Bay Nature magazineSpring 2021

Botany

Listen Closely, the Trees are Talking

March 30, 2021
Lorenzo Washington
Lorenzo Washington. (Photo by Clara Mokri)

I lean back against the picnic table until the canopy finally gives way to blue sky, enjoying how the sunlight dances over the very tops of the redwoods. I’ve always loved that a quick hike into the hills can so easily separate you from the sights and sounds of the city, with Reinhardt Redwood Regional Park taking it up a notch by surrounding you with trees that give the not-so-distant buildings a run for their money. The much-needed mid-hike break gives me time to relax, but I catch myself reaching for my phone before realizing there is no internet service this deep into the park. Slipping the phone back into my pocket, I envision returning to an area with service and again diving into an ocean of information and awareness that stretches the globe. But right now, I can’t tell you what’s happening after the trail curves off a few hundred feet ahead.

My sudden disconnection from one of our biggest innovations has me thinking about how other species tackle the issue of communication, and as a plant biologist I’m most interested in the approach of our stationary and silent friends. How do the trees around me know what’s going on beyond their own branches? If I suggested that the trees had their own system sometimes referred to as the Wood Wide Web, you’d probably call me cheesy. If I then said this system was made by sharing their roots with vast networks of fungi connecting all the plants nearby, you might think I watched James Cameron’s Avatar too much. But what we’ve learned, and part of what I am pursuing in my PhD program at UC Berkeley and through research at Lawrence Berkeley National Laboratory, is that plants and fungi collaborate to create a cross-kingdom innovation, allowing them to trade resources and information far beyond the edges of their roots, challenging our very understanding of how plants, and the earth, have come to be.

When people say that trees “talk” to each other, that’s a concept that rests, in part, on an extraordinary and microscopic process that depends on arbuscular mycorrhizal (AM) fungi,a distinct type of fungi and a subset of mycorrhizal relationships that form a very close and mutually beneficial relationship with plant roots. The fungi help take up important nutrients and water from the soil, passing them to plants in exchange for the sugars and fats plants make, thanks to photosynthesis. Weaving its way through soil and between root systems, an individual fungus can connect to many different plants and sometimes other fungi. In turn, each plant can connect with a variety of AM fungi at a time, creating what scientists call a “promiscuous relationship.” Picture that chain of connections growing in all directions and you realize there’s a massive and busy trading market just beneath our feet!

Imagine the fungi as threadlike tubes, called hyphae, weaving an underground maze of pipes and wires that, similar to the setup in a city, links each building to necessary infrastructure.All the while, the hyphae shuttle various forms of carbon, water, and essential nutrients, such as phosphorus and nitrogen, across distances and between organisms, blurring boundaries of the individual and complicating our understanding of how plants obtain resources. Thanks to the Wood Wide Web, the sapling growing on a dark patch of the forest floor could rely on resources made and found a few hundred yards over, where supply is ample. Suddenly a lone tree isn’t necessarily competing for survival in isolation; instead, it is part of a community not unlike the ones we humans form.

Despite the nickname Wood Wide Web, this phenomenon isn’t restricted to forests or even to trees. Around 80 to 90 percent of land plants associate with AM fungi, and fungi in general are so prevalent that if you took a gram of soil, roughly one teaspoon, you could find enough mycelium (what we call masses of hyphae) to stretch out anywhere from more than 300 feet to six miles. While AM fungi only make up a small portion of all the fungi that inhabit soil, you’d be hard-pressed to find them missing outside of extreme environments. So unlike myself and other hikers in Redwood Regional in the forest without service, plants growing in urban environments still have access to the local fungal web. If you see a plant in the soil, there’s a good chance it’s sharing that space with a fungal partner (or a few)! This connectivity prompts many questions, most of which remain unanswered but in the last three decades have come under study in research universities and the private sector around the world. So how much do we know, and what are the biggest mysteries we have yet to solve?

