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Effect of Transgenic Bt Rice on the Survival of Three Nontarget Stored Product Insect Pests

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Effect of Transgenic Bt Rice on the Survival of Three Nontarget Stored Product Insect Pests TRANSGENIC PLANTS AND INSECTS Effect of Transgenic Bt Rice on the Survival of Three Nontarget Stored Product Insect Pests 1,2 1 1 3 JORDI RIUDAVETS, ROSA GABARRA, M. JOSE´ PONS, AND JOAQUIMA MESSEGUER Environ. Entomol. 35(5): 1432Ð1438 (2006) ABSTRACT The effects of Bacillus thuringiensis (Bt) transgenic Ariete and Senia rice lines devel- Downloaded from https://academic.oup.com/ee/article/35/5/1432/341097 by guest on 23 September 2021 oped for the control of Chilo suppressalis Walker were evaluated on three nontarget stored product insect pests: the lepidopteran Plodia interpunctella (Hu¨ bner), the coleopteran Sitophilus oryzae L., and the psocid Liposcelis bostrichophila (Badonnel). Two different cry genes (cry1B and cry1Aa) under the control of a constitutive plant promoter (ubi) and a wound inducible promoter (mpi) were tested. Plodia interpunctella was unable to survive in rice semolina obtained from the two Ariete and Senia lines, which contained the ubi:cry1B gene. A reduction in S. oryzae adult progeny was observed in cultivar Senia rice containing the ubi:cry1B gene but not in cultivar Ariete rice. Moreover, a sublethal effect on S. oryzae adult progeny weight was observed in both of the rice cultivar treatments that constitutively expressed this gene. The number of L. bostrichophila emerging from Ariete rice containing the ubi:cry1B gene also was reduced. Both a reduction in the number of emerged adults and a delay in the development of P. interpunctella were observed for Ariete rice semolina containing the mpi:cry1B gene. However, no lethal or sublethal effects were observed for P. interpunctella reared on a transformed Senia rice line expressing the ubi:cry1Aa gene, suggesting possible tolerance to the toxin present in the rice grains. Although no increase in mortality was observed with S. oryzae fed ubi:cry1Aa rice, there was a sublethal effect on adult progeny weight. KEY WORDS Bacillus thuringiensis, transgenic rice, Plodia interpunctella, Sitophilus oryzae, Lipo- scelis bostrychophila Bacillus thuringiensis (Bt) produces a variety of insec- pollinators, decomposers, and natural enemies (Losey ticide crystal proteins on sporulation that are encoded et al. 2004, OÕCallaghan et al. 2005). by a number of cry genes. These proteins are highly With regard to rice crops, transgenic Bt lines have toxic to lepidopteran, dipteran, and coleopteran in- been developed as alternative tools for preventing sects, interacting with the larval midgut epithelium losses caused by the incidence of the striped stem and causing a disruption in membrane integrity, ulti- borer, Chilo suppressalis Walker (Lepidoptera: Pyrali- mately leading to insect death (Gill et al. 1992). Bt cry dae) (Dirie et al. 2000, Breitler et al. 2004). Transgenic genes have been successfully engineered into a num- rice lines have been obtained with high expression of ber of crops. Several insect-resistant transgenic plant genes encoding insecticidal cry proteins through the cultivars of maize, cotton, and potato have been use of constitutive promoters. An alternative to the widely commercialized (James 2004). In these crops, continuous expression of insecticidal proteins through Bt toxins produced by plant tissues reduce attacks all of a plantÕs tissues is a conditional expression di- from target pest species such as the European corn rected by a wound inducible promoter, which could borer, Ostrinia nubilalis (Hu¨ bner) (Lepidoptera: direct toxin production both spatially and temporally Pyralidae), the noctuids Heliothis spp. and Helicoverpa (Breitler et al. 2004). spp. (Lepidoptera: Noctuidae), and the Colorado po- Several stored product pest species such as Plodia tato beetle, Leptinotarsa decemlineata (Say) (Co- interpunctella (Hu¨ bner) (Lepidoptera: Pyralidae) leoptera: Chrysomelidae). A beneÞt of Bt crops is the (Indianmeal moth), Sitophilus oryzae L. (Coleoptera: reduced reliance on broad-spectrum insecticide treat- Curculionidae) (Rice weevil), and Liposcelis ments (Shelton et al. 2002). Bt toxins also may have a bostrychophila (Badonnel) (Psocoptera: Liposcelidi- negative effect on other nontarget insect herbivores, dae) (Booklouse psocid) are common in rice and cause high economic losses during the postharvest period (Cogburn and Vick 1981, Riudavets et al. 2002). 