Dynamic environmental interactions shaped by vegetative plant volatiles.

Covering: up to November 2022Plants shape terrestrial ecosystems through physical and chemical interactions. Plant-derived volatile organic compounds in particular influence the behavior and performance of other organisms. In this review, we discuss how vegetative plant volatiles derived from leaves, stems and roots are produced and released into the environment, how their production and release is modified by abiotic and biotic factors, and how they influence other organisms. Vegetative plant volatiles are derived from different biosynthesis and degradation pathways and are released via distinct routes. Both biosynthesis and release are regulated by other organisms as well as abiotic factors. In turn, vegetative plant volatiles modify the physiology and the behavior of a wide range of organisms, from microbes to mammals. Several concepts and frameworks can help to explain and predict the evolution and ecology of vegetative plant volatile emission patterns of specific pathways: multifunctionality of specialized metabolites, chemical communication displays and the information arms race, and volatile physiochemistry. We discuss how these frameworks can be leveraged to understand the evolution and expression patterns of vegetative plant volatiles. The multifaceted roles of vegetative plant volatiles provide fertile grounds to understand ecosystem dynamics and harness their power for sustainable agriculture.

Leafminer attack accelerates the development of soil-dwelling conspecific pupae via plant-mediated changes in belowground volatiles.

Herbivore population dynamics are strongly influenced by the interactions established through their shared host. Such plant-mediated interactions can occur between different herbivore species and different life developmental stages of the same herbivore. However, whether these interactions occur between leaf-feeding herbivores and their soil-dwelling pupae is unknown. We studied whether tomato (Solanum lycopersicum) leaf herbivory by the American serpentine leafminer Liriomyza trifolii affects the performance of conspecific pupae exposed to the soil headspace of the plant. To gain mechanistic insights, we performed insect bioassays with the jasmonate-deficient tomato mutant def-1 and its wild-type, along with phytohormones, gene expression and root volatiles analyses. Belowground volatiles accelerated leafminer metamorphosis when wild-type plants were attacked aboveground by conspecifics. The opposite pattern was observed for def-1 plants, in which aboveground herbivory slowed metamorphosis. Leafminer attack induced jasmonate and abscisic acid accumulation and modulated volatile production in tomato roots in a def-1-dependent manner. Our results demonstrate that aboveground herbivory triggers changes in root defence signalling and expression, which can directly or indirectly via changes in soil or microbial volatiles, alter pupal development time. This finding expands the repertoire of plant-herbivore interactions to herbivory-induced modulation of metamorphosis, with potential consequences for plant and herbivore community dynamics.

Constitutive and Inducible Resistance to Thrips Do Not Correlate With Differences in Trichome Density or Enzymatic-Related Defenses in Chrysanthemum.

Western flower thrips (WFT), Frankliniella occidentalis, is a serious insect pest of Chrysanthemum [Chrysanthemum × morifolium Ramat. (Asteraceae)]. Here we have investigated whether genotypic variation in constitutive and inducible resistance to WFT correlates with phenotypic differences in leaf trichome density and the activity of the defense-related enzyme polyphenol oxidase (PPO) in chrysanthemum. Non-glandular and glandular leaf trichome densities significantly varied among ninety-five chrysanthemum cultivars. Additional analyses in a subset of these cultivars, differing in leaf trichome density, revealed significant variation in PPO activities and resistance to WFT as well. Constitutive levels of trichome densities and PPO activity, however, did not correlate with chrysanthemum resistance to WFT. Further tests showed that exogenous application of the phytohormone jasmonic acid (JA) increased non-glandular trichome densities, PPO activity and chrysanthemum resistance to WFT, and that these effects were cultivar dependent. In addition, no tradeoff between constitutive and inducible resistance to WFT was observed. JA-mediated induction of WFT resistance, however, did not correlate with changes in leaf trichome densities nor PPO activity levels. Taken together, our results suggest that chrysanthemum can display both high levels of constitutive and inducible resistance to WFT, and that leaf trichome density and PPO activity may not play a relevant role in chrysanthemum defenses against WFT.

Site-dependent induction of jasmonic acid-associated chemical defenses against western flower thrips in Chrysanthemum.

