When you smell the roses, do they smell you back?

When you smell the roses, do they smell you back?

Scientists have found that plants like Canada goldenrod deploy defenses against insects on scent

Because most plants are firmly rooted in place, they have to adapt to whatever Mother Nature throws at them. As a result, they have become the armored tanks of nature, evolving sophisticated defensive systems to take on all comers.

One of the most widespread is the inducible defense system, a suite of responses that are only turned on when plants sense danger, such as when they feel the footsteps of an insect on their leaves. In addition to touch, researchers have shown that plants are always listening, feeling, and tasting their surroundings to gather as much intel as possible.

The lines between these senses are blurry for plants – they don't have the organ systems we associate with them. But a new study published recently in Nature Communications shows that, without noses or brains, plants can even smell: they are somehow are able to sense, identify, and react to the odor of their predators.

It was only in 2013 that Anjel Helms and her colleagues, all from the Department of Entomology at Penn State, reported the first, and so far only, case of a plant responding to an insect-derived odor. Canada goldenrod exposed to air contaminated by an insect predator, the goldenrod gall fly, were often passed over by flies looking for a place to lay their eggs. In line with this, plants exposed previously to gall fly odor also suffered less leaf damage than plants that had not encountered the stink. Somehow, plants that processed the same air as the flies were less desirable prey

A male gall fly on its host plant.

 Ian Grettenberger

To try and find out how Canada goldenrod did this, the gang from 2013, with a few reinforcements, got back together to delve deeper. And they found that the plants were able to pick up on tiny, tiny amounts of odors produced by flies, and use that cue to rally their anti-predator defense mechanisms.

The first step in understanding how plants used airborne signals to prepare for the attack of the flies was to figure out exactly what it was about eau de gall fly that sent the plants into such a tizzy. To do this, the researchers needed a lot of air that smelled like flies, so they stuffed 90 male flies into a bachelor pad (a small, glass chamber with a filter to trap airborne compounds) and let them stew overnight.

When the gas mixture was analyzed, they realized that while there were almost 20 different fly odors, only three chemical compounds made up more than 95 percent of the blend – E-conophthorin, the alcohol 1-nonanol, and a less stable form of E-conophthorin. Conophthorin is a spiroacetal, a class of organic compounds that are common in nature and have a variety of biological effects. 1-nonanol is similar to ethanol (it can even cause similar symptoms as drunkenness when consumed). It was probably one of these more abundant compounds, reasoned the scientists, which plants keyed into as a reliable cue for fly invasion.

The team exposed plants to the complete gall fly emission blend (containing all the compounds), and synthetic versions of their candidate signal compounds (E-conophthorin, 1-nonanol, and two organic compounds with a similar structure to E-conophthorin), before releasing predatory flies. After 24 hours, they checked up on the plants to see how they were doing. As expected, exposing plants to the full gall fly scent led to reduced levels of leaf damage when encountering flies. Only E-conophthorin produced a similar result to the unadulterated fly smell, leading the researchers to conclude that the plants used it to sniff out predatory flies.

This counterattack strategy helps plants save energy by only upping their defenses when attacks are imminent, and helps them fine tune their responses to very specific triggers. Inducible defense systems are extremely common in the plant world, and the counterattacks can take a variety of forms. One of the most elaborate belongs to the tobacco plant, which releases a specialized SOS signal when attacked by caterpillars that attracts predatory, caterpillar-eating bugs.

Other systems are much less complicated. For example, plants may accumulate bitter compounds in their leaves, or release insecticides when they sense damage to their leaves. The researchers hypothesized that perhaps the active ingredient in gall fly scent, E-conophthorin, induced some sort of defensive response in the goldenrod plant, and looked for evidence to support this. They found it in another compound, the plant hormone jasmonic acid, which accumulated in the leaves of plants exposed to the full gall fly stench blend or to E-conophthorin.

Jasmonic acid is involved in a number of physiological functions, including growth, immunity, and stress responses. One of its most interesting effects is that it causes the release of proteins that neutralize the digestive enzymes in insect saliva. This perhaps explains why plants received the signals for an impending attack mitigated leaf damage – the flies were not able to breakdown their leaf tissue as easily. This response was extremely sensitive – as little as a 10 percent dose of compound was enough to induce big changes in leaf damage, and the more signal plants received, the more jasmonic acid they accumulated.

Plants are able to smell, at least in some capacity, and use this newly characterized scent much like humans. (What’s the first thing you do when you find a questionable carton of milk in the back of the fridge? Much safer to smell it before tasting!) They sniff around and use that information to warn them about dangerous situations.

But there are still a lot of things we don’t know, like how far this sense of smell goes in an evolutionary sense: is it just a neat quirk of the Canada goldenrod to detect its co-evolved arch-nemesis? When you stop to smell the roses, do they smell you back? With the advent of new gene editing technologies like CRISPR, we may even be able to use harvest the olfactory abilities of to increase agricultural productivity by bumping up natural plant defenses.

Plants are a lot smarter than we give them credit for – and they understand a lot more about the world than we think. They are masters of survival, and keep surprising us with their advanced, innovative, and almost-human solutions to an evolutionary arms race that has been waged for millions of years.

Peer Commentary

Devang Mehta: This illustrates just how alien plants are to the other kingdoms of life. 

A few years ago, I heard a talk by Ian Baldwin, another scientist working on plant perception, where he described how plants were able to communicate the presence of herbivores solely by releasing chemicals into the environment. It stands to reason, then, that they can also detect chemicals released by insects and other predators. But actually learning this biochemical language is incredibly hard, and it’s amazing that in this study the researchers could narrow the signals down to three molecules. 

A word of caution though: many plant scientists find the idea of plants “communicating,” “remembering,” or “smelling” controversial. A lot of this is just semantics, since these terms are usually used to describe behavior occurring through the action of neurons, which plants obviously lack. 

However, we keep finding out that plants have gotten around the challenges of being fixed organisms in a world of mobile predators and scarce resources by using chemistry (instead of sophisticated cell biology, like animals have) in fantastic ways, including as shown here, by smelling and repelling insects. 

I also find the potential for agricultural innovation here exciting. If we could learn the biochemical cues used to repel crop pests, we could use these specific chemicals instead of toxic insecticides to protect our plants without causing as much wide-spread disruption to farming ecosystems. 

Cassie Freund: I'm still a skeptic about how this might scale out in nature. Plants do a lot more than we give them credit for, yes, but lab-based studies where plants are exposed to chemical compounds in close quarters are not necessarily good measures of how things work outdoors. There, a lot of other variables might interfere with signaling, like temperature and wind. 

And, how "expensive" are these defense compounds to make (in other words, how many resources do they require)? Resource limitation is huge for plants so I can imagine that, while this ability may be useful in the short-term, over the lifetime of a plant it may be more advantageous to accept a little bit of herbivory if the resources it takes to manufacture defense compounds could be better used in making seeds or growing more leaves. 

I wonder what the results of this study would look like if they studied the plants over a longer time scale. It's an interesting line of research, but I think much more needs to be done to answer basic questions about how plants sense their environments. 

Arunas Radzvilavicius: The authors of the original study believe that the plant becomes more resistant after 'smelling' the substance, conophthorin. But something to consider is that it's a well-known sex attractant in some insect species, and a strong repellent in others. I was left wondering if it could be a direct reaction of the flies to the smell of conophthorin that made them feed less, and not the plant's defenses?