Flowers Evolve Stench by Repurposing Detox Genes

Some plants lure pollinators not with sweet fragrances, but with the rank stench of decay. In a new study, researchers show how plants pull this off. In Asarum flowers, a gene typically used for detoxifying smelly compounds has instead evolved to produce unpleasant odors, the researchers report. The findings shed light on how plants co-opt widely conserved metabolic pathways for ecological advantage.

A key feature of foul-smelling flowers is the release of malodorous volatile compounds, particularly oligosulfides like dimethyl disulfide (DMDS) and dimethyl trisulfide (DMTS). These compounds mimic the chemical signals given off by decaying material. While it's known that these compounds originate from the bacterial breakdown of sulfur-containing amino acids, the biological mechanisms that allow flowers to produce them remain largely unknown. To explore this, Yudai Okuyama studied flowers from the Asarum genus, which display remarkable diversity in form and scent – traits believed to have evolved to lure a wide range of insect pollinators.

Through comparative genomics and functional assays, Okuyama et al. discovered that the floral emission of DMDS is linked to the expression of a gene from the selenium-binding protein family. In humans, the related protein, SELENBP1, typically detoxifies methanethiol – a compound with a strong, smelly odor that underlies clinical bad breath. It detoxifies methanethiol by converting it into less harmful substances.

In Asarum species, Okuyama et al. found three distinct types of methanethiol oxidase genes-SBP1, SBP2, and SBP3. By expressing these genes in bacteria and testing their enzymatic function, they found that SBP1 performs a unique reaction: instead of detoxifying methanethiol, it transforms it into DMDS. This ability arose through a small number of amino acid changes in SBP1, which switched SBP1's enzyme function from a methanethiol oxidase (MTOX) to a disulfide synthase (DSS). This appears to have evolved independently in at least three unrelated plant lineages, pointing to convergent evolution driven by similar ecological pressures. "It is notable that although methanethiol oxidation, the ancestral enzymatic activity, is also observed in humans, enzymatic oligosulfide synthase activity has only evolved in plants," write Lorenzo Caputi and Sarah O'Conner in a related Perspective. "This is likely to be because plants are under constant evolutionary pressure to produce complex chemistry for communication and defense."