Knockdown of MAPK p38-linked genes increases the susceptibility of chilo suppressalis larvae to various transgenic Bt rice strains

Authors: NIU, XURONG - Huazhong Agricultural University; JIANG, JIALIANG - Huazhong Agricultural University; SUN, YAJIE - Huazhong Agricultural University; Hull, Joe; MA, WEIHUA - Huazhong Agricultural University; HUA, HONGXIA - Huazhong Agricultural University; LIN, YONGJUN - Huazhong Agricultural University

Submitted to: International Journal of Biological Macromolecules
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/10/2024
Publication Date: 3/29/2024
Citation: Niu, X., Jiang, J., Sun, Y., Hull, J.J., Ma, W., Hua, H., Lin, Y. 2024. Knockdown of MAPK p38-linked genes increases the susceptibility of chilo suppressalis larvae to various transgenic Bt rice strains. International Journal of Biological Macromolecules. 266. Article 130815. https://doi.org/10.1016/j.ijbiomac.2024.130815.
DOI: https://doi.org/10.1016/j.ijbiomac.2024.130815

Interpretive Summary: During sporulation, the gram-positive bacterium Bacillus thuringiensis (Bt) produces crystalline (Cry) toxin proteins that perforate the insect midgut epithelium following ingestion. These effects can have significant fitness costs on insect development and are frequently lethal to the insect. Given this activity, Bt proteins have been commercially adapted for agricultural pest control and are considered among the most economically successful entomopathogens. Resistance to Bt proteins, however, has been reported in a number of insect pests. A less explored area of Bt resistance research focuses on identifying the gene networks and pathways activated in response to Cry toxin binding. One path known to play a role in the development of resistance is the mitogen-activated protein kinase (MAPK) p38 signaling pathway. High-throughput RNA screening of C. suppressalis larval midguts initially identified nine MAPK genes potentially critical to resistance. RNAi-mediated targeting of these genes confirmed the importance of four for increased tolerance to transgenic rice lines expressing a specific type of Bt Cry toxin. Two of these genes also provided protection to other types of Bt toxins. These results further expand our understanding of the mechanisms underlying Bt toxin resistance and underscore the specific role the MAPK signaling pathway plays. These insights can facilitate the development of new control strategies that could potentially be coupled with current Bt technologies.

Technical Abstract: Bacillus thuringiensis (Bt) toxins have provided exceptional control of agricultural insect pests, however, over reliance on the proteins has contributed to the development of field resistance. Developing new sustainable insect pest control methods that target the mechanisms underlying Bt resistance can potentially support the Bt control paradigm while also providing insights into basic insect physiology. The MAPK p38 pathway is strongly associated with Bt resistance in Chilo suppressalis, a major pest of rice. To gain insights into how this pathway impacts resistance, high-throughput screening of C. suppressalis larval midguts initially identified nine novel target genes. Increased larval sensitivity to the Cry1Ca transgenic rice strain T1C-19 was observed following RNA interference-mediated knockdown of four of the genes, Cscnc, Csgcp, Cszfp26, and CsZMYM1-1. Similar enhanced sensitivity to the TT51 and T2A-1 transgenic rice lines occurred when Cszfp26 and CsZMYM1-1 were knocked down. All four target genes are downstream of the MAPK p38 pathway but do not participate in negative feedback loop of the pathway. These results implicate Cscnc, Csgcp, Cszfp and CsZMYM1-1 in the C. suppressalis Cry1Ca transgenic rice resistance mechanism regulated by MAPK p38. These findings further enhance our understanding of the MAPK p38-dependent molecular mechanisms underlying Bt resistance in C. suppressalis and open new avenues of resistance management for development.