|
|
|
|
|
Azole selenourea disrupted the midgut and caused malformed development of Plutella xylostella
|
| GUO Xue-ying1, 2*, HUANG Zi-hao1*, XIONG Lan-tu1, DONG Li1, HUANG Yue-kun1, WEI Lin-hao1, TANG Ri-yuan1, 2#, WANG Zhi-lin1, XU Han-hong2 |
1 Department of Applied Chemistry, College of Materials and Energy, South China Agricultural University, Guangzhou 510642, P.R.China
2 Key Laboratory of Natural Pesticide & Chemical Biology of Ministry of Education, South China Agricultural University, Guangzhou 510642, P.R.China
|
|
|
|
|
摘要
以小菜蛾（Plutella xylostella）的消化系统为靶标的化学杀虫剂至今尚未报道。创制一款具有新型作用机制的用于小菜蛾防控的杀虫剂仍然是一个巨大的挑战。为了探索以小菜蛾中肠为靶标的新型杀虫剂，设计并合成了一系列以二氟甲基和硒修饰的新型氟唑硒脲（FASU）化合物。室内杀虫测试结果表明，化合物B4对小菜蛾的杀虫活性最高，3龄和2龄小菜蛾幼虫72 h的半致死浓度LC50值分别为32.33，4.63 μg mL-1。化合物B4导致小菜蛾中肠严重受损，诱发产生众多的红色斑点。超微结构显示小菜蛾中肠围食膜降解，上皮组织肿胀，微绒毛断裂及细胞消融解体。化合物B4亚致死浓度（LC10，LC25 和LC50）处理后，幼虫发育缓慢，幼虫历期显著延长，蛹重，化蛹率，羽化率均显著下降。此外，化合物B4可诱发畸形蛹，导致成虫不能破茧或翅膀畸形不能飞翔。以上结果表明，氟唑硒脲化合物对对小菜蛾具有较好的杀虫活性，在亚致死浓度下，可以降低小菜蛾的种群数量。值得注意的是，氟唑硒脲是首次报道的可诱导小菜蛾中肠损伤的合成杀虫剂先导化合物，其作用机理与现有商品化杀虫剂均不同。
Abstract
Chemical insecticides targeting the digestive system of diamondback moth (DBM), Plutella xylostella, have not been developed. The discovery of an insecticide with novel mode of action is a challenge for the control of DBM. In this study, a class of selenium- and difluoromethyl-modified azoles (fluoroazole selenoureas, FASU) were designed and synthesized for the control of DBM. Of these azoles, compound B4 showed the highest insecticidal activity against DBM. The LC50 of third- and second-instar larvae reached 32.3 and 4.6 μg mL–1, respectively. The midgut tissue of larvae was severely disrupted, and the larval intestinal tissue was dotted with unique red spots after treatment with compound B4. Compound B4 led to disintegration of the peritrophic matrix, swelling of the midgut epithelium, fracture of the microvilli, and extensive leakage of cellular debris in the midgut lumen. Surviving larvae grew very slowly, and the larval duration was significantly prolonged after exposure to compound B4 at sublethal doses (LC10, LC25 and LC50). Furthermore, the pupation rate, emergence rate and pupae weight were significantly decreased. Compound B4 also induced abnormal pupae, causing adults to be trapped in the cocoon or failure to fly due to twisted wings. These results demonstrated that FASU could reduce the population of DBM in sublethal doses. FASU is the first synthetic insecticidal lead compound that has been shown to disrupt the midgut tissue of the larvae of DBM, and its mode of action totally differs from that of commercial chemical insecticides.
|
|
Received: 29 March 2022
Accepted: 05 May 2022
|
| Fund:
This work was financially supported by funding from the Guangdong Basic and Applied Basic Research Foundation, China (2019B151502052), and the Program of Science and Technology of Guangzhou, China (202002030295).
|
| About author: Received 29 March, 2022 Accepted 5 May, 2022
GUO Xue-ying, E-mail: 13794375314@163.com; HUANG Zi-hao, E-mail: 2360482723@qq.com; #Correspondence TANG Ri-yuan, Mobile: +86-13825112030, E-mail: rytang@scau.edu.cn
* These authors contributed equally to this study. |
Cite this article:
GUO Xue-ying, HUANG Zi-hao, XIONG Lan-tu, DONG Li, HUANG Yue-kun, WEI Lin-hao, TANG Ri-yuan, WANG Zhi-lin, XU Han-hong.
