Flower odors that deceive and attract insects: Enzyme evolution occurred independently in three plant genera — National Museum of Nature and Science and others

Flowers that attract insects with the smell of rotting meat so they will carry pollen have been found to have evolved odor-related enzymes independently in three different plant genera, according to research by a group from the National Museum of Nature and Science and other organizations. The evolution occurred through the substitution of just two or three amino acids. The mechanisms of odor production have been clarified at the genetic level, suggesting this could serve as a representative example of "convergent evolution" in future biology textbooks.

Rafflesia and titan arum (Amorphophallus titanum), which bear giant flowers in Southeast Asia, deceive insects with the smell of rotting meat and lure them into their flowers. Insects that move around inside the flowers get pollen on them, and when these insects are attracted to other flowers, they carry out pollination. This is a typical example of biological mimicry called "carrion mimicry" and is a research topic in biological evolution. However, understanding how carrion mimicry evolved in plants requires comparative studies between closely related species that include both those that perform carrion mimicry and those that don't, and it is difficult to find such plant groups.

Senior Researcher Yudai Okuyama, who studies evolutionary biology at Tsukuba Botanical Garden in the National Museum of Nature and Science and his colleagues focused on the varying intensity of odors among 50 endemic Japanese species of the genus Asarum. After confirming that the source of the foul odor was dimethyl disulfide, which contains two sulfur atoms and a methyl group, they conducted transcriptome (total expressed gene) analysis on flowers from 26 species and 30 accessions of Asarum to determine which genes were highly active in each accession.

As a result, they discovered two genes involved in sulfur metabolism. When they produced recombinant proteins from these two genes, they found a protein called "SBP" consisting of approximately 500 amino acids. Functional analysis revealed that it had the enzymatic activity to produce dimethyl disulfide, the source of the odor.

The SBP enzyme, which appears to produce the odor source, had three subtypes based on differences in amino acid sequences. One of these had the same function as enzymes found in animals including humans and bacteria. Okuyama and his colleagues created a phylogenetic tree from SBP gene sequences, including not only Asarum (which belongs to the Aristolochiaceae family) but also Asarum Simile, Symplocarpus renifolius, Euroya japonica, and Amorphophallus titanum, which belong to different taxonomic groups at the family level but also produce malodorous flowers.

Tracing the evolutionary process of the genes revealed that gene duplication resulted in two SBP genes within the genome, with one SBP apparently changing to synthesize dimethyl disulfide. Comparison of SBP subtypes showed that the ability to synthesize odor or not was determined by differences in just two or three amino acids, with independent evolution occurring in each malodorous flower.

From these results, the evolutionary pathway to malodorous flowers appears to be limited, and the three plant groups that independently evolved malodorous flowers can be interpreted as having acquired enzymes with identical functions through exactly the same process.

Okuyama stated: "We have clarified the evolutionary mystery of how flowers came to produce 'foul odors' down to the molecular level and further demonstrated that the biosynthetic mechanisms for these foul odors represent molecular convergent evolution. This reveals a very clear example of the evolutionary mechanisms by which organisms acquire new abilities. I believe this is a result worthy of inclusion in textbooks."

The research was conducted in collaboration with the National Institute of Genetics, the University of Tokyo, Showa Medical University, Nagano Environmental Conservation Research Institute, the University of Miyazaki, Tohoku University, the Research Organization of Information and Systems Database Center for Life Science, Ryukoku University, and Keio University, with support from the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research and the Japan Science and Technology Agency (JST) Strategic Basic Research Programs. The results were published in the American scientific journal Science on May 8.