Plant immune defenses weaken during heat waves, making them more vulnerable to insects and pathogens under climate change. HHMI scientists have now understood why high temperatures knock out a key defense system and they have developed a strategy that boosts plant immunity.
Plants that sense heat face risks beyond wilting. During heat waves, plant defenses falter, making them more vulnerable to infections and infestations. This is all the more worrying as climate change makes heat waves more frequent and intense.
“Plants actually have a very strong innate immune system which is why they have survived on Earth for so long,” says plant scientist Sheng Yang He, who is a Howard Hughes Medical Institute (HHMI) researcher at Duke University. “But now we know that this immune system may not work as well in a hot climate, especially for many crops in cool weather. Continued climate warming could exacerbate this reduction in innate immunity and increase disease and insect infestations in the future.
His team has uncovered new clues as to why heat saps plant immunity. This allowed them to find a genetic solution to keep a key plant defense system online during periods of heat, the researchers report on June 29, 2022, at Nature.
Plant immune function requires the hormone salicylic acid, which helps coordinate the defenses that plants raise or lower. But smothering plants slow their production of salicylic acid, and researchers aren’t sure why.
He and his colleagues grew up Arabidopsis, a model plant and cousin of cruciferous vegetables, allowing plants to thrive in pleasant temperatures for four weeks before turning up the heat for a few days. Then they infected the plants with a pathogenic bacterium and observed that the hot plants had much lower levels of salicylic acid than the infected plants that had escaped the heat wave. Expression of plant genes allowed the team to discover regulatory genes that could be responsible for the lackluster production of salicylic acid in plants.
To determine which gene was the kingpin of salicylic acid, the team spent many years growing various transgenic or mutant plants. Each expressed a hijacked candidate gene to retain it during high temperatures. Eventually, He’s team landed on a gene called CBP60g, which was surprisingly far upstream of salicylic acid production. But the team still didn’t know why he collapsed in the heat.
“Plants actually have a very powerful innate immune system which explains why they have survived so long on Earth.”
Sheng Yang He, HHMI Investigator at Duke University
So he and his colleagues sifted through the gene’s known transcription factors and coactivators, exhausting all possibilities. None were found to be involved in the temperature sensitivity of CBP60g expression. “We were about to give up,” he says. But then immunologist John MacMicking published an article last year in Nature which provided a new clue to the puzzle. MacMicking, an HHMI researcher at Yale University, and colleagues have reported a new protein condensate, a bead of concentrated proteins formed by a process called phase separation, involved in the regulation CBP60gis expressed and produces salicylic acid upon infection. Therefore, he and MacMicking began a collaboration to investigate CBP60g’s role in loss of immunity under hot temperatures.
This protein bubble is located at CBP60gand appears to be essential for transcription, perhaps because it concentrates the molecules needed to start the process, he says. Such phase-separated structures, which resemble organelles yet self-assemble without a lipid bilayer membrane, have been studied in animals for more than a decade. But they have only been examined more closely in plants in recent years, MacMicking says. “It will be a very exciting time for plant biologists,” notes MacMicking. Protein condensates can be involved in germination, flowering and growth. And it seems that they can form, perform their tasks, and then disassemble. We must now revise our notion of the composition of a cell, he says.
His team found that their infected plants developed fewer protein bubbles at high temperatures. It’s still unclear exactly how heat-sensitive these condensates are during transcription, so He’s team found a workaround to jump-start salicylic acid production.
The researchers grew more transgenic plants, this time replacing CBP60g‘s promoter with a switch that was not temperature sensitive. This left the salicylic acid system still activated. And they discovered that the elevated immune response came with a trade-off: These plants sacrificed growth and produced smaller leaves.
Farmers don’t want stunted plants, so the team then turned to a promoter developed in 2017 by Duke University plant scientist Xinnian Dong, who is also an HHMI researcher. Dong’s swollen switch only turns on when infected. This allowed the Arabidopsis to have her salicylic acid defense at the ready, but only deploy it when attacked. This strategy also worked with rapeseed cultivation.
“There is great promise that plants can be engineered to preserve immunity in warmer conditions,” says Jian Hua, a plant biologist at Cornell University who was not part of this work. Understanding how other environmental factors affect plant immunity can help researchers develop more resilient plants, she says. “This work is a great example of fundamental research translating into an impactful solution to address climate change.”
His collaborators are currently testing the plants with the modified genes in the field. All plants have CBP60gso he and his colleagues want to figure out how to edit plant genes with CRISPR to alter the endogenous of plants CBP60g Genoa. Ultimately, the goal, which will take on a community of plant scientists, is to give plants an edge as new threats, from increasing droughts to new pathogens, arise.
Jong Hum Kim et al. “Increasing the resilience of plant immunity to global warming.” Nature. Published online June 29, 2022. doi: 10.1038/s41586-022-04902-y