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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    • "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.
    Journal of Chemical Ecology 06/2014; 40(7). DOI:10.1007/s10886-014-0468-3 · 2.75 Impact Factor
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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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    ABSTRACT: Non-protein amino acid, -amino-n-butyric acid (BABA), has been involved in diverse physiological processes including seedling growth, stress tolerance and disease resistance of many plant species. In the current study, treatment of kimchi cabbage seedlings with BABA significantly reduced primary root elongation and cotyledon development in a dose-dependent manner, which adverse effects were similar to the plant response to exogenous abscisic acid (ABA) application. BABA was synergistically contributing ABA-induced growth arrest during the early seedling development. Kimchi cabbage leaves were highly damaged and seedling growth was delayed by foliar spraying with high concentrations of BABA (10 to 20 mM). BABA played roles differentially in in vitro fungal conidial germination, mycelial growth and conidation of necrotroph Alternaria brassicicola causing black spot disease and hemibiotroph Colletotrichum higginsianum causing anthracnose. Pretreatment with BABA conferred induced resistance of the kimchi cabbage against challenges by the two different classes of fungal pathogens in a dose-dependent manner. These results suggest that BABA is involved in plant development, fungal development as well as induced fungal disease resistance of kimchi cabbage plant.
    The plant pathology journal 09/2013; 29(3). DOI:10.5423/PPJ.OA.12.2012.0191 · 0.72 Impact Factor
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    • "The current study is also the first to demonstrate that below-ground herbivory affects the responses of thrips species to their host plants (Figure 1), with the two thrips species responding differently to root damage on cotton. Studies on other insects have shown similar results [25], [53], [12]. Induced responses brought on by root herbivory have recently been shown to result in systemic responses in the shoots [42]. "
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    ABSTRACT: Changes in plants following insect attack are referred to as induced responses. These responses are widely viewed as a form of defence against further insect attack. In the current study we explore whether it is possible to make generalizations about induced plant responses given the unpredictability and variability observed in insect-plant interactions. Experiments were conducted to test for consistency in the responses of two congeneric thrips, Frankliniella schultzei Trybom and Frankliniella occidentalis Pergrande (Thysanoptera: Thripidae) to cotton seedlings (Gossypium hirsutum Linneaus (Malvales: Malvaceae)) damaged by various insect herbivores. In dual-choice experiments that compared intact and damaged cotton seedlings, F. schultzei was attracted to seedlings damaged by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Tetranychus urticae (Koch) (Trombidiforms: Tetranychidae), Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), F. schultzei and F. occidentalis but not to mechanically damaged seedlings. In similar tests, F. occidentalis was attracted to undamaged cotton seedlings when simultaneously exposed to seedlings damaged by H. armigera, T. molitor or F. occidentalis. However, when exposed to F. schultzei or T. urticae damaged plants, F. occidentalis was more attracted towards damaged plants. A quantitative relationship was also apparent, F. schultzei showed increased attraction to damaged seedlings as the density of T. urticae or F. schultzei increased. In contrast, although F. occidentalis demonstrated increased attraction to plants damaged by higher densities of T. urticae, there was a negative relationship between attraction and the density of damaging conspecifics. Both species showed greater attraction to T. urticae damaged seedlings than to seedlings damaged by conspecifics. Results demonstrate that the responses of both species of thrips were context dependent, making generalizations difficult to formulate.
    PLoS ONE 05/2013; 8(5):e63611. DOI:10.1371/journal.pone.0063611 · 3.23 Impact Factor
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