Plant communication
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Plants are 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,<ref>Wenke, Katrin; Kai, Marco; Piechulla, Birgit (2010-02-01). "Belowground volatiles facilitate interactions between plant roots and soil organisms". Planta. 231 (3): 499–506. Bibcode:2010Plant.231..499W. doi:10.1007/s00425-009-1076-2. PMID 20012987. S2CID 1409780.</ref> other plants<ref>Yoneya, Kinuyo; Takabayashi, Junji (2014-01-01). "Plant–plant communication mediated by airborne signals: ecological and plant physiological perspectives". Plant Biotechnology. 31 (5): 409–416. doi:10.5511/plantbiotechnology.14.0827a.</ref> (of the same or other species), animals,<ref>Leonard, Anne S.; Francis, Jacob S. (2017-04-01). "Plant–animal communication: past, present and future". Evolutionary Ecology. 31 (2): 143–151. Bibcode:2017EvEco..31..143L. doi:10.1007/s10682-017-9884-5. S2CID 9578593.</ref> insects,<ref name=":1">De Moraes, C. M.; Lewis, W. J.; Paré, P. W.; Alborn, H. T.; Tumlinson, J. H. (1998). "Herbivore-infested plants selectively attract parasitoids". Nature. 393 (6685): 570–573. Bibcode:1998Natur.393..570D. doi:10.1038/31219. S2CID 4346152.</ref> and fungi.<ref>Bonfante, Paola; Genre, Andrea (2015). "Arbuscular mycorrhizal dialogues: do you speak 'plantish' or 'fungish'?". Trends in Plant Science. 20 (3): 150–154. doi:10.1016/j.tplants.2014.12.002. hdl:2318/158569. PMID 25583176.</ref> 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.<ref name=":2">Dudareva, Natalia (April 2013). "Biosynthesis, function and metabolic engineering of plant volatile organic compounds". New Phytologist. 198 (1): 16–32. doi:10.1111/nph.12145. JSTOR newphytologist.198.1.16. PMID 23383981. S2CID 26160875.</ref> Due to the physical/chemical constraints most VOCs are of low molecular mass (< 300 Da), are hydrophobic, and have high vapor pressures.<ref>Rohrbeck, D.; Buss, D.; Effmert, U.; Piechulla, B. (2006-09-01). "Localization of Methyl Benzoate Synthesis and Emission in Stephanotis floribunda and Nicotiana suaveolens Flowers". Plant Biology. 8 (5): 615–626. Bibcode:2006PlBio...8..615R. doi:10.1055/s-2006-924076. PMID 16755462. S2CID 40502773.</ref> 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 <ref name=":1" /> to the induction of chemical defenses of a neighboring plant before it is being attacked.<ref name=":0">Baldwin, Jan T.; Schultz, Jack C. (1983). "Rapid Changes in Tree Leaf Chemistry Induced by Damage: Evidence for Communication between Plants". Science. 221 (4607): 277–279. Bibcode:1983Sci...221..277B. doi:10.1126/science.221.4607.277. JSTOR 1691120. PMID 17815197. S2CID 31818182.</ref> 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.<ref>Hedrich, Rainer; Neher, Erwin (March 2018). "Venus Flytrap: How an Excitable, Carnivorous Plant Works" (PDF). Trends in Plant Science. 23 (3): 220–234. doi:10.1016/j.tplants.2017.12.004. ISSN 1360-1385. PMID 29336976.</ref> While these VOCs typically lead to increased resistance to herbivory 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.<ref>Heil, Martin; Karban, Richard (2010-03-01). "Explaining evolution of plant communication by airborne signals". Trends in Ecology & Evolution. 25 (3): 137–144. doi:10.1016/j.tree.2009.09.010. ISSN 0169-5347. PMID 19837476.</ref> As related to the aspect of meaning-making, the field is also identified as phytosemiotics.<ref>Kull, Kalevi 2000. An introduction to phytosemiotics: Semiotic botany and vegetative sign systems. Sign Systems Studies 28: 326–350.</ref>
