Plant communication

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Plants are exposed to many stress factors such as disease, temperature changes, herbivory, injury and more. [1] 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, [2] other plants [3] (of the same or other species), animals, [4] insects, [5] and fungi. [6] 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. [7] Due to the physical/chemical constraints most VOCs are of low molecular mass (< 300 Da), are hydrophobic, and have high vapor pressures. [8] 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 [5] to the induction of chemical defenses of a neighboring plant before it is being attacked. [9] 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. [10] 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. [11] As related to the aspect of meaning-making, the field is also identified as phytosemiotics. [12]

Contents

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. [13]

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. [14]

Terpenoids

The terpenoid verbenone is a plant pheromone, signalling to insects that a tree is already infested by beetles. Verbenone3D.png
The terpenoid verbenone is a plant pheromone, signalling to insects that a tree is already infested by beetles.

Terpenoids facilitate communication between plants and insects, mammals, fungi, microorganisms, and other plants. [16] 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). [17]

Terpenoids are a large family of biological molecules with over 22,000 compounds. [18] 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. [19] The biosynthesis of terpenoids occurs via the methylerythritol phosphate (MEP) and mevalonic acid(MVA) pathways [7] both of which include isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) as key components. [20] The MEP pathway produces hemiterpenes, monoterpenes, diterpenes, and volatile carotenoid derivatives while the MVA pathway produces sesquiterpenes. [7]

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. [21] However, the mechanisms behind this electrical signaling are not well known and are a current topic of ongoing research. [22] A plant may produce electrical signaling in response to wounding, temperature extremes, high salt conditions, drought conditions, and other various stimuli. [22] [23]

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.” [24] This is the understood mechanism for how plant action potentials are initiated: [25] [26] [24] [27] [28] [29] [30]

Plant resting membrane potentials range from -80 to -200 mV. [26] [25] High H+-ATPase activity corresponds with hyperpolarization (up to -200mV), making it harder to depolarize and fire an action potential. [25] [24] [27] [31] This is why it is essential for calcium ions to inactivate H+-ATPase activity so that depolarization can be reached. [24] [27] 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. [24] [27]

Calcium's interaction with the H+-ATPase is through a kinase. [27] Therefore, calcium's influx causes the activation of a kinase that phosphorylates and deactivates the H+-ATPase so that the cell can depolarize. [27] 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). [27] [28] [29] [30]

Variation potentials have proven hard to study and their mechanism is less well known than action potentials. [32] Variation potentials are slower than action potentials, are not considered “all or nothing,” and they themselves can trigger several action potentials. [26] [32] [31] [33] 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. [26] [34] This hydraulic wave may activate pressure gated channels due to the sudden change in pressure. [35] Their ionic mechanism is very different from action potentials and is thought to involve the inactivation of the P-type H+-ATPase. [26] [36]

Long distance electrical signaling in plants is characterized by electrical signaling that occurs over distances greater than the span of a single cell. [37] In 1873, Sir John Burdon-Sanderson described action potentials and their long-distance propagation throughout plants. [33] Action potentials in plants are carried out through a plants vascular network (particularly the phloem), [38] a network of tissues that connects all of the various plant organs, transporting signaling molecules throughout the plant. [37] Increasing the frequency of action potentials causes the phloem to become increasingly cross linked. [39] 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. [40] Alternatively, the transport of action potentials over short, local distances is distributed throughout the plant via plasmodesmatal connections between cells. [38]

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. [41] [42] [43] [44] In particular, the response of a plant to a wound is triphasic. [42] Phase 1 is an immediate great increase in expression of target genes. [42] Phase 2 is a period of dormancy. [42] Phase 3 is a weakened and delayed upregulation of the same target genes as phase 1. [42] 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. [42] [43] [44]

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. [42] 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. [43] In particular, protease inhibitors and calmodulin exhibit rapid upregulated gene expression. [43] Additionally, ethylene has shown quick upregulation in the fruit of a plant as well as jasmonate in neighboring leaves to a wound. [45] [46] Aside from gene expression, action potentials and variation potentials also can result in stomatal and leaf movement. [47] [48]

