Manual Long-Distance Systemic Signaling and Communication in Plants: 19

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Contents

  1. Cell signaling
  2. CSIRO PUBLISHING | Functional Plant Biology
  3. Similar titles

However, quenching can also be a factor in ROS diffusing through a symplastic connection. An alternative model for propagating the ROS wave from cell to cell is that a different signaling molecule is used as a relay to traverse the symplastic or apoplastic connections. A third alternative is the propagation of an electrical signal along the PM connection through the PD.

Further research is needed to address this and all other questions outlined above. In addition to the currently open question as to the precise route that transfers rapid systemic signals between adjacent plant cells, understanding the role that the plant cell types or tissues play in mediating these systemic signals also holds promise to help reveal mechanism and function.

From the standpoint of number, size and PD characteristics, phloem tissue, companion cells and the epidermis contain a high number of cellular connections and could be a good pathway for the transfer of different systemic signals that propagate through both the apoplast and PD. Thus, rapid acidification of the apoplast in response to inoculation of the roots with chlamydospores of the mycorrhizal fungus Piriformospora indica was observed in the root elongation zone within seconds to minutes in barley Hordeum vulgare L.

This variability in speeds may well relate to the type of stress triggering the signaling events e. This secretome analysis during pollen tube growth hints at the wealth of macromolecules that are dynamically released to the apoplast. However, whether such signals are contributing to modulating systemic signaling or potentially even move in a systemic manner themselves remains to be fully defined. The specificity of the systemic signal is dependent on the ability of that signal to elicit responses in unaffected tissue to protect or defend the plant from a second occurrence of that same or tightly associated stress e.

These types of experiments indicate that a significant degree of overlap exists between systemic signaling events and the mechanisms that respond to it. From an evolutionary point of view, sending a general stress message to all parts of the plant may be an efficient means to rapidly prepare all of its tissues for the upcoming challenges and increase its survival chances. Are they dependent or independent? These genes may represent the frontline of general systemic response to the initial priming signal common to most abiotic stresses. Clues to this process may again be seen in the ROS responsive network.

The authors apologize to the many research groups whose work is not cited in this review due to space limitation. Volume 90 , Issue 4. If you do not receive an email within 10 minutes, your email address may not be registered, and you may need to create a new Wiley Online Library account. If the address matches an existing account you will receive an email with instructions to retrieve your username.

The Plant Journal Volume 90, Issue 4. Jeffrey Harper Corresponding Author E-mail address: jfharper unr. Tools Request permission Export citation Add to favorites Track citation. Share Give access Share full text access.

Movement of RNA and proteins in plants

Share full text access. Please review our Terms and Conditions of Use and check box below to share full-text version of article. A recent study, however, demonstrates how the plastidial methylerythritol phosphate MEP pathway may be involved in biotic stress signal- ling in addition to the production of isoprenoids via an isoprenoid precursor, MEcPP Xiao et al.

Another possible retrograde signalling molecule is a phosphonucleotide 30 -phosphoadenosine 50 -phosphate [PAP] , which accumulates in response to drought and HL stress Estavillo et al. PAP can be transported out of the chloroplast Gigolashvilia et al. Pogson Estavillo et al. There are, however, likely to be additional unknown pathways present, further complicating the signalling processes. Additional complications from the crosstalk that occurs between many of the pathways under HL as well as between signals from different abiotic stresses make it difficult to isolate individual pathways Laloi et al.

One type of antagonistic crosstalk particularly relevant to HL signalling is between the two distinct ROS signalling pathways. The basal presence of EDS1 favours the default response of cell death Straus et al. EDS1 was originally associated with the development of the hypersensitive response HR to pathogen attack and innate immunity Keen ; Shinozaki and Yamaguchi-Shinozaki The major characteristic of HR is the formation of a zone of dead cells around the infected area similar to the development of patches of bleached tissue within leaves undergoing oxidative stress.

It is proposed that the EDS1 regulatory switch controlling accumulation of ROS in the apoplast is part of a universal stress signalling network and part of cross-tolerance between biotic and abiotic stresses Miller et al. Intercellular signalling has been a major focus of more recent SAA studies. Miller et al. The lsd1 mutant also fails to acclimate to HL stress and succumbs to photooxidative stress Mateo et al. Another study shows that H2O2 accumulates specifically in BSCs that surround the vasculature, as well as in their surrounding apoplastic spaces Galvez-Valdivieso et al.

