Evolution of sensitivity to warning cues from kin in plants with a structured population.

Plants exchange a variety of information intra- and interspecifically by using various mediating cues. For example, plant individuals that are injured by herbivores release volatile chemicals, which induce receiver plants to express anti-herbivore resistance. Remarkably, some plant species were known to represent kin specificity in the response, where cues from a damaged individual induce a higher level of resistance in a kin receiver than in a non-kin receiver. Such higher sensitivity to warning cues from kin could be advantageous via two mechanisms. If each herbivore tends to attack plants with a certain genotype, plants should be more sensitive to warning cues from kin that share genetic properties. In addition, if herbivores successively attack the neighboring plant with a high probability, and if related plants tend to grow in close proximity, plants may be more sensitive to warning cues from neighboring kin under the presence of a trade-off between sensitivity to kin and non-kin. In the present study, we constructed a mathematical model including those mechanisms to investigate the evolutionary process of the higher sensitivity to warning cues from kin than sensitivities to cues from non-kin. According to the analysis of evolutionary dynamics, we revealed that both mechanisms could contribute, although higher sensitivity to cues from kin is more likely to evolve when the spatial range of competition is greater than the range of effective alarm cues. This result highlights the importance of the competition regime in the evolution of signaling among kin.

Plant Molecular Phenology and Climate Feedbacks Mediated by BVOCs.

Climate change profoundly affects the timing of seasonal activities of organisms, known as phenology. The impact of climate change is not unidirectional; it is also influenced by plant phenology as plants modify atmospheric composition and climatic processes. One important aspect of this interaction is the emission of biogenic volatile organic compounds (BVOCs), which link the Earth's surface, atmosphere, and climate. BVOC emissions exhibit significant diurnal and seasonal variations and are therefore considered essential phenological traits. To understand the dynamic equilibrium arising from the interplay between plant phenology and climate, this review presents recent advances in comprehending the molecular mechanisms underpinning plant phenology and its interaction with climate. We provide an overview of studies investigating molecular phenology, genome-wide gene expression analyses conducted in natural environments, and how these studies revolutionize the concept of phenology, shifting it from observable traits to dynamic molecular responses driven by gene-environment interactions. We explain how this knowledge can be scaled up to encompass plant populations, regions, and even the globe by establishing connections between molecular phenology, changes in plant distribution, species composition, and climate. Expected final online publication date for the Annual Review of Plant Biology, Volume 75 is May 2024. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The exposure of field-grown maize seedlings to weed volatiles affects their growth and seed quality.

Plants exposed to volatiles emitted from artificially damaged conspecific or heterospecific plants exhibit increased resistance to herbivorous insects. Here, we examined whether volatiles from artificially damaged weeds affect maize growth and reproduction. Seven days after germination, maize seedlings were exposed to volatiles emitted by artificially damaged mugwort (Artemisia indica var. maximowiczii) or tall goldenrod (Solidago altissima) plants either separately, or as a mixture of the two, for seven days. Unexposed seedlings were used as controls. Treated and control seedlings were cultivated in an experimental field without any insecticides applied. Plants exposed to either of the three volatile treatments sustained significantly less damage than controls. Additionally, seedlings exposed to either goldenrod or mixed volatiles produced more leaves and tillers than control plants. Furthermore, a significant increase in the number of ears was observed in plants exposed to the volatile mixture. In all treated plants, ear sugar content was significantly higher than that in the controls. Further, we cultivated seedlings that were either exposed to the volatile mixture or unexposed, under the conventional farming method using pesticides. Similar significant differences were observed for sugar content, number of tillers, leaves, damaged leaves, and ears. Laboratory experiments were conducted to further evaluate the mechanisms involved in the improved performance of volatile-treated plants. A significant reduction in the growth of common armyworm (Mythimna separata) larvae was observed when maize plants were exposed to the volatile mixture. This treatment did not affect the amount of jasmonic acid in the seedlings, whereas salicylic acid content increased upon exposure. The characteristic differences in chemical composition of mugwort and goldenrod volatiles were confirmed and, in turn, the volatile mixture differed significantly from the volatiles of either species.

