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Arabidopsis thaliana Plants with Different Levels of Aliphatic- and Indolyl-Glucosinolates Affect Host Selection and Performance of Bemisia tabaci

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Abstract

Generalist insects show reduced selectivity when subjected to similar, but not identical, host plant chemical signatures. Here, we produced transgenic Arabidopsis thaliana plants that over-express genes regulating the aliphatic- and indolyl- glucosinolates biosynthetic pathways with either a constitutive (CaMV 35S) or a phloem-specific promoter (AtSUC2). This allowed us to examine how exposure to high levels of aliphatic- or indolyl-glucosinolates in homogenous habitats (leaf cage apparatus containing two wild-type or two transgenic leaves) and heterogeneous habitats (leaf cage apparatus containing one wild-type and one transgenic leaf) affects host selection and performance of Bemsia tabaci, a generalist phloem-feeding insect. Data from homogenous habitats indicated that exposure to A. thaliana plants accumulating high levels of aliphatic- or indolyl-glucosinolates negatively affected the performance of both adult females and nymphs of B. tabaci. Data from heterogeneous habitats indicated that B. tabaci adult females selected for oviposition plants on which their offspring perform better (preference-performance relationship). However, the combinations of wild-type and transgenic plants in heterogeneous habitats increased the period of time until the first choice was made and led to increased movement rate on transgenic plants, and reduced fecundity on wild-type plants. Overall, our findings are consistent with the view that both performance and selectivity of B. tabaci decrease in heterogeneous habitats that contain plants with closely-related chemical signatures.

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Acknowledgments

This work was supported by the Israel Science Foundation grant 848/08 and the Binational Agricultural Research and Development Fund (BARD) research grant No. IS-4169-08 R.

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Authors and Affiliations

  1. Department of Entomology, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, 76100, Israel

    Oshry Markovich, Dinesh Kafle, Moshe Elbaz & Shai Morin

  2. Department of Plant Sciences, Weizmann Institute of Science, Rehovot, 76100, Israel

    Oshry Markovich, Sergey Malitsky & Asaph Aharoni

  3. Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany

    Alexander Schwarzkopf & Jonathan Gershenzon

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  1. Oshry Markovich
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Correspondence to Shai Morin.

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Fig. S1

Specially designed two leaf-cage apparatus. In each replicate of the choice experiments, three adult pairs (male and female) were isolated at the late fourth instar stage and placed in the middle chamber of the specially designed two leaf-cage apparatus. After emergence, adults were allowed to choose between rosette sink leaves (placed in the left and right chambers) of OX-MYB and WT plants. Control (no-choice) treatments used two plants of the same type. In egg to adult development and survival experiments, 12 pairs (male and female) of Bemisia tabaci adults, 3 d old, were released in the middle chamber while two sink rosette leaves of the same plant type (WT, 35S-MYB28, 35S-MYB51, pSUC-MYB28, and pSUC-MYB51) were placed in the left and right chambers. (PPT 591 kb)

Fig. S2

Images of Bemisia tabaci behavior in selected homogeneous (WT/WT and 35S-MYB51/35S-MYB51) or heterogeneous (WT/35S-MYB51) habitats. Cages were prepared using small 35 mm Petri dishes. Two similar-sized holes were made on two sides of the lower and upper covers of the Petri dish to allow the insertion of non-detached leaves (A–B). A plastic film at the size of upper cover was prepared with two cuts of equal size, around 14 × 7 mm each (C). Sink rosette leaves were inserted through the two cuts in the Petri dish and kept between the plastic film and the upper cover (D). This set up prevented the insects from moving to the adaxial side of the leaf and in addition, provided equal leaf areas for the insects. Two different cameras were used to record B. tabaci behavior: a Sony Digital Handycam (DCR-PC 110E PAL) (E) and a Dino-Lite Plus Digital Microscope (AM313T+) (F). The behavior of newly emerged B. tabaci female individuals (in red cicrcle) was recorded for five days (G). (PPT 1631 kb)

Fig. S3

Analysis of AtMYB28/AtMYB51 gene expression by quantitative real-time PCR (qRT-PCR). 2−ΔΔCt data were log- transformed. Dunnett’s post-hoc test was used to compare means of WT plants to those of OX-MYB plants (T-20 for 35S-MYB51, T-9 for 35S-MYB28, T-45 for pSUC-MYB51, and T-29 for pSUC-MYB28). Asterisks indicate significant differences between the means (P ≤ 0.05). Error bars represent standard error of the means (N = 3). (PPT 80 kb)

Fig. S4

Bemisia tabaci behavior in homogenous or heterogeneous habitats. The behavior of newly emerged B. tabaci female individuals was videotaped for five days in selected homogeneous no choice (WT/WT and 35S-MYB51/35S-MYB51) or heterogeneous choice (WT/35S-MYB51) habitats. Each plant genotype is coded with a different color (see legend on figure). Columns with a single color code represent homogenous habitats while dotted columns with two-color codes represent specific heterogeneous habitats (see legend on figure). Genotypes marked in bold in the heterogeneous (Het) habitat indicate which data are presented (WT/35S-MYB51 for WT data and WT/35S-MYB51 for 35S-MYB51 data). (A) Time on the first leaf choice. (B) Mean feeding time (duration on each leaf divided by the number of movements observed during the period) on the first leaf choice. (C) Mean feeding time on the second leaf choice. (D) Mean feeding time during the compete experiment (5 days), excluding the feeding periods on the first and second leaves. Comparisons were made between similar leaf genotypes (WT or 35S-MYB51) in homogeneous and heterogeneous habitats. (#) indicates P-value of 0.09. (PPT 70 kb)

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Markovich, O., Kafle, D., Elbaz, M. et al. Arabidopsis thaliana Plants with Different Levels of Aliphatic- and Indolyl-Glucosinolates Affect Host Selection and Performance of Bemisia tabaci . J Chem Ecol 39, 1361–1372 (2013). https://doi.org/10.1007/s10886-013-0358-0

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