Stopping to smell the roses? You're inhaling flower farts

Flowers use little protein motors to expel their fragrances

Abrahim El Gamal

Marine Chemical Biology

Scripps Institution of Oceanography

Plants famously keep our air clean using that bit of alchemy known as photosynthesis, harnessing the energy from the sun to convert carbon dioxide and water into oxygen and sugar. But did you know that 10 percent of the carbon dioxide that plants capture is actually used to make a flower's fragrance?

Scientifically speaking, fragrance is caused by "volatile organic compounds"—molecules that escape the plant as gas—hence reaching our nostrils. In addition to providing an enjoyable sensory experience for humans, these molecules serve other useful functions. They are signaling molecules that attract pollinators like birds and bees, and they trigger different life stages, such as ripening in fruits and seed-formation.

While scientists are starting to understand how these important molecules are made inside plant cells, we still know next to nothing about how these molecules exit the cell. A new study shows how they expel it. That is to say, how they fart.

Detail of The Garden of Earthly Delights, center panel, by Hieronymus Bosch

Image via Wikimedia Commons

The longstanding assumption among scientists was that plants allow volatiles to leak out of their cells passively, like air from a slowly deflating balloon. But this theory is problematic, because volatiles are actually quite toxic to plants. If allowed to linger, they would kill them, one cell at a time. So a team of scientists from Purdue University sought to reexamine the assumption. The resulting paper, published in the journal Science last month, provides for the first time a description of the cellular pump that actively helps flush volatile organic compounds out of plants.

The team, lead by biochemist Natalia Dudareva, chose to study how volatile compounds are released from petunias, because their flowers are known to release volatile compounds at specific times but not others. In petunias, the early bud stage is the time of lowest release of volatiles, while the bloom stage (when the flower opens up) has the highest volatile release. By comparing and contrasting these 'on' and 'off' states, the researchers hoped to be able to identify the cellular mechanism of volatile release.

All things in biology comes down to genetics – specifically, to what genes in an organism are turned on, and when. The Purdue scientists reasoned that if they could compare what genes were turned on in the bud stage (when no volatiles were released) to the bloom stage (the point of maximum volatile release), they might be able to zero in on which gene(s) are responsible for emitting volatile organic compounds from petunias.

To do this, they looked at how the flowers expel other, similar materials. They noted that plants use a type of transporter called an ATP-binding cassette (ABC) transporter to pump wax used as leaf coating, which repels water, out of their cells. In order to escape from a cell, the wax must first pass through a hydrophilic layer into a hydrophobic one, which they won't want to leave. Their final ticket out of the cell is through another dreaded hydrophilic layer. But if they don't cross it, it builds up and starts to loosen up the cell's membrane so that it starts to leak its innards.

Volatiles are similarly hydrophobic, and their accumulation in a cell membrane also becomes toxic to the cell. Therefore, they focused their search on ABC transporters, whose genes were most ramped up when the flowers bloomed.

With a candidate gene in hand, the researchers now wanted to check what happened to levels of volatiles in petunia cells if that gene was disrupted. So they blocked the gene of interest from being turned on. This led to a dramatic increase in the accumulation of volatile organic compounds inside the petunia cells compared to flowers in which the cells were not disrupted, providing indirect evidence that the gene impacted volatile export.

To directly demonstrate the function of the newly identified volatile pump, the researchers introduced the candidate gene into the cells of tobacco, a plant often used in plant research due to the ease of handling, and which ordinarily do not possess the volatile transporter gene found in petunias. They next treated these cells with a cocktail of the two most abundant volatile molecules produced by petunia. After the incubation period, they measured how much of the compounds were left in the cells and found that the cells with the transporters had fewer volatiles than those that lacked them. This showed that the function of the transporters could be transferred to cells that normally do not have the capacity to export volatiles produced by petunias, providing direct evidence for their function.

Lastly, the researchers revisited their hypothesis that plants lacking a means of actively transporting out the volatiles they produce fall victim to their own toxins. To this end, they again looked to the petunia cell lines with the transporters turned off, employing two different dyes as indicators of the the health of the cell membrane. The first dye was only able to enter cells with leaky cell membranes, while the second dye was able to pass through the healthy membrane, but could only pass back out if the membrane was leaky. In the first case, cells with the silenced transporter showed accumulation of the dye. In the second case, the same cells did not retain the dye. This is how Dudareva and colleagues confirmed that cells lacking a means of actively removing volatiles had compromised cell membranes.

Through a series of elegant experiments, Dudareva and her team of scientific sleuths shattered the status quo of volatile transport out of plants with implications for everything from fundamental plant biology up to the atmosphere. Maybe one day scientists will be able to use this information to program plants to spray on command like biological air fresheners, or to control the weather.

At any rate, it gives a whole new dimension to stopping to smell the roses. Or, in the words of Shakespeare: "The rose looks fair, but fairer we it deem / For that sweet odour [fart] which doth in it live."

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