Meristematic Connectome: A Cellular Coordinator of Plant Responses to Environmental Signals?

Donato Chiatante,Antonio Montagnoli,Thomas L Rost,Dalila Trupiano,John Bryant,Gabriella S Scippa,Gabriella Sferra

doi:10.3390/cells10102544

Donato Chiatante, Antonio Montagnoli + Show 5 more

Open Access

https://doi.org/10.3390/cells10102544

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Abstract

Mechanical stress in tree roots induces the production of reaction wood (RW) and the formation of new branch roots, both functioning to avoid anchorage failure and limb damage. The vascular cambium (VC) is the factor responsible for the onset of these responses as shown by their occurrence when all primary tissues and the root tips are removed. The data presented confirm that the VC is able to evaluate both the direction and magnitude of the mechanical forces experienced before coordinating the most fitting responses along the root axis whenever and wherever these are necessary. The coordination of these responses requires intense crosstalk between meristematic cells of the VC which may be very distant from the place where the mechanical stress is first detected. Signaling could be facilitated through plasmodesmata between meristematic cells. The mechanism of RW production also seems to be well conserved in the stem and this fact suggests that the VC could behave as a single structure spread along the plant body axis as a means to control the relationship between the plant and its environment. The observation that there are numerous morphological and functional similarities between different meristems and that some important regulatory mechanisms of meristem activity, such as homeostasis, are common to several meristems, supports the hypothesis that not only the VC but all apical, primary and secondary meristems present in the plant body behave as a single interconnected structure. We propose to name this structure “meristematic connectome” given the possibility that the sequence of meristems from root apex to shoot apex could represent a pluricellular network that facilitates long-distance signaling in the plant body. The possibility that the “meristematic connectome” could act as a single structure active in adjusting the plant body to its surrounding environment throughout the life of a plant is now proposed.

Highlights

In the second series of experiments with Fraxinus and Populus, we have investigated the response to mechanical stress, induced by the application of bending, along the root axis of a plant lacking all primary tissues
The published in silico model [24] showed that, within each sector, tension forces are active on the convex side whereas compression forces occur on the opposite concave side
The data from the bending treatment showed that plants remain viable, responding to mechanical stress through a unidirectional formation of reaction wood (RW) and new lateral roots (LRs)

Summary

Introduction

Several experiments performed by our research group [16,17,18,19,20] have demonstrated that roots respond to mechanical stresses through the action of the vascular cambium (VC) even when they lack all root primary tissues, including the root apical meristem (RAM) and the TZ This fact casts a serious shadow over the proposal that TZ could play a role of “brain” of the plant. This supports our observations regarding the similarity of VC behaviour along the root-stem axis For this reason, it is not unreasonable to suggest that homologous regulatory mechanisms could be active along the sequence of meristems that in a plant are organized (according to a bottom-top direction) to form (i) RAM, (ii) root procambial bundles (root PRC), (iii) root and shoot VC, (iv) shoot procambial bundles (shoot PRC), and (v) shoot apical meristem (SAM). The “meristematic connectome” could function as a cellular network for rapid communication through the distant plant body’s compartments while being involved in responses to environmental signals

Pruning and Bending Treatments

Pruning

Unidirectional production

Meristematic Connectome and the Coordination of Plant Response to

Crosstalk between Different Components of the “Meristematic Connectome”