Plant Circadian Clock Drives Molecular Salt Stress Defenses

Salty soil is a growing threat to crops worldwide. Hotter, drier weather has increased evaporation rates, drawing moisture from the soil and leaving behind concentrated mineral salts. At the same time, water shortages are forcing farmers to irrigate using water from lower-quality, saline or recycled sources. Scientists estimate that around half of the world's irrigated farmland is now affected by salinity to some degree.

A new study from Washington University in St. Louis reveals how a plant's internal clock helps it to respond to dangerous salts in its environment. Understanding how plants time their defenses against salt could eventually help scientists develop crops that hold up better against salt stress.

The research, published Oct. 14 in Science Advances, was led by biologist Xuehua Zhong, the Dean's Distinguished Professorial Scholar in WashU Arts & Sciences, and WashU postdoctoral fellow Wenwen Tian, an expert in circadian biology.

Biologists already knew that a plant's internal clock and its stress responses were connected - but not how the clock actually reaches the genes that protect the plant when trouble hits.

The link is surprisingly physical, Zhong said.

When a plant senses salt, a clock protein clusters into tiny droplets inside the nucleus, which frees protective genes to switch on. Because the clock protein is part of this switch, the plant's stress defenses are tied to its sense of time."

Xuehua Zhong, Washington University in St. Louis

Among the researchers' findings:

• A critical clock protein reacts to salt. Originally discovered and extensively studied in the model plant Arabidopsis thaliana, a clock protein called TIC ensures that biological rhythms synchronize properly with the 24-hour day-and-night cycle. Zhong and Tian found that when a plant is exposed to salt, TIC quickly gathers into tiny droplets inside the cell nucleus. "It's the first evidence that a clock component can respond directly to salt, linking the plant's sense of time with its sense of danger," Zhong said.
• Timing matters for survival. In this new study, plants that were modified to remove TIC were more vulnerable to salt. But these plants also had an internal clock that ran about 21 hours instead of 24. "When we grew them under 21-hour days that matched their clock, they actually handled salt better," Zhong said. "This shows that a plant copes with stress best when its internal clock is in sync with the outside world."
• Plants have a switch that turns on protective genes. As TIC droplets form, they pull on a group of enzymes that normally keep salt-protection genes turned down, Zhong said. With those enzymes partly out of the way, the genes switch on more strongly, helping the plant survive.

These findings open novel ways to think about building more resilient crops, the scientists said. Because TIC acts as a salt-responsive switch, it could become a target for breeding or gene editing. The new research also shows that plants cope with salt best when their internal clock matches their environment, a finding that suggests that tuning crop clocks could improve stress tolerance, Zhong said.

"The clock directly shapes stress responses," said Zhong, who also credited WashU undergraduate researcher Xinheng Lyu and visiting Stanford undergraduate student Grace Qian for making important contributions to this research as co-authors. "The same stress can produce different gene expression outcomes depending on when it occurs."