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August 14, 2009

Excitable Plants

548px-VFT_ne1 In researching last month's Origins essay on the origin of the nervous system, I was struck by the range of behavior and electrical excitability exhibited by organisms that lack nerve or muscle cells. Some sponges, for example, have a sneeze-like reflex that flushes out sediment (see a video), whereas others generate electrical "action potentials" much like the impulses that convey information in nerves and brains. Electrical signals have been recorded even in the single-celled Paramecium, where they appear to play a role in escape and avoidance behaviors.

And it doesn't stop there. As far back as the 1870s, researchers had measured action potentials in two plants: the Venus flytrap (Dionaea muscipula) (left) and the800px-Mimosa-pudica-ante touch-sensitive Mimosa pudica (right). To find out more, I recently visited Elizabeth Van Volkenburgh at the University of Washington (UW) in Seattle. She co-authored a provocative 2006 review paper on "plant neurobiology" in which she and colleagues argued that electrical excitability is just one of several signaling mechanisms used by both animals with nervous systems and plants to gather information about their environment and change their behavior accordingly. Yes, behavior. In plants.

In a tour of the UW greenhouse, Van Volkenburgh demonstrated two famous examples, the quick snap of a Venus flytrap and the folding leaves of a Mimosa plant (see video at bottom of page). Root growth is another well-studied example of plant behavior, Van Volkenburgh says. The tip of a growing root can seek out moisture and steer a course around rocks and other obstacles. "If you look at video clips of root growth, you see a lot of behavior 364px-Darwin_Movement_in_Plants that looks like worm behavior," she says. Charles Darwin made a similar observation in The Power of Movement in Plants, published in 1880: "It is hardly an exaggeration to say that the tip of the [root] … acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense‑organs, and directing the several movements."

More than a century later, scientists are still investigating the sensory abilities of plants. In 2006, researchers reported in Science that seedlings of the parasitic dodder plant can sniff out their preferred host, growing toward a tomato plant—or even a vial of tomato extract—and shunning wheat. Sensing light is crucial for plants, and Van Volkenburgh says there are likely dozens of plant photoreceptor proteins for detecting different wavelengths of light. "They're detecting the quality of light, the intensity of light, the direction light is coming from, … and they're doing it all over, in every single cell."

As in animals, photoreceptors stimulated by light can trigger electrical activity in plants, her lab has found. "When light is shined on a young leaf, one of the first things that happens is what looks like an action potential," she says. That electrical impulse kicks off a series of events that enable the leaf to grow bigger. Other researchers also have found evidence that plants use electrical signaling. A 1996 study, for example, found that damaging the leaf of a tomato plant evokes an action potential, followed by a boost in gene expression for a proteinase inhibitor that makes the plants indigestible to insects. Electrical stimulation alone, in the absence of leaf damage, had a similar effect. Earlier this year, researchers used arrays of fine microelectrodes like the ones used in some neurobiology experiments to demonstrate synchronized electrical activity in the root tips of maize plants.

Plants also make a number of compounds that function as neurotransmitters in animals, including glutamate, GABA, dopamine and serotonin (though little is known about their roles in plant physiology), and some researchers see a parallel between neurotransmitter release at synapses and the release of the plant hormone auxin. Like neurotransmitters, auxin is packaged in vesicles that fuse with the cell membrane to unload their cargo into the cleft between cells. František Baluška, a botanist at Rheinische Friedrich-Wilhelms-University Bonn in Germany has gone so far as to call this arrangement a plant synapse.

But Van Volkenburgh thinks that's reaching a bit. At synapses, an electrical signal triggers release of a neurotransmitter, which in turn triggers an electrical response in the neighboring cell. But that chain of events has not yet been demonstrated for auxin, she said. "I would love to see those questions answered."

The mix of plants, behavior, and neurobiology is a strange cocktail. Even Darwin sounds slightly less than sober when he conjures up the image of tiny brains in the tips of growing roots. All the same, as Darwin realized, and as Van Volkenburgh and others have argued more recently, plants are far more responsive and dynamic than most animal-centric researchers give them credit for. That they do what they do without a nervous system makes them all the more fascinating.

—Greg Miller

Credits (top to bottom): Noah Elhardt, Wikimedia Commons; Sten Porse, Wikimedia Commons; Wikimedia Commons


I love this picture

Thanks for a very interesting article on a fascinating area of research.

It seems that harnessing ion flow across membranes is a very old trick indeed - possibly one of the earliest inventions of cellular life - and has been put to service in a vast array of functions across the tree of life. All of this work reinforces the view that evolution is a tinkerer, continually reusing and combining old inventions to accomplish new feats.

Chris Farnet
Volunteer, Darwin Facebook Campaign
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