MAIN CONCLUSION: Local and systemic induction of JA-associated chemical defenses and resistance to western flower thrips in Chrysanthemum are spatially variable and dependent on the site of the JA application. Plants have evolved numerous inducible defense traits to resist or tolerate herbivory, which can be activated locally at the site of the damage, or systemically through the whole plant. Here we investigated how activation of local and systemic chemical responses upon exogenous application of the phytohormone jasmonic acid (JA) varies along the plant canopy in Chrysanthemum, and how these responses correlate with resistance to thrips. Our results showed that JA application reduced thrips damage per plant when applied to all the plant leaves or when locally applied to apical leaves, but not when only basal leaves were locally treated. Local application of JA to apical leaves resulted in a strong reduction in thrips damage in new leaves developed after the JA application. Yet, activation of a JA-associated defensive protein marker, polyphenol oxidase, was only locally induced. Untargeted metabolomic analysis further showed that JA increased the concentrations of sugars, phenylpropanoids, flavonoids and some amino acids in locally induced basal and apical leaves. However, local application of JA to basal leaves marginally affected the metabolomic profiles of systemic non-treated apical leaves, and vice versa. Our results suggest that JA-mediated activation of systemic chemical defense responses is spatially variable and depends on the site of the application of the hormone in Chrysanthemum.

Ultraviolet radiation enhances salicylic acid-mediated defense signaling and resistance to Pseudomonas syringae DC3000 in a jasmonic acid-deficient tomato mutant.

Ultraviolet radiation (UV) is an important modulator of plant defenses against biotic stresses. We have recently described that different supplemental UV exposure times and irradiance intensities enhanced tomato (Solanum lycopersicum) resistance to Western flower thrips (Frankliniella occidentalis). UV increased jasmonic acid-isoleucine (JA-Ile) and salicylic acid (SA) levels, as well as the expression of JA- and SA-responsive genes, before thrips herbivory. Here we report how UV affects tomato defense responses upon thrips infestation, and resistance to pathogens that are susceptible to the activation of SA-associated defenses. Our experiments reveal that, at 7 days after thrips infestation, UV did not enhance the levels of jasmonates, auxin or abscisic acid. UV also did not affect the expression of JA-responsive genes in the cultivar Moneymaker, the jasmonate deficient mutant def-1, the type-VI trichome deficient mutant od-2, or their wild-type Castlemart. However, UV strongly activated SA-associated defense responses in def-1 after thrips infestation. Further bioassays showed that UV increased def-1 resistance to the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato DC3000, which is susceptible to SA-mediated defenses. Our results suggest that UV might enhance tomato resistance to this pathogen in the JA deficient genotype through the activation of SA defenses.

Ultraviolet radiation exposure time and intensity modulate tomato resistance to herbivory through activation of jasmonic acid signaling.

Ultraviolet (UV) radiation can modulate plant defenses against herbivorous arthropods. We investigated how different UV exposure times and irradiance intensities affected tomato (Solanum lycopersicum) resistance to thrips (Frankliniella occidentalis) by assessing UV effects on thrips-associated damage and host-selection, selected metabolite and phytohormone contents, expression of defense-related genes, and trichome density and chemistry, the latter having dual roles in defense and UV protection. Short UV daily exposure times increased thrips resistance in the cultivar 'Moneymaker' but this could not be explained by changes in the contents of selected leaf polyphenols or terpenes, nor by trichome-associated defenses. UV irradiance intensity also affected resistance to thrips. Further analyses using the tomato mutants def-1, impaired in jasmonic acid (JA) biosynthesis, od-2, defective in the production of functional type-VI trichomes, and their wild-type, 'Castlemart', showed that UV enhanced thrips resistance in Moneymaker and od-2, but not in def-1 and Castlemart. UV increased salicylic acid (SA) and JA-isoleucine concentrations, and increased expression of SA- and JA-associated genes in Moneymaker, while inducing expression of JA-defensive genes in od-2. Our results demonstrate that UV-mediated enhancement of tomato resistance to thrips is probably associated with the activation of JA-associated signaling, but not with plant secondary metabolism or trichome-related traits.

Induced Resistance Against Western Flower Thrips by the Pseudomonas syringae-Derived Defense Elicitors in Tomato.

Western flower thrips (WFT) Frankliniella occidentalis (Pergande) is a key agricultural pest of cultivated tomatoes. Induced host plant resistance by activating jasmonic acid (JA) signaling pathway constitutes a promising method for WFT control. The phytotoxin coronatine (COR), produced by Pseudomonas syringae pv. tomato DC3000 (Pst), mimics the plant hormone JA-Isoleucine and can promote resistance against herbivorous arthropods. Here we determined the effect of Pst and COR on tomato resistance against WFT, induction of JA and salicylic acid (SA) associated defenses, and plant chemistry. Additionally, we investigated the presence of other components in Pst-derived and filtered culture medium, and their interactive effect with COR on tomato resistance to WFT. Our results showed that infiltration of COR or Pst reduced WFT feeding damage in tomato plants. COR and Pst induced the expression of JA-associated gene and protein marker. COR also induced expression of a SA-related responsive gene, although at much less magnitude. Activation of JA defenses in COR and Pst infiltrated plants did not affect density of type VI leaf trichomes, which are defenses reported to be induced by JA. An untargeted metabolomic analysis showed that both treatments induced strong changes in infiltrated leaves, but leaf responses to COR or Pst slightly differed. Application of the Pst-derived and filtered culture medium, containing COR but not viable Pst, also increased tomato resistance against WFT confirming that the induction of tomato defenses does not require a living Pst population to be present in the plant. Infiltration of tomato plants with low concentrations of COR in diluted Pst-derived and filtered culture medium reduced WFT feeding damage in a greater magnitude than infiltration with an equivalent amount of pure COR indicating that other elicitors are present in the medium. This was confirmed by the fact that the medium from a COR-mutant of Pst also strongly reduced silver damage. In conclusion, our results indicate that induction of JA defenses by COR, Pst infection, the medium of Pst and the medium of a Pst COR- mutant increased resistance against WFT. This was not mediated by the reinforcement of leaf trichome densities, but rather the induction of chemical defenses.