lotus japonicus
Lorenzo Washington grows Lotus japonicus — a forage legume that forms AM fungi relationships and is often used in research — to study several genes related to cell walls. (Photo courtesy Lorenzo Washington)

Not the Fungi on Your Pizza

AM fungi make up the phylum Glomeromycota, and unlike mushrooms you might find on rotting wood while foraging in the hills or the mold on the fruit you left out too long, these fungi have a role other than decomposer. They seek out plants and make themselves at home within the roots before getting to work finding and trading resources. This “seeking out” is possible because plants release plumes of chemical signals from their roots, forming a gradient that growing AM hyphae pick up and follow. More than a homing beacon, these plant chemicals induce AM spores to germinate and their hyphae to spread out while growing, producing chemical signals of their own as they approach the roots. The fungi signals in turn induce plant roots to branch out as they grow, increasing the root surface area with which AM hyphae can interact. AM fungi range from mysterious unclassified species to some, like Rhizophagus irregularis, that are found in almost any soil. Some AM fungus species appear to prefer partnering with a particular species of plants, while others are promiscuous, although such preferences remain largely an open question, partly due to just how interconnected the Wood Wide Web can become. The fungi can also form connections to plants during all developmental stages, from seedlings on up, thanks to an amazing dance that plays out at the microscopic level.

Once the hyphae of an AM fungus come in contact with the root of a compatible plant, a tightly regulated rearrangement of both the fungal and the plant cells begins. The AM fungus signals cause the plant to drastically change its gene expression, suppressing its own immune system so the AM fungus can grow inside the root, which in turn begins to dramatically alter the structure of the few root cells that will come in contact with the fungus. These cells degrade part of their cell wall and form a special membrane called the pre-penetration apparatus (PPA) that the fungi grow into and fill. The PPA ensures the fungus, and any other microbes, stay a safe distance from the cytoplasm of the plant. After a safe entry, the AM fungus begins to grow in the spaces between root cells, like moss growing between stones in a walkway, preparing to gather necessary resources before it can produce spores. It enters a plant cell for two reasons: to form a storage structure called a vesicle or a highly branched structure that happens to look like a tree, earning it the name arbuscule. The arbuscule (the origin of the name “arbuscular mycorrhizal fungi”) is where the plant and fungi pass resources, and whatever else, to each other. This router of sorts, set up by a microscopic chemical conversation between plant and fungus, is what connects the plant to the Wood Wide Web.

The PPA changes as it fills with nutrient transporters, proteins that monitor what’s being exchanged and other things specific to this membrane. The PPA is also where both parties, plant and fungi, monitor the benefits and costs of their partnership. Arbuscules aren’t permanent, and they regularly die back while re-forming in younger root tissue, so you could think of them like the local farmers’ market, breaking down in one space to appear in another later. Sometimes they won’t reappear however, due to failed negotiations of sorts. Several factors can play into this “decision” for either party. First, plants are quite skilled at determining whether or not sufficient essential nutrients exist nearby to meet their needs. If phosphorus, and to a lesser extent nitrogen, are in ample supply, a plant will suppress the genetic pathways that allow AM relationships to form while raising up all the walls of the immune system once again. Some of the proteins found on the plant’s arbuscular membrane keep track of the amount of phosphorus received from, and the amount of sugars and fat provided to, the fungus. If the partnership becomes too costly for the plant and the fungus isn’t helping by adjusting the cost of its services, the plant will reject the fungus. Much, much less is known about the fungal mechanisms, but we have observed a similar ability to keep track of their water and nutrient payment rate, if you will, and the fungi will abort a partnership they deem too costly. Reciprocity isn’t just a Kingdom Animalia thing.

