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Plant communication

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Plants can be exposed to many stress factors such as disease, temperature changes, herbivory, injury and more. Therefore, in order to respond or be ready for any kind of physiological state, they need to develop some sort of system for their survival in the moment and/or for the future. Plant communication encompasses communication using volatile organic compounds, electrical signaling, and common mycorrhizal networks between plants and a host of other organisms such as soil microbes,[1] other plants[2] (of the same or other species), animals,[3] insects,[4] and fungi.[5] Plants communicate through a host of volatile organic compounds (VOCs) that can be separated into four broad categories, each the product of distinct chemical pathways: fatty acid derivatives, phenylpropanoids/benzenoids, amino acid derivatives, and terpenoids.[6] Due to the physical/chemical constraints most VOCs are of low molecular mass (< 300 Da), are hydrophobic, and have high vapor pressures.[7] The responses of organisms to plant emitted VOCs varies from attracting the predator of a specific herbivore to reduce mechanical damage inflicted on the plant [4] to the induction of chemical defenses of a neighboring plant before it is being attacked.[8] In addition, the host of VOCs emitted varies from plant to plant, where for example, the Venus Fly Trap can emit VOCs to specifically target and attract starved prey.[9] While these VOCs typically lead to an increase in herbivory resistance in neighboring plants, there is no clear benefit to the emitting plant in helping nearby plants. As such, whether neighboring plants have evolved the capability to "eavesdrop" or whether there is an unknown tradeoff occurring is subject to much scientific debate.[10]

Volatile communication

In Runyon et al. 2006, the researchers demonstrate how the parasitic plant, Cuscuta pentagona (field dodder), uses VOCs to interact with various hosts and determine locations. Dodder seedlings show direct growth toward tomato plants (Lycopersicon esculentum) and specifically elicited tomato plant volatiles. This was tested by growing a dodder weed seedling in a contained environment, connected to two different chambers. One chamber contained tomato VOC's while the other had artificial tomato plants. After 4 days of growth, the dodder weed seedling showed a significant growth towards the direction of the chamber with tomato VOC's. Their experiments also showed that the dodder weed seedlings could distinguish between wheat (Triticum aestivum) VOCs and tomato plant volatiles. As when one chamber was filled with each of the two different VOCs, dodder weeds grew towards tomato plants as one of the wheat VOC's is repellent. These findings show evidence that volatile organic compounds determine ecological interactions between plant species and show statistical significance that the dodder weed can distinguish between different plant species by sensing elicited volatile organic compounds.[11]

Tomato plant to plant communication is further examined in Zebelo et al. 2012, which studies tomato plant response to herbivory. Upon herbivory by Spodoptera littoralis, tomato plants emit VOCs that are released into the atmosphere and induce responses in neighboring tomato plants. When the herbivory-induced VOCs bind to receptors on other nearby tomato plants, responses occur within seconds. The neighboring plants experience a rapid depolarization in cell potential and increase in cytosolic calcium. Plant receptors are most commonly found on plasma membranes as well as within the cytosol, endoplasmic reticulum, nucleus, and other cellular compartments. VOCs that bind to plant receptors often induce signal amplification by action of secondary messengers including calcium influx as seen in response to neighboring herbivory. These emitted volatiles were measured by GC-MS and the most notable were 2-hexenal and 3-hexenal acetate. It was found that depolarization increased with increasing green leaf volatile concentrations. These results indicate that tomato plants communicate with one another via airborne volatile cues, and when these VOC's are perceived by receptor plants, responses such as depolarization and calcium influx occur within seconds.[12]

Terpenoids

The terpenoid verbenone is a plant pheromone, signalling to insects that a tree is already infested by beetles.[13]
Further information: Terpenoid