Effective distance of volatile cues for plant-plant communication in beech.

In response to volatiles emitted from a plant infested by herbivorous arthropods, neighboring undamaged conspecific plants become better defended against herbivores; this is referred to as plant‒plant communication. Although plant‒plant communication occurs in a wide range of plant species, most studies have focused on herbaceous plants. Here, we investigated plant‒plant communication in beech trees in two experimental plantations in 2018 and one plantation in 2019. Approximately 20% of the leaves of a beech tree were clipped in half in the spring seasons of 2018 and 2019 (clipped tree). The damage levels to leaves in the surrounding undamaged beech trees were evaluated 90 days after the clipping (assay trees). In both years, the damage levels decreased with a reduction in the distance from the clipped tree. In 2019, we also recorded the damage levels of trees that were not exposed to volatiles (nonexposed trees) as control trees and found that those that were located <5 m away from clipped trees had significantly less leaf damage than nonexposed trees. By using a gas chromatograph-mass spectrometer, ten and eight volatile compounds were detected in the headspaces of clipped and unclipped leaves, respectively. Among them, the amount of (Z)-3-hexenyl acetate in clipped leaves was significantly higher than that in nonclipped leaves. Our result suggests that green leaf volatiles such as (Z)-3-hexenol and (Z)-3-hexenyl acetate and other volatile organic compounds emitted from clipped trees induced defenses in the neighboring trees within the 5 m radius. The effective distances of plant‒plant communication in trees were discussed from the viewpoint of the arthropod community structure in forest ecosystems.

Field-Grown Rice Plants Become More Productive When Exposed to Artificially Damaged Weed Volatiles at the Seedling Stage.

It is known that undamaged plants that have been exposed to volatiles from damaged con- or heterospecific plants become more resistant against herbivores. This is one of the plants' induced resistant responses against herbivores. To test whether this response can be used for rice production, we conducted the following experiments over 2 years (2012 and 2013). Rice seedlings were first planted in the rice seedling bed for 2 weeks in early May. There, half of the rice seedlings were exposed to artificially damaged weed volatiles three times for 12 days (treated plants). Weeds were randomly collected from the areas that were >100 m away from the seedling bed and the rice paddy fields. The remaining seedlings were not exposed (control plants). In the middle of May, bunches (ca. three seedlings per bunch) were transplanted to the rice paddy field. In July, leaf damage was observed. The total number of leaves in the treated and control plants was not significantly different. In contrast, the total number of damaged leaves in the treated plants was significantly lower than that in the control plants. In September, rice grains were harvested. The average weight of a rice grain from the treated and control plants was not significantly different. However, the weight of grains per bunch of treated plants was significantly higher than that of control plants; this indicated a significant increase of the number of grains by 23% in 2012 and by 18% in 2013 in the treated plants compared to that in the control plants. The volatiles emitted from the weeds included monoterpenoids (40.4% in total), green leaf volatiles (46.5%), short-chain alcohols (5.3%), short-chain ketone (5.4%), short-chain acetate (0.5%), short-chain aldehyde (1.1%), and hydrocarbon (0.7%). These results suggest that exposure of volatiles from artificially damaged weeds to rice seedlings has the potential to increase rice production.

Plant-plant communication and community of herbivores on tall goldenrod.

The volatiles from damaged plants induce defense in neighboring plants. The phenomenon is called plant-plant communication, plant talk, or plant eavesdropping. Plant-plant communication has been reported to be stronger between kin plants than genetically far plants in sagebrush.Why do plants distinguish volatiles from kin or genetically far plants? We hypothesize that plants respond only to important conditions; the induced defense is not free of cost for the plant. To clarify the hypothesis, we conducted experiments and investigations using goldenrod of four different genotypes.The arthropod community on tall goldenrods were different among four genotypes. The response to volatiles was stronger from genetically close plants to the emitter than from genetically distant plants from the emitter. The volatiles from each genotype of goldenrods were different; and they were categorized accordingly. Moreover, the arthropod community on each genotype of goldenrods were different. Synthesis: Our results support the hypothesis: Goldenrods respond to volatiles from genetically close plants because they would have similar arthropod species. These results are important clues elucidating adaptive significance of plant-plant communication. ​.