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, tomato plant volatile organic compounds. This was tested by growing a dodder weed seedling in a contained environment, connected to two different chambers. One chamber contained tomato VOCs 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 their VOCs.<ref>Runyon, Justin B.; Mescher, Mark C.; De Moraes, Consuelo M. (2006-09-29). "Volatile chemical cues guide host location and host selection by parasitic plants". Science. 313 (5795): 1964–1967. Bibcode:2006Sci...313.1964R. doi:10.1126/science.1131371. ISSN 1095-9203. PMID 17008532. S2CID 10477465.</ref>
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.<ref>Zebelo, Simon A.; Matsui, Kenji; Ozawa, Rika; Maffei, Massimo E. (2012-11-01). "Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication". Plant Science. 196: 93–100. doi:10.1016/j.plantsci.2012.08.006. ISSN 0168-9452. PMID 23017903. Retrieved 2020-10-20.</ref>
Terpenoids
Terpenoids facilitate communication between plants and insects, mammals, fungi, microorganisms, and other plants.<ref>Llusià, Joan; Estiarte, Marc; Peñuelas, Josep (1996). "Terpenoids and plant communication". Bull. Inst. Cat. Hist. Nat. 64: 125–133.</ref> 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).<ref>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.</ref>
Terpenoids are a large family of biological molecules with over 22,000 compounds.<ref>Hill, Ruaraidh; Connolly, J.D. (1991). Dictionary of terpenoids. Chapman & Hall. ISBN 978-0412257704. OCLC 497430488.</ref> 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.<ref>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.</ref> The biosynthesis of terpenoids occurs via the methylerythritol phosphate (MEP) and mevalonic acid(MVA) pathways<ref name=":2" /> both of which include isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) as key components.<ref>McGarvey, Douglas J.; Croteau, Rodney (July 1995). "Terpenoid Metabolism". The Plant Cell. 7 (7): 1015–1026. doi:10.1105/tpc.7.7.1015. JSTOR 3870054. PMC 160903. PMID 7640522.</ref> The MEP pathway produces hemiterpenes, monoterpenes, diterpenes, and volatile carotenoid derivatives while the MVA pathway produces sesquiterpenes.<ref name=":2" />
Electrical signaling
Many researchers have shown that plants have the ability to use electrical signaling to communicate from leaves to stem to roots. Starting in the late 1800s scientists, such as Charles Darwin, examined ferns and Venus fly traps because they showed excitation patterns similar to animal nerves.<ref>Darwin, Charles (1875). Insectivorous Plants. London.{{cite book}}: CS1 maint: location missing publisher (link)</ref> However, the mechanisms behind this electrical signaling are not well known and are a current topic of ongoing research.<ref name=":6">Hedrich, Rainer; Salvador-Recatalà, Vicenta; Dreyer, Ingo (2016-05-01). "Electrical Wiring and Long-Distance Plant Communication". Trends in Plant Science. 21 (5): 376–387. doi:10.1016/j.tplants.2016.01.016. ISSN 1360-1385. PMID 26880317.</ref> A plant may produce electrical signaling in response to wounding, temperature extremes, high salt conditions, drought conditions, and other various stimuli.<ref name=":6" /><ref>Furch, Alexandra C. U.; Zimmermann, Matthias R.; Will, Torsten; Hafke, Jens B.; van Bel, Aart J. E. (2010-08-01). "Remote-controlled stop of phloem mass flow by biphasic occlusion in Cucurbita maxima". Journal of Experimental Botany. 61 (13): 3697–3708. doi:10.1093/jxb/erq181. ISSN 0022-0957. PMC 2921205. PMID 20584788.</ref>
There are two types of electrical signals that a plant uses. The first is the action potential and the second is the variation potential.