2023.
Azole selenourea disrupted the midgut and caused malformed development of Plutella xylostella
. Journal of Integrative Agriculture, 22(4): 1104-1116.
|
Barbeta B L, Marshall A T, Gillon A D, Craiks D J, Anderson M A. 2008. Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proceedings of the National Academy of Sciences of the United States of America, 105, 1221–1225.
Broderick N A, Raffa K F, Handelsman J. 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proceedings of the National Academy of Sciences of the United States of America, 103, 15196–15199.
Byrne M J, Iadanza M G, Perez M A, Maskell D P, George R M, Hesketh E L, Beales P A, Zack M D, Berry C, Thompson R F. 2021. Cryo-EM structures of an insecticidal Bt toxin reveal its mechanism of action on the membrane. Nature Communications, 12, 2791.
Caccia S, Di Lelio I, La Storia A, Marinelli A, Varricchio P, Franzetti E, Banyuls N, Tettamanti G, Casartelli M, Giordana B, Ferre J, Gigliotti S, Ercolini D, Pennacchio F. 2016. Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proceedings of the National Academy of Sciences of the United States of America, 113, 9486–9491.
Casida J E. 2009. Pest toxicology: The primary mechanisms of pesticide action. Chemical Research in Toxicology, 22, 609–619.
Chen C, Chen H Y, Huang S J, Jiang T S, Wang C H, Tao Z, He C, Tang Q F, Li P J. 2021. Volatile DMNT directly protects plants against Plutella xylostella by disrupting the peritrophic matrix barrier in insect midgut. eLife, 10, e63938.
Chen W B, Liu C X, Lu G Q, Chen H M, She Z C, Wu K M. 2018. Effects of Vip3AcAa+Cry1Ac cotton on midgut tissue in Helicoverpa armigera (Lepidoptera: Noctuidae). Journal of Insect Science, 18, 1–6.
Cheung K P, Roe R M, Hammock B D, Judson C L, Montague M A. 1985. The apparent in vivo neuromuscular effects of the δ-endotoxin of Bacillus thuringiensis var. israelensis in mice and insects of four orders. Pesticide Biochemistry and Physiology, 23, 85–94.
Daquila B V, Scudeler E L, Dossi F C A, Moreira D R, Pamphile J A, Conte H. 2019. Action of Bacillus thuringiensis (Bacillales: Bacillaceae) in the midgut of the sugarcane borer Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae). Ecotoxicology and Environmental Safety, 184, 109642.
Deng J C, Gao Y C, Zhu Z, Xu L, Li Z D, Tang R Y. 2019. Sulfite-promoted synthesis of N‑difluoromethylthioureas via the reaction of azoles with bromodifluoroacetate and elemental sulfur. Organic Letters, 21, 545–548.
Dhillon G S, Brar S K, Kau S, Verma M. 2012. Green approach for nanoparticle biosynthesis by fungi: Current trends and applications. Critical Reviews in Biotechnology, 32, 49–73.
Ellis D R, Salt D E. 2003. Plants, selenium and human health. Current Opinion in Plant Biology, 6, 273–279.
Espallholz J E, Hoffman D J. 2002. Selenium toxicity: Cause and effects in aquatic birds. Aquatic Toxicology, 57, 27–37.
Freeman J L, Lindblom S D, Quinn C F, Fakra S, Marcus M A, Pilon-Smits E A H. 2007. Selenium accumulation protects plants from herbivory by Orthoptera via toxicity and deterrence. New Phytologist, 175, 490–500.
Freeman J L, Quinn C F, Marcus M A, Fakra S, Pilon-Smits E A H. 2006. Selenium-tolerant diamondback moth disarms hyperaccumulator plant defense. Current Biology, 16, 2181–2192.
Furlong M J, Wright D J, Dosdall L M. 2013. Diamondback moth ecology and management: Problems, progress, and prospects. Annual Review of Entomology, 58, 517–541.
Han G J, Li C M, Liu Q, Xu J. 2015. Synergistic effect of combining Plutella xylostella granulovirus and Bacillus thuringiensis at sublethal dosages on controlling of diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology, 108, 2184–2191.
Hanson B R, Lindblom S D, Miriam L L, Pilon-Smits E A H. 2004. Selenium protects plants from phloem-feeding aphids due to both deterrence and toxicity. New Phytologist, 162, 655–662.