Aboveground plant-to-plant communication reduces root nodule symbiosis and soil nutrient concentrations.

Aboveground communication between plants is well known to change defense traits in leaves, but its effects on belowground plant traits and soil characteristics have not been elucidated. We hypothesized that aboveground plant-to-plant communication reduces root nodule symbiosis via induction of bactericidal chemical defense substances and changes the soil nutrient environment. Soybean plants were exposed to the volatile organic compounds (VOCs) from damaged shoots of Solidago canadensis var. scabra, and leaf defense traits (total phenolics, saponins), root saponins, and root nodule symbiosis traits (number and biomass of root nodules) were measured. Soil C/N ratios and mineral concentrations were also measured to estimate the effects of resource uptake by the plants. We found that total phenolics were not affected. However, plants that received VOCs had higher saponin concentrations in both leaves and roots, and fewer root nodules than untreated plants. Although the concentrations of soil minerals did not differ between treatments, soil C/N ratio was significantly higher in the soil of communicated plants. Thus, the aboveground plant-to-plant communication led to reductions in root nodule symbiosis and soil nutrient concentrations. Our results suggest that there are broader effects of induced chemical defenses in aboveground plant organs upon belowground microbial interactions and soil nutrients, and emphasize that plant response based on plant-to-plant communications are a bridge between above- and below-ground ecosystems.

Evidence that ERF transcriptional regulators serve as possible key molecules for natural variation in defense against herbivores in tall goldenrod.

We collected Solidago altissima clones to explore their leaf damage resistance, and as a result identified five accessions that exhibited variable defense abilities against the generalist herbivore Spodoptera litura. In order to characterize molecules involved in such natural variation, we focused on ethylene response factors (ERFs) that exhibited distinct transcription patterns in the leaves of the five accessions (e.g., S1 and S2) after wounding: the transcript of SaERF1 and SaERF2 was induced in wounded S1 and S2 leaves, respectively. Although transcription levels of SaERFs in leaves of the five accessions did not correlate with the accessions' phytohormone levels, these transcription levels accorded with the possibility that ethylene and jasmonate signaling play crucial roles in wound-induced transcription of SaERF1 in S1 leaves, and SaERF2 in S2 leaves, respectively. SaERF1 was found to be a positive regulator of the GCC box and DRE element in the upstream regions of promoters of defense genes, whereas SaERF2 served as a negative regulator of genes controlled through the GCC box. Transgenic Arabidopsis plants expressing SaERF1 or SaERF2 showed enhanced and suppressed transcript levels, respectively, of a defensin gene, indicating that ERFs may be partly responsible for herbivore resistance properties of S. altissima accessions.

Targeting diamondback moths in greenhouses by attracting specific native parasitoids with herbivory-induced plant volatiles.

We investigated the recruitment of specific parasitoids using a specific blend of synthetic herbivory-induced plant volatiles (HIPVs) as a novel method of pest control in greenhouses. In the Miyama rural area in Kyoto, Japan, diamondback moth (DBM) (Plutella xylostella, Lepidoptera: Plutellidae) larvae are an important pest of cruciferous crops in greenhouses, and Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of DBM, is found in the surrounding areas. Dispensers of HIPVs that attracted C. vestalis and honey feeders were set inside greenhouses (treated greenhouses). The monthly incidence of DBMs in the treated greenhouses was significantly lower than that in the untreated greenhouses over a 2-year period. The monthly incidences of C. vestalis and DBMs were not significantly different in the untreated greenhouses, whereas monthly C. vestalis incidence was significantly higher than monthly DBM incidence in the treated greenhouses. Poisson regression analyses showed that, in both years, a significantly higher number of C. vestalis was recorded in the treated greenhouses than in the untreated greenhouses when the number of DBM adults increased. We concluded that DBMs were suppressed more effectively by C. vestalis in the treated greenhouses than in the untreated greenhouses.