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. [49] 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. [50] 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. [50]

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. [50] 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). [51] 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. [51] Moreover, Kegge et al. demonstrated that plants perceive the presence of neighbors through changes in water/nutrient availability, root exudates, and soil microorganisms. [52]

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). [50] 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. [53] 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. [54] 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. [55] 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. [55] 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. [56] 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

Studies have shown that plants can respond to airborne sounds at audible frequencies [57] and that they also produce airborne sounds at the ultrasonic range, presumably audible to multiple organisms including bats, mice, moths and other insects. [58]

See also

Related Research Articles

In cellular biology, active is the movement of molecules or ions across a cell membrane from a region of lower concentration to a region of higher concentration—against the concentration gradient. Active transport requires cellular energy to achieve this movement. There are two types of active transport: primary active transport that uses adenosine triphosphate (ATP), and secondary active transport that uses an electrochemical gradient. This process is in contrast to passive transport, which allows molecules or ions to move down their concentration gradient, from an area of high concentration to an area of low concentration, without energy.

<span class="mw-page-title-main">Action potential</span> Neuron communication by electric impulses

An action potential occurs when the membrane potential of a specific cell rapidly rises and falls. This depolarization then causes adjacent locations to similarly depolarize. Action potentials occur in several types of excitable cells, which include animal cells like neurons and muscle cells, as well as some plant cells. Certain endocrine cells such as pancreatic beta cells, and certain cells of the anterior pituitary gland are also excitable cells.

<span class="mw-page-title-main">Stimulus (physiology)</span> Detectable change in the internal or external surroundings

In physiology, a stimulus is a change in a living thing's internal or external environment. This change can be detected by an organism or organ using sensitivity, and leads to a physiological reaction. Sensory receptors can receive stimuli from outside the body, as in touch receptors found in the skin or light receptors in the eye, as well as from inside the body, as in chemoreceptors and mechanoreceptors. When a stimulus is detected by a sensory receptor, it can elicit a reflex via stimulus transduction. An internal stimulus is often the first component of a homeostatic control system. External stimuli are capable of producing systemic responses throughout the body, as in the fight-or-flight response. In order for a stimulus to be detected with high probability, its level of strength must exceed the absolute threshold; if a signal does reach threshold, the information is transmitted to the central nervous system (CNS), where it is integrated and a decision on how to react is made. Although stimuli commonly cause the body to respond, it is the CNS that finally determines whether a signal causes a reaction or not.

<span class="mw-page-title-main">Jasmonate</span> Lipid-based plant hormones

Jasmonate (JA) and its derivatives are lipid-based plant hormones that regulate a wide range of processes in plants, ranging from growth and photosynthesis to reproductive development. In particular, JAs are critical for plant defense against herbivory and plant responses to poor environmental conditions and other kinds of abiotic and biotic challenges. Some JAs can also be released as volatile organic compounds (VOCs) to permit communication between plants in anticipation of mutual dangers.

<span class="mw-page-title-main">Cardiac action potential</span> Biological process in the heart

Unlike the action potential in skeletal muscle cells, the cardiac action potential is not initiated by nervous activity. Instead, it arises from a group of specialized cells known as pacemaker cells, that have automatic action potential generation capability. In healthy hearts, these cells form the cardiac pacemaker and are found in the sinoatrial node in the right atrium. They produce roughly 60–100 action potentials every minute. The action potential passes along the cell membrane causing the cell to contract, therefore the activity of the sinoatrial node results in a resting heart rate of roughly 60–100 beats per minute. All cardiac muscle cells are electrically linked to one another, by intercalated discs which allow the action potential to pass from one cell to the next. This means that all atrial cells can contract together, and then all ventricular cells.

<span class="mw-page-title-main">Muscle contraction</span> Activation of tension-generating sites in muscle

Muscle contraction is the activation of tension-generating sites within muscle cells. In physiology, muscle contraction does not necessarily mean muscle shortening because muscle tension can be produced without changes in muscle length, such as when holding something heavy in the same position. The termination of muscle contraction is followed by muscle relaxation, which is a return of the muscle fibers to their low tension-generating state.

