Plant responsiveness to root-root communication of stress cues

Background and Aims

Phenotypic plasticity is based on the organism''s ability to perceive, integrate and respond to multiple signals and cues informative of environmental opportunities and perils. A growing body of evidence demonstrates that plants are able to adapt to imminent threats by perceiving cues emitted from their damaged neighbours. Here, the hypothesis was tested that unstressed plants are able to perceive and respond to stress cues emitted from their drought- and osmotically stressed neighbours and to induce stress responses in additional unstressed plants.

Methods

Split-root Pisum sativum, Cynodon dactylon, Digitaria sanguinalis and Stenotaphrum secundatum plants were subjected to osmotic stress or drought while sharing one of their rooting volumes with an unstressed neighbour, which in turn shared its other rooting volume with additional unstressed neighbours. Following the kinetics of stomatal aperture allowed testing for stress responses in both the stressed plants and their unstressed neighbours.

Key Results

In both P. sativum plants and the three wild clonal grasses, infliction of osmotic stress or drought caused stomatal closure in both the stressed plants and in their unstressed neighbours. While both continuous osmotic stress and drought induced prolonged stomatal closure and limited acclimation in stressed plants, their unstressed neighbours habituated to the stress cues and opened their stomata 3–24 h after the beginning of stress induction.

Conclusions

The results demonstrate a novel type of plant communication, by which plants might be able to increase their readiness to probable future osmotic and drought stresses. Further work is underway to decipher the identity and mode of operation of the involved communication vectors and to assess the potential ecological costs and benefits of emitting and perceiving drought and osmotic stress cues under various ecological scenarios.     

Induction of priming by cold stress via inducible volatile cues in neighboring tea plants

Plants have evolved sophisticated defense mechanisms to overcome their sessile nature. However, if and how volatiles from cold‐stressed plants can trigger interplant communication is still unknown. Here, we provide the first evidence for interplant communication via inducible volatiles in cold stress. The volatiles, including nerolidol, geraniol, linalool, and methyl salicylate, emitted from cold‐stressed tea plants play key role(s) in priming cold tolerance of their neighbors via a C‐repeat‐binding factors‐dependent pathway. The knowledge will help us to understand how plants respond to volatile cues in cold stress and agricultural ecosystems.     

Acquired immunity to herbivory and allelopathy caused by airborne plant emissions

Numerous plant species respond to volatile cues to adjust their defenses against herbivores. Some volatile chemicals, such as terpenoids and green leaf volatiles, that are responsible for communication between plants and arthropods are also required for intraspecific communication between plants and for coordination among branches within a single plant. We are now aware that some ‘receiver’ plants are able to eavesdrop on their neighbors and tailor their defenses to their current and expected risks caused by herbivores. By contrast, a suite of volatiles also serve as natural herbicides (allelochemicals) that are detrimental for receiver plants. Since various molecular and ecological mechanisms underlying these phenomena have been clarified, it is time to ask whether more plants eavesdrop on infochemical cues, and if these cues that allow them to adjust their defenses to suit their risk also increase their fitness as a result.     

One stimulus—Two responses: Host and parasite life‐history variation in response to environmental stress

Climate change stressors will place different selective pressures on both parasites and their hosts, forcing individuals to modify their life‐history strategies and altering the distribution and prevalence of disease. Few studies have investigated whether parasites are able to respond to host stress and respond by varying their reproductive schedules. Additionally, multiple environmental stressors can limit the ability of a host to respond adaptively to parasite infection. This study compared both host and parasite life‐history parameters in unstressed and drought‐stressed environments using the human parasite, Schistosoma mansoni, in its freshwater snail intermediate host. Snail hosts infected with the parasite demonstrated a significant reproductive burst during the prepatent period (fecundity compensation), but that response was absent in a drought‐stressed environment. This is the first report of the elimination of host fecundity compensation to parasitism when exposed to additional environmental stress. More surprisingly, we found that infections in drought‐stressed snails had significantly higher parasite reproductive outputs than infections in unstressed snails. The finding suggests that climate change may alter the infection dynamics of this human parasite.     