Synchronous Occurrences of the Diamondback Moth (Lepidoptera: Plutellidae) and its Parasitoid Wasp Cotesia vestalis (Hymenoptera: Braconidae) in Greenhouses in a Satoyama Area.

We characterized the correlation between the occurrences of diamondback moth, Plutella xylostella (L.), larvae and their dominant native parasitoid wasp, Cotesia vestalis (Haliday), in commercial greenhouses in a satoyama area, called Miyama, in Kyoto, Japan. In the three greenhouses used in this study, cruciferous 'mizuna' (Brassica rapa var. laciniifolia [Brassicales: Brassicaceae]) crops were grown. Pesticides against diamondback moth were not routinely applied in the greenhouses. We confirmed that populations of diamondback moth and C. vestalis were maintained on the wild crucifer plant Rorippa indica in the surrounding area from March to December. In the greenhouses, we observed several occurrences of diamondback moth larvae that were, in most cases, followed by occurrences of C. vestalis. We found that C. vestalis females were attracted by volatiles emitted from mizuna plants that were lightly infested with second-stadium diamondback moth larvae under laboratory conditions. The synchronous appearance of diamondback moth larvae and C. vestalis could be explained by the latter being attracted by the volatiles emitted from mizuna plants infested by diamondback moth larvae in the greenhouses.

Insect Herbivory Selects for Volatile-Mediated Plant-Plant Communication.

Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.

Effects of trans-2-hexenal and cis-3-hexenal on post-harvest strawberry.

Green leaf volatiles are emitted by green plants and induce defence responses. Those with antifungal activities in plants may replace chemicals as natural post-harvest treatments. We investigated the postharvest treatment of strawberry with trans-2-hexenal and cis-3-hexenal and observed a decrease in the mould infection rate. To determine the volatiles' functions, we conducted a component analysis of the volatiles released from trans-2-hexenal-treated strawberry and analysed gene expression. Several acetates, which were expected to be metabolites of trans-2-hexenal in fruit, were released from treated strawberry; however, these acetates did not inhibit fungal growth. The gene expression analysis suggested that postharvest strawberries were not protected by jasmonic acid-mediated signalling but by another stress-related protein. Harvested strawberries experience stress induced by harvest-related injuries and are unable to perform photosynthesis, which might result in different responses than in normal plants.

Multifunctionality of herbivory-induced plant volatiles in chemical communication in tritrophic interactions.

Uninfested plants emit only trace quantities of volatiles (constitutively emitted plant volatiles). In contrast, some plants emit relatively large quantities of volatiles in response to herbivory (herbivory-Induced plant volatiles: HIPVs). Organisms belonging to different trophic levels use plant volatiles in context-dependent manners; consequently, volatiles can be adaptive, non-adaptive, or maladaptive to the emitter plants. In this review, we focus on the multifunctional aspects of HIPVs, which vary qualitatively and quantitatively in emitting plant species and infesting herbivore species, in plant-carnivore interactions, plant-herbivore interactions, and plant-omnivore interactions. Additionally, we review the evidence of plant-plant communication and its effects on tritrophic interactions involving plants, herbivores, and carnivores. Prospects on interactions mediated by plant volatiles induced by herbivorous arthropods are discussed.

Identification of a Hexenal Reductase That Modulates the Composition of Green Leaf Volatiles.