Terpenoids facilitate communication between plants and insects, mammals, fungi, microorganisms, and other plants.[14] Terpenoids may act as both attractants and repellants for various insects. For example, pine shoot beetles (Tomicus piniperda) are attracted to certain monoterpenes ( (+/-)-a-pinene, (+)-3-carene and terpinolene) produced by Scots pines (Pinus sylvestris), while being repelled by others (such as verbenone).[15]

Terpenoids are a large family of biological molecules with over 22,000 compounds.[16] Terpenoids are similar to terpenes in their carbon skeleton but unlike terpenes contain functional groups. The structure of terpenoids is described by the biogenetic isoprene rule which states that terpenoids can be thought of being made of isoprenoid subunits, arranged either regularly or irregularly.[17] The biosynthesis of terpenoids occurs via the methylerythritol phosphate (MEP) and mevalonic acid(MVA) pathways[6] both of which include isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) as key components.[18] The MEP pathway produces hemiterpenes, monoterpenes, diterpenes, and volatile carotenoid derivatives while the MVA pathway produces sesquiterpenes.[6]

Electrical signaling

Plants also communicate via electrical signals, which is explored in Calvo et al. 2017. These electrical signals are mediated by cytosolic Ca2+ ions. Cytosolic calcium signals are mediated by hundreds of protein and protein kinases, and many of the signals also induce action potentials in plants. The phloem of the plant serves as the pathway for electrical communication, and as the plant grows and learns from its past, the phloem becomes increasingly cross linked. Electrical signals may be transmitted to other cells connected by symplasts through plasmodesmata. Plants respond to various environmental cues and elicit electrical responses internally to alter the function of the plant body. This can range from avoiding predation, releasing defense mechanisms, responding to changing temperature, changing growth direction, and sharing nutrients in the soil. This form of memory stored in the plant's phloem allows it to better respond to similar stimuli in the future and shows how electrical signaling allows a plant to communicate with itself and alter its own physiology to better suit certain environmental cues (Calvo et al. 2017).

Below-ground communication

Chemical Cues

Pisum sativum (garden pea) plants communicate stress cues via their roots to allow neighboring unstressed plants to anticipate an abiotic stressor. Pea plants are commonly grown in temperate regions throughout the world.[19] However, this adaptation allows plants to anticipate abiotic stresses such as drought. In 2011, Falik et al. tested the ability of unstressed pea plants to sense and respond to stress cues by inducing osmotic stress on a neighboring plant.[20] Falik et al. subjected the root of an externally-induced plant to mannitol in order to inflict osmotic stress and drought-like conditions. Five unstressed plants neighbored both sides of this stressed plant. On one side, the unstressed plants shared their root system with their neighbors to allow for root communication. On the other side, the unstressed plants did not share root systems with their neighbors.[20]

Falik et al. found that unstressed plants demonstrated the ability to sense and respond to stress cues emitted from the roots of the osmotically stressed plant. Furthermore, the unstressed plants were able to send additional stress cues to other neighboring unstressed plants in order to relay the signal. A cascade effect of stomatal closure was observed in neighboring unstressed plants that shared their rooting system but was not observed in the unstressed plants that did not share their rooting system.[20] Therefore, neighboring plants demonstrate the ability to sense, integrate, and respond to stress cues transmitted through roots. Although Falik et al. did not identify the chemical responsible for perceiving stress cues, research conducted in 2016 by Delory et al. suggests several possibilities. They found that plant roots synthesize and release a wide array of organic compounds including solutes and volatiles (i.e. terpenes).[21] They cited additional research demonstrating that root-emitted molecules have the potential to induce physiological responses in neighboring plants either directly or indirectly by modifying the soil chemistry.[21] Moreover, Kegge et al. demonstrated that plants perceive the presence of neighbors through changes in water/nutrient availability, root exudates, and soil microorganisms.[22]

