Time-lapse reveals the hidden dance of the roots



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DURHAM, NC – Researchers at Duke have studied something that is happening too slowly for our eyes to see. A team from the laboratory of biologist Philip Benfey wanted to see how the roots of plants burrow into the ground. So they installed a camera over the germinated rice seeds in a clear gel, taking a new photo every 15 minutes for several days after germination.

When they reread their images at 15 frames per second, compressing 100 hours of growth into less than a minute, they saw that rice roots use a trick to take their first foot in the ground: their growing spikes make corkscrew-like movements, wiggling and winding in a helical path.

Using their time-lapse images, along with a root-shaped robot to test ideas, the researchers gained new insight into how and why the root tips of plants spin as they grow.

The first clue came from something else the team noticed – some roots can’t do the corkscrew dance. The culprit, they found, is a mutation in a gene called HK1 that causes them to grow straight down, instead of spinning and meandering like other roots do.

The team also noted that the mutant roots grew twice as deep as normal roots. Which raised a question: “What does the more typical spiral spike growth do for the plant?” said Isaiah Taylor, a postdoctoral associate in Benfey’s lab at Duke.

Winding movements in plants were “a phenomenon that fascinated Charles Darwin” even 150 years ago, said Benfey. In the case of shoots, there is an obvious use: the twists and circles make it easier to grip as they ascend towards the sunlight. But how and why this happens in the roots was no longer a mystery.

Germination of seeds is a challenge, say the researchers. To survive, the first small root that emerges must anchor the plant and probe downward to suck up the water and nutrients the plant needs to grow.

Which got them thinking: Maybe in the roots, this spiraling growth is a search strategy – a way to find the best way forward, Taylor said.

In experiments conducted in the lab of physics professor Daniel Goldman at Georgia Tech, observations of normal and mutant rice roots growing on a perforated plastic plate revealed that normal spiral roots were three times more likely to find a hole and grow on the other side.

Collaborators from Georgia Tech and the University of California at Santa Barbara built a soft, flexible robot that unwinds from its tip like a root and releases it into an obstacle course made up of unevenly spaced stakes.

To create the robot, the team took two inflatable plastic tubes and nested them one inside the other. The change in air pressure pushed the soft inner tube from the inside to the outside, which extended the robot from the tip. The contraction of opposing pairs of artificial “muscles” caused the robot’s tip to bend from side to side as it grew.

Even without sophisticated sensors or controls, the robotic root was still able to climb over obstacles and find its way through the ankles. But when the side-to-side flexion stopped, the robot quickly got stuck against an ankle.

Finally, the team grew normal and mutant rice seeds in a soil mix used for baseball diamonds, to test them on any obstacles a root would actually encounter in the soil. Sure enough, while the mutants struggled to take root, normal roots with spiraling growth spikes were able to break through.

The growth of the corkscrew from one root tip is coordinated by the plant hormone auxin, a growth substance that researchers say can move around the tip of a growing root in a wave shape. The buildup of auxin on one side of the root causes these cells to elongate less than those on the other side, and the root tip bends in that direction.

Plants that carry the HK1 mutation cannot dance due to a defect in the way auxin is transported from cell to cell, the researchers found. Block this hormone and the roots lose their ability to spin.

This work is helping scientists understand how roots grow in hard, compacted soil.

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This work was supported by a grant from the National Science Foundation (PHY-1915445, 1237975, GRFP-2015184268), the Howard Hughes Medical Institute, the Gordon and Betty Moore Foundation (GBMF3405), the Foundation for Food and Agricultural Research (534683), the National Institutes of Health (GM122968) and the Dunn Family Professorship.

QUOTE: “Mechanism and Function of Root Circumnutation,” Isaiah Taylor, Kevin Lehner, Erin McCaskey, Niba Nirmal, Yasemin Ozkan-Aydin, Mason Murray-Cooper, Rashmi Jain, Elliot W. Hawkes, Pamela C. Ronald, Daniel I. Goldman , Philip N. Benfey. Proceedings of the National Academy of Sciences, February 19, 2021. DOI: 10.1073 / pnas.2018940118.

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