Green leaf volatiles (GLVs), including six-carbon (C6) aldehydes, alcohols, and esters, are formed when plant tissues are damaged. GLVs play roles in direct plant defense at wound sites, indirect plant defense via the attraction of herbivore predators, and plant-plant communication. GLV components provoke distinctive responses in their target recipients; therefore, the control of GLV composition is important for plants to appropriately manage stress responses. The reduction of C6-aldehydes into C6-alcohols is a key step in the control of GLV composition and also is important to avoid a toxic buildup of C6-aldehydes. However, the molecular mechanisms behind C6-aldehyde reduction remain poorly understood. In this study, we purified an Arabidopsis (Arabidopsis thaliana) NADPH-dependent cinnamaldehyde and hexenal reductase encoded by At4g37980, named here CINNAMALDEHYDE AND HEXENAL REDUCTASE (CHR). CHR T-DNA knockout mutant plants displayed a normal growth phenotype; however, we observed significant suppression of C6-alcohol production following partial mechanical wounding or herbivore infestation. Our data also showed that the parasitic wasp Cotesia vestalis was more attracted to GLVs emitted from herbivore-infested wild-type plants compared with GLVs emitted from chr plants, which corresponded with reduced C6-alcohol levels in the mutant. Moreover, chr plants were more susceptible to exogenous high-dose exposure to (Z)-3-hexenal, as indicated by their markedly lowered photosystem II activity. Our study shows that reductases play significant roles in changing GLV composition and, thus, are important in avoiding toxicity from volatile carbonyls and in the attraction of herbivore predators.

Pest management using mint volatiles to elicit resistance in soy: mechanism and application potential.

Plants can eavesdrop on volatile cues emitted from neighboring plants to boost their defense responses. When 10 categories of mints were tested for their effects on Glycine max (soybean) plants cultivated nearby, candy mint (Mentha × piperita cv. Candy) and peppermint (Mentha × piperita L.) induced the strongest enhancement in RNA levels of defense genes in the soybean leaves. The mechanism by which the mint volatiles enhanced these transcript levels was based on histone acetylation within the promoter regions of defense genes. These increases in transcript levels were induced when receiver plants were cultivated near to candy mint, but the priming of the defense responses was instead induced when receiver plants were cultivated at mid-length intervals. Field assays revealed that anti-herbivore ability of soy was strengthened both by co-cultivation and by pre-incubation of receiver plants with candy mint. The same held true for another receiver, Brassica rapa, when the receiver was co-cultivated or pre-incubated with peppermint. Exposure to mint volatiles resulted in lower damage to receiver plants, although ecological effects on the herbivores and predators probably also contributed. Together, our findings indicate that pest management systems relying on mint as companion plants might be commercially useful for reducing herbivore damage in crops.

Weeding volatiles reduce leaf and seed damage to field-grown soybeans and increase seed isoflavones.

Field experiments were conducted over 3 years (2012, 2013, and 2015), in which half of the young stage soybean plants were exposed to volatiles from cut goldenrods three times over 2-3 weeks, while the other half remained unexposed. There was a significant reduction in the level of the total leaf damage on exposed soybean plants compared with unexposed ones. In 2015, the proportion of damage to plants by Spodoptera litura larvae, a dominant herbivore, was significantly less in the exposed field plots than in the unexposed plots. Under laboratory conditions, cut goldenrod volatiles induced the direct defenses of soybean plants against S. litura larvae and at least three major compounds, α-pinene, ß-myrcene, and limonene, of cut goldenrod volatiles were involved in the induction. The number of undamaged seeds from the exposed plants was significantly higher than that from unexposed ones. Concentrations of isoflavones in the seeds were significantly higher in seeds from the exposed plants than in those from the unexposed plants. Future research evaluating the utility of weeding volatiles, as a form of plant-plant communications, in pest management programs is necessary.

Geographic dialects in volatile communication between sagebrush individuals.

Plants respond to volatile cues emitted by damaged neighbors to increase their defenses against herbivores. We examined whether plants communicated more effectively with local neighbors than distant neighbors in a reciprocal experiment at two sites. Three branches on focal plants were incubated with air from (1) a control, (2) an experimentally clipped "foreign" plant from 230 km away, or (3) an experimentally clipped "local" plant from the same population as the focal plant. Branches incubated with air from the controls experienced 50-80% more leaf damage than those receiving air from experimentally clipped plants. Of more interest, branches receiving volatiles from experimentally clipped "local" plants received 50-65% of the leaf damage as those receiving volatiles from experimentally clipped "foreign" plants. Sabinyl compounds and related terpinenes were found to differ consistently for plants from southern and northern sites. These results indicate that cues vary geographically in their effectiveness and suggest that sagebrush responds more strongly to local than foreign dialects.