Similar to action potentials in animals, action potentials in plants are characterized as “all or nothing.”<ref name=":7">Sukhov, Vladimir; Vodeneev, Vladimir (2009-11-17). "A Mathematical Model of Action Potential in Cells of Vascular Plants". Journal of Membrane Biology. 232 (1): 59–67. doi:10.1007/s00232-009-9218-9. ISSN 1432-1424. PMID 19921324. S2CID 13334600.</ref> This is the understood mechanism for how plant action potentials are initiated:<ref name=":8">Sukhov, Vladimir; Nerush, Vladimir; Orlova, Lyubov; Vodeneev, Vladimir (2011-12-21). "Simulation of action potential propagation in plants". Journal of Theoretical Biology. 291: 47–55. Bibcode:2011JThBi.291...47S. doi:10.1016/j.jtbi.2011.09.019. ISSN 0022-5193. PMID 21959317.</ref><ref name=":9">Fromm, Jörg; Lautner, Silke (2007). "Electrical signals and their physiological significance in plants". Plant, Cell & Environment. 30 (3): 249–257. doi:10.1111/j.1365-3040.2006.01614.x. ISSN 1365-3040. PMID 17263772.</ref><ref name=":7" /><ref name=":10">Vodeneev, V. A.; Opritov, V. A.; Pyatygin, S. S. (2006-07-01). "Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo". Russian Journal of Plant Physiology. 53 (4): 481–487. doi:10.1134/S102144370604008X. ISSN 1608-3407. S2CID 5037025.</ref><ref name=":11">Krol, Elzbieta; Dziubinska, Halina; Trebacz, Kazimierz (2003-05-15). "Low-Temperature Induced Transmembrane Potential Changes in the Liverwort Conocephalum conicum". Plant and Cell Physiology. 44 (5): 527–533. doi:10.1093/pcp/pcg070. ISSN 0032-0781. PMID 12773639.</ref><ref name=":13">Wacke, M.; Thiel, G.; Hütt, M.-T. (2003-02-01). "Ca2+ Dynamics during Membrane Excitation of Green Alga Chara: Model Simulations and Experimental Data". The Journal of Membrane Biology. 191 (3): 179–192. doi:10.1007/s00232-002-1054-0. ISSN 1432-1424. PMID 12571752. S2CID 15569873.</ref><ref name=":14">Tucker, E. B.; Boss, W. F. (June 1996). "Mastoparan-Induced Intracellular Ca2+ Fluxes May Regulate Cell-to-Cell Communication in Plants". Plant Physiology. 111 (2): 459–467. doi:10.1104/pp.111.2.459. ISSN 0032-0889. PMC 157856. PMID 12226302.</ref>
- A stimulus transitorily and reversibly activates calcium ion channels
- A short burst of calcium ions into the cell through the open calcium channels
- Calcium ions reversibly inactivate H+-ATPase activity
- Depolarization (due to calcium ion influx) activates voltage gated chloride channels causing chloride ions to leave the cell and cause further depolarization
- Calcium-ATPases decreases intracellular calcium concentration by pumping calcium ions to the outside of the cell (this allows for the H+-ATPase to be reactivated and repolarization to be initiated)
- Repolarization occurs when the activated H+-ATPase pumps H+ out of the cell and the open K+ channels allow for the flow of K+ to the outside of the cell
Plant resting membrane potentials range from -80 to -200 mV.<ref name=":9" /><ref name=":8" /> High H+-ATPase activity corresponds with hyperpolarization (up to -200mV), making it harder to depolarize and fire an action potential.<ref name=":8" /><ref name=":7" /><ref name=":10" /><ref name=":15">Johns, Sarah; Hagihara, Takuma; Toyota, Masatsugu; Gilroy, Simon (2021-04-02). "The fast and the furious: rapid long-range signaling in plants". Plant Physiology. 185 (3): 694–706. doi:10.1093/plphys/kiaa098. ISSN 1532-2548. PMC 8133610. PMID 33793939.</ref> This is why it is essential for calcium ions to inactivate H+-ATPase activity so that depolarization can be reached.<ref name=":7" /><ref name=":10" /> When the voltage gated chloride channels are activated and full depolarization occurs, calcium ions are pumped out of the cell (via a calcium-ATPase) after so that H+-ATPase activity resumes so that the cell can repolarize.<ref name=":7" /><ref name=":10" />
Calcium's interaction with the H+-ATPase is through a kinase.<ref name=":10" /> Therefore, calcium's influx causes the activation of a kinase that phosphorylates and deactivates the H+-ATPase so that the cell can depolarize.<ref name=":10" /> It is unclear whether all of the heightened calcium ion intracellular concentration is solely due to calcium channel activation. It is possible that the transitory activation of calcium channels causes an influx of calcium ions into the cell which activates intracellular stores of calcium ions to be released and subsequently causes depolarization (through the inactivation of H+-ATPase and activation of voltage gated chloride channels).<ref name=":10" /><ref name=":11" /><ref name=":13" /><ref name=":14" />