Integration of two herbivore‐induced plant volatiles results in synergistic effects on plant defence and resistance

Plants can use induced volatiles to detect herbivore‐ and pathogen‐attacked neighbors and prime their defenses. Several individual volatile priming cues have been identified, but whether plants are able to integrate multiple cues from stress‐related volatile blends remains poorly understood. Here, we investigated how maize plants respond to two herbivore‐induced volatile priming cues with complementary information content, the green leaf volatile (Z)‐3‐hexenyl acetate (HAC) and the aromatic volatile indole. In the absence of herbivory, HAC directly induced defence gene expression, whereas indole had no effect. Upon induction by simulated herbivory, both volatiles increased jasmonate signalling, defence gene expression, and defensive secondary metabolite production and increased plant resistance. Plant resistance to caterpillars was more strongly induced in dual volatile‐exposed plants than plants exposed to single volatiles.. Induced defence levels in dual volatile‐exposed plants were significantly higher than predicted from the added effects of the individual volatiles, with the exception of induced plant volatile production, which showed no increase upon dual‐exposure relative to single exposure. Thus, plants can integrate different volatile cues into strong and specific responses that promote herbivore defence induction and resistance. Integrating multiple volatiles may be beneficial, as volatile blends are more reliable indicators of future stress than single cues.     

Distinct responses to copper stress in the halophyte Mesembryanthemum crystallinum

Selective gene expression allows the halophyte Mesembryanthemum crystallinum to survive a salt stress. To broaden our understanding of the environmental cues initiating diverse stress responses in this higher plant, unstressed and 0.4 M NaCl‐stressed plants were compared to plants treated with several concentrations of copper (CuSO₄), an increasingly relevant environmental heavy metal pollutant. Comparisons of control and copper‐stressed plants included germination, chlorophyll content, accumulation of proline, heat shock protein (HSP) 60 and a Crassulacean acid metabolism (CAM)‐specific marker enzyme, phospho enol pyruvate carboxylase (PEPCase). In germination and whole plant tests, M. crystallinum was significantly more tolerant to copper than Arabidopsis thaliana. Mature M. crystallinum plants stressed with 50 ppm CuSO₄ for 48 h became dehydrated. These plants produced a 4‐fold increase in proline concentration and accumulated both the CAM‐specific PEPCase and HSP 60 compared to controls. Higher levels of copper stress resulted in a 10‐fold increase in leaf proline content, 10‐fold HSP 60 accumulation but no detectable PEPCase protein compared to unstressed controls. HSP 60 did not accumulate under NaCl stress. Concurrent with copper‐induced genetic responses to stress, copper was accumulated and concentrated in leaves (3 500 ppm). Together, these results suggest that this halophyte copes with copper metal exposure through distinct genetic mechanisms.     

Root allocation and foraging precision in heterogeneous soils

Root growth patterns respond to small-scale resource heterogeneity and the presence of roots of neighboring plants, but how a plant integrates its responses to these cues is not well understood. In the presence of neighbors, plants may shift allocation to roots as a consequence of plant size and root:shoot allometry, as a response to resource depletion by neighbors, or through a direct response to neighbor presence. The same response pathways also have the potential to alter proliferation in resource-rich patches in soil.Four species of grassland plants were grown in the greenhouse as single plants, monocultures, and mixtures. Root length allocation as a function of shoot mass was examined for background soil and fertilized patches. Plants grown with same-species neighbors followed the same allometric trajectory as single plants for root length in background soil, so any change in root allocation was due only to reduced plant size. Root proliferation in patches declined with neighbors, consistent with a response to resource depletion. Mixtures overproduced roots in both background soil and in patches, relative to plants of the same size in monocultures.     

