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Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences - PubMed

  • ️Tue Jan 01 2008

Comparative Study

Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Merijn R Kant et al. Proc Biol Sci. 2008.

Abstract

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.

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Figures

Figure 1
Figure 1

The amount of spider mite feeding damage negatively correlates with induced levels of defence genes. Tomato plants (cv. Moneymaker (C32) and cv. Castlemart (CM)) were infested with five adult female spider mites of lines KMT or KMB. (a) After 4 days, the extent of leaf area damaged by feeding was measured. Vertical bars indicate the means and standard errors (s.e.). Different letters above the bars indicate significant differences as reported in §3. (b) The same tomato cultivars were infested with 15 adult female spider mites of lines KMT and KMB for 1 day after which leaflets were collected for RNA isolation and assayed for WIPI-II mRNA levels by RNA gel blot analysis. One representative experiment (n=3) is shown. Ethidium bromide (EtBr) staining is shown to illustrate equal loading.

Figure 2
Figure 2

Resistance and susceptibility of spider mites to tomato defences do not always depend on induced JA defences. (a) Cultivar Castlemart (wt), def1 and 35S::prosystemin (PS) tomato plants were infested with five adult female spider mites of lines KOP, KMT and KMB, and after 4 days we assessed the average number of eggs produced per female per 4 days on each tomato genotype. Vertical bars indicate the means and s.e. and different letters above the bars indicate significant differences. (b) Tomato plants (def1 and PS) were infested with 15 adult female spider mites of the lines KOP, KMT and KMB, and after 4 days leaflets were collected for RNA isolation and assayed for WIPI-II mRNA levels. EtBr staining is shown to illustrate equal loading. (c) Castlemart tomato plants (wt) were infested with 15 adult female spider mites of lines KOP, KMT and KMB, and after 4 days leaflets were collected to determine PI activity relative to the control (uninfested plants). Vertical bars indicate the means and s.e. and an asterisk denotes a significant difference compared with the control while ‘n.s.’ stands for ‘not significantly different from the control’.

Figure 3
Figure 3

Differential induction of tomato leaf volatiles by individual spider mite lines. Cultivar Castlemart tomato plants (wt) were infested with 15 adult female spider mites of lines KOP, KMT and KMB on three leaflets (45 mites per plant), and during 3 days tomato volatiles were collected and analysed using GC/TOF-MS. Shown is the average emission of (a) β-phellandrene, (b) β-caryophyllene, (c) MeSA and (d) TMTT per day, expressed relative to the treatment that gave the lowest emission of that compound (‘fold emission’). The 1.0 relative emission corresponds to 2.6 μg of β-phellandrene, 0.32 μg of β-caryophyllene, 10.7 μg of MeSA and 41.8 μg of TMTT per day per gram fresh weight. Vertical bars indicate the means and s.e. and an asterisk denotes a significant difference compared with the control while ‘n.s.’ stands for ‘not significantly different from the control’.

Figure 4
Figure 4

Introducing KMT spider mites onto KMB-infested tomato leaflets positively affects KMB fecundity. (a) A tomato leaf was divided into two by a thin lanolin barrier. Fifteen inducer mites (in brackets) were placed near the petiole and five receiver mites near the leaf tip. Shown in (b) are the performances of KMB and KMT (eggs per 4 days) in the presence of the other phenotype (KMB with KMT and KMT with KMB) on the same leaflet or in the presence of mites with the same phenotype (KMB with KMB and KMT with KMT) on the same leaflet as controls. Vertical bars indicate the means and s.e. and different letters above the bars indicate significant differences as reported in §3.

Figure 5
Figure 5

The R+I+ phenotype of KOP manifests itself only on tomato whereas the R−I− phenotype of KMT manifests itself on four different plant species. Shown is the spider mite fecundity per 4 days on (a) tomato (S. lycopersicum cv. Castlemart), (b) spindle tree (E. europaea L.), (c) mouse-ear cress (A. thaliana Col-0) and (d) broad bean (Phaseolus vulgaris). Vertical bars indicate the means and s.e. and different letters above the bars indicate significant differences.

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References

    1. Agrawal A.A. Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. Ecology. 2000;81:500–508.
    1. Agrawal A.A, Vala F, Sabelis M.W. Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: adaptive plasticity? Am. Nat. 2002;159:553–565. doi:10.1086/339463 - DOI - PubMed
    1. Ament K, Kant M.R, Sabelis M.W, Haring M.A, Schuurink R.C. Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol. 2004;135:2025–2037. doi:10.1104/pp.104.048694 - DOI - PMC - PubMed
    1. Bates S.L, Zhao J.Z, Roush R.T, Shelton A.M. Insect resistance management in GM crops: past, present and future. Nat. Biotechnol. 2005;23:57–62. doi:10.1038/nbt1056 - DOI - PubMed
    1. Bede J.C, Musser R.O, Felton G.W, Korth K.L. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol. Biol. 2006;60:519–531. doi:10.1007/s11103-005-4923-y - DOI - PubMed

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