Variation potentials have proven hard to study and their mechanism is less well known than action potentials.<ref name=":16">Dziubińska, Halina; Trębacz, Kazimierz; Zawadzki, Tadeusz (2001-01-01). "Transmission route for action potentials and variation potentials in Helianthus annuus L." Journal of Plant Physiology. 158 (9): 1167–1172. doi:10.1078/S0176-1617(04)70143-1. ISSN 0176-1617.</ref> Variation potentials are slower than action potentials, are not considered “all or nothing,” and they themselves can trigger several action potentials.<ref name=":9" /><ref name=":16" /><ref name=":15" /><ref name=":17">Pickard, Barbara G. (1973). "Action Potentials in Higher Plants". Botanical Review. 39 (2): 172–201. Bibcode:1973BotRv..39..172P. doi:10.1007/BF02859299. ISSN 0006-8101. JSTOR 4353850. S2CID 5026557.</ref> The current understanding is that upon wounding or other stressful events, a plant's turgor pressure changes which releases a hydraulic wave throughout the plant that is transmitted through the xylem.<ref name=":9" /><ref>Stankovic, B.; Zawadzki, T.; Davies, E. (November 1997). "Characterization of the Variation Potential in Sunflower". Plant Physiology. 115 (3): 1083–1088. doi:10.1104/pp.115.3.1083. ISSN 0032-0889. PMC 158572. PMID 12223859.</ref> This hydraulic wave may activate pressure gated channels due to the sudden change in pressure.<ref>Farmer, Edward E.; Gao, Yong-Qiang; Lenzoni, Gioia; Wolfender, Jean-Luc; Wu, Qian (2020). "Wound- and mechanostimulated electrical signals control hormone responses". New Phytologist. 227 (4): 1037–1050. doi:10.1111/nph.16646. ISSN 1469-8137. PMID 32392391.</ref> Their ionic mechanism is very different from action potentials and is thought to involve the inactivation of the P-type H+-ATPase.<ref name=":9" /><ref>Stahlberg, Rainer; Cleland, Robert E.; Van Volkenburgh, Elizabeth (2006), Baluška, František; Mancuso, Stefano; Volkmann, Dieter (eds.), "Slow Wave Potentials — a Propagating Electrical Signal Unique to Higher Plants", Communication in Plants: Neuronal Aspects of Plant Life, Berlin, Heidelberg: Springer, pp. 291–308, doi:10.1007/978-3-540-28516-8_20, ISBN 978-3-540-28516-8, retrieved 2021-06-03</ref>
Long distance electrical signaling in plants is characterized by electrical signaling that occurs over distances greater than the span of a single cell.<ref name=":18">Thain, J.F.; Wildon, D.C. (1992). "Electrical signalling in plants". Science Progress (1933- ). 76 (3/4 (301/302)): 553–564. ISSN 0036-8504. JSTOR 43421317.</ref> In 1873, Sir John Burdon-Sanderson described action potentials and their long-distance propagation throughout plants.<ref name=":17" /> Action potentials in plants are carried out through a plants vascular network (particularly the phloem),<ref name=":19">Volkov, Alexander G.; Shtessel, Yuri B. (2020-01-01). "Underground electrotonic signal transmission between plants". Communicative & Integrative Biology. 13 (1): 54–58. doi:10.1080/19420889.2020.1757207. PMC 7202782. PMID 32395195.</ref> a network of tissues that connects all of the various plant organs, transporting signaling molecules throughout the plant.<ref name=":18" /> Increasing the frequency of action potentials causes the phloem to become increasingly cross linked.<ref>Calvo, Paco; Sahi, Vaidurya Pratap; Trewavas, Anthony (2017). "Are plants sentient?". Plant, Cell & Environment. 40 (11): 2858–2869. doi:10.1111/pce.13065. ISSN 1365-3040. PMID 28875517.</ref> In the phloem, the propagation of action potentials is dictated by the fluxes of chloride, potassium, and calcium ions, but the exact mechanism for propagation is not well understood.<ref>Fromm, Joerg; Hajirezaei, Mohammad-Reza; Becker, Verena Katharina; Lautner, Silke (2013). "Electrical signaling along the phloem and its physiological responses in the maize leaf". Frontiers in Plant Science. 4: 239. doi:10.3389/fpls.2013.00239. ISSN 1664-462X. PMC 3701874. PMID 23847642.</ref> Alternatively, the transport of action potentials over short, local distances is distributed throughout the plant via plasmodesmatal connections between cells.<ref name=":19" />
