Jasmonate-dependent plant defense restricts thrips performance and preference

Experimental Plant Division, RIKEN BioResource Center, Tsukuba 305-0074, Japan.
BMC Plant Biology (Impact Factor: 3.81). 08/2009; 9(1):97. DOI: 10.1186/1471-2229-9-97
Source: PubMed


The western flower thrips (Frankliniella occidentalis [Pergande]) is one of the most important insect herbivores of cultivated plants. However, no pesticide provides complete control of this species, and insecticide resistance has emerged around the world. We previously reported the important role of jasmonate (JA) in the plant's immediate response to thrips feeding by using an Arabidopsis leaf disc system. In this study, as the first step toward practical use of JA in thrips control, we analyzed the effect of JA-regulated Arabidopsis defense at the whole plant level on thrips behavior and life cycle at the population level over an extended period. We also studied the effectiveness of JA-regulated plant defense on thrips damage in Chinese cabbage (Brassica rapa subsp. pekinensis).
Thrips oviposited more on Arabidopsis JA-insensitive coi1-1 mutants than on WT plants, and the population density of the following thrips generation increased on coi1-1 mutants. Moreover, thrips preferred coi1-1 mutants more than WT plants. Application of JA to WT plants before thrips attack decreased the thrips population. To analyze these important functions of JA in a brassica crop plant, we analyzed the expression of marker genes for JA response in B. rapa. Thrips feeding induced expression of these marker genes and significantly increased the JA content in B. rapa. Application of JA to B. rapa enhanced plant resistance to thrips, restricted oviposition, and reduced the population density of the following generation.
Our results indicate that the JA-regulated plant defense restricts thrips performance and preference, and plays an important role in the resistance of Arabidopsis and B. rapa to thrips damage.

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    • "Attractiveness of the shoots of nematode-infected plants to L2 of F. occidentalis was significantly reduced. Similarly, Abe et al. (2008, 2009) showed that thrips feeding induces JA-regulated plant defence, which negatively affects thrips oviposition and population density. These authors also showed that exogenous application of JA and mJA onto the leaf surface significantly reduces attraction and settling of F. occidentalis. "
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    ABSTRACT: Above- and belowground plant parts are simultaneously attacked by different pests and pathogens. The host mediates these interactions and physiologically reacts, e.g. with local and systemic alterations of endogenous hormone levels coupled with coordinated transcriptional changes. This in turn affects attractiveness and susceptibility of the plant to subsequent attackers. Here, the model plant Arabidopsis thaliana is used to study stress hormone-based systemic responses triggered by simultaneous root parasitism by the cyst nematode Heterodera schachtii and shoot herbivory by the thrips Frankliniella occidentalis and the spider mite Tetranychus urticae. First, HPLC/MS and quantitative reverse transcriptase PCR are used to show that nematode parasitism strongly affects stress hormone levels and expression of hormone marker genes in shoots. Previous nematode infection is then demonstrated to affect the behavioural and life history performance of both arthropods. While thrips explicitly avoid nematode-infected plants, spider mites prefer them. In addition, the life history performance of T. urticae is significantly enhanced by nematode infection. Finally, systemic changes triggered by shoot-feeding F. occidentalis but not T. urticae are shown to make the roots more attractive for H. schachtii. This work emphasises the importance of above- and belowground signalling and contributes to a better understanding of plant systemic defence mechanisms against plant-parasitic nematodes. © The Author 2015. Published by Oxford University Press on behalf of the Society for Experimental Biology.
    Full-text · Article · Aug 2015 · Journal of Experimental Botany
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    • "Frankliniella occidentalis A. thaliana (Brassicaceae) Zhurov et al. 2014 (Thysanoptera) S. lycopersicum (Solanaceae) Li et al. 2002 A. thaliana (Brassicaceae) Abe et al. 2009 Piercing-sucking insects Myzus persicae (Hemiptera) A. thaliana (Brassicaceae) Ellis et al. 2002 Empoasca sp. (Hemiptera) Nicotiana attenuata (Solanaceae) Kessler et al. 2004 Leafminer insects Scaptomyza flava (Diptera) A. thaliana (Brassicaceae) Whiteman et al. 2011 Leaf/root chewing insects Manduca sexta (Lepidoptera) N. attenuata (Solanaceae) Howe et al. 1996; Kessler et al. 2004; Spodoptera frugiperda (Lepidoptera) S. lycopersicum (Solanaceae) Campos et al. 2009 Bradysia impatiens (Diptera) A. thaliana (Brassicaceae) McConn et al. 1997 Spodoptera exigua (Lepidoptera) Z. mays (Poaceae) Yan et al. 2012 Vertebrate herbivores Eurotestudo boettgeri A. thaliana (Brassicaceae) Mafli et al. 2012 et al. 2006; Wasternack and Hause 2013). "
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    ABSTRACT: The plant hormone jasmonate (JA) exerts direct control over the production of chemical defense compounds that confer resistance to a remarkable spectrum of plant-associated organisms, ranging from microbial pathogens to vertebrate herbivores. The underlying mechanism of JA-triggered immunity (JATI) can be conceptualized as a multi-stage signal transduction cascade involving: i) pattern recognition receptors (PRRs) that couple the perception of danger signals to rapid synthesis of bioactive JA; ii) an evolutionarily conserved JA signaling module that links fluctuating JA levels to changes in the abundance of transcriptional repressor proteins; and iii) activation (de-repression) of transcription factors that orchestrate the expression of myriad chemical and morphological defense traits. Multiple negative feedback loops act in concert to restrain the duration and amplitude of defense responses, presumably to mitigate potential fitness costs of JATI. The convergence of diverse plant- and non-plant-derived signals on the core JA module indicates that JATI is a general response to perceived danger. However, the modular structure of JATI may accommodate attacker-specific defense responses through evolutionary innovation of PRRs (inputs) and defense traits (outputs). The efficacy of JATI as a defense strategy is highlighted by its capacity to shape natural populations of plant attackers, as well as the propensity of plant-associated organisms to subvert or otherwise manipulate JA signaling. As both a cellular hub for integrating informational cues from the environment and a common target of pathogen effectors, the core JA module provides a focal point for understanding immune system networks and the evolution of chemical diversity in the plant kingdom.
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    • "BTH has been commercialized as an effective compound in the market by several manufacturers. Jasmonic acid (JA), fatty acid-derived compound confers plant tolerance to necrotrophic fungi and herbivores (Abe et al., 2009; Rowe et al., 2010). JA occasionally acts antagonistically with SA-dependent defense signalling during plant-pathogen interactions (Smith et al., 2009). "
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