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. 2021 Sep 26;10(10):2544.
doi: 10.3390/cells10102544.

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

Donato Chiatante  1 , Antonio Montagnoli  1 , Dalila Trupiano  2 , Gabriella Sferra  2 , John Bryant  3 , Thomas L Rost  4 , Gabriella S Scippa  2
Affiliations

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

Donato Chiatante et al. Cells. .

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.

Keywords: Arabidopsis thaliana L.; Populus nigra L.; connectome; meristems; root apical meristem; root procambial bundles; shoot apical meristem; vascular cambium.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Pruning treatments in Populus nigra seedlings. (A) Seedlings before pruning showing the LRs. (B) Seedlings after pruning treatment with new LRs formation (white arrow). (C) New LRs are produced internally to the taproot axis by the VC before protruding from the cork (white arrow).
Figure 2
Figure 2
Unidirectional RW production in concave side of Populus nigra bent taproot. (A) The VC initials present in the concave side of the bent taproot are characterized by a very high mitotic activity shown by the high number of cells produced. (B) The VC initials present in the convex side of the bent taproot are characterized by a reduced mitotic activity shown by the lower number of cells produced XY = xylem; ph = phloem. Scale bars = 20 µm.
Figure 3
Figure 3
Emergence of a LR produced by the VC initials in the convex side of Populus nigra bent taproot. The cross section shows the production of a new lateral root (LR) that is formed by the activity of some VC initials and that grows toward the external convex side of the bent taproot. cc = cortical cells; xy = xylem; ph = phloem; fb = mechanical fibers. Scale bar = 200 µm.
Figure 4
Figure 4
The “meristematic connectome” formed by the sequence of all meristems—RAM, root PRC, root VC, shoot VC, shoot PRC, SAM—represents the ideal network able to induce a rapid signalling between cells/tissues sensing the maximum stress and distant plant compartments.
Figure 5
Figure 5
Single confocal laser scanning microscopy (CLSM) sections of A. thaliana root tips after α-tubulin immunostaining. (A) Central root section revealing a uniform transverse orientation of cortical microtubules in all the developmental zones (RAM, TZ and elongation zones) and all the tissues/cell types. The root zones appear compressed because the root was growing in thick soil (Scale bar = 150 µm). (B) Higher magnification of the stele at the border between the meristematic and TZ. All the cell types, including PRC cells, exhibit transverse cortical microtubules (Scale bar = 10 µm).
Figure 6
Figure 6
3D-modelling of the longitudinal and transverse mechanical forces distribution. (A) Cylindrical structure representing the taproot axis in which the different tissues are represented by four concentric layers. (B) In cross-section, 12 rays separate adjacent units (theoretically cell) of the same layer (theoretically same tissue); the continuity between rays 1 and 7 represent the average point concave-convex direction and letters (from a to i) are used to indicate where the force were measured along this direction; (C) full-length model of the bent taproot. Each box reports the mean force magnitude of three bent sectors (ABS, BS and BBS) in concave-convex direction (a to i) of a sector flanked by its magnitude scale. In the graphical representations VC is shown as a yellow line in the transverse section while in the boxes the corresponding magnitude of forces is reported.
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