Organ-to-Organ signalling

Organ-to-organ signalling: the emerging picture

Elucidating how long-distance wound signalling pathways operate in plants, organisms that lack neurons, is an exciting challenge. One goal is to have a quantitative understanding of how fast wound signals travel from cell to cell, and how quickly jasmonate (JA) synthesis occurs upon arrival of these signals. Each new insight provides surprises. For example, if we wound the tip of a leaf and measure electrical activity 1 cm from the wound we find that it takes on average about 15 s for the signal to arrive at the electrode. More remarkably, it takes only 45 s for jasmonate to accumulate in the tissue distal to the wound, therefore, JA accumulation is initiated only about 30 s after arrival of the electrical signal. Finding this was surprising because JA synthesis involves several cellular compartments (http://www.bioone.org/doi/abs/10.1199/tab.0129). The numbers are from Nature 500, 422 for electrical signals, and J. Biol. Chem. 283, 16400 & 284, 34506 and from New Phytol. 197, 566 for JA measurements. Following is a broader overview of what we’ve found out so far.

Cotyledon wounding activates jasmonate signalling in root tissue and this can be visualised in real time (Nature Commun. 6, 6043). Wounding the aerial tissues of seedlings affects the growth of roots through jasmonate-dependent inhibition of cell division and cell elongation (PLoS Genetics, 11(6): e1005300). The major part of jasmonate signalling seen in the roots when cotyledons are wounded involves jasmonate transport from shoot to root (Plant Physiol. 169, 2244).

The story is somewhat different for leaf-to-leaf wound signalling. In that case long-distance electrical signals generated in the wounded leaf travel to distal leaves to stimulate jasmonate synthesis far from the wound (Nature 500, 422). These leaf-to-leaf long-distance signals travel through parastichies; domains in which leaves are connected to each other directly through the vasculature (J. Biol. Chem. 284, 34506). That is, it’s possible to predict which other leaves will respond when a particular leaf is wounded. Furthermore, mutations in genes encoding clade 3 glutamate receptor-like (GLR) proteins block leaf-to-leaf electrical signalling. These GLR genes play the role of extending the range of tissues that respond to the wound and make jasmonate (Nature 500, 422).

Once the electrical signals reach distal leaves they activate jasmonate synthesis in small populations of xylem contact cells, a specialised type of xylem parenchyma (New Phytol. 197, 566). Remarkably, these cells export JA (or a JA precursor) radially over distances of at least 125 μm corresponding to at least 8 layers of cells (Plant Physiol. 169, 2244).

We suspect that wound-induced pressure changes propagated through the xylem make up part of the leaf-to-leaf wound signal. However, we also found evidence for GLR-dependent electrical signals in phloem (New Phytol. 203, 674). At present we believe that two tissues (xylem and phloem) participate in the propagation of the long-distance GLR-dependent signal (New Phytol. 204, 288).

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