Limited fitness advantages of crop-weed hybrid progeny containing insect-resistant transgenes (Bt/CpTI) in transgenic rice field

Abstract

Background: The spread of insect-resistance transgenes from genetically engineered (GE) rice to its coexisting weedy rice (O. sativa f. spontanea) populations via gene flow creates a major concern for commercial GE rice cultivation. Transgene flow to weedy rice seems unavoidable. Therefore, characterization of potential fitness effect brought by the transgenes is essential to assess environmental consequences caused by crop-weed transgene flow.

Methodology/principal findings: Field performance of fitness-related traits was assessed in advanced hybrid progeny of F(4) generation derived from a cross between an insect-resistant transgenic (Bt/CpTI) rice line and a weedy strain. The performance of transgene-positive hybrid progeny was compared with the transgene-negative progeny and weedy parent in pure and mixed planting of transgenic and nontransgenic plants under environmental conditions with natural vs. low insect pressure. Results showed that under natural insect pressure the insect-resistant transgenes could effectively suppress target insects and bring significantly increased fitness to transgenic plants in pure planting, compared with nontransgenic plants (including weedy parent). In contrast, no significant differences in fitness were detected under low insect pressure. However, such increase in fitness was not detected in the mixed planting of transgenic and nontransgenic plants due to significantly reduced insect pressure.

Conclusions/significance: Insect-resistance transgenes may have limited fitness advantages to hybrid progeny resulted from crop-weed transgene flow owning to the significantly reduced ambient target insect pressure when an insect-resistant GE crop is grown. Given that the extensive cultivation of an insect-resistant GE crop will ultimately reduce the target insect pressure, the rapid spread of insect-resistance transgenes in weedy populations in commercial GE crop fields may be not likely to happen.

Figure 1. Insect index (%) calculated based on the ratio of blasted tillers and folded leaves on weedy parent (above) and transgene-negative hybrid progeny (below) in different cultivation modes (pure vs. mixed) under natural or low insect pressure.

The comparison was made among pure and mixed planting under natural insect and low insect pressure. Different letters above the columns indicate significant differences according to Duncan’s multiple range tests after Bonferroni correction. “Pure” indicates pure planting, “Mixed” indicates mixed planting. Bars represent standard error. Levels of significance: P<0.05.

Figure 2. The average number of filled seeds per plant produced by weedy rice parent (W), transgene-positive (TP), and transgene-negative (TN) hybrid progeny under natural vs. low insect pressure in pure cultivation.

The comparison was made among weedy rice parent, transgene-positive, and transgene-negative hybrid progeny. Different letters above the columns indicate significant differences according to Duncan’s multiple range tests after Bonferroni correction. Bars represent standard error. Levels of significance: P<0.05.

Figure 3. The average number of filled seeds per plant produced by weedy rice parent, transgene-positive (W), and transgene-negative (TP) hybrid progeny under natural vs.

low insect pressure in mixed cultivation. The comparison was made between transgene-positive and transgene-negative, transgene-positive and weedy rice parent, or transgene-negative and weedy rice parent, based on the paired t-tests. Bars represent standard error. Levels of significance: P<0.05.