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Stressed plant roots warn the rest of the plant of looming dangers

Natural disasters. Humans can’t avoid those. But we have systems in place to predict their activity so we minimize loss of life through preventative measures. Take a hurricane. Meteorologists track it with satellites, airplanes, and forecasting models, so people in risk-prone areas can be warned to prepare for the big hit.

It seems plants work the same when under stress, according to a new Michigan State University study. Scientists have shown that when a stress response common to many plant species – the expand iconunfolded protein response (UPR) – is triggered in the roots, the rest of that plant feels it too. The study is in the journal, Nature Communications.

Here’s how the UPR works: inside each plant cell is a massive factory, called the expand iconendoplasmic reticulum (ER). It produces one third of a cell’s proteins and other building blocks that keep plants healthy and working.

But the factory can get overloaded with production demands during times of disease, extreme heat, even cell growth spurts that demand more new proteins than usual. These stresses cause the ER to make defective expand iconproteins that could harm the plant. So, cellular alarm bells go off, and the UPR kicks in to tame the cells. It destroys or fixes bad proteins and ‘resets’ the factory to produce healthy ones.

“We have assumed this response happens on the cellular level,” says Ya-Shiuan Lai, co-author and recent graduate from the lab of Federica Brandizzi. “Then my mentor asked me, if a cell experiences ER stress in one part of the plant, does the rest of the plant feel it too?”

To answer the question, Lai first developed a way to track the UPR throughout a plant. The control experiment was to attach a fluorescent molecule to a gene found at the center of plant roots. As expected, the fluorescent molecule lit up the root’s center, indicating the gene stayed there. Then, Lai added a UPR genetic trigger – called bzip60 – to the combination of fluorescent molecule/central root gene. After treating the roots with a toxic chemical that causes stress, the fluorescent molecule moved to the outside layers of the root.

Fluorescent microscopy images
Left panels: control experiment where the green fluorescent molecule stays at the root center; Right panels: the UPR genetic trigger causes the green signal to move to root edges, which indicates the stress response was communicated over a certain distance.
By Ya-Shiuan Lai and Brandizzi Lab. Ya-Shiuan Lai, Federica Brandizzi, Nature Communications, 2018, CC BY 4.0

That meant that the genetic trigger had caused the movement. “We also found that the UPR was activated in those areas where the fluorescent molecule lit up,” Lai adds. “That indicates that the gene triggered the stress response wherever it went.”

Splitting a plant cuts off contact

With the help of Starla Zemelis, a lab technician in the Brandizzi lab, Lai confirmed the idea through an elegant, but challenging, micro-grafting experiment that took years to perfect. They modified the roots of an Arabidopsis plant - the lab rat for plant scientists - so that the ER could not trigger the UPR in those root cells.

Then they grafted healthy, unmutated plant shoots on top of those mutated roots. When the researchers stressed root cells, the warning signal did not make it to the shoots. But in healthy plants, they saw a long-distance movement of the signal from root to shoots.

“We think the signal moves between cells through the plasmodesmata, which is one of the contact points between neighboring cells. It is as if the cells in those healthy plants ‘pass the baton’ to help the gene travel and trigger the UPR across the entire plant,” Lai says.

According to Federica Brandizzi, Lai’s mentor, the fact the gene moves from roots to shoots, and not the other way around, is likely important.

“Roots are sensitive organs. They have to explore the ground and warn the plant about potential stresses,” Brandizzi says. “In the case of the UPR, we think that long-distance communication is a warning from the roots to the plants to prepare for the big ‘hit’ and to allocate resources appropriately.”

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