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Comparative Study
. 2011;6(7):e22690.
doi: 10.1371/journal.pone.0022690. Epub 2011 Jul 28.

Infestation of Transgenic Powdery Mildew-Resistant Wheat by Naturally Occurring Insect Herbivores Under Different Environmental Conditions

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Free PMC article
Comparative Study

Infestation of Transgenic Powdery Mildew-Resistant Wheat by Naturally Occurring Insect Herbivores Under Different Environmental Conditions

Fernando Álvarez-Alfageme et al. PLoS One. .
Free PMC article

Abstract

A concern associated with the growing of genetically modified (GM) crops is that they could adversely affect non-target organisms. We assessed the impact of several transgenic powdery mildew-resistant spring wheat lines on insect herbivores. The GM lines carried either the Pm3b gene from hexaploid wheat, which confers race-specific resistance to powdery mildew, or the less specific anti-fungal barley seed chitinase and β-1,3-glucanase. In addition to the non-transformed control lines, several conventional spring wheat varieties and barley and triticale were included for comparison. During two consecutive growing seasons, powdery mildew infection and the abundance of and damage by naturally occurring herbivores were estimated under semi-field conditions in a convertible glasshouse and in the field. Mildew was reduced on the Pm3b-transgenic lines but not on the chitinase/glucanase-expressing lines. Abundance of aphids was negatively correlated with powdery mildew in the convertible glasshouse, with Pm3b wheat plants hosting significantly more aphids than their mildew-susceptible controls. In contrast, aphid densities did not differ between GM plants and their non-transformed controls in the field, probably because of low mildew and aphid pressure at this location. Likewise, the GM wheat lines did not affect the abundance of or damage by the herbivores Oulema melanopus (L.) and Chlorops pumilionis Bjerk. Although a previous study has revealed that some of the GM wheat lines show pleiotropic effects under field conditions, their effect on herbivorous insects appears to be low.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Powdery mildew infection of the wheat plants grown in the convertible glasshouse.
Infection was scored using a 0 to 9 scale (0 = no symptoms, 9 = fully diseased). Area under disease progress curve (AUDPC) (±SE) was calculated with data from 9 and 6 sampling dates in 2008 and 2009, respectively. Therefore, AUDPC values are not comparable between years. White bars represent transgenic lines while black bars represent non-transformed lines. (N = 8). Significant differences were recorded between the non-transformed line Sb#1 and the conventional varieties Frisal and Rubli (Tukey HSD test, p<0.001), and between transgenic Pm3b#1 plants and their control line Sb#1 over both years of study (Tukey HSD test, p<0.001).
Figure 2
Figure 2. Densities of aphids and Oulema melanopus larvae on wheat grown in the convertible glasshouse.
Cumulative numbers (± SE) of (A) aphids and (B) O. melanopus were calculated with 11 and 9 sampling dates in 2008 and 2009, respectively. White bars represent transgenic lines while black bars represent non-transformed lines. (N = 8). For aphid densities, significant differences were recorded between the transgenic Pm3b#1 and their non-transformed control line Sb#1 over both years of study (Tukey HSD test, p = 0.025).
Figure 3
Figure 3. Powdery mildew infection of plants grown in the field.
Percentage of the leaf surface infected with powdery mildew was estimated in (A) 2008 and (B) 2009. The area under disease progress curve (AUDPC) (± SE) was calculated with data from 5 sampling dates in both years. White bars represent transgenic lines while black bars represent non-transformed lines. (2008: N = 4; 2009: N = 5). Significant differences were recorded between Bobwhite plants and the other conventional wheat varieties as well as barley and triticale in 2008 (Tukey HSD test, p<0.05). Likewise, significant differences were observed between transgenic Pm3b and their respective non-transformed Sb plants (Pm3b#1/Sb#1: F 1,14 = 22.7, p<0.001; Pm3b#2/Sb#2: F 1,14 = 6.18, p = 0.026; Pm3b#3/Sb#3: F 1,6 = 11.44, p = 0.015, Pm3b#4/Sb#4: F 1,6 = 4.53, p = 0.077).
Figure 4
Figure 4. Densities of aphids, Oulema melanopus larvae, and damaged by Chlorops pumilionis in the field.
Cumulative numbers (± SE) of (A) aphids and (B) O. melanopus were calculated with data from 7 and 6 sampling dates in 2008 and 2009, respectively, whereas (C) percentage of tillers damaged by C. pumilionis was calculated at the end of both growing seasons. White bars represent transgenic lines while black bars represent non-transformed lines. (2008: N = 4; 2009: N = 5). Significant differences were recorded for C. pumilionis larvae between barley plants and the conventional wheat lines and triticale in 2008 and 2009 (Tukey HSD test, p<0.05, and p<0.001, respectively).
Figure 5
Figure 5. Correlation between abundance per tiller of and damage by Oulema melanopus larvae.
Data were retrieved from the convertible glasshouse (grey dots) and the field (white dots) in 2008 and 2009.

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