Rocío Escobar‐Bravo

University of Bern

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Peter G. L. Klinkhamer

Leiden University

Kirsten A. Leiss

Wageningen University & Research

Bernardus C. J. Schimmel

University of Bern

Gang Chen

Sichuan Agricultural University

Matthias Erb

University of Bern

Gaétan Glauser

University of Neuchâtel

Hye Kyong Kim

Leiden University

Merijn R. Kant

University of Amsterdam

Christelle A. M. Robert

Edinburgh Cancer Research

Nicole M. van Dam

Leibniz Institute of Vegetable and Ornamental Crops

Cooperative Institutions

Wageningen University & Research

Leiden University

University of Bern

University of Amsterdam

Utrecht University

Consejo Superior de Investigaciones Científicas

Centre for BioSystems Genomics

Max Planck Institute for Chemical Ecology

Institute of Plant Biology

Graduate School Experimental Plant Sciences

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Far-red light increases maize volatile emissions in response to volatile cues from neighboring plants

bioRxiv (Cold Spring Harbor Laboratory) (2022)

Rocío Escobar‐Bravo Bernardus C. J. Schimmel Yaqin Zhang Lei Wang Christelle A. M. Robert

Abstract Plants perceive the presence and defense status of their neighbors through light and volatile cues, but how plants integrate both stimuli is poorly understood. We investigated if and how low Red to Far red light (R:FR) ratios, indicative of shading or canopy closure, affect maize ( Zea mays ) responses to herbivore-induced plant volatiles (HIPVs), including the green leaf volatile ( Z )-3-hexenyl acetate. We modulated light signaling and perception by using FR supplementation and a phyB1phyB2 mutant, and we determined volatile release as a response readout. To gain mechanistic insights, we examined expression of volatile biosynthesis genes, hormone accumulation, and photosynthesis. Exposure to a full blend of HIPVs or ( Z )-3-hexenyl acetate induced maize volatile release. Short-term FR supplementation increased this response. In contrast, prolonged FR supplementation or constitutive phytochrome B inactivation in phyB1phyB2 plants showed the opposite response. Short-term FR supplementation enhanced photosynthesis and stomatal conductance and ( Z )-3-hexenyl acetate-induced JA-Ile levels. We conclude that a FR-enriched light environment can prompt maize plants to respond more strongly to HIPVs emitted by neighbors, which might be explained by changes in photosynthetic processes and phytochrome B signaling. Our findings reveal interactive responses to light and volatile cues with potentially important consequences for plant-plant and plant-herbivore interactions.

10.1101/2022.09.12.507519

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Citations (3)

Plant Glandular Trichomes as Targets for Breeding or Engineering of Resistance to Herbivores

International Journal of Molecular Sciences (2012)

Joris J. Glas Bernardus C. J. Schimmel Juan M. Alba Rocío Escobar‐Bravo Robert C. Schuurink

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.

Trichome

10.3390/ijms131217077

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Citations (502)

Far‐red light increases maize volatile emissions in response to volatile cues from neighbouring plants

Plant Cell & Environment (2024)

Rocío Escobar‐Bravo Bernardus C. J. Schimmel Yaqin Zhang Lei Wang Christelle A. M. Robert

Abstract Plants perceive the presence and defence status of their neighbours through light and volatile cues, but how plants integrate both stimuli is poorly understood. We investigated if and how low Red to Far red light (R:FR) ratios, indicative of shading or canopy closure, affect maize ( Zea mays ) responses to herbivore‐induced plant volatiles (HIPVs), including the green leaf volatile ( Z )−3‐hexenyl acetate. We modulated light signalling and perception by using FR supplementation and a phyB1phyB2 mutant, and we determined volatile release as a response readout. To gain mechanistic insights, we examined expression of volatile biosynthesis genes, hormone accumulation, and photosynthesis. Exposure to a full blend of HIPVs or ( Z )−3‐hexenyl acetate induced maize volatile release. Short‐term FR supplementation increased this response. In contrast, prolonged FR supplementation or constitutive phytochrome B inactivation in phyB1phyB2 plants showed the opposite response. Short‐term FR supplementation enhanced photosynthesis and stomatal conductance and ( Z )−3‐hexenyl acetate‐induced JA‐Ile levels. We conclude that a FR‐enriched light environment can prompt maize plants to respond more strongly to HIPVs emitted by neighbours, which might be explained by changes in photosynthetic processes and phytochrome B signalling. Our findings reveal interactive responses to light and volatile cues with potentially important consequences for plant‐plant and plant‐herbivore interactions.