Oviposition acceptance and larval development of Chilo partellus stemborers in drought‐stressed wild and cultivated grasses of East Africa

Maternal host choices during oviposition by herbivorous insects determine the fitness of their offspring and may be influenced by environmental changes that can alter host‐plant quality. This is of particular relevance to ‘push‐pull’ cropping systems where host preferences are exploited to manage insect pest populations. We tested how drought stress in maize and companion plants that are used in these systems affect oviposition preference, larval feeding, and development of the spotted stemborer, Chilo partellus Swinhoe (Lepidoptera: Crambidae). Five host species were tested (all Poaceae): maize (Zea mays L.), Napier grass (Pennisetum purpureum Schumach), signal grass [Brachiaria brizantha (A. Rich) Stapf], Brachiaria cv. ‘Mulato’, and molasses grass [Melinis minutiflora (Beauv.)]. Under drought stress, maize experienced as much oviposition as control unstressed maize in choice and no‐choice experiments. Similarly, larval leaf damage was not significantly different in drought‐stressed vs. unstressed maize. In contrast, oviposition occurred less on drought‐stressed than on unstressed Napier and signal grass. Oviposition acceptance and leaf damage remained low in both drought‐stressed and unstressed molasses grass and Mulato. Larval survival and development remained high in drought‐stressed maize, but not in Napier, signal, and molasses grass and Mulato, where survival and development were low in both drought‐stressed and unstressed plants. Our results indicate that herbivore responses to drought‐stressed plants depend on the plant species and that drought stress can change host preference and acceptance rankings. In particular, trap‐crops such as Napier grass may not divert oviposition from the main maize crop under drought stress conditions.     

Oviposition Preference for Water-Stressed Plants in <Emphasis Type="Italic">Orius insidiosus</Emphasis> (Hemiptera: Anthocoridae)

Plant species affect the oviposition behavior of the zoophytophagous predator Orius insidiosus. This study was conducted to determine whether manipulating plant quality, via stress, within a single plant species (Phaseolus vulgaris L.) would affect the oviposition behavior of O. insidiosus and the subsequent performance of its offspring. Plants that had water withheld (water-stressed treatment) had about 20% less total dry weight than plants that were watered to alleviate the drought stress (unstressed treatment). In comparison to unstressed plants, unifoliolate leaves and petioles of water-stressed plants had about 20 and 12% less relative water content, 54 and 29% greater sap osmotic potential, and 19 and 70% greater concentrations of amino-nitrogen, respectively. Reproductive O. insidiosus were then presented stressed and unstressed plants in a two choice test to determine oviposition preference. First instar survival on the two treatments was evaluated in no-choice tests. Orius insidiosus laid 70% more eggs per cm² on the stressed plants. The lifespan of newly-hatched nymphs was the same in both treatments. Eggs were more frequently laid on the leaf vein than the petiole of unstressed plants, whereas in stressed plants oviposition on these parts occurred at equal frequency. These findings suggest that physiological changes in water-stressed bean plants created conditions more favorable for O. insidiosus oviposition. As there was no increase in offspring performance, it is hypothesized that females chose oviposition sites near preferred feeding sites or plant tissues that were less prone to desiccation.     

Osmotic adjustment in indoor grown cassava in response to water stress

The water content-water potential relation in stressed and unstressed cassava ( Man-ihot species) was examined to ascertain (i) the magnitude of osmotic adjustment in response to water stress and (ii) the mechanisms of such adjustments.
Water stress resulted in a displacement of the water content-potential relation such that at any leaf water potential the water content was higher in the stressed plants. The osmotic potentials of turgid leaves (100% relative water content) were -0.97 and -1.00 MPa in the unstressed cultivars CMC 9 and MCOL 113 respectively. In the stressed plants, the values were-1.13 MPa (CMC 9) and-1.14 MPa (MCOL 113). The 0.14 to 0.16 MPa osmotic potential difference between the stressed and unstressed plants suggests that a stress-induced osmotic adjustment occurred in both cultivars. The biiSk volumetric elastic moduli at turgor pressures above 0.10 MPa were 9.84 MPa (CMC 9) and 13.58 MPa (MCOL 113) in the unstressed plants. Tbe higher values found in the stressed plants, 14.56 MPa in CMC 9 and 16.91 MPa in MCOL 113, suggest a stress-induced decrease in cell wall elasticity. Hence, the observed shift in the wafer content-potential relations in the cassava involved both an osmotic adjustment and a decrease in cell wall elasticity. Increasing the number of stress cycles per plant did not cause a further displacement of the water content-potential curves.     

