Volatile signal in plants activates defense and inhibits growth processes

An international research team, including investigators from the Max Planck Institute for Chemical Ecology, has performed a new study that revealed that Arabidopsis thaliana plants create beta-cyclocitral when attacked by herbivores, and also demonstrated that this volatile signal suppresses the pathway of methylerythritol 4-phosphate (MEP).

Volatile signal in plants activates defense, inhibits growth processes
Feeding by herbivores not only causes plants to produce defense compounds, but also leads to a slowdown in growth processes. Cleavage of beta-carotene (a photosynthetic pigment) via reactive forms of oxygen (ROS = reactive oxygen species), forms beta-cyclocitral (βCC), which directly inhibits the rate-controlling enzyme of the MEP pathway located in the chloroplast. Image Credit: Kimberly Falk, Moves Like Nature.

The study has been published in the PNAS journal.

The MEP pathway is crucial in the processes of plant growth, like the synthesis of pigments for photosynthesis. Not only does the beta-cyclocitral down-regulates the MEP pathway but it also improves the plants’ defenses against herbivores.

Furthermore, since the MEP pathway is found only in microorganisms and plants but not in animals, a better understanding of a signal molecule, such as beta-cyclocitral, offers new opportunities for developing antimicrobial agents or herbicides that inhibit the MEP pathway.

Trade-offs between defense and growth processes in plants

For a long time, scientists have known that plants have limited resources, which they can invest in reproduction and growth or use them to defend themselves from enemies, based on their environmental conditions. Several studies have previously demonstrated that when plants are attacked by insects, they increase their defenses by producing, for instance, inhibitors of digestive enzymes or toxins that harm their enemies. But scientists have limited knowledge on how the growth processes in plants are affected by herbivore attackers.

We wanted to investigate how herbivory might affect photosynthesis and the methylerythritol 4-phosphate (MEP) pathway, a pathway making metabolites for growth that is directly supplied from photosynthesis.”

Sirsha Mitra, Study First Author and Assistant Professor, Savitribai Phule Pune University

Mitra began working on this study at the Max Planck Institute, and she is currently an assistant professor at Savitribai Phule Pune University in Pune, India.

For many years, the MEP pathway has been a topic of research at the Max Planck Institute for Chemical Ecology in Jena, Germany.

The MEP pathway makes the building blocks for plant isoprenoids or terpenoids, a very large family of plant metabolites involved in growth, defense, and signaling.”

Jonathan Gershenzon, Study Author and Head of Department of Biochemistry, Max Planck Institute for Chemical Ecology

Beta-cyclocitral activates defense and inhibits growth

The international team of researchers, which also involved associates from the Universitat Ramon Llull in Barcelona, Spain, the Technical University in Lyngby, Denmark, and the University of Toronto, Canada, showed that when plants, belonging to the thale cress Arabidopsis thaliana species, were fed to caterpillars of the African cotton leafworm—a generalist feeder that attacks several different species of plants—they tend to increase their defenses and, at the same time, reduce their growth processes.

Using a wide range of methods from analytical chemistry and molecular biology, and also caterpillar bioassays, the researchers were able to demonstrate that a certain volatile compound, called beta-cyclocitral—created by the cleavage of beta-carotene as a result of a reactive form of oxygen—accounts for this change in resources.

Although beta-cyclocitral serves as a chemical signal to boost defenses, it also reduces the formation of compounds in the MEP pathway by directly suppressing the rate-regulating enzyme of the MEP pathway.

Of particular importance to our study was the exposure of plants to isotopically labeled carbon dioxide (13CO2) instead of the dominant atmospheric carbon dioxide (12CO2). Carbon dioxide is easily introduced into the MEP pathway via photosynthesis. This allowed us to track how the metabolic flux in the MEP pathway changed when plants switched to a defensive mode after herbivore attack and beta-cyclocitral slowed down the MEP pathway.”

Louwrance Wright, Study Co-Lead Author, Max Planck Institute for Chemical Ecology

Wright is currently working in South Africa.

Caterpillars that feed on plants treated with beta-cyclocitral showed reduced growth when compared to caterpillars that feed on untreated plants. This fact further demonstrates the significance of this volatile signal in plant defense.

Potential benefits in agriculture and medicine

When plants are attacked by enemies, they may have to halt their growth processes to discharge adequate resources for their defense. Beta-cyclocitral signaling is a kind of mechanism that accurately regulates this change in resources. Hence, beta-cyclocitral, or a more stable derivative, could be used on crops to trigger defenses during the outbreak of pests.

Since the MEP pathway is found in all plants and many microorganisms, but not in animals, it is of particular interest for the development of herbicides, as well as drugs with antimicrobial activity,” added Gershenzon, describing the possible applications of this study.

Additional analyses in India will currently examine whether beta-cyclocitral can boost insect resistance in crops, including tomatoes, and whether it communicates with other familiar defense signals.

Source:
Journal reference:

Mitra, S., et al. (2021) Negative regulation of plastidial isoprenoid pathway by herbivore-induced β-cyclocitral in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America. doi.10.1073/pnas.2008747118.

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