Networking in Nature: Plant Talks

In nature's rich tapestry, plant-plant communication represents a remarkable and often underappreciated facet of the complex relationships that shape ecosystems. Being organisms rooted in place, plants face a multitude of environmental threats, ranging from herbivore attacks to changes in climatic conditions. In response to these challenges, plants have evolved mechanisms to interact with their surroundings but they also hold the potential to orchestrate a multi-organism defense strategy. These interactions are formed both above and below ground. Above ground, they release chemical signals that allow them to interact with their neighboring plants and other organisms. Below ground, a different kind of communication takes place through common mycorrhizal networks, where plants and trees are connected through intricate fungal networks, sometimes referred to as the "Wood Wide Web". This subterranean dialogue allows them to exchange information, resources, and, possibly, warnings. It further contributes to the resilience and survival of individual plants and the cohesiveness of entire ecological communities, where plants and other organisms collaborate and compete in order to learn more about their environment. This dual system of plant-plant communication, above and underground, emphasizes the complexity and interconnectedness of life in the plant kingdom as well as other organisms surrounding them.

Figure 1: Plant-plant communication (Rasheed et al., 2023).

Plant-Plant Communication

Plants have various defense strategies against environmental threats. These include defenses that are continually present in plant tissues, as well as inducible defenses that are activated when plants detect a threat, such as herbivore feeding or the presence of herbivore eggs. These defenses can be direct, such as the release of toxic compounds in plant tissue, or indirect, such as herbivore-induced plant volatiles (HIPVs) that attract natural enemies of herbivores. Thus, plants can release chemical cues or signals that enable them to interact with neighboring plants and the surrounding community of herbivorous and beneficial arthropods. These above-ground or "wireless" interactions are usually mediated by volatile organic compound (VOC) emissions (Rasheed et al., 2023). When plants are exposed to these volatile emissions, they often exhibit a faster and stronger activation of defense responses, a phenomenon known as "defense priming". Primed plants show enhanced resistance to subsequent herbivore attacks, which suggests that the emission of these volatiles can prepare plants to defend themselves more effectively (Hu et al., 2021).

Although it was discussed above that plants can communicate with their neighbors through signaling via air transportation of messenger compounds, it is now highlighted that plant species are able to send warnings to each other via a common mycelial network. Suzanne Simard and her colleagues were among the first scientists who discussed the interconnectedness of plants within communities and their ability to exchange resources through a common network of hyphae. The researchers used reciprocal labeling with isotopes (13C and 14C) in the field to examine the movement of carbon between the trees (Betula papyrifera and Pseudotsuga menziesii ), which is crucial for understanding how carbon is shared within the plant community. The conclusion was that plants with common mycorrhizal associates tend to form groups or guilds based on these shared fungal partners. This mutualism influences how plants interact with one another and share resources (Simard et al., 1997). Below-ground or "wired" interactions like these involve pathways like common mycorrhizal networks (CMNs), volatile emissions, and chemical exudates (Rasheed et al., 2023). The hypothesis that mycorrhizal mycelia can connect two or more plants of the same or different species is referred to as common mycelial networks, or the "Wood Wide Web" (Rhodes, 2017). Hence, these networks can make associations with multiple plant and fungal species, forming an environment of optimal fitness for both organisms.

Plants that are connected via fungal mycelia tend to show quick behavioral responses such as the production of fine roots, the adjustment of their photosynthesis rate, and the adjustment of the secretion of plant hormones such as auxin, which modifies their growth (Gorzelak et al., 2015). Since the interaction between mycelia of many fungal species and plants does not constitute a specific interaction, in a non-disturbed forest ecosystem such an interaction can be thought of as plant species interconnecting together through a series of mycelia (Read, 2017), the "Wood Wide Web".

Figure 2: Mutualistic mycorrhizae (Orchard of Flavours).

The symbiotic relationship between fungi and plant roots is called mycorrhiza, which can only happen after the fungus' colonization of the plant's roots, either intercellularly or extracellularly. This interaction is usually mutualistic, meaning that the two species can benefit from each other, but, pathogenic fungi where either one of the organisms is causing harm to the host also exist (Rhodes, 2017). In the case of symbiosis, the fact that mycorrhiza can be found anywhere where plant species grow makes them the optimal candidate to increase the surface area of the roots to enhance nutrient and water absorption. In turn, plant species send sugar stored in their leaves down to fungi as a food source. By maintaining a two-sided mutualistic interaction, mycorrhizal fungi play an important role in the cycling of natural elements such as carbon, nitrogen, phosphorus as well as potassium and sulfur (Shi et al., 2023). Pathogenic fungi are harmful to their host plants because they cause diseases and use the resources of the plant without providing any benefit in return. In some rare cases, certain mycorrhizal fungi can turn parasitic or potentially pathogenic under specific conditions or when they interact with a host plant they are not well-adapted to. An example of this could be when some temperate forest orchids such as the genera Epipactis and Cephalanthera form mycorrhizal associations that are considered 'mixotrophic' meaning that they can supplement their nutrition by partially parasitizing the fungi they associate with rather than doing photosynthesis (Lallemand et al., 2019). However, these are exceptions, and mycorrhizal associations are generally considered beneficial to plants where each organism has a gain.