Despite the fluidity and complexity of these relationships, it’s generally true that older plants frequently have a wider fungal network. Our current level of understanding, however, makes it very difficult to even appropriately estimate how extensive these networks can become. Each individual AM fungus partnered with a plant has a constantly fluctuating number of arbuscules along the roots and, as previously mentioned, can be connected to other plants with unique AM fungal partners or even directly fuse with other AM fungi. On top of this constant turnover, the hyphae are barely visible to the naked eye and are quite fragile. 

Due to these difficulties, there have been few attempts to visualize the spatial extent of these networks. Studies quite limited in scope to specific species of plants and fungi over small areas, thus capturing only a small portion of the potential whole picture, nevertheless reveal how quickly mycorrhizal networks grow from a couple of connections to sprawling over dozens of meters and connecting dozens to hundreds of plants. Akin to any large complex network, like air travel or the internet, a few highly connected plants act as hubs, shortening the distance between almost any two plants to a few steps. Characteristics like this are part of what earned the network the nickname Wood Wide Web.

root section of Lotus japonicus
A root section of Lotus japonicus is stained so that the AM fungus Rhizophagus irregularis appears fluorescent green. The bushy structures are arbuscules growing into an individual root cell, the eye-like structure is a storage vesicle, and the fainter threads are hyphae. (Photo courtesy Lorenzo Washington)

The Network is About More than Food and Water

It isn’t just water and nutrients that are shuttled across the Wood Wide Web. Newer research shows that a range of phenomena, from defense signals to toxins, can spread throughout the network. For example, a bean plant beset with pests alerted bean plants nearby of the threat more quickly and effectively when they all shared a fungal network. Typically a plant only produces defense signal molecules, which activate certain aspects of plant immune systems, in direct response to a pest infestation or to airborne molecules released by nearby plants. In an experiment that prevented plants from perceiving airborne signals, healthy plants that were connected to an infested plant through a fungal network still produced defense compounds, confirming this mode of communication is possible. Scientists have replicated the findings with other types of plants and mycological networks. 

This isn’t to say that AM fungi are a bastion of community development, upholding altruistic values for the sake of all involved. When viewed from the fungi perspective, these seemingly altruistic or community behaviors undertaken on behalf of the plant become a move to ensure a stable source of food for the fungus, even in trying times. It also isn’t always all cooperation within these networks; competitiveness is present as well. Some plants produce toxins that harm other nearby plants. Normally these toxins spread through the soil, limiting their range, but one experiment demonstrated a toxin leached from fallen walnut leaves spread through a fungal network and accumulated around the roots of tomato plants, impacting their growth. 

For all the benefits AM fungi provide, they still mirror the ever-opportunistic dynamics of natural life. Varieties of AM fungi and plants alike differ dramatically in behavior, ranging from mutualism to parasitism, based on the partners involved and the situation at large. Some AM varieties trade nutrients at more expensive “rates” than others or seem to care less about managing their network equitably, preferentially sharing resources with the largest and healthiest plants that have the most to give them in return. Some plants can behave “greedily” and even capitalize on the extensive fungal network to forgo photosynthesis altogether! While hiking around the Bay Area, Northern California, or the Sierras during late spring and early summer, you may stumble on the striking red snow flower (Sarcodes sanguinea) or sugarstick (Allotropa virgata). By being great hubs for mycorrhizal fungi, these plants have become mycoheterotrophic, meaning they survive by taking resources from the fungi in the Wood Wide Web and have lost the ability to photosynthesize, technically making them parasites, albeit quite beautiful ones.

As in most complicated relationships, plants and AM fungi appear to have a long history together. Fossil evidence of arbuscule-like structures in plants dates back 400 million years, and it is quite possible plants and their AM partners existed before plants with roots. Think about what AM fungi do for an individual plant without using the words “fungi” or “root” and we could find ourselves confusing the two. The prevailing idea within the field suggests AM fungi helped the first plants adjust to life on dry land, prior to plants evolving roots. Compared to the oceans and seas plants evolved in, the land was harsh and desolate, and soil had yet to make an appearance. While land-dwellers benefited from more sunlight and the bump in energy that came with it, they weren’t equipped for the new environment; they were little more than algae or moss. This is where some fungi saw an opportunity to step in and net some easy food, laying the foundation for plants to spread and change the earth’s landscape into one more suitable for complex life. 

