Transcriptomic response of wolf spider, Pardosa pseudoannulata, to transgenic rice expressing Bacillus thuringiensis Cry1Ab protein

Genetically modified (GM) technology has reshaped the agricultural industry since its insertion in the late1990s [1]. From 1996 to 2012, the global acreage of GM crops has increased dramatically from 1.7 to 160.4 million hectares [2]. The ecological benefits from rapid development and adoption of GM crops include a significant reduction in both insecticide and herbicide usage and greenhouse gas emissions [3]. A meta-analysis in 2014 showed a 37% reduction in synthetic pesticide use, 22% increase in crop yield, and 68% increase in farmer profits [4].

Besides yield and profit gains and environmental benefits, non-monetary incentives include time savings, ease of use, and more flexibility in planning [5]. With limited arable land in China, GM technology provides a potential solution to improve agricultural productivity and sustainability. Currently, transgenic Bacillum thuringiensis (Bt) cotton, resistant to Lepidoptera pests, is the most successful commercial GM crop in China [6]. In 2012, acreage of Bt cotton has reached 3.59 million hectares, representing 80% of total cotton area in China. Bt cotton increased yield by 10%, reduced insecticide use by 60% and generated additional US $220 profit per hectare on average [7]. Even with the success of Bt cotton, consumers still have doubts about GM crops, partially due the lack of knowledge regarding the ecological risks [5, 8, 9]. Bt rice is facing the same challenges for the public acceptance.

The community structure of a rice field is primarily composed of soil organisms, rice, insect herbivores, predators, and parasitoids. While insect herbivores are exposed to Bt toxins by direct feeding, other community members can access Bt toxins through trophic interactions. Previous risk assessment studies showed no harmful effect of Bt rice on diversity, dominant species and abundance of non-target arthropods among the arthropod community in the field [10, 11]. Laboratory studies, on one hand, did not detect adverse impacts of Bt rice on non-target arthropods. For example, the developmental time, fecundity and survival rate of herbivorous insects Nilaparvata lugens and Sogatella furcitera were unaffected when exposed to Cry1C, Cry2A, and Cry1AC proteins, respectively [12, 13]. No significant effects were found on life history traits for predators as well, including Chrysoperia sinica, Propylea japonica, Cyrtorhinus lividipennis, and Ummeliata insecticeps [14–17]. On the other hand, some reports show non-target organisms may be susceptible to Bt toxins. A significant longer developmental time of Pirata subpiraticus was recorded when it prayed on Bt rice fed Cnaphalocrocis medinalis [18]. Significantly lower catalase activity was found in Fosomia candida fed on Bt rice in comparison to those fed on non-Bt rice [19]. Due to the varing degradation of Bt toxin protein in soils with different physicochemical properties [20, 21], researchers did not find consistent differences in soil microorganism communities between Bt and non Bt rice fields [22]. For parasitoids, effects of Bt rice is also inconsistent, which depends on the host species, target or non-target insects [22]. As a whole, risk assessment of Bt rice has been focusing on the organismal level impacts, suborganismal impacts are largely unknown. The advent of genomics era, however, allows us to evaluate ecological risks of transgenic Bt rice on non-target organism at the transcription and translational level.

The wolf spider Pardosa pseudoannulata is one of the dominant predators in South China, playing a crucial role in maintaining the stability of the rice agroecosystem [23]. In this study, we carried out a comparative transcriptome analysis of the 5th instar spiders fed on N. lugens maintained on Bt- and non-Bt rice, respectively. Developmental time from the 2nd to 8th instars was recorded to reveal the potential impacts of Bt rice on P. pseudoannulata and to correlate the biological impacts with differentially expressed genes.