首页 » 文章 » 文章详细信息
eLife Volume 9 ,2020-12-10
A gustatory receptor tuned to the steroid plant hormone brassinolide in Plutella xylostella (Lepidoptera: Plutellidae)
Ecology
Ke Yang 1 , 2 Xin-Lin Gong 1 , 2 Guo-Cheng Li 1 , 2 Ling-Qiao Huang 1 Chao Ning 1 , 2 Chen-Zhu Wang 1 , 2
Show affiliations
DOI:10.7554/eLife.64114
Received 2020-10-17, accepted for publication 2020-12-10, Published 2020-12-10
PDF
摘要

Feeding and oviposition deterrents help phytophagous insects to identify host plants. The taste organs of phytophagous insects contain bitter gustatory receptors (GRs). To explore their function, the GRs in Plutella xylostella were analyzed. Through RNA sequencing and qPCR, we detected abundant PxylGr34 transcripts in the larval head and adult antennae. Functional analyses using the Xenopus oocyte expression system and 24 diverse phytochemicals showed that PxylGr34 is tuned to the canonical plant hormones brassinolide (BL) and 24-epibrassinolide (EBL). Electrophysiological analyses revealed that the medial sensilla styloconica of 4th instar larvae are responsive to BL and EBL. Dual-choice bioassays demonstrated that BL inhibits larval feeding and female oviposition. Knock-down of PxylGr34 by RNAi attenuates the taste responses to BL, and abolishes BL-induced feeding inhibition. These results increase our understanding of how herbivorous insects detect compounds that deter feeding and oviposition, and may be useful for designing plant hormone-based pest management strategies.

关键词

Other;oviposition bioassays;feeding;brassinolide;RNAi;functional analysis;gustatory receptor;Plutella xylostella

授权许可

© 2020, Yang et al
http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

通讯作者
推荐引用方式

Ke Yang,Xin-Lin Gong,Guo-Cheng Li,Ling-Qiao Huang,Chao Ning,Chen-Zhu Wang. A gustatory receptor tuned to the steroid plant hormone brassinolide in Plutella xylostella (Lepidoptera: Plutellidae). eLife ,Vol.9(2020)

您觉得这篇文章对您有帮助吗?
分享和收藏
0

是否收藏?

