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A plant hormone and growth in the dark

All multicellular organisms, including plants, produce hormones. One of the hormones plants produce is the phytohormone jasmonic acid, which has for a long time mainly been known as a second messenger substance that is released when plants are attacked by pathogens. Some years ago, Dr. Michael Riemann from the Karlsruhe Institute of Technology (KIT) discovered that jasmonic acid acts as a major growth regulator of phytochrome-mediated responses in plant seedlings. What is the molecular relationship between the photoreceptors of plants and the jasmonic acid system? This is one of several questions Riemann’s team is trying to solve. The botanists from Karlsruhe use rice, the staple food of many people around the world, as a model plant. Riemann’s research might lead to new biotechnological strategies to make rice varieties more resistant to pathogens and disease as well as increasing their yield.

Wild-type seedling (left) and two mutant seedlings that have been under constant light and have grown a very long coleoptile. © Dr. Michael Riemann

While he was doing his doctoral thesis, Michael Riemann discovered a strange phenomenon. He was working with a rice mutant whose seedlings behaved in the opposite way to wild-type rice seedlings. In soil (darkness), a normal rice seedling always grows upwards against the force of gravity (geotropic reaction) for several days. During its upward growth, the seedling's coleoptile, the pointed protective sheath covering the emerging shoot, elongates and expands. Upon the perception of light when the coleoptile reaches the surface, it stops growing and breaks along a predetermined seam. The first leaves then penetrate the top of the coleoptile. "Everything happens in a mirror-inverted way in the mutant we have investigated," said Riemann who has since received his PhD and now heads up a team of researchers at the Karlsruhe Institute of Technology (KIT). "When the mutant is kept in darkness, the coleoptile does not grow at all. It only starts to grow when it detects light. " A much greater surprise still was the discovery of a defect that caused this mirror-inverted behaviour. Riemann's team had originally suspected that auxin played a role in this process since it has been known for a long time that this phytohormone plays an essential role in light-dependent plant growth. The researchers then discovered by pure chance that their rice mutants did not produce jasmonic acid.

A molecule and the global hunger problem

Jasmonic acid is a plant hormone (phytohormone). Plant cells that are attacked by insects, for example, release jasmonic acid. This hormone then induces a complex defence reaction against the insect in the environment of the wound. The defence against pathogens is the most important function of jasmonic acid and numerous groups of researchers are focusing on this topic. However, jasmonic acid has many more functions: For example, as a volatile pheromone it is involved in plant communication and also triggers the release of pollen from stamina. In addition, jasmonic acid also induces measures to counteract abiotic stress (e.g., high salt content of the soil). “It has previously not been known that jasmonic acid also plays a role in the photomorphogenesis of rice seedlings, i.e. the light-controlled growth,” said Riemann referring to a discovery that might also be of interest to industry despite the fact that Riemann and his team are currently mainly focusing on basic research. As far as rice, which is the most important staple food for a large part of the world’s population, is concerned, the understanding of the relationship between pathogen defence, light-controlled growth and survival strategies of plants grown in oversalted soil might be of great importance, for example in the attempts to make the plants more resistant to pathogens and disease and produce higher yields. It is assumed that jasmonic acid is the molecular interceptor of these three signalling systems.

Scanning electron microscope image of a seedling exposed to light in which the coleoptile has opened. © Dr. Michael Riemann

After making their discovery, Riemann and his team went on to search for mechanisms that were responsible for the strange behaviour of their mutant rice seedlings. In cooperation with partners from Japan, who have the devices and know-how for carrying out special mutation analyses in rice (so-called map-based cloning), the researchers discovered several defective genes in the mutants. "The genes we discovered are all involved in the biosynthesis of jasmonic acid or in the network of signals that controls the phytohormone's function as second messenger," said Riemann who spent some time in Japan working with his collaborators. The results of the mutation analyses are soon to be published. But the question as to why the coleoptile of the rice mutants that do not produce jasmonic acid does not grow in the dark as it should but only when exposed to light still needs to be answered. What is the role of jasmonic acid in the molecular processes that regulate the correct growth and breaking up of the coleoptilde?

Suicide for correct growth?

Riemann and his team are carrying out a number of projects to try to come up with answers to these questions. One of the hypotheses the team is working on concerns the breaking up of the coleoptile. “We assume that this has something to do with programmed cell death,” said Riemann. “When exposed to light, we assume that jasmonic acid is activated and induces the cells of the predetermined rupture site to undergo apoptosis.” However, the researchers still need to prove their hypothesis. In addition, Riemann and his team are interested in the biochemical steps that are necessary for jasmonic acid to be turned into an active form. Jasmonic acid is known to be a precursor of molecules with a signalling effect. Which enzymes are necessary to turn jasmonic acid into an active form? What exactly do the enzymes do? A completely new project, which is not directly related to investigating light-induced growth, looks into the role of jasmonic acid in plants grown in oversalted soils. Are there mutants that are more or less effective in dealing with salt stress than others? Does this knowledge help us gain more detailed insights into the molecular mechanisms used by plants to protect themselves against abiotic stress?

One of the LED fields to which the rice seedlings are exposed and which the Karlsruhe researchers can use to simulate different light conditions. © Dr. Michael Riemann

Riemann's team owns a mutant collection that is used to propagate seeds in cooperation with the Karlsruhe botanical garden. The team's Japanese collaboration partners deal with the sophisticated analysis of hormones to determine the very small phytohormone concentrations in plant samples. The Karlsruhe researchers carry out experiments on the regulation of genes in the seedlings. They can also produce recombinant proteins, extract RNAs, test enzymes and carry out microscopic analyses. Using LED lamps, the researchers can manipulate the light conditions under which the rice seedlings are grown. For example, they use the lamps to simulate the darkness of soil or daylight conditions. These experiments provide the researchers with information as to which genes and enzymes are activated under which conditions. Riemann's team consists of four scientists. "But we are very well integrated in the Institute of Botany at the KIT," said Riemann. "Many of our projects have thematic aspects in common with the projects of other teams and we support each other wherever we can."

Further information:

Dr. Michael Riemann
Institute of Botany - Dept. 1 Molecular Cell Biology
Building 10.40
Kaiserstr. 2
76131 Karlsruhe
Tel.: +49(0)1522/1965500
E-mail: Michael.Riemann(at)bio.uni-karlsruhe.de

Website address: https://www.biooekonomie-bw.de/en/articles/news/a-plant-hormone-and-growth-in-the-dark