Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity.

Myxobacteria and dictyostelids are prokaryotic and eukaryotic multicellular lineages, respectively, that after nutrient depletion aggregate and develop into structures called fruiting bodies. The developmental processes and resulting morphological outcomes resemble one another to a remarkable extent despite their independent origins, the evolutionary distance between them and the lack of traceable homology in molecular mechanisms. We hypothesize that the morphological parallelism between the two lineages arises as the consequence of the interplay within multicellular aggregates between generic processes, physical and physicochemical processes operating similarly in living and non-living matter at the mesoscale (~10-3-10-1 m) and agent-like behaviors, unique to living systems and characteristic of the constituent cells, considered as autonomous entities acting according to internal rules in a shared environment. Here, we analyze the contributions of generic and agent-like determinants in myxobacteria and dictyostelid development and their roles in the generation of their common traits. Consequent to aggregation, collective cell-cell contacts mediate the emergence of liquid-like properties, making nascent multicellular masses subject to novel patterning and morphogenetic processes. In both lineages, this leads to behaviors such as streaming, rippling, and rounding-up, as seen in non-living fluids. Later the aggregates solidify, leading them to exhibit additional generic properties and motifs. Computational models suggest that the morphological phenotypes of the multicellular masses deviate from the predictions of generic physics due to the contribution of agent-like behaviors of cells such as directed migration, quiescence, and oscillatory signal transduction mediated by responses to external cues. These employ signaling mechanisms that reflect the evolutionary histories of the respective organisms. We propose that the similar developmental trajectories of myxobacteria and dictyostelids are more due to shared generic physical processes in coordination with analogous agent-type behaviors than to convergent evolution under parallel selection regimes. Insights from the biology of these aggregative forms may enable a unified understanding of developmental evolution, including that of animals and plants.

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

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.

Dynamical patterning modules in plant development and evolution.

Broad comparative studies at the level of developmental processes are necessary to fully understand the evolution of development and phenotypes. The concept of dynamical patterning modules (DPMs) provides a framework for studying developmental processes in the context of wide comparative analyses. DPMs are defined as sets of ancient, conserved gene products and molecular networks, in conjunction with the physical morphogenetic and patterning processes they mobilize in the context of multicellularity. The theoretical framework based on DPMs originally postulated that each module generates a key morphological motif of the basic animal body plans and organ forms. Here, we use a previous definition of the plant multicellular body plan and describe the basic DPMs underlying the main features of plant development. For each DPM, we identify characteristic molecules and molecular networks, and when possible, the physical processes they mobilize. We then briefly review the phyletic distribution of these molecules across the various plant lineages. Although many of the basic plant DPMs are significantly different from those of animals, the framework established by a DPM perspective on plant development is essential for comparative analyses aiming to provide a truly mechanistic explanation for organic development across all plant and animal lineages.