Electrical signals, the cytoskeleton, and gene expression: A hypothesis on the coherence of the cellular responses to environmental insult

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.