Seasonal variation of responses to herbivory and volatile communication in sagebrush (Artemisia tridentata) (Asteraceae).

Plants can respond to insect herbivory in various ways to avoid reductions in fitness. However, the effect of herbivory on plant performance can vary depending on the seasonal timing of herbivory. We investigated the effects of the seasonal timing of herbivory on the performance of sagebrush (Artemisia tridentata). Sagebrush is known to induce systemic resistance by receiving volatiles emitted from clipped leaves of the same or neighboring plants, which is called volatile communication. Resistance to leaf herbivory is known to be induced most effectively after volatile communication in spring. We experimentally clipped 25 % of leaves of sagebrush in May when leaves were expanding, or in July when inflorescences were forming. We measured the growth and flower production of clipped plants and neighboring plants which were exposed to volatiles emitted from clipped plants. The treatment conducted in spring reduced the growth of clipped plants. This suggests that early season leaf herbivory is detrimental because it reduces the opportunities for resource acquisition after herbivory, resulting in strong induction of resistance in leaves. On the other hand, the late season treatment increased flower production in plants exposed to volatiles, which was caused mainly by the increase in the number of inflorescences. Because the late season treatment occurred when sagebrush produces inflorescences, sagebrush may respond to late herbivory by increasing compensation ability and/or resistance in inflorescences rather than in leaves. Our results suggest that sagebrush can change responses to herbivory and subsequent volatile communication seasonally and that the seasonal variation in responses may reduce the cost of induced resistance.

Cry-wolf signals emerging from coevolutionary feedbacks in a tritrophic system.

For a communication system to be stable, senders should convey honest information. Providing dishonest information, however, can be advantageous to senders, which imposes a constraint on the evolution of communication systems. Beyond single populations and bitrophic systems, one may ask whether stable communication systems can evolve in multitrophic systems. Consider cross-species signalling where herbivore-induced plant volatiles (HIPVs) attract predators to reduce the damage from arthropod herbivores. Such plant signals may be honest and help predators to identify profitable prey/plant types via HIPV composition and to assess prey density via the amount of HIPVs. There could be selection for dishonest signals that attract predators for protection from possible future herbivory. Recently, we described a case in which plants release a fixed, high amount of HIPVs independent of herbivore load, adopting what we labelled a 'cry-wolf' strategy. To understand when such signals evolve, we model coevolutionary interactions between plants, herbivores and predators, and show that both 'honest' and 'cry-wolf' types can emerge, depending on the assumed plant-herbivore encounter rates and herbivore population density. It is suggested that the 'cry-wolf' strategy may have evolved to reduce the risk of heavy damage in the future. Our model suggests that eco-evolutionary feedback loops involving a third species may have important consequences for the stability of this outcome.

Airborne signals of communication in sagebrush: a pharmacological approach.

When plants receive volatiles from a damaged plant, the receivers become more resistant to herbivory. This phenomenon has been reported in many plant species and called plant-plant communication. Lab experiments have suggested that several compounds may be functioning as airborne signals. The objective of this study is to identify potential airborne signals used in communication between sagebrush (Artemisia tridentata) individuals in the field. We collected volatiles of one branch from each of 99 sagebrush individual plants. Eighteen different volatiles were detected by GC-MS analysis. Among these, 4 compounds; 1.8-cineol, ß-caryophyllene, α-pinene and borneol, were investigated as signals of communication under natural conditions. The branches which received either 1,8-cineol or ß-caryophyllene tended to get less damage than controls. These results suggested that 1,8-cineol and ß-caryophyllene should be considered further as possible candidates for generalized airborne signals in sagebrush.