<span class="mw-page-title-main">T-tubule</span> Extensions in cell membrane of muscle fibres

T-tubules are extensions of the cell membrane that penetrate into the center of skeletal and cardiac muscle cells. With membranes that contain large concentrations of ion channels, transporters, and pumps, T-tubules permit rapid transmission of the action potential into the cell, and also play an important role in regulating cellular calcium concentration.

<span class="mw-page-title-main">Guard cell</span> Paired cells that control the stomatal aperture

Guard cells are specialized plant cells in the epidermis of leaves, stems and other organs that are used to control gas exchange. They are produced in pairs with a gap between them that forms a stomatal pore. The stomatal pores are largest when water is freely available and the guard cells become turgid, and closed when water availability is critically low and the guard cells become flaccid. Photosynthesis depends on the diffusion of carbon dioxide (CO2) from the air through the stomata into the mesophyll tissues. Oxygen (O2), produced as a byproduct of photosynthesis, exits the plant via the stomata. When the stomata are open, water is lost by evaporation and must be replaced via the transpiration stream, with water taken up by the roots. Plants must balance the amount of CO2 absorbed from the air with the water loss through the stomatal pores, and this is achieved by both active and passive control of guard cell turgor pressure and stomatal pore size.

<span class="mw-page-title-main">Systemin</span> Plant peptide hormone

Systemin is a plant peptide hormone involved in the wound response in the family Solanaceae. It was the first plant hormone that was proven to be a peptide having been isolated from tomato leaves in 1991 by a group led by Clarence A. Ryan. Since then, other peptides with similar functions have been identified in tomato and outside of the Solanaceae. Hydroxyproline-rich glycopeptides were found in tobacco in 2001 and AtPeps were found in Arabidopsis thaliana in 2006. Their precursors are found both in the cytoplasm and cell walls of plant cells, upon insect damage, the precursors are processed to produce one or more mature peptides. The receptor for systemin was first thought to be the same as the brassinolide receptor but this is now uncertain. The signal transduction processes that occur after the peptides bind are similar to the cytokine-mediated inflammatory immune response in animals. Early experiments showed that systemin travelled around the plant after insects had damaged the plant, activating systemic acquired resistance, now it is thought that it increases the production of jasmonic acid causing the same result. The main function of systemins is to coordinate defensive responses against insect herbivores but they also affect plant development. Systemin induces the production of protease inhibitors which protect against insect herbivores, other peptides activate defensins and modify root growth. They have also been shown to affect plants' responses to salt stress and UV radiation. AtPEPs have been shown to affect resistance against oomycetes and may allow A. thaliana to distinguish between different pathogens. In Nicotiana attenuata, some of the peptides have stopped being involved in defensive roles and instead affect flower morphology.

<span class="mw-page-title-main">Synapse</span> Structure connecting neurons in the nervous system

In the nervous system, a synapse is a structure that permits a neuron to pass an electrical or chemical signal to another neuron or to the target effector cell. In case of electrical synapses, neurons are coupled bidirectionally in continuous-time to each other and are known to produce synchronous network activity in the brain.

The sodium-calcium exchanger (often denoted Na+/Ca2+ exchanger, exchange protein, or NCX) is an antiporter membrane protein that removes calcium from cells. It uses the energy that is stored in the electrochemical gradient of sodium (Na+) by allowing Na+ to flow down its gradient across the plasma membrane in exchange for the countertransport of calcium ions (Ca2+). A single calcium ion is exported for the import of three sodium ions. The exchanger exists in many different cell types and animal species. The NCX is considered one of the most important cellular mechanisms for removing Ca2+.