10.1111/pce.14995

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Citations (2)

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

Journal of Experimental Botany (2018)

Merel Steenbergen Ahmed Abd‐El‐Haliem Petra Bleeker Marcel Dicke Rocío Escobar‐Bravo

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.

Western flower thrips

Crop Protection

10.1093/jxb/ery060

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Citations (72)

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

Frontiers in Plant Science (2017)

Rocío Escobar‐Bravo Peter G. L. Klinkhamer Kirsten A. Leiss

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.

Arthropod

Metabolome

Defence mechanisms

Biotic component

Plant Physiology

10.3389/fpls.2017.00278

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Citations (147)

Leafminer attack induces plant-mediated facilitation of conspecific pupae in the soil

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Rocío Escobar‐Bravo Bernardus C. J. Schimmel Gaétan Glauser Peter G. L. Klinkhamer Matthias Erb

Summary 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 between different life developmental stages of the same herbivore. Yet, 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 Lyriomiza trifolii affects the performance of conspecific pupae in the soil adjacent to the plant. To gain mechanistic insights, we performed insect bioassays with the jasmonate-deficient tomato mutant def-1 and its wild type, along with the analysis of phytohormones, gene expression and root volatiles. Leafminer metamorphosis in the soil was accelerated when wild type plants were attacked aboveground by conspecifics, but the opposite was observed in def-1 . Changes in pupal developmental rate were mediated by belowground volatiles. Accordingly, leafminer herbivory differentially modulated jasmonate and abscisic acid signaling and the accumulation of specific volatiles in the roots of wild type versus def-1 plants Our results demonstrate that aboveground herbivores can facilitate their soil-dwelling pupae by inducing def-1 -dependent systemic responses. This study expands the repertoire of plant-herbivore interactions to herbivory-induced modulation of metamorphosis, with potentially important consequences for plant and herbivore community dynamics.

Jasmonate

Jasmonic acid

10.1101/2020.10.07.329763

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Citations (0)

Preface

Entomologia Experimentalis et Applicata (2022)

Rocío Escobar‐Bravo Suzanne T. E. Lommen

Abstract Originally, the 17th Symposium on Insect‐Plant Relationships (SIP‐17) was scheduled to take place in Leiden, The Netherlands, in July 2020. However, due to the COVID‐19 pandemic, the symposium was postponed to July 2021 and held in an exclusively online format. This exceptional edition has resulted in four strong contributions to the journal. It is with great pleasure that we now present a themed issue including the proceedings of SIP‐17, supplemented with eight regular articles within the subject of insect‐plant relationships.

10.1111/eea.13200

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

Plant Signaling & Behavior (2019)

Rocío Escobar‐Bravo Gang Chen Katharina Grosser Nicole M. van Dam Kirsten A. Leiss

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.

Jasmonic acid

Pseudomonas syringae

Western flower thrips

Jasmonate

10.1080/15592324.2019.1581560

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Citations (18)

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

Journal of Chemical Ecology (2020)

Gang Chen Peter G. L. Klinkhamer Rocío Escobar‐Bravo

Abstract 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.

Trichome

Western flower thrips

Chrysanthemum morifolium

Jasmonic acid

10.1007/s10886-020-01222-1

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Citations (4)

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

Plant Science (2018)

Gang Chen Peter G. L. Klinkhamer Rocío Escobar‐Bravo Kirsten A. Leiss

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.

Trichome

Jasmonic acid

Western flower thrips

10.1016/j.plantsci.2018.08.007

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Citations (54)