Hogan G R, Razniak H G. 1991. Selenium-induced mortality and tissue distribution studies in Tenebrio molitor (Coleoptera: Tenebrionidae). Environmental Entomology, 20, 790–794.
Jiang X Y, Yang S, Yan Y, Lin F, Zhang L, Zhao W J, Zhao C, Xu H H. 2020. Design, synthesis, and insecticidal activity of 5,5-disubstituted 4,5-dihydropyrazolo(1,5-a)quinazolines as novel antagonists of GABA receptors. Journal of Agricultural and Food Chemistry, 68, 15005–15014.
Kessi J, Ramuz M, Wehrli E, Spycher M, Bachofen R. 1999. Reduction of selenite and detoxification of elemental selenium by the phototrophic bacterium Rhodospirillum rubrum. Applied and Environmental Microbiology, 65, 4734–4740.
Kora A J, Rastogi L. 2016. Biomimetic synthesis of selenium nanoparticles by Pseudomonas aeruginosa ATCC 27853: An approach for conversion of selenite. Journal of Environmental Management, 181, 231–236.
Li Z Y, Feng X, Liu S S, You M S, Furlong M J. 2016. Biology, ecology, and management of the diamondback moth in China. Annual Review of Entomology, 61, 277–296.
Ma C S, Zhang W, Peng Y, Zhao F, Rudolf V H W. 2021. Climate warming promotes pesticide resistance through expanding overwintering range of a global pest. Nature Communications, 12, 5351.
Mason C J, Ray S, Shikano I, Peiffer M, Jones A G, Luthe D S, Hoover K, Felton G W. 2019. Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proceedings of the National Academy of Sciences of the United States of America, 116, 15991–15996.
Mechora S. 2019. Selenium as a protective agent against pests: A review. Plants (Basel), 8, 262.
Mithofer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. Annual Review of Plant Biology, 63, 431–450.
Mohan S, Ma P W K, Pechan T, Bassford E R, Williams W P, Luthe D S. 2006. Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. Journal of Insect Physiology, 52, 21–28.
Napoleao T H, Albuquerque L P, Santos N D L, Nova I C V, Lima T A, Paiva P M G, Pontual E V. 2019. Insect midgut structures and molecules as targets of plant-derived protease inhibitors and lectins. Pest Management Science, 75, 1212–1222.
Pechan T, Cohen A, Williams W P, Luthe D S. 2002. Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proceedings of the National Academy of Sciences of the United States of America, 99, 13319–13323.
Percy J, Fast P G. 1983. Bacillus thuringiensis crystal toxin: Ultrastructural studies of iits effect on silkworm midgut cells. Journal of Invertebrate Pathology, 41, 86–98.
Qi Z J, Xue X P, Wu W J, Zhang J W, Yang R Y. 2006. Preparation of monoclonal antibody against celangulin V and immunolocalization of receptor in the oriental armyworm, Mythimna separata walker (Lepidoptera: Noctuidae). Journal of Agricultural and Food Chemistry, 54, 7600–7605.
Quinn C F, Galeas M L, Freeman J L, Pilon-Smits E A H. 2007. Selenium: Deterrence, toxicity, and adaptation. Integrated Environmental Assessment and Management, 3, 460–462.
Ryan C A. 1990. Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 28, 425–449.
Schiavon M, Pilon-Smits E A H. 2017. The fascinating facets of plant selenium accumulation - biochemistry, physiology, evolution and ecology. New Phytologist, 213, 1582–1596.
Takahashi K, Suzuki N, Ogra Y. 2020. Effect of gut microflora on nutritional availability of selenium. Food Chemistry, 319, 126537.
Vadlamudi R K, Weber E, Ji I, Ji T H, Bulla L A. 1995. Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. Journal of Biological Chemistry, 270, 5490–5494.
Wu L, Enberg A, Biggar J A. 1994. Effects of elevated selenium concenteation on selenium accumulation and nitrogen fixation symbiotic activity of Melilotus indica L. Ecotoxicology and Environmental Safety, 27, 50–63.
Xu Z F, Qi C C, Zhang M Y, Zhu J Y, Hu J, Feng K Y, Sun J Y, Wei P, Shen G M, Zhang P, He L. 2021. Selenium mediated host plant-mite conflict: Defense and adaptation. Pest Management Science, 77, 2981–2989.
Zhang L, Peng X M, Damu G L V, Geng R X, Zhou C H. 2014. Comprehensive review in current developments of imidazole-based medicinal chemistry. Medicinal Research Reviews, 34, 340–437.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
