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

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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

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The Crazy Things Plants do for Nitrogen

What’s the big deal with nitrogen, you ask? Nitrogen is the key ingredient in proteins. In biology, if our DNA does the talkin’, proteins do the walkin’. Proteins can be enzymes that help reactions happen. In plants, the sugar-making part of photosynthesis, (aka the dark cycle) is run by an enzyme called RuBisCO, which also happens to be the most abundant enzyme on earth. The remarkable thing about this super important enzyme, responsible for turning CO2 into sugars, is that it is a super slow, clunky enzyme. Plants often compensate for its slowness by making more of it. More enzyme=more protein. Plants need nitrogen to make proteins.

I thought about naming this post: “Nodules, photosynthetic pathways, and carnivorous plants, oh my!” But the number of syllables got in my way. Still, these three evolutionary wonders all help plants deal with limited nitrogen, and deserve to show up in a blog post together.

But why are plants so nitrogen-limited in nature?

The answer includes a terrifying word from Intro to Chemistry: stoichiometry. (Which I recently learned from this fantastic paper: Nitrogen and Nature.)

The number of nitrogen molecules in plants is small among all of the carbon molecules, which drives the ratio of carbon to nitrogen molecules the leaf litter, overwhelming the soil with carbon and making nitrogen hard to come by. Further, nitrogen is typically stuck directly to carbon in a covalent bond, which is harder to break off than ionic bonds that work like magnets. Even when nitrogen is in this “magnetic” form, these ions are negatively charged—just like soil particles—and easily leech from the soil with rainwater.

Yes, that is why nitrogen is limited in the soil, but most of the nitrogen in the world is in the air; isn’t there plenty of it in the air that plants could use? The atmosphere is made up of roughly 79% nitrogen. Unfortunately, that nitrogen is not accessible to plants. Each nitrogen is tightly bound to a second nitrogen atom like this: N≡N, and triple bonds are especially tough to break, even for a plant.

But some bacteria can break all three bonds!! Microbes have crazy metabolic pathways, many of which are crucial to the chemical balance of the world existing as we know it. By turning N≡N into fertilizer in a process called nitrogen fixation, the nitrogen cycle is driven by microbes.

Evolutionary wonder #1: Some plants figured this out (over evolutionary time), and formed a symbiotic relationship with nitrogen-fixing bacteria. These groups of bacteria: rhizobia, Frankia, and cyanobacteria, live in nodules on their plant hosts’ roots and provide a source of house-made fertilizer in exchange for sugars. Plants, which do photosynthesis, that have nitrogen-fixing bacteria in their roots represent the interface of two important geochemical cycles: the nitrogen and carbon cycles.

Not only are plants solar-powered sugar factories, but some plants can make sugars through several different metabolic pathways: C3, C4, and CAM. For perspective- we don’t even have one carbon assimilating pathway, but the plant kingdom has three.

Evolutionary Wonder #2: In “normal photosynthesis”, or C3 photosynthesis, plants lose water through pores called stomata when they take in carbon to turn into sugars. Some plants reduce the amount of water they lose by either opening their stomata at night when the air is cooler (Crassulacean Acid Metabolism or CAM), or by concentrating the CO2 in a separate compartment with those super slow enzymes (C4). Why are these nitrogen-limited adaptations? Because making enzymes more efficient helps plants with the initial problem of needing nitrogen to churn out tons of slow, clunky enzymes.

Yet some plants carry out old fashioned C3 photosynthesis without any N-fixing bacteria in root nodules and are able to live in extremely nitrogen-poor soil. Their secret? Eat the tiny packets of nitrogen buzzing and crawling everywhere around them.

Evolutionary wonder #3: Carnivorous plants are exciting because they deviate from our basic understanding of what plants do. When my mom let me buy a $4.99 Venus fly trap at City Market, my mind was blown. I wrote songs and recorded one too many home videos about the plant that eats flies!

Even Darwin himself was excited by this menacing behavior and laid some groundwork for research on how Venus flytraps close in on their prey.

Despite the diversity of strategy, ranging from pitcher plants that collect bugs that slip into the plants’ digestive juices to sticky plants that catch bugs with glandular hairs, carnivorous plants evolved to deal with stressful environments lacking that not-so-secret ingredient in all proteins:

Nitrogen.

How to Catch a Bee

During my days as a summer camp unit director, one of my campers brought me a flower. When I looked closer, I realized this 11-year-old was not interested in the flower, but the bee and spider on top of the flower, head to head. I assumed they were fighting, but they were both pretty still, and it dawned on me that the bee was a goner, locked in the “jaws” of the spider, whom I figured had won the fight. I was still wrong, and the reality of this interaction is even cooler than I had imagined:

The spider hunts by hiding in flowers that attract their prey, the bees.

The unsuspecting pollinator. #entomology #ecology #biology #tritrophicinteractions #pollination…almost.

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I posted my spider-bee-flower pic on Instagram recently, which received more interest than I had expected. I even had comments asking about the evolution of this flower-sitting ambush spider, so I looked it up, and I stumbled upon a cool chemical ecology story.

The first thing I learned is that, when given a choice, both the bees and this group of spiders, crab spiders, pick the same flowers. By covering the flower with saran-wrap and watching the spiders’ flower choice change, scientists were able to figure out that spiders are choosing their flowers by following chemical signals in the air, aka smells. This means these spiders are adapted to smelling out flowers that are more likely to attract their dinner.

Do bees fall for this trap? Bees not only fall for this ambush, but are more attracted to flowers with spiders than to safe, spider-free flowers.  Why would a bee fly closer to a purple flower that has a white, hungry spider in the middle?

Clearly, bees see differently from us. As I was perfecting my Instagram post, I was struck by my black and white Instagram filter, which showed the flower and spider as same shade of white (Figure 1). Even without extensive training in bee sensory biology, I figured there must be some sort of visual trick at play.

Figure 1. Screenshot of my Instagram post with 100% of the color saturation removed.

Too bad there is no UV filter on insta, because bees can see ultraviolet. Flowers take advantage of the bees’ visible spectrum in UV and often attract bees with target-like patterns, using dark UV spots in the middle. Darker UV target patterns can mean more pollination, so this trait is selected for in both flowers and bees.

So why are bees attracted to the crab spider flowers? Crab spiders have a layer of transparent cells covering spider skin cells that can change color! There are a few types of this pigment- the ommochrome pigment, which either allows spiders to or yellowish to red, or allows white spiders to have UV fluorescent patterns. With a UV pattern on their backs, flowers with spiders look like an extra dark flower target and attract bees more effectively than flowers without spiders.

Of course, natural selection goes both ways. Native bees in Australia fly close to, but can recognize and veer away from native crab spiders, whereas introduced honeybees have not adapted to recognize this danger.

Plants interact with insects and their predators. Scientists use the term “tritrophic interactions” to describe three trophic levels, or links in the food chain, interacting and affecting one another. As my thrilled camper and curious Instagram “fans” could pick up on, tritrophic interactions are fascinating! From an applied science perspective, knowing the intricacies of tritrophic interactions is essential to fully understand the side effects of potential global solutions in food security, and pest management, and conserving biodiversity.

-A

Note: All the papers I cite in this post are by Dr. Astrid M. Heiling, who has many other fantastic papers. Check her work out!

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.