Stress-induced changes in carbon sources for isoprene production in Populus deltoides

Isoprene is emitted from leaves of numerous plant species and has important implications for plant metabolism and atmospheric chemistry. The ability to use stored carbon (alternative carbon sources), as opposed to recently assimilated photosynthate, for isoprene production may be important as plants routinely experience photosynthetic depression in response to environmental stress. A CO₂‐labelling study was performed and stable isotopes of carbon were used to examine the role of alternative carbon sources in isoprene production in Populus deltoides during conditions of water stress and high leaf temperature. Isotopic fractionation during isoprene production was higher in heat‐ and water‐stressed leaves (?8.5 and ?9.3‰, respectively) than in unstressed controls (?2.5 to ?3.2‰). In unstressed plants, 84–88% of the carbon in isoprene was derived from recently assimilated photosynthate. A significant shift in the isoprene carbon composition from photosynthate to alternative carbon sources was observed only under severe photosynthetic limitation (stomatal conductance < 0.05 mol m^?2 s^?1). The contribution of photosynthate to isoprene production decreased to 77 and 61% in heat‐ and water‐stressed leaves, respectively. Across water‐ and heat‐stress experiments, allocation of photosynthate was negatively correlated to the ratio of isoprene emission to photosynthesis. In water‐stressed plants, the use of alternative carbon was also related to stomatal conductance. It has been proposed that isoprene emission may be regulated by substrate availability. Thus, understanding carbon partitioning to isoprene production from multiple sources is essential for building predictive models of isoprene emission.     

Effects of preconditioning on electrolyte leakasge and lipid composition in black spruce (Picea mariand) stressed with polyethylene giycol

Black spruce ( Picea mariana Mill. B. S. P.) rooted cuttings were grown in solution culture and preconditioned by osmotically stressing plants with polyethylene glycol. After relief from preconditioning stress, water relations, membrane leakiness, and the composition of lipids and fatty acids were compared in preconditioned and control, unconditioned plants. Both groups of plants were subsequently subjected to a severe osmotic stress with polyethylene glycol and examined again. Osmotic stress decreased shoot water potentials and increased the leakage of electrolytes from shoots of stressed, compared with unstressed, plants. However, both unstressed and stressed preconditioned plants leaked less electrolytes compared with unconditioned plants. Changes in sterol, phospholipid and glycolipid composition were observed in preconditioned unstressed and stressed plants. Sterol and phospholipid levels de clined as a result of stress, and preconditioning resulted in a decline in sterol: phospholipid ratios in plants.     

Plant stress and larval performance of a dipterous gall former

According to the plant vigour hypothesis, galling insects should respond positively and perform better on vigorous plants or plant parts, the opposite of the predictions of the plant stress hypothesis. I carried out field experiments to analyse the effects of sustained abiotic stress on the interactions between the common reed (Phragmites australis) and a gall-forming fly (Lipara lucens). The reed shoot diameter (a measure of plant vigour) is strongly affected by environmental conditions, where dry and/or nutrient-poor habitats produce thinner (stressed) shoots. L. lucens gall density is negatively correlated with shoot diameter. In a survival experiment with a wide range of shoot diameters, larval mortality was also highly correlated with shoot quality. Gall formation was higher on thinner, stressed shoots. An analysis of the gall tissues revealed that galls induced by L. lucens contain a high amount of a nutrient-rich feeding tissue. The impact of L. lucens is higher on thinner shoots. The results of this study showed that L. lucens performs better on stressed hosts, which contradicts the plant vigour hypothesis for galling insects. The low nutrient availability in the stressed shoots can be compensated by the production of galls with a nutrient-rich feeding tissue.     