Type VI glandular trichome density and their derived volatiles are differently induced by jasmonic acid in developing and fully developed tomato leaves: Implications for thrips resistance.

Variation in the induction of plant defenses along the plant canopy can determine distribution and colonization of arthropod herbivores within the plant. In tomato, type VI glandular trichomes, which are epidermal defensive structures, and their derived volatiles are induced by the phytohormone jasmonic acid (JA). How JA-mediated induction of these trichome-associated chemical defenses depends on the leaf developmental stage and correlates with resistance against herbivory is unknown. We showed that application of JA reduced thrips-associated damage, however the amplitude of this response was reduced in the fully developed leaves compared to those still developing. Although JA increased type-VI trichome densities in all leaf developmental stages, as well as JA-inducible defensive proteins, these increases were stronger in developing leaves. Remarkably, the concentration of trichome-derived volatiles was induced by JA to a larger degree in developing leaves than in fully developed leaves. In fully developed leaves, the increase in trichome-derived volatiles was explained by an enhanced production per trichome, while in developing leaves this was mainly caused by increases in type-VI trichome densities. Together, we showed that JA-mediated induction of trichome density and chemistry depends on leaf development stage, and it might explain the degree of thrips-associated leaf damage in tomato.

Light Intensity-Mediated Induction of Trichome-Associated Allelochemicals Increases Resistance Against Thrips in Tomato.

In cultivated tomato (Solanum lycopersicum), increases in photosynthetically active radiation (PAR) induce type VI leaf glandular trichomes, which are important defensive structures against arthropod herbivores. Yet, how PAR affects the type VI trichome-associated leaf chemistry and its biological significance with respect to other photomorphogenic responses in this agronomically important plant species is unknown. We used the type VI trichome-deficient tomato mutant odorless-2 (od-2) and its wild type to investigate the influence of PAR on trichome-associated chemical defenses against thrips (Frankliniella occidentalis). High PAR increased thrips resistance in wild-type plants, but not in od-2. Furthermore, under high PAR, thrips preferred od-2 over the wild type. Both genotypes increased type VI trichome densities under high PAR. Wild-type plants, however, produced more trichome-associated allelochemicals, i.e. terpenes and phenolics, these being undetectable or barely altered in od-2. High PAR increased leaf number and thickness, and induced profound but similar metabolomic changes in wild-type and od-2 leaves. Enhanced PAR also increased levels of ABA in wild-type and od-2 plants, and of auxin in od-2, while the salicylic acid and jasmonate concentrations were unaltered. However, in both genotypes, high PAR induced the expression of jasmonic acid-responsive defense-related genes. Taken together, our results demonstrate that high PAR-mediated induction of trichome-associated chemical defenses plays a prominent role in tomato-thrips interactions.

Thrips advisor: exploiting thrips-induced defences to combat pests on crops.

Plants have developed diverse defence mechanisms to ward off herbivorous pests. However, agriculture still faces estimated crop yield losses ranging from 25% to 40% annually. These losses arise not only because of direct feeding damage, but also because many pests serve as vectors of plant viruses. Herbivorous thrips (Thysanoptera) are important pests of vegetable and ornamental crops worldwide, and encompass virtually all general problems of pests: they are highly polyphagous, hard to control because of their complex lifestyle, and they are vectors of destructive viruses. Currently, control management of thrips mainly relies on the use of chemical pesticides. However, thrips rapidly develop resistance to these pesticides. With the rising demand for more sustainable, safer, and healthier food production systems, we urgently need to pinpoint the gaps in knowledge of plant defences against thrips to enable the future development of novel control methods. In this review, we summarize the current, rather scarce, knowledge of thrips-induced plant responses and the role of phytohormonal signalling and chemical defences in these responses. We describe concrete opportunities for breeding resistance against pests such as thrips as a prototype approach for next-generation resistance breeding.

Interactive Effects of UV-B Light with Abiotic Factors on Plant Growth and Chemistry, and Their Consequences for Defense against Arthropod Herbivores.

