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Roots Down, Shoots Up. But How Does a Plant Know Which is Which?

This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American


From the Brockhaus and Efron Encyclopedic Dictionary. Credit: Wikimedia

When an avalanche tears down a mountain, a revealing, if inadvertant, botanical experiment is sometimes begun. Though trees in the path of the angry snow are often ripped from their roots and deposited unceremoniously downhill, occasionally, overturned trees hold fast. Some roots of these partially upturned trees break and die of exposure. But some remain plugged into the soil. The tree survives and goes about its business, albeit in a very un-tree-like prone position. And almost immediately, something fascinating happens.

The overturned tree makes a hard turn, and begins growing vertically again. If you encounter such a tree in the forest many years hence, it will seem as if as a sapling, it decided to join a rebellious arboreal counterculture and then suddenly realized somewhere in young adulthood that it had better get serious about growing tall and making cones.


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What this means, of course, is that trees can sense gravity. And, as it turns out, so can all plants. You may have never considered that plants might possess this magical ability, but they do. A potted tomato plant will do the same thing as the pine if left on its side. And if inverted (and rooted in a potting medium that won't respond to gravity by landing on your shoes), the plant will make a U-turn.

Here's a time-lapsed example of a popular houseplant called Coleus.

Possibly even more amazingly, re-oriented root tips -- which never see the light of day and are physically constrained by soil -- will abruptly change direction too, and start growing once more toward Earth's core.

You could probably have deduced that plants sense gravity just by looking at trees growing on a steep slope. They don't grow perpendicular to the soil. They grow perpendicular to the sky.

Scientists have a a name for this phenomenon: gravitropism. What they lack is a complete explanation of how it works. How does an organism that remains in one place its whole life know it's been overturned, and, once that much is ascertained, how does it know which way is the new up? Once it knows which way is up, how does it go about making that hard right?

Whatever ideas you might have on this subject must also accommodate this startling fact: If you mount a plant sideways on machine that rotates it like a pig on a spit, the plant will *not* make a hard turn toward space. Instead, it will keep growing horizontally as if it had no ability to sense gravity at all.

Scientists have been studying this question a long time, and they are reasonably confident they know the answer to the first part of the question: how plants know which way is up.

Plants sense gravity, in essence, the way a snow globe does. Instead of fake snow, they use particles called statoliths. In conifers and flowering plants, the statoliths are food storage vessels called amyloplasts. Plants synthesize and store starch (polymers of glucose, which plants manufacture in their green parts from light, water, and carbon dioxide) in these granules. Inside the amyloplasts of the common bean the starch granules resemble variously sized cotton balls stuffed into a balloon. Although amyloplasts are usually white, the amyloplasts in this carrot root appear to be pigmented -- perhaps they have been stained:

 

From Blancaflor 2012, American Jounal of Botany 100:1 143-152. Click image for link.

 

Under normal circumstances amyloplasts do nothing more than sit on the bottom of special gravity-sensing cells in the central column (columella) of root caps, and in shoots next to the vascular bundles that transport water and sugar. When a plant is knocked over, the amyloplasts slide from what was recently the bottom of the cell onto a formerly vertical wall, as you can see above.

This is where things get fuzzy. Somehow, this movement is sensed and relayed to cells that secrete the growth-regulating plant hormone auxin on the new undersides of root and shoot. The hormone has opposite effects in the two locations, triggering growth suppression on the underside of roots and growth enhancement on the underside of shoots. As a result, roots veer earthward; shoots veer skyward. Once the root or shoot reorients, the amyloplasts slide down into their original position and the auxin equilibrium is restored.

What is particularly fascinating about the way higher plants sense gravity is that the gross mechanism is not so different from our own. Plants and animals have independently produced similar solutions to a common problem. This is called convergent evolution, and it happens quite a lot on Earth.

Inside the vestibule of your inner ear are two chambers called the utriculus and sacculus. The cells of the lining bristle with sensory hairs. The hairs, in turn, are embedded in gelatinous goo. And sitting on top of the goo are multi-faceted calcium carbonate crystals called otoliths.

Otoliths, like amyloplasts, move. When you tilt forward, they slide, pulling down the goo and hairs with them, as you can see here. The pull of the hairs triggers signals to your brain, which are interpreted appropriately. Once again, sedimenting particles are the gravity sensor.

But in plants, sensor and effector are not connected by a handy brain. In fact, how they are connected is particularly puzzling because sensing and physical response are often separated by a fair distance:

 

From Blancaflor 2012, American Jounal of Botany 100:1 143-152. Click image for link.

 

The distance can extend to a few millimeters. You can see the issue here.

Scientists aren't at all sure how the signal generated by the amyloplasts reaches the cells that generate auxin. A recent review article by Elison Blancaflor in the American Journal of Botany spotlighted experiments that have provided a few clues as to how plants translate falling amyloplasts into swerving extremities.

Early theories focused on actin -- the part of the cell's skeleton that builds thin fibers called microfilaments -- because these fibers support and probe all parts of the cell and often transmit information. If amyloplasts suddenly shifted, it seemed likely that the cytoskeleton would be in a good position to notice.

Originally, scientists thought that actin might directly sense and relay the force of falling statoliths. But upon closer inspection, there was a problem: in roots, chemicals that disrupt actin microfilaments strengthened -- not dampened -- plants' gravity sensing. And in other experiments, the lack of a fully developed cytoskeleton in the appropriate root cells didn't inhibit gravity sensing either. How could this be if actin directly sensed amyloplast movements?

Actin could still be involved in regulating gravity sensing if it inhibits it, and the fact that altering actin had an effect at all on gravity sensing suggests this. Experiments reviewed in the Journal of Botany suggest that actin microfilaments may form a sieve-like network that regulates how easily amyloplasts move around. They could also regulate gravity sensing if they bind to or help lift amyloplasts off the floor of the cell, since how hard amyloplasts press their substrate seems to correlate with the strength of the gravity response.

Yet strangely, experiments with an alga called Chara have shown that at least in this plant, the actual weight of the statoliths is not what the cell uses to gauge gravity.

In Chara, gravity sensing and the growth response all occur in the same cells in the root-like structures of the plant. Chara uses yet a third heavy particle to sense gravity: vesicles packed with the high-density chemical barium sulfate. Someone interested in how Chara senses gravity decided to send some on a joy ride in a Vomit Comet -- a plane, popular with astronaut trainees and Stephen Hawking, that flies in high-amplitude waves, producing the experience of weightlessness on descent.

They discovered that when functionally weightless, gravity sensing still worked in Chara as long as the statoliths were still physically touching the cell's plasma membrane. The investigators suggested that it is physical contact with the membrane, not the pressure generated by the weight of the statolith, that triggers gravity sensing. There may be a protein expressed on the surface of amyloplasts that binds to a receptor on floor of the cell. The more the amyloplast pushes down on the membrane, the more proteins come into contact with receptors, and the stronger the gravity perception. Clearly, we still have a lot to learn about how plants transmit amyloplasts' gravity signals to auxin-producing cells far afield.

Let's now return to our plant-on-a-spit puzzle. You may now grasp why the plant acts as if it doesn't know up from down: as the plant is slowly rotated, so too are the amyloplasts, like rocks in a tumbler. The result is a continuously changing growth direction signal as they sequentially stimulate all sides of the cell. The sum of these omni-directional vectors is zero. To the plant, the message is clear: full speed ahead.

 

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