1 Departament de Proteccio´ Vegetal, IRTA, Centre de Cabrils, Ctra. All three species are polyphagous, and P. interpunctella Cabrils s/n, 08348 Cabrils (Barcelona), Spain. and L. bostrychophila are pests of cereals and semi- 2 Corresponding author, e-mail: [email protected]. processed products, whereas S. oryzae is a pest of 3 Consorci laboratori CSICÐIRTA de Gene`tica Molecular Vegetal, Departament de Gene`tica Vegetal, IRTA, Centre de Cabrils, Ctra. whole grain cereals (Gorham 1991). Brown rice, with Cabrils s/n, 08348 Cabrils (Barcelona), Spain. its external grain layers and embryo, is more favorable 0046-225X/06/1432Ð1438$04.00/0 ᭧ 2006 Entomological Society of America October 2006 RIUDAVETS ET AL.: EFFECT OF TRANSGENIC Bt RICE ON STORED PRODUCT PESTS 1433 for S. oryzae preimaginal development, survival, and Table 1. List of Ariete and Senia Bt-transformed lines tested reproduction than is white polished rice (Lucas and against P. interpunctella and L. bostrichophila on semolina and Riudavets 2000). S. oryzae on white rice In the United States, Bt has been commercially Line Treatment Gene Promoter applied for stored-product insect control since the Ariete AControl Non-Bt 1970s (Golob et al. 2002), while high levels of insec- A3.4 cry1B ubi ticidal activity have been observed in laboratory stud- A3.4E cry1B ubi ies involving the use of different cry protoxins and A9.1 cry1B mpi toxins against P. interpunctella (Herrero et al. 2001). A9.1E cry1B mpi Senia SControl Non-Bt Nevertheless, the resistance of some P. interpunctella S98.9 cry1B ubi strains to sprayable Bt proteins has been shown (Mc- S05 cry1Aa ubi Gaughey 1985, McGaughey and Johnson 1994). Cry proteins present in transgenic maize kernels from hy- Brown rice semolina treatments (A3.4E and A9.1E) containing the Downloaded from https://academic.oup.com/ee/article/35/5/1432/341097 by guest on 23 September 2021 brids with the CaMV/35s promoter expressing cry1Ab embryo and endosperm only were tested against P. interpunctella. and cry9C genes reduced the survival and reproduc- tion of P. interpunctella, and developmental time also ler et al. 2000) or through Agrobacterium, following was delayed (Giles et al. 2000, Hanley et al. 2004). the procedures detailed in Sallaud et al. (2003) and Similarly, Sedlacek et al. (2001) found that emergence Pons et al. (2000) for Ariete and Senia, respectively. and fecundity of P. interpunctella were lower and de- Synthetic cry1B and cry1Aa genes are Bt ␦-endo- velopmental times longer for individuals reared on Bt toxin genes. The synthetic cry1B gene corresponds to transgenic maize hybrids expressing cry1Ab genes. In the 1Ð1,944 region of the cry1Ba1 gene originally iso- contrast, no differences in P. interpunctella develop- lated from Bt strain HD2 by Brizzard and Whiteley mental time and survival were observed between (1988) and encodes the active toxin plus 29 amino transgenic maize hybrids with the phosphoenolpyru- acids at the N-terminal end. The synthetic cry1Aa vate carboxylase promoter expressing the same gene (M. Royer, unpublished data) corresponds to the cry1Ab genes or transgenic hybrids expressing cry1Ac 1Ð1,854 region of the cry1Aa gene isolated from Bt versus their isolines (Giles et al. 2000). strain FU2Ð7 by Udayasuriyan et al. (1994). In an artiÞcial maize seed bioassay, Bt cry1A and Homozygous Ariete line A3.4 and Senia S05 and cry1B toxins had no effect on S. oryzae mortality (Pit- S98.9 integrated the cry gene under the control of the tendrigh et al. 1997). However, transgenic rice ex- maize ubiquitin (ubi) promoters Þrst intron and Þrst pressing the trypsin inhibitor Itr1 gene encoding the exon (Christensen and Quail 1996), whereas Ariete BTI-CMe toxin reduced the survival rate of S. oryzae line A9.1 integrated the cry gene under the control of (Alfonso-Rubõ´ et al. 2003). The effects of Bt toxins the wound inducible (mpi) promoter (Breitler et al. produced by transgenic rice on stored-product rice 2001). Details of the materials used from each one of pests have not been reported. these lines are provided in Table 1. Transgenic commercial rice lines will be approved Insect Cultures. All colonies were originally estab- in the near future in several countries. One of the Þrst lished from individuals collected in 1997 from storage candidates likely will be rice lines resistant to attack by areas located in the northeast of Spain. P. interpunc- stem borers. The objective of this study was to eval- tella was reared on a diet based on wheat bran and uate the extent to which harvested grain from trans- glycerin. S. oryzae was reared on brown rice (cultivar genic rice expressing the cry1B and cry1Aa genes, Tebre). L. bostrichophila was reared on a diet of wheat especially designed for controlling C. suppressalis, ßour and yeast. Rearing and experiments were con- could affect nontarget pests present in stored rice such ducted in a climatic chamber at 25 Ϯ 1ЊC, 75 Ϯ 15% as the lepidopteran P. interpunctella, the coleopteran RH, and at a photoperiod of 16:8 (L:D). S. oryzae, and the psocid L. bostrichophila. We eval- Testing Method. The experimental arenas were uated the effect of transgenic rice lines harboring the ventilated glass jars (110 ml) containing 30 g of rice cry1B gene with constitutive and wound inducible kernels or 20 g of rice semolina. Brown rice (with promoters and the cry1A gene with a constitutive embryo and external layers) was polished to obtain promoter on adult weight and survival rates. Addi- white rice (only endosperm) using a laboratory pol- tionally, the effects of the cry1B gene under the con- isher (Univeral Brevetto 65378, vertical type; A. trol of both promoters in brown and white rice on GuidÕetti, Italy), and white rice was milled to obtain P. interpunctella life parameters were studied.
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