Plant water stress and gall formation (Cecidomyiidae: Asphondylia spp.) on creosote bush

Abstract. 1. Populations of creosote bush ( Larrea tridentata (DC) Coville), were studied in Arizona to determine whether associated gallformers (Cecidomyiidae: Asphondylia spp.) were more abundant on water-stressed or nonstressed plants. Gall densities were measured along a steep elevational gradient that extended from mesic, higher elevations to lower elevations in the desert; and in the Grand Canyon where severely water-stressed and relatively unstressed plants occurred adjacently. At the Grand Canyon site, the responses of creosote bush to water stress were also studied.
2. The number and densities of Asphondylia species increased both at lower elevations and locally on water-stressed plants in the Grand Canyon, indicating that climatic and local conditions influence gallformer abundance in the same way.
3. Five of the eight Asphondylia species studied at the Grand Canyon site were more abundant on stressed plants, two species were more abundant on nonstressed plants and one species showed no preference for either plant type.
4. Densities of most species on stressed plants were positively correlated with the number of meristematic terminals per branch, which were more numerous on stressed plants, due to a bushier architecture. Flower gallformers were more abundant on nonstressed plants, which produced more flowers. Gall densities did not correlate with chemistry measurements, although these parameters also varied with level of stress.
5. These results suggest that gallforming species respond variably to plant stress, even within a closely-related lineage, and that there are effects of stress on plants, including architectural changes, that may be more important to herbivores than biochemical effects emphasized by White (1984) and others.     

Kin recognition affects plant communication and defence

The ability of many animals to recognize kin has allowed them to evolve diverse cooperative behaviours; such ability is less well studied for plants. Many plants, including Artemisia tridentata, have been found to respond to volatile cues emitted by experimentally wounded neighbours to increase levels of resistance to herbivory. We report that this communication was more effective among A. tridentata plants that were more closely related based on microsatellite markers. Plants in the field that received cues from experimentally clipped close relatives experienced less leaf herbivory over the growing season than those that received cues from clipped neighbours that were more distantly related. These results indicate that plants can respond differently to cues from kin, making it less likely that emitters will aid strangers and making it more likely that receivers will respond to cues from relatives. More effective defence adds to a growing list of favourable consequences of kin recognition for plants.     

Plant age, communication, and resistance to herbivores: young sagebrush plants are better emitters and receivers

Plants progress through a series of distinct stages during development, although the role of plant ontogeny in their defenses against herbivores is poorly understood. Recent work indicates that many plants activate systemic induced resistance after herbivore attack, although the relationship between resistance and ontogeny has not been a focus of this work. In addition, for sagebrush and a few other species, individuals near neighbors that experience simulated herbivory become more resistant to subsequent attack. Volatile, airborne cues are required for both systemic induced resistance among branches and for communication among individuals. We conducted experiments in stands of sagebrush of mixed ages to determine effects of plant age on volatile signaling between branches and individuals. Young and old control plants did not differ in levels of chewing damage that they experienced. Systemic induced resistance among branches was only observed for young plants. Young plants showed strong evidence of systemic resistance only if airflow was permitted among branches; plants with only vascular connections showed no systemic resistance. We also found evidence for volatile communication between individuals. For airborne communication, young plants were more effective emitters of cues as well as more responsive receivers of volatile cues.     