Although the underlying mechanism behind stress cues emitted by roots remains largely unknown, Falik et al. suggested that the plant hormone abscisic acid (ABA) may be responsible for integrating the observed phenotypic response (stomatal closure).[20] Further research is needed to identify a well-defined mechanism and the potential adaptive implications for priming neighbors in preparation for forthcoming abiotic stresses; however, a literature review by Robbins et al. published in 2014 characterized the root endodermis as a signaling control center in response to abiotic environmental stresses including drought.[23] They found that the plant hormone ABA regulates the root endodermal response under certain environmental conditions. In 2016 Rowe et al. experimentally validated this claim by showing that ABA regulated root growth under osmotic stress conditions.[24] Additionally, changes in cytosolic calcium concentrations act as signals to close stomata in response to drought stress cues. Therefore, the flux of solutes, volatiles, hormones, and ions are likely involved in the integration of the response to stress cues emitted by roots.

Mycorrhizal networks

Main article: Plant to plant communication via mycorrhizal networks

Another form of plant communication occurs through their complex root networks. Through roots, plants can share many different resources including nitrogen, fungi, nutrients, microbes, and carbon. This transfer of below ground carbon is examined in Philip et al. 2011. The goals of this paper were to test if carbon transfer was bi-directional, if one species had a net gain in carbon, and if more carbon was transferred through the soil pathway or common mycorrhizal network (CMN). CMNs occur when fungal mycelia link roots of plants together.[25] To test this, the researchers followed seedlings of paper birch and Douglas-fir in a greenhouse for 8 months, where hyphal linkages that crossed their roots were either severed or left intact. The experiment measured amounts of CO2 in both seedlings. It was discovered that there was indeed a bi-directional sharing of CO2 between the two trees, with the Douglas-fir receiving a slight net gain in CO2. Also, the carbon was transferred through both soil and the CMN pathways, as transfer occurred when the CMN linkages were interrupted, but much more transfer occurred when the CMN's were left unbroken. This experiment showed that through fungal mycelia linkage of the roots of two plants, plants are able to communicate with one another and transfer nutrients as well as other resources through below ground root networks.[25] Further studies go on to argue that this underground “tree talk” is crucial in the adaptation of forest ecosystems. Plant genotypes have shown that mycorrhizal fungal traits are heritable and play a role in plant behavior. These relationships with fungal networks can be mutualistic, commensal, or even parasitic. It has been shown that plants can rapidly change behavior such as root growth, shoot growth, photosynthetic rate, and defense mechanisms in response to mycorrhizal colonization.[26] Through root systems and common mycorrhizal networks, plants are able to communicate with one another below ground and alter behaviors or even share nutrients depending on different environmental cues.

See also

References

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  14. ^ Llusià, Joan; Estiarte, Marc; Peñuelas, Josep (1996). "Terpenoids and plant communication". Bull. Inst. Cat. Hist. Nat. 64: 125–133.
  15. ^ Byers, J. A.; Lanne, B. S.; Löfqvist, J. (1989-05-01). "Host tree unsuitability recognized by pine shoot beetles in flight". Experientia. 45 (5): 489–492. doi:10.1007/BF01952042. ISSN 0014-4754. S2CID 10669662.
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  17. ^ Ružička, Leopold (1953). "The isoprene rule and the biogenesis of terpenic compounds". Cellular and Molecular Life Sciences. 9 (10): 357–367. doi:10.1007/BF02167631. PMID 13116962. S2CID 44195550.
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  24. ^ Rowe, James H.; Topping, Jennifer F.; Liu, Junli; Lindsey, Keith (July 2016). "Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin". New Phytologist. 211 (1): 225–239. doi:10.1111/nph.13882. ISSN 0028-646X. PMC 4982081. PMID 26889752.
  25. ^ a b Philip, L., S. Simard, and M. Jones. 2010. Pathways for below-ground carbon transfer between paper birch and Douglas-fir seedlings. Plant Ecology & Diversity 3:221–233.
  26. ^ Gorzelak, M. A., A. K. Asay, B. J. Pickles, and S. W. Simard. 2015. Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB PLANTS 7. Oxford Academic.
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