The earliest scientific descriptions of AM relationships appear less than 150 years ago, and there was little progress in our understanding of them until the late 20th century. Nowadays, exciting discoveries are being made about AM fungi’s influence on the flow of carbon across ecosystems, a process observable through live imaging and radio-labeling, with implications for increasing the amount of carbon plants can put back into the soil. My research, on the other hand, focuses on understanding the microscopic dance we see when the AM fungi and plant directly interface. Specifically, I’m interested in the involvement of certain parts of the cell wall and plasma membrane and whether this can inform us about other microbial relationships in the roots.

Illustration by Kelly Murphy

AM Fungi Can Change Agriculture and Conservation

All of this knowledge could help radically change how we approach matters like agriculture and ecosystem management and restoration. Previous approaches to boost agricultural productivity, for example, have been very plant-centric, with ever more fertilizers, pesticides, and herbicides used to reduce disease and competition and breeding programs that don’t account for mutualistic relationships. The growth of research into AM and similar relationships, where plants and microbes work together to solve problems that humans have taken upon themselves to deal with when growing crops, provides a new perspective to explore for solutions. 

The most apparent potential solution is to breed or engineer plants that consistently make strong and sustained connections with AM fungi that provide a low “cost” for their services. This would result in the need for less fertilizer, as more of it would be retained in the soil, and plants would benefit from all the interesting community actions that AM relationships facilitate. For small-scale farming operations, that could result in plants more resilient to stresses or issues with soil quality and less reliant on agricultural practices that mostly benefit from large-scale implementation. This is much easier said than done, as current crops have been bred with fertilizer use in mind, and there are still many missing pieces of the genetics that both plants and AM fungi rely on to form their relationships. Still, with ongoing research becoming more interdisciplinary and gaining greater attention with each passing year, many bright and creative minds are working to realize a new, not-so-plant-individualistic future for agriculture. 

The potential for AM fungal research application includes natural ecosystems. How might AM fungi play a role in ecosystem recovery after a major fire? Just how vast are these fungal networks in old-growth forests, and how much can they influence resource flux? Since the fungi are so connected, can we use these relationships to gauge soil and ecosystem health? Whether we’re thinking about ecosystem dynamics or want to ask a basic exploratory question involving plants, knowing about AM relationships helps us account for all the moving parts of a system. In the same way that discoveries of the inner workings of photosynthesis drastically altered our understanding of plant function, discoveries involving AM fungi could provide entirely new insight and opportunities for innovation. To lean back into the Wood Wide Web analogy, imagine if an alien being was studying humans and didn’t know about the internet. They’d be missing a very important piece of information that has the power to influence their studies! 

Before returning to my hike, I examine the soil beneath the towering redwoods and wonder what other plants are using those sugars made so high up among the treetops. Without AM fungi, Reinhardt Redwood Regional Park, and this planet, would look a lot different. The fungi fill a role many plants cannot, and allow for community action in ways that make you rethink your definition of plants. Entirely different kingdoms of life coincide, connecting massive swaths of an ecosystem, and cracking the code for survival in a way that seems unreal. This innovation was so profound it changed the face of the earth: barren rock gave way to forests like this park and led to conditions that allowed you and me to be here. Life is even more connected than we thought, and you can’t paint the whole picture without capturing all the microscopic details.

About the Author

Lorenzo Washington is a PhD candidate in Plant & Microbial Biology at UC Berkeley and received a BS in Bioenvironmental Sciences from Texas A&M in 2018. He studies how the plant cell wall and plasma membrane influence the establishment and regulation of beneficial microbial relationships in the root system.

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