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Spatiotemporal signalling in plant development

Key Points

  • Plants are sessile organisms and have developed unique signalling mechanisms that allow the integration of external cues in order to continuously modulate developmental processes.

  • The integration of multiple signalling pathways is important for plant development. These pathways include short- and long-range signals that give rise to a whole-organism response.

  • Short-range signals, such as peptides, transcription factors and noncoding small RNAs, are used to provide local communication between plant cells that are constrained by a cell wall.

  • Long-range signals, such as phytohormones, use diverse regulatory and integration mechanisms to elicit a broad range of signal outputs.

Abstract

Plants, being sessile organisms, need to respond to changing environments, and as a result they have evolved unique signalling mechanisms that allow rapid communication between different parts of the plant. The signalling mechanisms that direct plant development include long-range effectors, such as phytohormones, and molecules with a local intra-organ range, such as peptides, transcription factors and some small RNAs. In this Review, we highlight recent advances in understanding plant signalling mechanisms and discuss how different classes of signalling networks can integrate with gene regulatory networks and contribute to plant development. In some cases, we also address the evolutionary context of mechanisms and discuss possible links between the lifestyle of plants and selection for different signalling mechanisms.

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Figure 1: Schematic representation of Arabidopsis thaliana meristems and types of signalling.
Figure 2: Routes of intercellular movement.
Figure 3: Peptide signalling in meristem maintenance.
Figure 4: Transcription factor and small non-coding RNA movement in the root meristem.
Figure 5: Dynamics of auxin responses.

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Acknowledgements

Work in the Benfey laboratory is funded by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3405) to P.N.B., as well as by grants from the US National Institutes of Health (R01-GM043778), the US National Science Foundation and the Defense Advanced Research Projects Agency.

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Glossary

Phytohormones

Signal molecules produced in plants that elicit diverse effects depending on context.

Meristems

Groups of dividing cells (in the root and shoot), which include the stem cells that give rise to new tissues and organs.

Organizing centre

A group of meristem cells in the shoot that have low mitotic activity and that are required for the maintenance of the stem cells.

Quiescent centre

A group of meristem cells in the root that have low mitotic activity and that are required for maintenance of the stem cells.

Initial cells

Progenitor cells of a tissue or an organ.

Cell wall

A structure composed of cellulose, hemicellulose and pectin that surrounds plant cells (and some other organisms such as fungi), contributes towards the overall firmness of the organism and prevents cellular movement.

Kinase-dead

Contains a kinase domain identified by its sequence, but without kinase activity; that is, the ability to add phosphate to a substrate.

Morphogen

A signal gradient that has a single source that results in differential output (that is, cell fate) as a readout of the local concentration.

Florigen

A universal mobile signal, originating from leaves, that is necessary for the initiation of flowering in plants.

Hypophysis

The most proximal cell of the suspensor that will initiate the columella and quiescent centre.

Suspensor

A cell population that connects the embryo proper to the endosperm feeding tissue. It forms as a result of asymmetric division of the zygote and functions similarly to the placenta in animals.

Feedforward loops

(FFLs). Gene network motifs in which a protein, X (usually a transcription factor), regulates a target gene, Z, directly as well as indirectly through another regulator, Y. The input of X and Y can be either positive or negative. X and Y might both be required (AND gate) or either one might be sufficient on its own (OR gate).

Hill function

A function used in biochemistry to describe cooperative binding. It usually reflects the enhanced efficiency of ligand binding as a result of other ligand molecules that are already bound to a receptor.

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Sparks, E., Wachsman, G. & Benfey, P. Spatiotemporal signalling in plant development. Nat Rev Genet 14, 631–644 (2013). https://doi.org/10.1038/nrg3541

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