of multicellularity. (A) Plasmodesma. (B) Desmosome. (C) Tight junctions. (D) Gap junctions. AP, attachment plaque (plakoglobins); CSF, cytoskeletal filaments (keratin); CW, cell wall; DTP, desmotubular proteins; ER, endoplasmic reticulum; ICS, intercellular space; PM, plasma membrane.

FIGURE 7

Serial schematic of the ways four DPMs have contributed to the evolution of complex multicellularity in the land plants (see also, Figure 5). (A) The ancestral unicellular condition within the Streptophytes (the green algae and the land plants) with a flagellar apparatus and associated eyespot, nucleus, and parietal chloroplast. (B) The future cell wall (FCM) module operates along the longitudinal cell axis in conjunction with the polarity (POL) module to specify the plane of cell division (dashed lines). (C) The cell-to-cell adhesion (ADH) module establishes the colonial body plan (show here by two adjoining cells). (D) Symplastic continuity between adjoining cells is established by means of plasmodesmata. (E) The POL module shifts the frame of reference for the FCW module (now orthogonal to the cell longitudinal axis) to form an unbranched filament. (F) The differentiation (DIF) module is deployed for the evolution of specialized cells. (G) The POL module operates to now specify a second plain of cell division to produce a branched filament. The role of the POL module in establishing a third plane of cell division (and thus the development of parenchyma) is not shown here. e, eyespot; fl., flagellar apparatus; n, nucleus; chl, chloroplast.