Ultraviolet-B (UV-B) light plays a crucial role in plant-herbivorous arthropods interactions by inducing changes in constitutive and inducible plant defenses. In particular, constitutive defenses can be modulated by UV-B-induced photomorphogenic responses and changes in the plant metabolome. In accordance, the prospective use of UV-B light as a tool to increase plant protection in agricultural practice has gained increasing interest. Changes in the environmental conditions might, however, modulate the UV-B -induced plant responses. While in some cases plant responses to UV-B can increase adaptation to changes in certain abiotic factors, UV-B-induced responses might be also antagonized by the changing environment. The outcome of these interactions might have a great influence on how plants interact with their enemies, e.g., herbivorous arthropods. Here, we provide a review on the interactive effects of UV-B and light quantity and quality, increased temperature and drought stress on plant biochemistry, and we discuss the implications of the outcome of these interactions for plant resistance to arthropod pests.

Induction of Jasmonic Acid-Associated Defenses by Thrips Alters Host Suitability for Conspecifics and Correlates with Increased Trichome Densities in Tomato.

Plant defenses inducible by herbivorous arthropods can determine performance of subsequent feeding herbivores. We investigated how infestation of tomato (Solanum lycopersicum) plants with the Western flower thrips (Frankliniella occidentalis) alters host plant suitability and foraging decisions of their conspecifics. We explored the role of delayed-induced jasmonic acid (JA)-mediated plant defense responses in thrips preference by using the tomato mutant def-1, impaired in JA biosynthesis. In particular, we investigated the effect of thrips infestation on trichome-associated tomato defenses. The results showed that when offered a choice, thrips preferred non-infested plants over infested wild-type plants, while no differences were observed in def-1. Exogenous application of methyl jasmonate restored the repellency effect in def-1. Gene expression analysis showed induction of the JA defense signaling pathway in wild-type plants, while activating the ethylene signaling pathway in both genotypes. Activation of JA defenses led to increases in type-VI leaf glandular trichome densities in the wild type, augmenting the production of trichome-associated volatiles, i.e. terpenes. Our study revealed that plant-mediated intraspecific interactions between thrips are determined by JA-mediated defenses in tomato. We report that insects can alter not only trichome densities but also the allelochemicals produced therein, and that this response might depend on the magnitude and/or type of the induction.

A Jasmonate-Inducible Defense Trait Transferred from Wild into Cultivated Tomato Establishes Increased Whitefly Resistance and Reduced Viral Disease Incidence.

Whiteflies damage tomatoes mostly via the viruses they transmit. Cultivated tomatoes lack many of the resistances of their wild relatives. In order to increase protection to its major pest, the whitefly Bemisia tabaci and its transmitted Tomato Yellow Leaf Curl Virus (TYLCV), we introgressed a trichome-based resistance trait from the wild tomato Solanum pimpinellifolium into cultivated tomato, Solanum lycopersicum. The tomato backcross line BC5S2 contains acylsucrose-producing type-IV trichomes, unlike cultivated tomatoes, and exhibits increased, yet limited protection to whiteflies at early development stages. Treatment of young plants with methyl jasmonate (MeJA) resulted in a 60% increase in type-IV trichome density, acylsucrose production, and enhanced resistance to whiteflies, leading to 50% decrease in the virus disease incidence compared to cultivated tomato. Using transcriptomics, metabolite analysis, and insect bioassays we established the basis of this inducible resistance. We found that MeJA activated the expression of the genes involved in the biosynthesis of the defensive acylsugars in young BC5S2 plants leading to enhanced chemical defenses in their acquired type-IV trichomes. Our results show that not only constitutive but also these inducible defenses can be transferred from wild into cultivated crops to aid sustainable protection, suggesting that conventional breeding strategies provide a feasible alternative to increase pest resistance in tomato.

Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores.

Glandular trichomes are specialized hairs found on the surface of about 30% of all vascular plants and are responsible for a significant portion of a plant's secondary chemistry. Glandular trichomes are an important source of essential oils, i.e., natural fragrances or products that can be used by the pharmaceutical industry, although many of these substances have evolved to provide the plant with protection against herbivores and pathogens. The storage compartment of glandular trichomes usually is located on the tip of the hair and is part of the glandular cell, or cells, which are metabolically active. Trichomes and their exudates can be harvested relatively easily, and this has permitted a detailed study of their metabolites, as well as the genes and proteins responsible for them. This knowledge now assists classical breeding programs, as well as targeted genetic engineering, aimed to optimize trichome density and physiology to facilitate customization of essential oil production or to tune biocide activity to enhance crop protection. We will provide an overview of the metabolic diversity found within plant glandular trichomes, with the emphasis on those of the Solanaceae, and of the tools available to manipulate their activities for enhancing the plant's resistance to pests.