When a plant responds to stimuli, sometimes the response time is nearly instantaneous which is much faster than chemical signals are able to travel. Current research suggests that electrical signaling may be responsible.<ref>Wildon, D. C.; Thain, J. F.; Minchin, P. E. H.; Gubb, I. R.; Reilly, A. J.; Skipper, Y. D.; Doherty, H. M.; O'Donnell, P. J.; Bowles, D. J. (November 1992). "Electrical signalling and systemic proteinase inhibitor induction in the wounded plant". Nature. 360 (6399): 62–65. Bibcode:1992Natur.360...62W. doi:10.1038/360062a0. ISSN 1476-4687. S2CID 4274162.</ref><ref name=":20">Vian, Alain; Henry-Vian, Chantal; Davies, Eric (October 1999). "Rapid and Systemic Accumulation of Chloroplast mRNA-Binding Protein Transcripts after Flame Stimulus in Tomato". Plant Physiology. 121 (2): 517–524. doi:10.1104/pp.121.2.517. ISSN 0032-0889. PMC 59414. PMID 10517843.</ref><ref name=":21">Stanković, Bratislav; Davies, Eric (1997-07-01). "Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato". Planta. 202 (4): 402–406. Bibcode:1997Plant.202..402S. doi:10.1007/s004250050143. ISSN 1432-2048. S2CID 5018084.</ref><ref name=":23">Roux, David; Vian, Alain; Girard, Sébastien; Bonnet, Pierre; Paladian, Françoise; Davies, Eric; Ledoigt, Gérard (2006). "Electromagnetic fields (900 MHz) evoke consistent molecular responses in tomato plants". Physiologia Plantarum. 128 (2): 283–288. doi:10.1111/j.1399-3054.2006.00740.x. ISSN 1399-3054.</ref> In particular, the response of a plant to a wound is triphasic.<ref name=":20" /> Phase 1 is an immediate great increase in expression of target genes.<ref name=":20" /> Phase 2 is a period of dormancy.<ref name=":20" /> Phase 3 is a weakened and delayed upregulation of the same target genes as phase 1.<ref name=":20" /> In phase 1, the speed of upregulation is nearly instantaneous which has led researchers to theorize that the initial response from a plant is through action potentials and variation potentials as opposed to chemical or hormonal signaling which is most likely responsible for the phase 3 response.<ref name=":20" /><ref name=":21" /><ref name=":23" />
Upon stressful events, there is variation in a plant's response. That is to say, it is not always the case that a plant responds with an action potential or variation potential.<ref name=":20" /> However, when a plant does generate either an action potential or variation potential, one of the direct effects can be an upregulation of a certain gene's expression.<ref name=":21" /> In particular, protease inhibitors and calmodulin exhibit rapid upregulated gene expression.<ref name=":21" /> Additionally, ethylene has shown quick upregulation in the fruit of a plant as well as jasmonate in neighboring leaves to a wound.<ref>Inaba, Akitsugu; Manabe, Taro; Tsuji, Hiroyuki; Iwamoto, Tomotada (1995). "Electrical Impedance Analysis of Tissue Properties Associated with Ethylene Induction by Electric Currents in Cucumber (Cucumis sativus L.) Fruit". Plant Physiology. 107 (1): 199–205. doi:10.1104/pp.107.1.199. ISSN 0032-0889. JSTOR 4276290. PMC 161186. PMID 12228354.</ref><ref>Salvador-Recatalà, Vicenta; Tjallingii, W. Freddy; Farmer, Edward E. (2014). "Real-time, in vivo intracellular recordings of caterpillar-induced depolarization waves in sieve elements using aphid electrodes". New Phytologist. 203 (2): 674–684. doi:10.1111/nph.12807. ISSN 1469-8137. PMID 24716546. S2CID 19489725.</ref> Aside from gene expression, action potentials and variation potentials also can result in stomatal and leaf movement.<ref>Devireddy, Amith R.; Arbogast, Jimmie; Mittler, Ron (2020). "Coordinated and rapid whole-plant systemic stomatal responses". New Phytologist. 225 (1): 21–25. doi:10.1111/nph.16143. ISSN 1469-8137. PMID 31454419.</ref><ref>Kurenda, Andrzej; Nguyen, Chi Tam; Chételat, Aurore; Stolz, Stéphanie; Farmer, Edward E. (2019-12-17). "Insect-damaged Arabidopsis moves like wounded Mimosa pudica". Proceedings of the National Academy of Sciences. 116 (51): 26066–26071. Bibcode:2019PNAS..11626066K. doi:10.1073/pnas.1912386116. ISSN 0027-8424. PMC 6926025. PMID 31792188.</ref>
In summary, electric signaling in plants is a powerful tool of communication and controls a plant's response to dangerous stimuli (like herbivory), helping to maintain homeostasis.
