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Transgene x environment interactions in genetically modified wheat.

Zeller SL, Kalinina O, Brunner S, Keller B, Schmid B - PLoS ONE (2010)

Bottom Line: In the field these results were reversed.Our results demonstrate that, depending on the insertion event, a particular transgene can have large effects on the entire phenotype of a plant and that these effects can sometimes be reversed when plants are moved from the glasshouse to the field.However, it remains unclear which mechanisms underlie these effects and how they may affect concepts in molecular plant breeding and plant evolutionary ecology.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Ecology and Environmental Studies, University of Zurich, Zurich, Switzerland. simon.zeller@ieu.uzh.ch

ABSTRACT

Background: The introduction of transgenes into plants may cause unintended phenotypic effects which could have an impact on the plant itself and the environment. Little is published in the scientific literature about the interrelation of environmental factors and possible unintended effects in genetically modified (GM) plants.

Methods and findings: We studied transgenic bread wheat Triticum aestivum lines expressing the wheat Pm3b gene against the fungus powdery mildew Blumeria graminis f.sp. tritici. Four independent offspring pairs, each consisting of a GM line and its corresponding non-GM control line, were grown under different soil nutrient conditions and with and without fungicide treatment in the glasshouse. Furthermore, we performed a field experiment with a similar design to validate our glasshouse results. The transgene increased the resistance to powdery mildew in all environments. However, GM plants reacted sensitive to fungicide spraying in the glasshouse. Without fungicide treatment, in the glasshouse GM lines had increased vegetative biomass and seed number and a twofold yield compared with control lines. In the field these results were reversed. Fertilization generally increased GM/control differences in the glasshouse but not in the field. Two of four GM lines showed up to 56% yield reduction and a 40-fold increase of infection with ergot disease Claviceps purpurea compared with their control lines in the field experiment; one GM line was very similar to its control.

Conclusions: Our results demonstrate that, depending on the insertion event, a particular transgene can have large effects on the entire phenotype of a plant and that these effects can sometimes be reversed when plants are moved from the glasshouse to the field. However, it remains unclear which mechanisms underlie these effects and how they may affect concepts in molecular plant breeding and plant evolutionary ecology.

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Related in: MedlinePlus

Effects of the transgene in the glasshouse on mildew infection and plant performance traits.The mildew infection equals the proportion of pots with strong powdery mildew infection up to flag leaves. Phenological stage, plant height, vegetative mass, seed number and seed yield were measured to assess the plant performance. A: mean of four lines (Control  =  S3b#1–4; GM  =  Pm3b#1–4) at different soil nutrient levels (circles  =  high fertilizer, squares  =  medium fertilizer, triangles  =  no additional fertilizer); significant transgene × fertilizer environment interactions indicated by asterisks (vegetative mass: P = 0.035, seed number: P<0.001, seed yield: P<0.001); light grey lines were drawn to make these interactions visible; error bars represent ±1 standard error (back-transformed, see methods) and are sometimes hidden behind the symbols. B: proportional difference between GM and control plants for each of the four offspring lines but averaged across nutrient levels (white bars  =  offspring pair 1 (Pm3b#1 vs. S3b#1), light grey  =  offspring pair 2, dark gray  =  offspring pair 3, black bars  =  offspring pair 4); x-axis log-scale with original values (100 * GM/control); bars extending to the right from the vertical zero line indicate higher values in GM than in control plants; significant GM/control x offspring pair interactions indicated by asterisks (* P<0.05; ***P<0.001).
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pone-0011405-g002: Effects of the transgene in the glasshouse on mildew infection and plant performance traits.The mildew infection equals the proportion of pots with strong powdery mildew infection up to flag leaves. Phenological stage, plant height, vegetative mass, seed number and seed yield were measured to assess the plant performance. A: mean of four lines (Control  =  S3b#1–4; GM  =  Pm3b#1–4) at different soil nutrient levels (circles  =  high fertilizer, squares  =  medium fertilizer, triangles  =  no additional fertilizer); significant transgene × fertilizer environment interactions indicated by asterisks (vegetative mass: P = 0.035, seed number: P<0.001, seed yield: P<0.001); light grey lines were drawn to make these interactions visible; error bars represent ±1 standard error (back-transformed, see methods) and are sometimes hidden behind the symbols. B: proportional difference between GM and control plants for each of the four offspring lines but averaged across nutrient levels (white bars  =  offspring pair 1 (Pm3b#1 vs. S3b#1), light grey  =  offspring pair 2, dark gray  =  offspring pair 3, black bars  =  offspring pair 4); x-axis log-scale with original values (100 * GM/control); bars extending to the right from the vertical zero line indicate higher values in GM than in control plants; significant GM/control x offspring pair interactions indicated by asterisks (* P<0.05; ***P<0.001).

Mentions: The Pm3b transgene had the desired phenotypic effect and increased resistance to powdery mildew in the glasshouse experiment (Figure 1; P<0.001 for difference GM/control plants, see Table S1). The yield of the GM lines doubled (from 1.60 to 3.23 tonnes per ha−1) compared to the susceptible control lines. GM plants had also more seeds and higher vegetative biomass than control plants in the glasshouse (Figure 2; both P<0.001; see Table S2). Phenological development and plant height were not affected by the transgene, indicating that these traits may be genetically more constrained than the other traits.


Transgene x environment interactions in genetically modified wheat.

