Circadian Protein Helps Plants Manage Short- and Long-Term Stresses

Researchers at the Keck School of Medicine of the University of Southern California, have uncovered new insights into how plants regulate their responses to stress, which may aid future efforts to engineer crops that are better able to thrive in the face of drought or high soil salinity levels associated with climate change.

The investigators found that plants use their circadian clocks to respond to changes in external water and salt levels throughout the day. That same circuitry—an elegant feedback loop controlled by a protein known as ABF3—also helps plants adapt to extreme conditions such as drought.

“The bottom line is plants are stuck in place,” said research lead Steve A. Kay, PhD, University and Provost Professor of Neurology, biomedical engineering and quantitative Computational Biology at the Keck School of Medicine and director of the USC Michelson Center for Convergent Bioscience. “They can’t run around and grab a drink of water. They can’t move into the shade when they want to or away from soil that has excess salt. Because of that, they’ve evolved to use their circadian clocks to exquisitely measure and adapt to their environment.”

Kay and colleagues reported on their results in the journal Proceedings of the National Academy of Sciences (PNAS), in a paper titled “The interplay between the circadian clock and abiotic stress responses mediated by ABF3 and CCA1/LHY,” in which they concluded that their findings “… offer valuable insights for developing genetic and molecular approaches to enhance plant resilience in the face of climate change.”

Climate change is a global concern for all life on our planet, including humans and plants, the authors noted. “As sessile organisms, plants must constantly adapt to the environment and cope with various stresses, such as drought, salinity, and extreme temperatures,” they wrote. “Understanding how plants respond to abiotic stresses is crucial for addressing this challenge.” One of the most crucial mechanisms in plants is the ABA signaling pathway, the team further explained. “ABA is a plant hormone that plays a key role in regulating responses to abiotic stress such as drought, high salinity, and high temperatures.”

The newly reported study builds on a long line of research from Kay’s lab on the role of circadian clock proteins in both plants and animals. “As the internal timekeeping machinery, the circadian clock enables plants to synchronize with daily and seasonal environmental changes and directly controls many developmental processes throughout the life cycle,” the authors further explained. In the model plant organism Arabidopsis, the circadian clock includes what the researchers described as “… a plethora of oscillating proteins” that are expressed and function in an orchestrated manner. “Studies in crops also revealed the important role of the circadian clock in regulating stress responses,” they added.

Clock proteins regulate biological changes over the course of the day, and may provide a shrewd solution to an ongoing challenge in crop engineering. Creating drought-resistant plants is difficult because plants respond to stress by slowing their own growth and development—an overblown stress response means an underperforming plant. “There’s a delicate balance between boosting a plant’s stress tolerance while maximizing its growth and yield,” Kay said. “Solving this challenge is made all the more urgent by climate change.”

Previous plant biology research showed that clock proteins regulate about 90% of genes in plants and are central to their responses to temperature, light intensity and day length, including seasonal changes that determine when they flower. But one big outstanding question was whether and how clock proteins control the way plants handle changing water and soil salinity levels.

To explore the link, Kay and his team studied Arabidopsis, which is commonly used in research because it is small, has a rapid life cycle, a relatively simple genome and shares common traits and genes with many agricultural crops. They created a library of all of the more than 2000 Arabidopsis transcription factors, which are proteins that control the way genes are expressed under different circumstances. Transcription factors can provide key insights about regulation of biological processes. The researchers then built a data analysis pipeline to analyze each transcription factor and search for associations.

“We got a really big surprise: that many of the genes the clock was regulating were associated with drought responses,” Kay said, particularly those controlling the hormone abscisic acid, a type of stress hormone that plants produce when water levels are very high or very low. The analysis revealed that abscisic acid levels are controlled by clock proteins as well as the transcription factor ABF3 in what Kay calls a “homeostatic feedback loop.”

The authors wrote, “We demonstrate how the circadian clock influences ABF3 expression, which in turn delivers stress signals to core clock genes and adjusts the circadian period in response to stress … Our study reveals a unique mechanism of the interplay between the circadian clock and abiotic stress responses mediated by ABF3 and CCA1/LHY.”

The findings indicated that during the course of a day, clock proteins regulate ABF3 to help plants respond to changing water levels, then ABF3 feeds information back to clock proteins to keep the stress response in check. That same loop helps plants adapt when conditions become extreme, for instance during a drought. Genetic data also revealed a similar process for handling changes in soil salinity levels. “Specifically, we found that CCA1 and LHY regulate the expression of ABF3 under diel conditions, as well as seed germination under salinity. Conversely, ABF3 controls the expression of core clock genes and orchestrates the circadian period in a stress-responsive manner,” they stated. “Our research also uncovers a unique function of ABF3 in modulating the circadian clock. ABF3 controls the expression of core clock genes and modulates the circadian period in a stress-responsive manner.”

Kay added, “What’s really special about this circuit is that it allows the plant to respond to external stress while keeping its stress response under control, so that it can continue to grow and develop.”

The authors claim that elucidating the regulatory pathways and feedback loops involving CCA1, LHY, and ABF3, has offered up a deeper understanding of how plants coordinate their physiological and developmental responses to environmental challenges. “Understanding the intricate relationship between the circadian clock and abiotic stress response at the molecular level may aid in the development of targeted strategies to enhance plant resilience in the face of climate change,” they concluded.

The findings point to two new approaches that may help boost crop resilience. For one, agricultural breeders can search and select for naturally occurring genetic diversity in the circadian ABF3 circuit that gives plants a slight edge in responding to water and salinity stress. Even a small increase in resilience could substantially improve crop yield on a large scale. Kay and colleagues also plan to explore a genetic modification approach, using CRISPR to engineer genes that promote ABF3 in order to design highly drought-resistant plants. “This could be a significant breakthrough in thinking about how to modulate crop plants to be more drought resistant,” Kay said.

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