Secret Code Mends Troubled Relationship

Kobe University

A plant uses a rare scent to guide its pollinator to male flowers first and to female flowers later. The Kobe University study uncovers a precise chemical system that not only keeps this partnership specific but also helps ensures it remains beneficial to both parties.

Many plants recruit insects to carry pollen from flower to flower, and in return some offer a part of their body as a brood site for the insects' young. Take for example the climbing plant Smilax insularis, growing on islands from Okinawa to Taiwan. Recently it was found that a gall midge, Dasineura heterosmilacicola, lays its eggs into the male flowers and carries pollen from the male to the female flowers, while the developing larvae in the male flowers feed on surplus pollen. This system constitutes a classic example of what biologists call " brood-site pollination ." Kobe University botanist SUETSUGU Kenji says: "The larvae were reported only in male flowers. So how do the female plants remain part of the system? And what keeps the system specific to this insect? I felt there must be some hidden mechanism governing this interaction."

Biologists have been discussing that a "private channel," an unusual odorant that is sent and received by only the intended partners, might be at work in some such relationships. However, field studies that explicitly search for such secret codes have been rare. "Our group is in a special position to tackle this issue. We are willing to spend the time needed to search an obscure plant and observe it for long periods across five islands. So, we have the field perspective, but we also have collaborators who can synthesize candidate compounds so we can test them under natural conditions. Connecting such very different approaches is why we are able to move from a fascinating observation to understanding its mechanism," explains Suetsugu about his group's research approach.

In the journal Current Biology, the Kobe University team now publishes that they identified dihydroedulan I as the main component of Smilax's scent, a rare compound not previously known as the dominant floral scent component in any plant, and that it is also able to attract the gall midge specifically. No other insect was attracted by the chemical in their field tests, and if the chemical was even just slightly different, for example, twisted in different ways, the gall midge could also not be attracted. "It is a private chemical password," remarks Suetsugu.

Crucially, the same chemical is emitted by both the male flowers and the female flowers, but at different times of the day. The male flowers containing the pollen open and emit the scent in the early morning, attracting the insects. And while the female insects stick their abdomens into the flowers to lay eggs, they collect the pollen. The female flowers open only a few hours later, in the late morning up until around noon. The insects, attracted by the same scent, again stick their abdomen into the flowers, depositing the pollen, but only rarely lay eggs.

We don't know exactly which cues cause the midges to avoid laying eggs in female flowers. Likewise, when larvae do occur in female flowers, they do not consume developing seeds, and the reason for this is also still unclear. What is clear, however, is that the scent common to male and female flowers and released at slightly different times promotes reliable pollen transfer and so keeps the female flower as part of the system. Suetsugu says: "I am really excited about this combination of chemical precision and ecological balance. One more thing I want to cover in future studies is how Smilax can produce a floral scent so strongly dominated by one compound, especially since this particular one may originally have functioned as an insect repellent. If we can thus connect ecology, behavior and biosynthesis, we will be much closer to understanding how plants evolve what is essentially a chemical language only the right partner can read."

This research was funded by the Japan Society for the Promotion of Science (grants JP25H00944, JP24H01749) and the Japan Science and Technology Agency (grants JPMJPR21D6, JPMJPR21D3, JPMJFR2339). It was conducted in collaboration with researchers from Chiba University and the University of Tokyo.

Kobe University is a national university with roots dating back to the Kobe Higher Commercial School founded in 1902. It is now one of Japan's leading comprehensive research universities with over 16,000 students and over 1,700 faculty in 11 faculties and schools and 14 graduate schools. Combining the social and natural sciences to cultivate leaders with an interdisciplinary perspective, Kobe University creates knowledge and fosters innovation to address society's challenges.

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