Zeller SL, Kalinina O, Brunner S, Keller B, Schmid B - PLoS ONE (2010)

Effects of the transgene in the glasshouse on mildew infection and plant performance traits.The mildew infection equals the proportion of pots with strong powdery mildew infection up to flag leaves. Phenological stage, plant height, vegetative mass, seed number and seed yield were measured to assess the plant performance. A: mean of four lines (Control  =  S3b#1–4; GM  =  Pm3b#1–4) at different soil nutrient levels (circles  =  high fertilizer, squares  =  medium fertilizer, triangles  =  no additional fertilizer); significant transgene × fertilizer environment interactions indicated by asterisks (vegetative mass: P = 0.035, seed number: P<0.001, seed yield: P<0.001); light grey lines were drawn to make these interactions visible; error bars represent ±1 standard error (back-transformed, see methods) and are sometimes hidden behind the symbols. B: proportional difference between GM and control plants for each of the four offspring lines but averaged across nutrient levels (white bars  =  offspring pair 1 (Pm3b#1 vs. S3b#1), light grey  =  offspring pair 2, dark gray  =  offspring pair 3, black bars  =  offspring pair 4); x-axis log-scale with original values (100 * GM/control); bars extending to the right from the vertical zero line indicate higher values in GM than in control plants; significant GM/control x offspring pair interactions indicated by asterisks (* P<0.05; ***P<0.001).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2902502&req=5

pone-0011405-g002: Effects of the transgene in the glasshouse on mildew infection and plant performance traits.The mildew infection equals the proportion of pots with strong powdery mildew infection up to flag leaves. Phenological stage, plant height, vegetative mass, seed number and seed yield were measured to assess the plant performance. A: mean of four lines (Control  =  S3b#1–4; GM  =  Pm3b#1–4) at different soil nutrient levels (circles  =  high fertilizer, squares  =  medium fertilizer, triangles  =  no additional fertilizer); significant transgene × fertilizer environment interactions indicated by asterisks (vegetative mass: P = 0.035, seed number: P<0.001, seed yield: P<0.001); light grey lines were drawn to make these interactions visible; error bars represent ±1 standard error (back-transformed, see methods) and are sometimes hidden behind the symbols. B: proportional difference between GM and control plants for each of the four offspring lines but averaged across nutrient levels (white bars  =  offspring pair 1 (Pm3b#1 vs. S3b#1), light grey  =  offspring pair 2, dark gray  =  offspring pair 3, black bars  =  offspring pair 4); x-axis log-scale with original values (100 * GM/control); bars extending to the right from the vertical zero line indicate higher values in GM than in control plants; significant GM/control x offspring pair interactions indicated by asterisks (* P<0.05; ***P<0.001).
Mentions: The Pm3b transgene had the desired phenotypic effect and increased resistance to powdery mildew in the glasshouse experiment (Figure 1; P<0.001 for difference GM/control plants, see Table S1). The yield of the GM lines doubled (from 1.60 to 3.23 tonnes per ha−1) compared to the susceptible control lines. GM plants had also more seeds and higher vegetative biomass than control plants in the glasshouse (Figure 2; both P<0.001; see Table S2). Phenological development and plant height were not affected by the transgene, indicating that these traits may be genetically more constrained than the other traits.

Bottom Line: In the field these results were reversed.Our results demonstrate that, depending on the insertion event, a particular transgene can have large effects on the entire phenotype of a plant and that these effects can sometimes be reversed when plants are moved from the glasshouse to the field.However, it remains unclear which mechanisms underlie these effects and how they may affect concepts in molecular plant breeding and plant evolutionary ecology.

View Article: PubMed Central - PubMed

Affiliation: Institute of Evolutionary Ecology and Environmental Studies, University of Zurich, Zurich, Switzerland. simon.zeller@ieu.uzh.ch

ABSTRACT

Background: The introduction of transgenes into plants may cause unintended phenotypic effects which could have an impact on the plant itself and the environment. Little is published in the scientific literature about the interrelation of environmental factors and possible unintended effects in genetically modified (GM) plants.

Methods and findings: We studied transgenic bread wheat Triticum aestivum lines expressing the wheat Pm3b gene against the fungus powdery mildew Blumeria graminis f.sp. tritici. Four independent offspring pairs, each consisting of a GM line and its corresponding non-GM control line, were grown under different soil nutrient conditions and with and without fungicide treatment in the glasshouse. Furthermore, we performed a field experiment with a similar design to validate our glasshouse results. The transgene increased the resistance to powdery mildew in all environments. However, GM plants reacted sensitive to fungicide spraying in the glasshouse. Without fungicide treatment, in the glasshouse GM lines had increased vegetative biomass and seed number and a twofold yield compared with control lines. In the field these results were reversed. Fertilization generally increased GM/control differences in the glasshouse but not in the field. Two of four GM lines showed up to 56% yield reduction and a 40-fold increase of infection with ergot disease Claviceps purpurea compared with their control lines in the field experiment; one GM line was very similar to its control.

Conclusions: Our results demonstrate that, depending on the insertion event, a particular transgene can have large effects on the entire phenotype of a plant and that these effects can sometimes be reversed when plants are moved from the glasshouse to the field. However, it remains unclear which mechanisms underlie these effects and how they may affect concepts in molecular plant breeding and plant evolutionary ecology.

Show MeSH
Related in: MedlinePlus