These studies only make observations on how a signal is directed within a single leaf or, in the case of the rbohD study, the floral bolt of a flowering plant Galvez-Valdivieso et al. Two models have been proposed that focus on local lesion spread within the one leaf Mittler et al. While both explain the local response of a signal between different cell types such as the mesophyll and bundle sheath cells of a single leaf, it is still not understood how the signal can then travel through the vasculature to other leaves within the Arabidopsis rosette, or how a plant produces different responses to specific types of stress.

Further application of techniques used to study biotic long-distance signalling needs to be applied to abiotic stress signalling research, particularly in regard to how an abiotic signal is able to rapidly travel through the vasculature from leaf to leaf. Systemic Photooxidative Stress Signalling 4.

An Arabidopsis leaf is characterised by a midvein which is continuous with the stem vascular bundles. A layer of bundle sheath cells BSCs entirely surrounds the vascular tissues and acts as an interface between these and the mesophyll tissues Kinsman and Pyke ; Leegood While BSCs are able to sense stress signals within xylem sap and can control the flux of solutes and water from the xylem to the mesophyll via the downregulation of plant aquaporin AQP activity Shatil-Cohen et al. Possible mechanisms involve either free movement through the apoplast Evert et al.

Early studies of xylem-mesophyll flow speculated that the osmotic water permeability of the BSC membrane was too low to support the transpiration stream Boyer The apoplastic route was therefore initially considered to be the major route for xylem-sap transport; however, the discovery of suberin deposits in leaf BSCs has since indicated otherwise Sack and Holbrook Mutant analysis of gdu1, with a mutation in a vascular glutamine transporter, and ost, defective in ABA signalling and stomata closure, also demonstrates the existence of a hydraulic and solute transport barrier within BSCs Ache et al.

A more recent study additionally demonstrates that BSCs are not only able to block small solutes but also water Shatil-Cohen et al. Along with the discovery of plant aquaporins AQPs , these findings indicate that the BSC plasma membrane is able to support active water and solute transport. Interestingly, both mesophyll and BSCs contain chloroplasts, and an as yet unanswered question remains as to whether BSC chloroplasts have a specialised purpose in sensing rapid stress induction and relaying these signals directly into the phloem vascular stream.

Fluxes of water are controlled by the hydraulic conductiv- ity of the leaf Kleaf Martre et al. Also, stress-induced H2O2 was shown to accumulate locally in the surrounding intercellular spaces of BSCs, but not in the mesophyll Fryer et al. At the whole-plant level, plasmodesmata Pd have important roles in photoassimilate translocation from source to sink leaves through the phloem.

Pogson sheath and phloem parenchyma cells is first exported into the apoplast and is then actively loaded into the sieve element companion cell CC complex Lalonde et al. The signal must be loaded into the phloem stream via CC then move from this site to the shoot apical meristem SAM. Arrival at the SAM requires post-phloem transport involving local cell-to-cell transport Turnbull For a rapid signal, questions remain regarding whether a signal could bypass the SAM and travel directly to distal leaves. A widely accepted hypothesis is that environmental cues are sensed by mature organs and this information is transported to meristematic regions where newly formed tissues adopt a new developmental fate Lough and Lucas Two outcomes of long-distance pathogen defence signalling are to either pre-emptively activate defence mechanisms in distal parts of the plant or to prime those tissues as a way of preparing them for an augmented response to future attack.

Priming is less costly than activating defence mechanisms Heil and Ton , although whether abiotic SAA can be classified as a priming response is as yet unclear. Three strategies to prove signal transmission according to Turnbull is to demonstrate the movement of the putative signal molecule, a phenotypic change, and the altered expression of a molecular target.

While transcriptional and pheno- typic changes have been predominantly studied, proof of signal movement is more difficult. Traditional methods for studying long-distance signals have involved two different approaches: biochemical approaches that follow the physical movement of the signal and grafting experiments that include mutants defective in either the production or the perception of the signal Heil and Ton The vascular system of a plant acts as a transport pathway for water and nutrients as well as a long- distance communication network, specifically interorgan communication.

Plants with large vasculature such as tomato and tobacco have been the model organisms of choice for the study of long-distance signalling in plants.

Cell signaling

However, adapting these techniques for use in Arabidopsis where most molecular and physiological studies have been performed would be of more use Bainbridge et al. It was also recently shown that microarrays of and fold HL treatments of 6 h and 12 h duration showed that the ABA response is not associated with the HL response at these time points Oelze et al. There is, however, strong evidence supporting the involvement of ABA signalling, if not the hormone itself, in certain cell types such as guard cells and BSCs that could then initiate the unknown long- distance signal Mullineaux and Baker This suggests the involvement of ABA in retrograde signalling or indeed a novel plant hormone.

