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Insect feeding retards plant growth and decreases crop productivity. Plants respond to insect feeding at the molecular, cellular and physiological levels. The roles of the plant hormones jasmonic acid (JA), ethylene (ET) and salicylic acid (SA) in plant responses to insect feeding have been studied. However, these studies are focused on the plant responses to feeding by well-studied caterpillar type insects or aphid pests. In contrast, we have focused on a minute insect pest, the western flower thrips (Frankliniella occidentalis). Analyses of the responses of hormone-related mutants of Arabidopsis (i.e., JA-insensitive mutant coi1-1, ET-insensitive mutants ein2-1 and ein3-1, and SA-deficient mutant eds16-1) and transcriptome-based comparative analyses indicate the central role of JA in plant responses to thrips feeding. Our work clearly shows that JA signaling, but not JA/ET signaling, is involved in plant tolerance to thrips feeding. We intend to examine the utility and suitability of the Arabidopsis-thrips system in studies of plant responses to insect feeding.
The western flower thrips (Fig. 1) is one of the most important insect herbivores and is an exotic pest in greenhouse production in many countries. Thrips use their mouthparts to pierce plant cells and draw out the contents. This feeding mode differs from those of well-studied caterpillars and aphids.1,2 Thrips can also act as virus vectors.3 Their thigmokinetic behavior and the emergence of insecticide resistance make them difficult to control with insecticides.4 Therefore, elucidation of the molecular mechanisms of plant responses to feeding by the thrips will support the development of new methods to prevent damage.
In our associated study, we analyzed the expression of JA-, ET- or SA-inducible marker genes in Arabidopsis after feeding by thrips to evaluate the roles of plant immunity-related hormones. Feeding induced expression of VSP2 and LOX2, marker genes of the JA pathway; chiB and PDF1.2, marker genes of the JA/ET pathway; and of the SA-inducible genes PR1 and BGL2. Further analyses with hormone-related mutants supported the involvement of these hormones in plant responses to thrips feeding. Specifically, expression of the marker genes of the JA and JA/ET pathways was reduced in the JA-insensitive coi1-1 mutant;5 that of marker genes of the JA/ET pathway was reduced in the ET-insensitive mutants ein2-16 and ein3-1;7 and that of marker genes of the SA pathway was markedly reduced in the SA-deficient mutant eds16-1.8,9
Insect feeding leads to mechanical wounding.10 Yet a recent study clearly showed that plants respond differently to insect feeding and mechanical wounding.11 JA and ET have important functions in plant responses to mechanical wounding.12 However, the molecular mechanisms of the different responses by insect feeding and mechanical wounding have not been well elucidated. Interestingly, thrips feeding induced the expression of marker genes of the SA pathway, which is not activated in mechanical wounding. The expression of marker genes of the SA pathway was remarkably reduced in the eds16-1 mutant, yet comparative transcriptome analyses did not indicate the importance of SA in the plant responses to thrips feeding. One possible reason is the involvement of a basal level of SA for plant response. Recently, Zarate et al.,13 reported that feeding by silverleaf whitefly activated SA signaling but not JA or JA/ET signaling. They hypothesized that silverleaf whitefly uses SA signaling to suppress JA-regulated plant defense. The biological significance of the induction of SA pathway marker genes by thrips feeding is unclear. However, investigations to clarify how Arabidopsis plants respond to thrips feeding through the antagonistic plant hormones JA and SA could reveal the difference between wounding and insect feeding.
Comparative transcriptome analyses also dismissed the importance of ET but showed the importance of JA, the level of which was increased after thrips feeding. Positive and negative interactions between JA and ET are well understood.12 The importance of JA and ET in plant responses to insect feeding has been reported.14,15 However, the exact pathway that regulates responses to feeding is not well understood. To dissect the precise signaling pathway, we analyzed the effect of JA and ET application on plant tolerance to thrips feeding. JA but not ET increased the tolerance. In other words, wounding signals, which are regulated by JA, function in plant responses and tolerance to thrips feeding.
We showed in our recent paper that the application of JA to Arabidopsis decreased injury caused by western flower thrips. However, JA also inhibits plant growth. Therefore, JA on its own would seem to be impractical for application. Screening to find specific compounds that regulate plant responses to insect attack offers a promising approach. Alternatively, we could identify the chemicals used in direct defense against insect pest. Among several such compounds, Konno et al.,16 reported that cysteine proteases such as papain, ficin and bromelain showed toxicity to two notorious polyphagous pests, Mamestra brassicae and Spodoptera litura. Most well-analyzed endogenous compounds produced in defense against insect pests are isothiocyanates, volatile breakdown products of glucosinolates with biological activity against herbivores and pathogens.17–19 Sasaki-Sekimoto et al.,20 reported that the biosynthesis of glucosinolate is regulated by JA. Thus, glucosinolate may be one of the metabolites used in JA-regulated chemical defense.
Arabidopsis is a useful experimental plant with massive genomic resources and information. However, it is not a suitable plant species for analyzing responses to popularly studied caterpillars, which can devour a whole plant within a short period. On the other hand, the minute western flower thrips is too small to devour a whole Arabidopsis plant. Moreover, it can complete its life cycle on the one Arabidopsis plant. This makes it ideal for analyzing the response of Arabidopsis over generations. Further analyses using the Arabidopsisthrips system will help clarify the mechanisms of plant defense responses to insect attack.
Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/5556