Plants with Benefits

Maintaining relationships, even great ones, can be challenging.

Some plants juggle multiple relationships ALL of the time.

Think of an organism that does something helpful for a plant. Bees, hummingbirds, and other pollinators may come to mind. But plants also recruit toucans, black bears, and other seed dispersers as well as predatory insects such as ants and wasps for defense.

And then there are microbes.

My goal for this research paper was to show how one microbe in particular, nitrogen-fixing bacteria called rhizobia, can alter a plants’ entire network of relationships—from the bottom-up.

Rhizobia live inside nodules on plant roots in a tight-knit symbiotic relationship, exchanging fertilizer for sugars from photosynthesis. Plants that form this relationship benefit immensely from the nitrogen, but providing sugar in return can tax the plant.

Plants like dip n' dots too. #rhizobia #nitrogenfixation #biopsu

A post shared by Adrienne Godschalx (@agodschalx) on

Plants also use their homemade sugar to secrete extrafloral nectar. Nectar typically attracts pollinators, but in the case of extrafloral nectar, plants produce nectar to attract ants, which patrol their sugar source like bodyguards. By evicting intruding bugs attempting to feed on the host plant, extrafloral nectar can be an effective indirect plant defense…

…as long as the ants show up to do their part.

But the key result from our paper is that ants are less attracted to plants that have nitrogen-fixing rhizobia in root nodules belowground. Keep in mind- the ants and bacteria do not interact directly. What connects ant to bacteria?

The plant between them.

Plant chemistry changes when plants form symbiosis with rhizobia. Plants with nitrogen-fixers make more of the nitrogen-based traits, protein and cyanogenesis. Surprise. But these plants also secrete less sugary nectar, therefore attracting fewer ants.

Even in the plant world, some relationships can be more demanding than others.

How do rhizobia cause plants to compromise their ant relationships?

It could be that rhizobia demand so much sugar to keep the nitrogen flowing that the plant’s excess sugar supply is exhausted, leaving little to serve as ant lures. Alternatively, why would plants that get a constant supply of nitrogen to make cyanide need to attract ants anyways?

Either way, we now know rhizobia can change plant relationships with ants.

But why would that matter?
Ants are everywhere- so are rhizobia. Both play important roles in how ecosystems function, but the fact that they can indirectly affect one another may have strong and widely overlooked impacts on plant ecology.

© Adrienne Godschalx (adrg@pdx.edu) August 19, 2015

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

What is plant defense?

Let’s start with plant defense in general. To follow this blog, here are some key things to know:

Plants can’t run away from their attackers. Instead, over evolutionary time, plants have developed secondary metabolism (aka, not photosynthesis- that is primary metabolism) to make toxic, tough, unpalatable, or otherwise unpleasant experiences for the bugs that try to eat the plants (I use the term bug here loosely to include all herbivorous arthropods, fully knowing that technically a true bug belongs to the phylogenetic order Hemiptera). Plant defense is when plants resist being eaten by bugs.

Plant defense has many flavors:

Chemical defense: the toxic and bitter stuff. We like to consume many of these things that plants designed in order to kill their opponents. (Small apology- I will only minimally anthropomorphize plants throughout my blog.)

Mechanical defense: the tough stuff. Usually this comes in the form of thicker and rougher leaves, or leaves covered in trichomes (fancy word for hair, and very effective: picture walking on velcro as an aphid… difficult right?).

Direct defense: the plant makes a toxic or tough compound that deters bugs.

Indirect defense: the plant relies on predators to provide the defensive service. (This is my personal favorite!) Here is how it works: plants under attack send out a cry for help either as a sugar reward or a signal in the air to attract predator bugs (ants, wasps, or spiders) that fill a hit-man role and kill or evict the herbivore from the plant. Badass! Can you attract ants to be your bodyguards? Didn’t think so.

Inducible defense: This is the on/off switch for plant defense. Usually it behooves the plant to use energy defending themselves when herbivores are around, and to save that energy when they are not under attack.

Constitutive defense: Leaving the secondary metabolite lights on all the time, even when there is nobody home (aka no herbivore attack)

That’s all for vocabulary today. I know, plant biology can get pretty crazy exciting. Get ready for the underlying evolutionary tradeoffs and hypotheses explaining why, how, and when plants defend themselves.