Who’s who?
That sounds like a good system, but it raises a problem. Roots
are immersed in a Mardi Gras of microbes benign, beneficent, and
bellicose. How does the plant tell which is which?
The secret, says molecular biologist B.W. “Joe” Poovaiah, lies
in the molecular dialog between root and microbe. He and his
research team have decoded a crucial part of the conversation in
legumes. Those are the plants, such as peas and beans, that form
symbiotic relationships with bacteria that convert atmospheric
nitrogen into a form the plant can use to make proteins and other
organic compounds.
Here’s how the conversation starts: Delicate root hairs that
grow from the main roots exude chemicals called flavonoids.
Bacteria in the soil are attracted by the flavonoids. They sidle up
to the root hairs and, in effect, ask to come in. Poovaiah calls it
“knocking on the door.”
When helpful, nitrogen-fixing bacteria are trying to establish a
relationship with a plant, they knock by secreting a chemical
called Nod factor. Harmful bacteria don’t secret Nod factor—and the
plant knows that.
When a root hair cell receives the Nod message, it begins to
move calcium around. Poovaiah’s coworkers at the John Innes Centre
in the UK showed this with special microscope equipment that
allowed them to make a movie in which different levels of calcium
appear as different colors: blue for low, red for high. Running in
real time, the movie shows a blob of red squishing back and forth
inside the root hair cell. It looks like a pixilated image of a
beating heart. (To view the movie, see sidebar, bottom.)
“This is not just calcium going in,” says Poovaiah. “It’s not a
flood. It is very rhythmic, coordinated in the intensity and the
duration. That’s the beauty.”
The calcium pulses carry a message. Soon after they begin, the
cell turns on specific genes, and the root hair bends around the
bacteria like an enfolding arm. Eventually, the bacteria and root
hair combine to form a nodule, visible to the naked eye, in which
each partner supplies something that benefits the other.
“The door is only open to the bacteria that have the key, that
sent in this Nod factor [and caused the calcium pulses],” says
Poovaiah. “The enemies cannot create that.” If a root hair
encounters harmful bacteria, he says, the hair “would just stay
there and say, ‘I’m not going to talk to you.’ That is the mystery:
only friends come in. Enemies stay out.”
Sathyanarayanan Puthanveettil (’01 Ph.D.), then a student in
Poovaiah’s lab, worked on one of the proteins involved in this
sequence of events. It’s a kinase, an enzyme that binds to calcium
and then promotes changes in other proteins in the pathway.
Poovaiah calls it a “decoder” that interprets the encrypted signal
carried by the calcium pulses, and triggers the next steps in the
pathway.
Biologists have long known that calcium plays a key role in
animal systems. It’s important in nerve transmission and muscle
action, in addition to its structural role in bones and shells.
Over the past 30 years, Poovaiah has established that the mineral
is just as important to plant adaptation and survival. His lab has
shown that calcium is the major player in a messenger system that
helps the plant monitor and respond to more than a dozen
environmental variables—functions that, in animals, are performed
by the nervous system.
Still, he and Puthanveettil were startled when they realized
that a large part of their kinase is very similar to a kinase found
in mammalian brains. The mammalian kinase is called a “memory
molecule,” because it plays a key role in the formation of
long-term memories.
“When we cloned the gene for this kinase, we thought, 'There
must be something wrong here. It cannot be,'” recalls Poovaiah. “So
we went back [and checked again] and we said, 'No, that’s the way
it is.'”
Other scientists were surprised, too—and impressed.
Puthanveettil was recruited to do postdoctoral research at Columbia
University in the lab of Eric Kandel, who won the Nobel Prize in
Medicine in 2000 for his work on signal processing in the nervous
system and the biochemical mechanisms of memory storage.
“I thought I would like to challenge myself in a very complex
system—the brain,” says Puthanveettil. He is now analyzing kinases
and other proteins involved in learning in a marine mollusk called
Aplysia.
Poovaiah was invited to present his work on calcium signaling at
a conference in Beijing in May 2006. The meeting is hosted by the
Society for Plant Neurobiology.
You read that right: plant neurobiology.
That term doesn’t make sense to psychologist Wright. Plants
don’t have nerve cells or nervous systems, after all.
On the other hand, they clearly have a system of biochemical
communication between cells, a system that allows a plant to direct
its own behavior and interact in specific ways with other
organisms. Neurobiologists say that 99 percent of all communication
in an animal’s brain is chemical, not electrical. Why couldn’t
plants be doing something similar?
Pressed for an opinion about plant “brains,” Poovaiah laughs.
“You want the Poovaiah model? Plants don’t have one big brain, they
have tiny brains everywhere.” Control is diffuse rather than
centralized. Different parts of the plant direct different aspects
of behavior.
The root tip, for example, senses gravity and directs the root
to grow downward. Cut off the tip, and the root wanders aimlessly.
Replace it, and it heads downward again. Charles Darwin did that
experiment in the mid-1800s.
“He said the root tip is like the brain of a small animal, like
maybe an earthworm,” says Poovaiah. “We do know there’s something.
They’re not as passive as we thought. They do have the ability to
sense changes and respond. In that sense, they are
intelligent.”
There’s that word again.
“I think the problem is starting with definitions we can all
live with,” says psychologist Wright. He thinks it will be
difficult to figure out whether plants act in a flexible,
problem-solving (i.e., intelligent) way, or whether they simply
execute “fixed action patterns” they are genetically programmed to
do.
For instance, a plant whose root recognizes and embraces helpful
bacteria will thrive better and leave more offspring than plants
without that ability; a plant that embraces the wrong kind of
bacteria might not live long enough to reproduce at all. A complex
behavior that looks intelligent could have arisen and been highly
refined through eons of evolutionary pressure.
Poovaiah is intrigued by the current speculation about plant
“intelligence,” but for now, he is content to learn more about how
calcium signals work, and what they reveal about the inner life of
plants.
“It was private,” he says with a sly smile. “But now we have
opened the door.”
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