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.<ref name=":02">"PEA Pisum sativum" (PDF). United States Department of Agriculture Natural Resources Conservation Service.</ref> 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.<ref name=":12">Falik, Omer; Mordoch, Yonat; Quansah, Lydia; Fait, Aaron; Novoplansky, Ariel (2011-11-02). Kroymann, Juergen (ed.). "Rumor Has It…: Relay Communication of Stress Cues in Plants". PLOS ONE. 6 (11): e23625. Bibcode:2011PLoSO...623625F. doi:10.1371/journal.pone.0023625. ISSN 1932-6203. PMC 3206794. PMID 22073135.</ref> 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.<ref name=":12" />
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.<ref name=":12" /> 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).<ref name=":22">Delory, Benjamin M.; Delaplace, Pierre; Fauconnier, Marie-Laure; du Jardin, Patrick (May 2016). "Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions?". Plant and Soil. 402 (1–2): 1–26. Bibcode:2016PlSoi.402....1D. doi:10.1007/s11104-016-2823-3. ISSN 0032-079X.</ref> 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.<ref name=":22" /> Moreover, Kegge et al. demonstrated that plants perceive the presence of neighbors through changes in water/nutrient availability, root exudates, and soil microorganisms.<ref name=":3">Kegge, Wouter; Pierik, Ronald (March 2010). "Biogenic volatile organic compounds and plant competition". Trends in Plant Science. 15 (3): 126–132. doi:10.1016/j.tplants.2009.11.007. PMID 20036599.</ref>
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).<ref name=":12" /> 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.<ref name=":4">Robbins, N. E.; Trontin, C.; Duan, L.; Dinneny, J. R. (2014-10-01). "Beyond the Barrier: Communication in the Root through the Endodermis". Plant Physiology. 166 (2): 551–559. doi:10.1104/pp.114.244871. ISSN 0032-0889. PMC 4213087. PMID 25125504.</ref> 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.<ref name=":5">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.</ref> 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
Another form of plant communication occurs through their root networks. Through roots, plants can share many different resources including carbon, nitrogen, and other nutrients. 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.<ref name=philip2010>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.</ref> 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 labeled carbon exchanged between seedlings. It was discovered that there was indeed a bi-directional sharing of carbon between the two tree species, with the Douglas-fir receiving a slight net gain in carbon. 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.<ref name=philip2010/> 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.<ref>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.</ref> 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.
Acoustic communication
Recent works have shown that plants can respond to airborne sounds at audible frequencies <ref>Veits, M., Khait, I., Obolski, U., Zinger, E., Boonman, A., Goldshtein, A., Saban, K., Seltzer, R., Ben-Dor, U., Estlein, P., Kabat, A., Peretz, D., Ratzersdorfer, I., Krylov, S., Chamovitz, D., Sapir, Y., Yovel, Y. and Hadany, L. (2019), Flowers respond to pollinator sound within minutes by increasing nectar sugar concentration. Ecol Lett, 22: 1483-1492. https://doi.org/10.1111/ele.13331</ref> and that they also produce airborne sounds at the ultrasonic range (for example, tomato and tobacco plants when cut with scissors), presumably audible to multiple organisms including bats, mice, moths and other insects.<ref>Khait I, Lewin-Epstein O, Sharon R, Saban K, Goldstein R, Anikster Y, Zeron Y, Agassy C, Nizan S, Sharabi G, Perelman R, Boonman A, Sade N, Yovel Y, Hadany L. Sounds emitted by plants under stress are airborne and informative. Cell. 2023 Mar 30;186(7):1328-1336.e10. doi: 10.1016/j.cell.2023.03.009. PMID 37001499.</ref>
See also
References
Further reading
- Peter Wohlleben; Suzanne Simard; Tim Flannery (2016). The Hidden Life of Trees: What They Feel, How They Communicate―Discoveries from A Secret World. Translated by Jane Billinghurst. Greystone Books. ISBN 978-1771642484.