Not all droughts are created equal? The effects of stress severity on insect herbivore abundance

Predicting interactions between drought and plant–insect interactions has been a challenge. Currently, we are unable to accurately predict herbivore abundance on stressed plants despite over 500 publications and half a dozen formal hypotheses. With drought predicted to increase in severity with climate change, determining herbivore abundance on stressed plants is critical for continued agricultural and natural system management. During drought, plants increase concentrations of nutrients and also suffer from water loss. Many empirical studies test drought on plants using severe continuous stress, but studies suggest drought may benefit herbivores when it is intermittent (pulsed). In our study, we tested intermittent and severe stress on herbivore and arthropod abundance in a cotton agro-ecosystem. Our goal was to determine how these types of drought influence herbivore abundance on stressed plants and the relationship between herbivore abundance and stress-related nutrients. We found that intermittent and severe water-deficit stress had different effects on insect herbivores, signifying that drought severity influences herbivore abundance. Piercing–sucking herbivores such as thrips, stink bugs, and leafhoppers were more abundant on intermittently stressed plants than on severely stressed plants. Drought did not significantly affect chewing herbivores, and their abundance was inconsistent on stressed and well-watered plants. Furthermore, nutrient concentrations were similar between stressed and unstressed plants, but herbivore abundance was greater on intermittently stressed plants, suggesting that other physiological characteristics of stressed plants and herbivore feeding ecology must be considered. Our study suggests that the drought severity must be considered when predicting herbivore abundance on stressed plants.     

Light spectral quality, phytochrome and plant competition

The light environment experienced by plants in natural vegetation is strongly dependent upon interactions with neighbors. For plants in dense stands, reduced irradiance can lead to reductions in growth and fitness. Spectral light quality is also altered beneath a leaf canopy, and can serve as an important signal of competition for light. Recent physiological studies indicate that plants can perceive the quality of light reflected from neighbors as an accurate predictor of future competition, and respond morphologically even before they are directly shaded. These findings have important implications for plant population biology, and provide a valuable opportunity for the study of adaptive plasticity.     

Plant stress and insect behavior: cottonwood,ozone and the feeding and oviposition preference of a beetle

Summary Adults and larvae of the beetle Plagiodera versicolora preferred to feed on and consumed more of cottonwood, Populus deltoides, plant material that had been previously exposed to an acute dose of ozone (0.20 ppm, 5 h), compared to controls in choice experiments. However, females preferred to oviposit on the unexposed controls. Results were consistent for 2 cottonwood clones over 3 years in disc, leaf and whole-plant choice tests. The differential feeding and oviposition response of this insect to stressed plants could have at least 3 unexpected consequences: 1. An immediate increase in damage to stressed trees, but a subsequent decrease in damage. 2. A subsequent increase in damage to unstressed adjacent trees. 3. Changes in the insect and pathogen communities of both stressed and unstressed trees. These complex scenarios show that predicting outcomes of plant stress on plant-insect interactions will require comprchensive examination of behavioral, growth and reproductive responses of insects to stressed plants.     

Aphids in a changing world: testing the plant stress,plant vigour and pulsed stress hypotheses

• 1 The plant stress, plant vigour and pulsed stress hypotheses describe the relationships between drought stress, plant quality and herbivore performance. We used an aphid‐Brassica system to test these hypotheses under different drought treatments.
• 2 The quantity of water added per plant/week was 75%, 50% and 25% of the control (unstressed) water regime for low, medium and high drought stress, respectively, and 50% applied fortnightly for pulsed drought stress. The performance of a ‘senescence’ (generalist) and a ‘flush’ feeder (specialist) aphid species and host plant quality were assessed.
• 3 Drought treatments had a similar effect on the fecundity and intrinsic rate of increase of both aphid species. Aphid performance on unstressed and highly drought‐stressed plants was significantly lower compared with medium drought stress. On average, 20% greater fecundity and 40% greater intrinsic rates of increase were recorded for both aphid species at medium drought stress compared with unstressed plants.
• 4 Plant biomass and relative water contents were significantly greater for unstressed plants compared with high and pulsed drought treatments. Foliar nitrogen concentration was significantly greater in the high drought stress and pulsed treatments, and the dominant glucosinolate (glucobrassicin) concentration was significantly greater in drought stress treatments.
• 5 The present study supports the plant stress hypothesis, although the plant vigour and pulsed stress hypotheses are not supported by our data. The implications of these findings for plant–herbivore interactions under changing environmental conditions are discussed.