References

21
Electrical Signals, the Cytoskeleton,
and Gene Expression: a Hypothesis
on the Coherence of the Cellular
Responses to Environmental Insult
Eric Davies, Bratislav Stankovic
Abstract When plant tissue is abiotically injured by crushing, cutting, heat-wounding,
electrical stimulation, or by several other means, the injured (perceiving) tissue generates
electrical signals (action potentials and variation potentials) and transmits them to distant
(responding) tissue. Here they evoke apparently disparate responses, such as callose formation,
closing of plasmodesmata, stoppage of cytoplasmic streaming, inhibition of ribosome
movement along messenger RNA (mRNA), and ultrarapid but transient accumulation of
over 100 transcripts, which are degraded without being translated. These apparently disparate
responses can be reconciled by one fundamental hypothesis that assumes that “the
plant does not know what hit it” and thus “expecting the worst” mounts a holistic defense
response against its most potent nemesis, a putative viral invasion. We postulate that the basis
for this response is calcium influx into the cytoplasm via voltage-gated channels (action
potential) associated with the microtubules, or via mechano-sensitive channels (variation
potential) associated with microfilaments. The calcium interacts with calcium and/or
calmodulin-dependent cytoskeleton-associated protein kinases. This causes the phosphorylation
of myosin, which stops cytoplasmic streaming, and of elongation factor 2F, which
slows elongation and termination and causes ribosomes to pile up on polyribosomes. This
decreases protein synthesis, but protects preexisting “host” transcripts from degradation.
The phosphorylation signal then passes into the nucleus, where it phosphorylates RNA
polymerase II, which goes into overdrive (i.e., does not stop at accuracy checkpoints), thus
causing the synthesis of large amounts of mismade mRNA. The mRNA is transported into
the cytoplasm, where it is scanned (checked for accuracy) by ribosomes, and found to be incorrect.
This surveillance mechanism stimulates ribonuclease activity, which degrades the
free (non-polysome-associated), mismade RNA, but leaves the original, “host” transcripts
unscathed since they are protected by ribosomes. The ribonuclease also (and here is the
crux of the matter) attacks other free mRNAs, including viral mRNAs, so these are disposed
of before they can be translated. Within minutes this reaction is over, cytoplasmic steaming
resumes, translation continues, ribosomes are released and so can be used to translate new
(correctly made) transcripts.
21.1
Introduction to the Hypothesis
There are several different kinds of electrical activities in plants, including
action potentials (APs), variation potentials (VPs), voltage spikes or voltage
transients, and rhythmic electrical activities but their role is far from
understood (Davies 1987b, 2004; Davies et al. 1991). They all involve ion
fluxes across membranes and bring about changes in membrane potential.
Communication in Plants
F. Baluška, S. Mancuso, D. Volkmann (Eds.)
© Springer-Verlag Berlin Heidelberg 2006