Host-induced gene silencing of brown planthopper glutathione S-transferase gene enhances rice resistance to sap-sucking

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ORIGINAL PAPER

Host‑induced gene silencing of brown planthopper glutathione S‑transferase gene enhances rice resistance to sap‑sucking insect pests Jun Yang1 · Xiao‑Qin Sun1 · Keyan Zhu‑Salzman3 · Qing‑Ming Qin4,5 · Hui‑Qiang Feng4 · Xiang‑Dong Kong1 · Xu‑Guo Zhou6 · Qing‑Nian Cai1,2  Received: 22 October 2019 / Revised: 28 October 2020 / Accepted: 3 November 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Host-induced gene silencing (HIGS) of insect growth and development is a promising measure for pest control in practice; the feasibility of disarming insect detoxification of toxic phytochemicals via HIGS of insect detoxification enzymes remains largely unexplored. In this study, a HIGS system was applied to interfere with glutathione S-transferase (GST) gene expression in brown planthopper (BPH, Nilaparvata lugens), a key insect pest in rice of Asia, and regulate rice resistance to the insect. The recombination vector in transgenic plants was expressed in almost all organs, especially in vascular bundle tissues, mesophyll, epidermal cells and leaf sheath sap, but not in xylem. Target BPH NlGST1-1 was successfully integrated into rice genome, the resultant transgenic rice lines harbored a single-copy of BPH NlGST1-1 dsRNA, and expression of NlGST1-1 dsRNA was detected in leaves and leaf sheaths of transgenic lines. However, the content of phytochemical gramine, an inherent alkaloid in gramineous plants, did not change in these transgenic plants. BPH nymphs reared on the transgenic rice expressing NlGST1-1 dsRNA displayed significant reductions in NlGST1-1 transcript expression and GST activity. The transgenic plants significantly retarded relative growth rate of the nymphs and the insect female fecundity, the plants also showed enhanced resistance when attacked by BPH. Our study demonstrated the feasibility of reinforcing gramine-mediated plant defense via HIGS of GSTs in herbivorous insects. HIGS-mediated suppression of the herbivore adaptive mechanism has significant implications for efficiently managing BPH and other pests in rice. Keywords  Host-induced gene silencing (HIGS) · Glutathione S-transferase genes · RNAi · Plant defense · Molecular breeding · Oryza sativa (rice) · Phytochemicals · Nilaparvata lugens Abbreviations ANOVA The analysis of variance ATMT  Agrobacterium tumefaciens-mediated transformation BPH Brown planthopper Bt  Bacillus thuringiensis DIG Digoxigenin Communicated by G. Smagghe. Jun Yang and Xiao-Qin Sun have contributed equally to this work. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1034​0-020-01296​-6) contains supplementary material, which is available to authorized users. * Qing‑Nian Cai [email protected] Extended author information available on the last page of the article

dsRNA Double-stranded RNA EDTA Ethylenediaminetetraacetic acid GFP Green fluorescent protein GST Glutathione S-transferase GE Genetically engineered GUS  β-Glucuronidase HIGS Host-induced gene silencing LSD The least s