Saitama University clarifies the moment when plants perceive 'smell': Collective defense response in preparation for attack

A research group led by Graduate Student Yuri Aratani, Postdoctoral Fellow Takuya Uemura, Graduate Student Takuma Hagihara, and Professor Masatsugu Toyota, all of the Graduate School of Science and Engineering at Saitama University, in collaboration with Professor Kenji Matsui of the Graduate School of Sciences and Technology for Innovation at Yamaguchi University announced that they have successfully visualized calcium (Ca²⁺) signals generated when neighboring plants sense the 'smell' of injured plants. Using the Arabidopsis plant, which has a biosensor gene that glows bright green upon binding with Ca²⁺, the research group found that the molecular components released from grass when it is injured (e.g., by human mowing activity) are sensed by the plant approximately 1 minute after volatilization. The plant then generates Ca²⁺, triggering a collective defense response in preparation for further attack. The results were published on October 17 in the international journal Nature Communications.

Although there have long been reports of plant-plant communication, how they perceive 'smells' had yet to be clarified. The research group took advantage of the fact that fluorescent biosensors glow brightly when the intracellular Ca²⁺ concentration increases. Arabidopsis, which expresses a fluorescent biosensor, was used to visualize the same sensory signal generated in plants. When the 'smell' released from a tomato plant damaged by larval feeding was sprayed onto an Arabidopsis plant, the leaves of the plant began to glow brightly, one by one.

An analysis of various green leaf volatiles, terpenes, and jasmonic acids released by plants also revealed that (Z)-3-hexenal and (E)-2-hexenal (leaf aldehydes belonging to green leaf volatiles) generate both electrical and Ca²⁺ signals, and that Ca²⁺ signals are required for the expression of stress-related defense genes.

Analysis at the cellular level revealed the same Ca²⁺ signal being generated in the stomata approximately 1 minute after the green leaf volatiles began to diffuse into the air. The signal then appeared in the mesophyll cells, and after approximately 5 minutes, in the epidermal cells.

The green leaf volatiles released by plants upon being eaten by insects are taken up by the stomata of the leaves of nearby plants. These volatiles are speculated to increase the plant's resistance to insects by triggering Ca²⁺ signal generation in mesophyll and other cells.

Toyota commented, "Experiments with volatile substances are easily affected by the temperature and air currents in the laboratory, so we need to carefully determine the conditions to obtain stable results. Ms. Aratani spent more than 3 years building a microscope system to visualize the moment when plants exchange information with each other using volatile organic compounds. Plants do not have a sense of smell, but they must have receptors that sense volatile organic compounds. In the future, we hope to understand how plants sense such 'smells.'"

Journal Information
Publication: Nature Communications
Title: Green leaf volatile sensory calcium transduction in Arabidopsis
DOI: 10.1038/s41467-023-41589-9