<span class="mw-page-title-main">Plant perception (physiology)</span> Plants interaction to environment

Plant perception is the ability of plants to sense and respond to the environment by adjusting their morphology and physiology. Botanical research has revealed that plants are capable of reacting to a broad range of stimuli, including chemicals, gravity, light, moisture, infections, temperature, oxygen and carbon dioxide concentrations, parasite infestation, disease, physical disruption, sound, and touch. The scientific study of plant perception is informed by numerous disciplines, such as plant physiology, ecology, and molecular biology.

<span class="mw-page-title-main">Gating (electrophysiology)</span>

In electrophysiology, the term gating refers to the opening (activation) or closing of ion channels. This change in conformation is a response to changes in transmembrane voltage.

In biology, electrotropism, also known as galvanotropism, is a kind of tropism which results in growth or migration of an organism, usually a cell, in response to an exogenous electric field. Several types of cells such as nerve cells, muscle cells, fibroblasts, epithelial cells, green algae, spores, and pollen tubes, among others, have been already reported to respond by either growing or migrating in a preferential direction when exposed to an electric field.

<span class="mw-page-title-main">Mycorrhizal network</span> Underground fungal networks that connect individual plants together

A mycorrhizal network is an underground network found in forests and other plant communities, created by the hyphae of mycorrhizal fungi joining with plant roots. This network connects individual plants together. Mycorrhizal relationships are most commonly mutualistic, with both partners benefiting, but can be commensal or parasitic, and a single partnership may change between any of the three types of symbiosis at different times.

A variation potential (VP) is a hydraulically propagating electrical signal occurring exclusively in plant cells. It is one of three propagating signals in plants, the other two being action potential (AP) and wound potential (WP). Variation potentials are responsible for the induction of many physiological processes and are a mechanism for plant systematic responses to local wounding. They induce changes in gene expression; the production of abscisic acid, jasmonic acid, and ethylene; temporary decreases in photosynthesis; and increases in respiration. Variation potentials have been widely shown in vascular plants.

<span class="mw-page-title-main">Floral scent</span>

Floral scent, or flower scent, is composed of all the volatile organic compounds (VOCs), or aroma compounds, emitted by floral tissue. Other names for floral scent include, aroma, fragrance, floral odour or perfume. Flower scent of most flowering plant species encompasses a diversity of VOCs, sometimes up to several hundred different compounds. The primary functions of floral scent are to deter herbivores and especially folivorous insects, and to attract pollinators. Floral scent is one of the most important communication channels mediating plant-pollinator interactions, along with visual cues.

In plant biology, plant memory describes the ability of a plant to retain information from experienced stimuli and respond at a later time. For example, some plants have been observed to raise their leaves synchronously with the rising of the sun. Other plants produce new leaves in the spring after overwintering. Many experiments have been conducted into a plant's capacity for memory, including sensory, short-term, and long-term. The most basic learning and memory functions in animals have been observed in some plant species, and it has been proposed that the development of these basic memory mechanisms may have developed in an early organismal ancestor.

Hydraulic signals in plants are detected as changes in the organism's water potential that are caused by environmental stress like drought or wounding. The cohesion and tension properties of water allow for these water potential changes to be transmitted throughout the plant.

Chemical defenses in <i>Cannabis</i> Defense of Cannabis plant from pathogens

Cannabis (/ˈkænəbɪs/) is commonly known as marijuana or hemp and has two known strains: Cannabis sativa and Cannabis indica, both of which produce chemicals to deter herbivory. The chemical composition includes specialized terpenes and cannabinoids, mainly tetrahydrocannabinol (THC), and cannabidiol (CBD). These substances play a role in defending the plant from pathogens including insects, fungi, viruses and bacteria. THC and CBD are stored mostly in the trichomes of the plant, and can cause psychological and physical impairment in the user, via the endocannabinoid system and unique receptors. THC increases dopamine levels in the brain, which attributes to the euphoric and relaxed feelings cannabis provides. As THC is a secondary metabolite, it poses no known effects towards plant development, growth, and reproduction. However, some studies show secondary metabolites such as cannabinoids, flavonoids, and terpenes are used as defense mechanisms against biotic and abiotic environmental stressors.

References

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