Types of Mycorrhizae

Depending on the hyphal structure, mycorrhizae can be divided into two types:

• ectomycorrhizal fungi (the hyphae do not penetrate root cells)

• endomycorrhizal fungi (the hyphae penetrate through the cell wall of root cells and cause invagination of the cell membrane) (Huey et al., 2020).

One of the most commonly observed endomycorrhizal fungi is arbuscular mycorrhizas, whose hyphae can travel through the cells of plants and increase the contact surface area between the hyphae and cell cytoplasm to facilitate nutrient transfer. These arbuscular mycorhizal fungi are able to link more than one plant of the same or different species. Survival of some plant species such as Orchids is highly dependent on the orchid mycorrhizal fungi where the distribution and population dynamics of these plants are arranged based on their interaction with the mycorrhiza (Liet al., 2021). Some mycorrhizal interactions reveal that these fungi can function as decay organisms by making slow-released nutrients more mobile to feed the plant species in their vicinity.

Figure 3: Orchid living in symbiosis with fungi, (A) pelotons of the fungi in the roots (B, C) (from Research in Bavaria).

Another type of endomycorrhizae fungi, the ericoid mycorrhizal fungi, form a mutualistic symbiotic relationship with some plants where it colonizes the plant's root tissues, forming specialized structures called ericoid mycorrhizal structures (EMS). These structures are different from the typical arbuscular mycorrhizal structures found in many other mycorrhizal associations (Vohník, 2020). Ectomycorrhizal fungi, on the other hand, play a major role in establishing the early development of trees and in protecting them from parasitic organisms (Janowski & Leski, 2023). Since ectomycorrhizal fungi play a role in the tolerance of plants in terms of nutrient absorption as well as recovery after parasitic invasions, some studies reveal that the nature of these fungi can be effective in forest restoration programs. In particular, forest soil that has been contaminated with heavy metals can be restored by the activity of certain fungi species to absorb them, making metals immobilized so that they are bioavailable (Policelli et al., 2020).

Nevertheless, not everything that is transported among plants is harmless to the plant: the transportation of toxins that prevent other plant species' growth (allelopathy) can also be possible within this regulated network. Some plants are also able to release chemicals with allopathic properties in order to gain a competitive advantage over other plants by altering their growth, showing "territorial behavior". Some invasive plant species such as garlic mustard (Alliaria petiolata) or Himalayan balsam (Impatiens glandulifera) have been shown to disrupt the beneficial mycorrhizal associations in native plants, leading to a reduction in their fitness. (McCoy et al., 2022). Conversely, the plant microbiome, including beneficial bacteria and fungi, can play a role in mitigating the effects of allelopathic chemicals which can help detoxify or degrade allelopathic compounds, thereby reducing the harm caused by these chemicals to nearby plants. This demonstrates the complexity of plant-microbe interactions and their role in mediating the effects of allelopathy.

Figure 4: Mycellium (photo from Vail Daily).

The "Wood Wide Web" Theory

The idea of "Wood Wide Web" was popularized by a German forest scientist, Peter Wohlleben, who described this phenomenon in his book as the idea of a complex underground network of mycorrhizal fungi connecting trees and other plants in a forest (Wohlleben, 2016). From the moment it was discussed that plant species can be included in the mycorrhizal networks to communicate with each other, the term "Wood Wide Web" has been a point of discussion among many scientists. The idea is that if plants can communicate with each other via volatile organic chemicals, trees that are found within a forest ecosystem might also be able to convey information to one another via this underground network. Thus, up until now, because it opens the question of whether the forest can be identified as a single superorganism rather than a merge of different organisms, this has been a controversial debate. Nevertheless, due to a lack of scientific data and research on this area, researchers suggest that there is a lot of variability within the forest itself that needs to be considered before making conclusions about the theory. For example, if the association between plants and fungi is somehow damaged due to other organisms, there would be a major gap in the network itself which would eventually affect the life cycles of organisms that reside within the same ecosystem. In addition, the idea that common mycorrhizal networks are used to provide seedlings with sources tends to have alternative explanations or the evidence present is not significant enough to reach a definitive conclusion on the concept of underground communication of plant species (Karst et al., 2023). Nevertheless, what is important to remember is that plants that especially inhabit big ecosystems are highly dependent on the mycorrhizal networks and disruption to either one would cause a significant impact on the whole ecosystem (Hunter, 2023).

Conclusion

The intricate communication network below ground allows plant species to respond to these challenges in a coordinated manner. If one plant in the mycorrhizal network experiences stress, it can communicate with the neighboring plants through the fungal network to increase their chance of survival. Looking ahead, studies of plant-plant communication hold exciting prospects and potential for further revelations. As research in this field continues to unfold, it is likely to shed light on the mechanisms and nuanced signaling pathways that govern plants' interactions with their surroundings. The future of plant communication research may uncover new aspects of above-ground signaling through volatile compounds, potentially revealing the extent of the chemical vocabulary that plants employ to respond to environmental cues. Furthermore, investigations into the role of common mycorrhizal networks would potentially uncover novel findings of layers of plant cooperation and warning systems. The insights gained from these future perspectives could have far-reaching implications, from enhancing our understanding of ecological dynamics to harness plant communication for sustainable agriculture, and ecosystem management. As we delve further into the enigmatic realm of plant communication, the horizons of discovery in both above and underground interactions are entitled to expand, unlocking the secrets of this remarkable facet of the natural world.

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