While chemical signals have been increasingly demonstrated to be responsible for root-shoot signalling, particularly in response to drought stress, there is also evidence supporting hydraulic signals, usually in a source-to-sink direction Jia and Zhang Hydraulic root-derived signals have been shown to be major regulators of stomatal behaviour potentially through modification of chemical concentration in the vasculature as a result of changes in water flux Fuchs and Livingston Hydraulics have the potential to transport complex signals as even though very low water potential does not appear to have a direct effect on stomatal aperture, it has still been shown to promote ABA-induced stomatal closure Tardieu and Davies Whether changes in plant hydraulics could result in a HL-derived signal being transported between photosynthesising tissues in the aerial part of the plant is unknown; however, signal movement from the vasculature to BSCs may very well be functioning in a similar way to ABA-transported vascular signals into stomatal guard cells.

There is also evidence of a rapid pH-based systemic drought signalling mecha- nism where foliar and xylem sap pH changes have been linked with ABA concen- tration within leaves Wilkinson and Davies Alterations in pH can be one of the first chemical changes measurable in xylem sap from plants exposed to drying soil Sobeih et al.

Pogson In terms of the root-shoot systemic regulation of stomatal aperture, ABA promotes ROS production that results in increases in cytosolic calcium leading to stomatal closure Kwak et al. The symplast of an adjacent cell is thought to remove ABA from the xylem or a leaf apoplast and is pH dependent. More alkaline sap pH values have been detected under stress conditions which reduced ABA-removing pH gradient across the membrane. In the case of guard cells, ABA accumulates to high enough levels to cause stomatal closure Jia and Zhang ; Wilkinson and Davies In addition to water and nutrients, recent studies of phloem sap have revealed the presence of numerous RNA transcripts and proteins Buhtz et al.

Small RNAs sRNAs would be ideal candidates for a long-distance signal as they are able to spread from cell to cell as well as through the vasculature in a non-cell autonomous manner Chitwood and Timmermans They also move in a predominantly source-to-sink direction leading to the hypoth- esis that sRNAs, along with photoassimilates, are transported into growing meristems Palauqui et al. The effect of potassium nutrition on pest and disease resistance in plants.

The interaction of plant biotic and abiotic stresses: from genes to the field. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Reduced growth of Alaskan white spruce in the twentieth century from temperature-induced drought stress. The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone.

Wound-induced hydraulic signals: survey of occurrence in a range of species. Signal crosstalk and induced resistance: straddling the line between cost and benefit. Signal conflicts and synergies in induced resistance to multiple attackers. Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. Leaf growth and turgor in growing cells of maize Zea mays L. Comparison between gradient-dependent hydraulic conductivities of roots using the root pressure probe: the role of pressure propagations and implications for the relative roles of parallel radial pathways.

Google Preview. Temperate forest tree and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Dynamics of membrane potential variation and gene expression induced by Spodoptera littoralis , Myzus persicae , and Pseudomonas syringae in Arabidopsis. Robotic mechanical wounding MecWorm versus herbivore-induced responses: early signaling and volatile emission in Lima bean Phaseolus lunatus L.

Interplay between insects and plants: dynamic and complex interactions that have coevolved over millions of years but act in milliseconds. Whole tree hydraulic conductance and water loss regulation in Quercus during drought: evidence for stomatal control of embolism. Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Effect of heat and drought stress on sorghum Sorghum bicolor.

Grain yield. Stomatal control by chemical signalling and the exploitation of this mechanism to increase water use efficiency in agriculture. Root signals and the regulation of growth and development of plants in drying soil. Determining water use by trees and forests from isotopic, energy balance and transpiration analyses: the roles of tree size and hydraulic lift. Del Amor. Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Role of nutrients in controlling plant diseases in sustainable agriculture: a review.

A comparison of growth, photosynthetic capacity and water stress in Eucalyptus globulus coppice regrowth and seedlings during early development. Temperature sensitivity of genes for resistance in wheat to Puccinia recondita. Resistance to broomrape Orobanche spp. Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells. Variation in vessel length and diameter in stems of six tropical and subtropical lianas. Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves.

Abiotic stress responses in plants: integrative genetic pathways and overlapping reactions between abiotic and biotic stress responses. Long-distance electrical signaling and physiological functions in higher plants. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Environmental stimuli and physiological responses: the current view on electrical signalling. A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling.

