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Acidification tells plants it's deadly freezing

Image of a snowy landscape

A new study from the Benning lab shows how plants sense freezing temperatures through increased cellular acidification. The results, published in the July issue of Plant Physiology, have ramifications into biofuel and food security solutions.

 “We know a lot about how plants sense some things,” says Rebecca Roston, former Benning lab postdoc and currently an assistant professor at University of Lincoln Nebraska. “But how they sense and react to the environment is a relatively new field in plant biology.”

Cellular ‘gated communities’

Figure of a plant cell indicating that membranes surround all the interior components.

“Most of what we see when we look at pictures of cells is membranes,” Rebecca says. “They are important because they separate parts of the cell, called organelles, from each other by selectively controlling the flow of products. This is crucial, because just a small amount of leakage from some organelle membranes is enough to kill the cell.”

Cell membranes are constantly remodeled to adapt to growth and stress, much like how bones grow to support kids’ changing structures. And during cold temperatures, membranes are remodeled to reduce damage in response to low temperatures.

Freezing damage

But not all plants that survive the cold make it through freezing temperatures.

“Freezing is an additional stress that causes ice crystals to form outside the cell. Water then rushes out due to osmosis, leaving behind the cell organelles, now tightly packed together.”

“Freezing also destabilizes cell membranes and reduces their ability to separate cell components.”

“Both tightly packed organelles and unstable membranes result in organelles vulnerable to fusing and susceptible to leakage and damage.”

“When freezing ends, water rushes back into the helpless cell, overfilling and killing it.”

Proteins to the rescue

Dr. Christoph Benning’s lab had previously identified a protein – SFR2 (sensitive to freezing) – which only activates during freezing conditions. “We found that SFR2 protects the chloroplast, the plant’s energy factory. We also found that SFR2 requires Magnesium (Mg) for activation,” says Christoph.

That experiment was limited to isolated proteins. “This time around,” says Rebecca, “we wanted to test SFR2 in its native context, at the chloroplast, leaf tissue, and whole-plant levels, to see if our earlier study held. And what we found was unexpected and fantastically interesting: freezing causes a rise in acidity in the cytoplasm, basically most of the rest of the cell, and SFR2 actually responds to this acidification.”

This is what Rebecca and Christoph believe happens during freezing. Normally, chloroplasts contain high levels of acidic Mg, which is kept separate from the relatively less acidic cytoplasm (pH in the diagrams).  

Figure of a normal cell

But when freezing damages cell membranes, Mg passes freely through the chloroplast into the cell, raising the cell’s acid levels. That activates SFR2.

Figure of a cell with packed organelles and leaked magnesium in the cytoplasm

The acidification trend was confirmed at the leaf tissue and whole-plant level.

Acidification as signal

“We also found out that artificially raising acid levels while maintaining normal temperatures caused the plant to perform changes that occurred during freezing, indicating that acidification is a general signal for freezing protective measures.”

“It’s like a lighthouse, which is a general sign of land and message to keep boats away. But if you take a flashlight one night and make it look like there is a lighthouse on a clifftop, boats will avoid your area.”

Towards biofuels and food security

SFR2 activity increases oil production in plant cells, although the reason is unknown. “Perhaps the plant is storing high energy compounds in anticipation of resuming normal function once freezing is over.” Interestingly, these oils are precursors for commercially usable biofuels, another area of interest to the Benning lab.

Understanding freezing responses could also help improve plant yields. “Even though our climate is getting warmer, we will continue getting cold extremes, and seasonal cold remains a critical factor for agricultural stability. For example, a study found that grasses tolerant to low temperatures were up to 59% more productive than maize in temperate areas. That gap is huge.”

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