Researchers studying thale cress plants have discovered that the microbiome, a collection of benign bacteria that live in and on the plant, stimulates a common immune response that helps train the immune system to combat harmful pathogens.
The findings, published Monday in Nature Plants, could have implications for protecting crops against pathogens, which, together with pests, cost the global agricultural industry $540 billion per year.
"Although these microbes are harmless and not pathogenic, the plant mounts a common response, [which] is important for later encounters [with] pathogens," said senior author Julia Vorholt, a professor of microbiology at ETH Zurich.
In addition to its implications for plant health, the study also identified an interesting parallel between plant and human immunity. Just after birth, humans start to play host to millions of harmless bacteria that impact the number of white blood cells in the body and also help train the immune system to combat malicious infections throughout life.
Plants also host a microbiome, which "may have beneficial functions for the plant that are currently not well understood," according to Vorholt. Despite a growing understanding of the human microbiome, only recently have researchers turned to the microbes on plants to gain insights into their biology.
"Plant biology needs to embrace the microbiome," she said.
The researchers conducted an exploratory study with a set of 39 endogenous bacterial strains found on the leaves of Arabidopsis thaliana, the thale cress. This species has proved to be an ideal model organism in plant biology because, while it is small and easy to grow, it is closely related to economically important plants, such as turnip, cabbage, broccoli and canola.
"I am convinced that our findings can translate to other plant species, including crops," Vorholt said. "The plant immune system is conserved across plants, and also, the microbiota of different plants resemble each other."
The team wanted to know how the plant would respond to each of the individual bacteria in the lab, which required growing nearly 4,000 plants to get a dataset comprehensive enough to draw conclusions. The researchers compared the gene expression and presence of certain metabolic compounds in the experimental plants to those that had never encountered any bacteria.
The researchers found that across all 39 strains, there was a common group of genes that were activated in the plant by the presence of the bacteria, forming a response that the team called the "general non-self response," or GNSR.
"The name reflects that the plants respond to 'non-self,' as the GNSR is only induced when they are colonized by a microbe," Vorholt said.
The team was also able to compare this general response to previous data about the response of plants to pathogens to determine whether the GNSR also occurred when plants got sick, an important step in applying the findings to solving practical problems.
"The analysis clearly indicated overlap in the response," Vorholt confirmed.
The last piece of the puzzle was determining whether the GNSR was in any way involved in the plant defending itself against pathogens. The team used Pseudomonas syringae, a model bacterial strain that has been used in thale cress studies for decades. Originally associated with tomato plants, this species is now known to infect a wide variety of plants, causing fruit damage, leaf destruction and bud death.
The researchers found that plants that lacked even part of the GNSR genes were significantly more vulnerable to the Pseudomonas.
"This suggests that the GNSR constitutes an adaptive defense strategy triggered by the plant microbiota," Vorholt said.
That means the harmless bacteria living in and on the plant indirectly protect the plant from pathogens by stimulating a protective response, suggesting that, as in humans, these bacteria are training the immune system for later battles with harmful microbes.
Now that the team has discovered the GNSR, the next step will be evaluating how the response affects the bacteria themselves. The researchers are also hopeful that insights like theirs will encourage others to consider the microbiome when studying plants.
"Plants are always colonized by [microbes], which means there are no "germ-free" plants. … We need to keep in mind that they are not organisms by themselves, but come with a microbiota that originated from the soil or other sources," Vorholt said. "We are only at the beginning of understanding the molecular basis of how plants integrate all the inputs from the environment."
The study, "A general non-self response as part of plant immunity," published May 17 in Nature Plants, was authored by Benjamin A. Maier, Patrick Kiefer, Christopher M. Field, Lucas Hemmerle, Miriam Bortfeld-Miller, Barbara Emmenegger, Martin Schäfer, Sebastian Pfeilmeier, Shinichi Sunagawa, Christine M. Vogel and Julia A. Vorholt, ETH Zürich.