Spatial and temporal dynamics of jasmonate synthesis and accumulation in Arabidopsis in response to wounding. Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves. Do trees use reserve or newly assimilated carbon for their defense reactions? A 13 C labeling approach with young Scots pines inoculated with a bark-beetle-associated fungus Ophiostoma brunneo ciliatum. Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora. A comprehensive analysis of the combined effects of high light and high temperature stresses on gene expression in sunflower.

Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying.


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Comparative effect of water, heat and light stresses on photosynthetic reactions in Sorghum bicolor L. Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced abscisic acid signals. Initiation and regulation of water deficit-induced abscisic acid accumulation in maize leaves and roots: cellular volume and water relations. Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation.

In situ 13 CO 2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. Induced systemic resistance to rice blast fungus in rice plants infested by white-backed planthopper. Some aspects of induced resistance to rice blast fungus, Magnaporthe grisea , in rice plant infested by white-backed planthopper, Sogatella furcifera. Influence of rhizomania disease on gas exchange and water relations of a susceptible and a tolerant sugar beet variety.

Defensive function of herbivore-induced plant volatile emissions in nature. Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea.

Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Characteristics of electrical signals in poplar and responses in photosynthesis. Drought tolerance, xylem sap abscisic acid and stomatal conductance during soil drying: a comparison of canopy trees of three temperate deciduous angiosperms. Tree shoot bending generates hydraulic pressure pulses: a new long-distance signal.

Excitation of Characeae cell membranes as a result of activation of calcium and chloride channels. Effects of feeding Spodoptera littoralis on lima bean leaves. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Kinetics of wound-induced hydraulic signals and variation potentials in wheat seedlings.

An hydraulic interpretation of rapid, long-distance wound signalling in tomato. Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera. Contributions of natural and anthropogenic forcing to changes in temperature extremes over the United States.

CSIRO PUBLISHING | Functional Plant Biology

Combined effects of atmospheric CO 2 and N availability on the belowground carbon and nitrogen dynamics of aspen mesocosms. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv.

High-temperature effects on hypersensitive resistance to tomato spotted wilt tospovirus Tswv in pepper Capsicum-Chinense Jacq. Salinity stress inhibits bean leaf expansion by reducing turgor, not wall extensibility. Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Photosynthetic acclimation to simultaneous and interacting environmental stresses along natural light gradients: optimality and constraints. Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs.

Evidence for the transmission of information through electric potentials in injured avocado trees. The effect of root geometry on the yield of wheat growing on stored water. Regulation of hormonal responses of sweet pepper as affected by salinity and elevated CO 2 concentration.

Signaling events in plants: stress factors in combination change the picture. Growth and physiological responses of canola Brassica napus to three components of global climate change: temperature, carbon dioxide and drought. Day and night heat stress trigger different transcriptomic responses in green and ripening grapevine Vitis vinifera fruit.

Circadian rhythm of heat resistance in cotton seedlings synthesis of heat shock proteins. The combined effect of drought stress and heat shock on gene expression in tobacco. When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis.

Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange. On the electromotive properties of the leaf of Dionaea in the excited and unexcited states. Effects of short periods of drought and high temperature on grain growth and starch accumulation of two malting barley cultivars. Nonlinear temperature effects indicate severe damages to U. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants.

Decrement and amplification of slow wave potentials during their propagation in Helianthus annuus L. Slow wave potentials—a propagating electrical signal unique to higher plants. Comparison of electric and growth responses to excision in cucumber and pea seedlings. Short-distance effects are a result of wounding.

Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. Slow wave potentials in cucumber differ in form and growth effect from those in pea seedlings. Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato. Intercellular communication in plants: electrical stimulation of proteinase inhibitor gene expression in tomato. Action potentials and variation potentials in sunflower: an analysis of their relationships and distinguishing characteristics. Carbon fluxes to the soil in a mature temperate forest assessed by 13 C isotope tracing.

The cohesion—tension mechanism and the acquisition of water by plant roots. Signal interactions in pathogen and insect attack: systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum. Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Root pressurization affects growth-induced water potentials and growth in dehydrated maize leaves. Role of hydraulic and chemical signals in leaves, stems and roots in the stomatal behaviour of olive trees under water stress and recovery conditions.

The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Water-storage capacity of Thuja, Tsuga and Acer stems measured by dehydration isotherms. The contribution of capillary water and cavitation. Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia.

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System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Consequences of simultaneous elevation of carbon dioxide and temperature for plant—herbivore interactions: a metaanalysis. All rights reserved.

Long distance mirror signalling.

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