参考文献
[1] X Li, MA Schuler, MR Berenbaum. (2002). Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes. Nature.419:712-715. DOI: 10.1007/s11103-008-9435-0.
[2] B Li, CN Dewey. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics.12. DOI: 10.1007/s11103-008-9435-0.
[3] KJ Livak, TD Schmittgen. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta delta C(T)) Method. Methods.25:402-408. DOI: 10.1007/s11103-008-9435-0.
[4] H Guo, T Cheng, Z Chen, L Jiang. et al.(2017). Expression map of a complete set of gustatory receptor genes in chemosensory organs of. Insect Biochemistry and Molecular Biology.82:74-82. DOI: 10.1007/s11103-008-9435-0.
[5] S Rimal, Y Lee. (2019). Molecular sensor of nicotine in taste of. Insect Biochemistry and Molecular Biology.111. DOI: 10.1007/s11103-008-9435-0.
[6] PD Gupta, AJ Thorsteinson. (1960). Food plant relationships of the diamond-back moth ( maculipennis (Curt.)) II. Sensory regulation of oviposition of the adult female. Entomologia Experimentalis et Applicata.3:305-314. DOI: 10.1007/s11103-008-9435-0.
[7] A Stamatakis. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics.30:1312-1313. DOI: 10.1007/s11103-008-9435-0.
[8] HM Robertson, CG Warr, JR Carlson. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in. PNAS.100:14537-14542. DOI: 10.1007/s11103-008-9435-0.
[9] T Lv, XE Zhao, S Zhu, Z Ji. et al.(2014). Development of an efficient HPLC fluorescence detection method for brassinolide by ultrasonic-assisted dispersive liquid–liquid microextraction coupled with derivatization. Chromatographia.77:1653-1660. DOI: 10.1007/s11103-008-9435-0.
[10] BJ Haas, A Papanicolaou, M Yassour, M Grabherr. et al.(2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols.8:1494-1512. DOI: 10.1007/s11103-008-9435-0.
[11] J Rozewicki, S Li, KM Amada, DM Standley. et al.(2019). MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Research.14:W5-W10. DOI: 10.1007/s11103-008-9435-0.
[12] X Teng, Z Zhang, G He, L Yang. et al.(2012). Validation of reference genes for quantitative expression analysis by real-time RT-PCR in four lepidopteran insects. Journal of Insect Science.12:1-17. DOI: 10.1007/s11103-008-9435-0.
[13] MD Grove, GF Spencer, WK Rohwedder, N Mandava. et al.(1979). Brassinolide, a plant growth-promoting steroid isolated from pollen. Nature.281:216-217. DOI: 10.1007/s11103-008-9435-0.
[14] AD Briscoe, A Macias-Muñoz, KM Kozak, JR Walters. et al.(2013). Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLOS Genetics.9. DOI: 10.1007/s11103-008-9435-0.
[15] S Capella-Gutiérrez, JM Silla-Martínez, T Gabaldón. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics.25:1972-1973. DOI: 10.1007/s11103-008-9435-0.
[16] N Thorne, C Chromey, S Bray, H Amrein. et al.(2004). Taste perception and coding in. Current Biology.14:1065-1079. DOI: 10.1007/s11103-008-9435-0.
[17] EA Bernays, RF Chapman. (1994). Host-Plant Selection by Phytophagous Insects. DOI: 10.1007/s11103-008-9435-0.
[18] S Takasaki. (2013). Methods for selecting effective siRNA target sequences using a variety of statistical and analytical techniques. Methods in Molecular Biology.942:17-55. DOI: 10.1007/s11103-008-9435-0.
[19] BN Chaitanya, R Asokan, T Sita, KB Rebijith. et al.(2017). Silencing of JHEH and EcR genes of (Lepidoptera: Plutellidae) through double stranded RNA oral delivery. Journal of Asia-Pacific Entomology.20:637-643. DOI: 10.1007/s11103-008-9435-0.
[20] YT Qiu, JJA van Loon, P Roessingh. (1998). Chemoreception of oviposition inhibiting terpenoids in the diamondback moth. Entomologia Experimentalis et Applicata.87:143-155. DOI: 10.1007/s11103-008-9435-0.
[21] Y Lee, SJ Moon, C Montell. (2009). Multiple gustatory receptors required for the caffeine response in. PNAS.106:4495-4500. DOI: 10.1007/s11103-008-9435-0.
[22] Y Lee, SJ Moon, Y Wang, C Montell. et al.(2015). A gustatory receptor required for strychnine sensation. Chemical Senses.40:525-533. DOI: 10.1007/s11103-008-9435-0.
[23] JI Glendinning, A Davis, S Ramaswamy. (2002). Contribution of different taste cells and signaling pathways to the discrimination of "bitter" taste stimuli by an insect. The Journal of Neuroscience.22:7281-7287. DOI: 10.1007/s11103-008-9435-0.
