Armed and Delicious.

Go to your spice rack, make a kale smoothie, have a cup of coffee. Just about everything we use to add flavor to our lives comes from a co-evolutionary battle between an herbivore and a plant protecting its leaves.

That bite on your tongue from an arugula salad? The sulfur-containing cyanide molecules you taste are the result of glucosinolates, a characteristic defense of the mustard plant family. Mustard plants—e.g. horseradish, wasabi, mustard—all use this metabolic pathway because the burning sensation, which many people enjoy with oysters, actually works as an effective anti-herbivore toxic defense. When bugs break open cells, the enzyme myrosinase cuts a precursor to release nitriles, isothiocyanates, and other various bioactive toxic compounds. Plants in a population that are slightly more toxic survive the constant herbivore attack better and can pass on their genes to the next generation. Ah, bittersweet natural selection.

How do we know it is the bugs that put the pressure on? This paper (also summarized in a great article here) swapped mustard plants from Colorado and Montana, and found that not only did the unique spice of each plant stay consistent, but bugs preferred the visiting treat—plants that did not adapt to the local suite of herbivores. The difference in plant survival in this case is an example of local adaptation, all starting from bugs preferring the new mustard spice.

Just like these bugs and everything else in nature, we choose what we eat based on the flavors we like and what won’t kill us.

So why do we intentionally eat so many compounds plants use to make feeding difficult? Often these same toxins are essential for nutrition. The darkest green vegetables, pungent garlic, soothing mint—all play a health benefit role because of the energy plants put into making defense compounds. Bioactive toxins in low doses continue to do their toxic, bad-self thing: the alkaloid caffeine in your coffee stimulates the nervous system, the indole-3-carbinole in your kale salad degrades excess hormones that can lead to cancer, and the terpenes in oak barrel-aged wine rich in phenolic tannins can prevent carcinogens from binding to DNA and reduce the risk of harmful blood clots. The underlying theme here is that many toxins are reactive, for better or for worse.

Disclaimer: Some plant defenses are toxic to humans in high concentrations, and some plants are just plain poisonous at any dose. Don’t start eating everything toxic. Instead, appreciate the nutrients plants invest in creating highly reactive compounds in order to protect themselves, as well as the coevolutionary arms race that made plants with these exciting products succeed.

Velcro: a catchy defense.

My first claim to fame in grad school was about tiny hook-shaped plant hairs.

Exciting right? You’d be surprised how a simple observation leads to better understanding the big picture. Here is the happy hour version of my first publication that helped us understand how plants use different combinations of defenses to protect their leaves from being eaten.

First, why would plants have more than one defense? Remember, plants are unlike many organisms because they make food for themselves via photosynthesis. All of the non-photosynthesizing critters also need to eat, and they do so in many different ways. Caterpillars, aphids, and fungi all see leaves as an appetizing snack, so plants respond to the chewing, phloem-sucking, and pathogen infections with an arsenal of defenses.

Releasing toxic cyanide is one way to deter picnickers. The more bugs munch and rupture plant cells, the more cell contents mix, and enzymes previously separated from precursors start producing hydrogen cyanide.

Cyanogenesis- Releasing toxic cyanide from injured cells, chemical defense.

So with such a toxic defense, why would any plant need more protection? When aphids use their stylet like a straw to pierce and suck sugar-water out of the plant’s bloodstream, they avoid the mechanism that releases cyanide. Conveniently, these same plants with unfulfilled cyanogenic potential also have tiny hooked hairs, which likely act as Velcro, trapping small phloem-sucking bugs.

Trichomes- Plant hairs, mechanical defense.

What about diseases? Fungal pathogens can also consume leaves, forming a lesion. How far the infection spreads depends on the plant’s anti-fungal defenses. Polyphenol oxidases form sheets of proteins that act as walls to quarantine the infected cells.

Polyphenol oxidases- antifungal, chemical defense, comes from the plant when needed (direct, inducible defense).

Firm edges around the outside of a lesion indicates such a defense is working to stop the infection from spreading. When this process is lacking or interrupted, the infection appears faint, and spreads into the leaf’s veins. This is how my advisor and his team noticed the physiological tradeoff in lima bean plants between polyphenol oxidases and cyanogenesis. Cyanide is toxic because it interrupts many enzymes that allow our mitochondria powerhouses to function. Releasing cyanide also breaks down other enzymatic functions, such as this anti-fungal defense compound. So plants with lots of cyanide are vulnerable to fungi, while plants with less cyanide are vulnerable to herbivore attack, but are protected against disease. Here we begin to see relationships among these traits, and in this case, two defenses tradeoff.

Why are tradeoffs so fascinating to scientists? Because tradeoffs limit adaptation.

Plant defense is widely considered to limit adaptations in growth or reproductive traits because defense compounds cost the plant resources and energy. The solution many plants find to balance this dilemma is to use varying defense strategies and call for help. Predators scare off or attack the plant’s enemies by following plant cues or rewards. Nectar is typically associated with pollination, but many plants also produce extrafloral nectar: droplets of nectar designed to attract ants and other predatory bugs.

Extrafloral nectar- sugary liquid to attract carnivorous bodyguards (usually ants), indirect defense.

Plants under attack can turn up the production of volatile organic compounds, which serve many functions, one of which is attracting wasps that parasitize and kill the source of damage by laying eggs in the herbivore.

Volatile organic compounds (VOCs)- Chemical cues floating in the air to attract parasitoid wasps, indirect defense.

Traits that show up together in the same plant form a defense syndrome. Syndromes tell us which combinations of defenses help plants survive better, and which adaptations work best in concert. I assembled the defense syndromes for wild and cultivated lima beans to see how the tiny hook-shaped hairs fall into the big plant-protection picture. Two patterns emerged: 1. Plants with many trichomes also have lots of cyanide, and 2. Plants with low cyanide and fewer trichomes produce more extrafloral nectar and VOCs.

Why does this matter?

The tradeoff between direct chemical defense and indirect defense is well complemented by mechanical defense in the existing defense syndromes. As a plant, if your strategy is to be toxic, but some bugs can avoid the toxic effects, it makes sense to have a Velcro-like surface so it is harder to move around or even get to the plant to feed. If your strategy is to call for help, having a tricky surface to navigate hinders the protective ability of the predators that come to the rescue.

Therefore, chemical and mechanical defenses co-vary in lima bean, which ultimately tells us how different kinds of defenses work together to minimize munching.

-A