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Front. Plant Sci. | doi: 10.3389/fpls.2018.00871

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

Mariana Benítez1, Valeria Hernández- Hernández2,  Stuart A. Newman3 and  Karl J. Niklas4*
  • 1Centro de Ciencias de la Complejidad, Instituto de Ecología, Universidad Autónoma de Mexico, Mexico
  • 2Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, France
  • 3Department of Cell Biology and Anatomy, New York Medical College, United States
  • 4Plant Biology Section, School of Integrative Plant Science, Cornell University, United States

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: Plant evolution, Plasmodesmata, Algal evolution, convergent evolution, dynamical patterning modules

Received: 13 Apr 2018; Accepted: 04 Jun 2018.

Edited by:

Verónica S. Di Stilio, University of Washington, United States

Reviewed by:

Daniel H. Chitwood, Michigan State University, United States
Olivier Hamant, École Normale Supérieure de Lyon, France  

Copyright: © 2018 Benítez, Hernández- Hernández, Newman and Niklas. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Karl J. Niklas, Cornell University, Plant Biology Section, School of Integrative Plant Science, 412 Mann Library, Tower Road, Cornell University, Ithaca, 14850, New York, United States, kjn2@cornell.edu