[24] S Poudel, Y Kim, YT Kim, Y Lee. et al.(2015). Gustatory receptors required for sensing umbelliferone in. Insect Biochemistry and Molecular Biology.66:110-118. DOI: 10.1007/s11103-008-9435-0.
[25] K Ozaki, M Ryuda, A Yamada, A Utoguchi. et al.(2011). A gustatory receptor involved in host plant recognition for oviposition of a swallowtail butterfly. Nature Communications.2. DOI: 10.1007/s11103-008-9435-0.
[26] Y Lee, SH Kim, C Montell. (2010). Avoiding DEET through insect gustatory receptors. Neuron.67:555-561. DOI: 10.1007/s11103-008-9435-0.
[27] S Poudel, Y Kim, JS Gwak, S Jeong. et al.(2017). Gustatory receptor 22e is essential for sensing chloroquine and strychnine in. Insect Biochemistry and Molecular Biology.88:30-36. DOI: 10.1007/s11103-008-9435-0.
[28] L Gong, X Yang, B Zhang, G Zhong. et al.(2011). Silencing of Rieske iron-sulfur protein using chemically synthesised siRNA as a potential biopesticide against. Pest Management Science.67:514-520. DOI: 10.1007/s11103-008-9435-0.
[29] SD Clouse, JM Sasse. (1998). Brassinosteroids: Essential regulators of plant growth and development. Annual Review of Plant Physiology and Plant Molecular Biology.49:427-451. DOI: 10.1007/s11103-008-9435-0.
[30] JJA van Loon. (1990). Chemoreception of phenolic acids and flavonoids in larvae of two species of. Journal of Comparative Physiology A.166:889-899. DOI: 10.1007/s11103-008-9435-0.
[31] KD Tsirigos, C Peters, N Shu, L Käll. et al.(2015). The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Research.43:W401-W407. DOI: 10.1007/s11103-008-9435-0.
[32] T Cheng, J Wu, Y Wu, RV Chilukuri. et al.(2017). Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest. Nature Ecology & Evolution.1:1747-1756. DOI: 10.1007/s11103-008-9435-0.
[33] AJ Thorsteinson. (1953). The chemotactic responses that determine host specificity in an oligophagous insect ( (Curt.) Lepidoptera). Canadian Journal of Zoology.31:52-72. DOI: 10.1007/s11103-008-9435-0.
[34] PJ Clyne, CG Warr, JR Carlson. (2000). Candidate taste receptors in. Science.287:1830-1834. DOI: 10.1007/s11103-008-9435-0.
[35] SJ Moon, Y Lee, Y Jiao, C Montell. et al.(2009). A gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Current Biology.19:1623-1627. DOI: 10.1007/s11103-008-9435-0.
[36] MAT Zullo, G Adam. (2002). Brassinosteroid phytohormones - structure, bioactivity and applications. Brazilian Journal of Plant Physiology.14:143-181. DOI: 10.1007/s11103-008-9435-0.
[37] KA Justus, BK Mitchell. (1996). Oviposition site selection by the diamondback moth, (L.) (Lepidoptera: Plutellidae). Journal of Insect Behavior.9:887-898. DOI: 10.1007/s11103-008-9435-0.
[38] SJ Moon, M Köttgen, Y Jiao, H Xu. et al.(2006). A taste receptor required for the caffeine response. Current Biology.16:1812-1817. DOI: 10.1007/s11103-008-9435-0.
[39] G Krouk, S Ruffel, RA Gutiérrez, A Gojon. et al.(2011). A framework integrating plant growth with hormones and nutrients. Trends in Plant Science.16:178-182. DOI: 10.1007/s11103-008-9435-0.
[40] ZJ Zhang, SS Zhang, BL Niu, DF Ji. et al.(2019). A determining factor for insect feeding preference in the silkworm,. PLOS Biology.17. DOI: 10.1007/s11103-008-9435-0.
[41] DS Zhou, CZ Wang, JJA van Loon. (2009). Chemosensory basis of behavioural plasticity in response to deterrent plant chemicals in the larva of the small cabbage white butterfly. Journal of Insect Physiology.55:788-792. DOI: 10.1007/s11103-008-9435-0.
[42] C Notredame, DG Higgins, J Heringa. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology.302:205-217. DOI: 10.1007/s11103-008-9435-0.
[43] M Kasubuchi, F Shii, K Tsuneto, T Yamagishi. et al.(2018). Insect taste receptors relevant to host identification by recognition of secondary metabolite patterns of non-host plants. Biochemical and Biophysical Research Communications.499:901-906. DOI: 10.1007/s11103-008-9435-0.
[44] Z Wang, A Singhvi, P Kong, K Scott. et al.(2004). Taste representations in the brain. Cell.117:981-991. DOI: 10.1007/s11103-008-9435-0.
[45] VG Dethier. (1937). Gustation and olfaction in lepidopterous larvae. The Biological Bulletin.72:7-23. DOI: 10.1007/s11103-008-9435-0.
[46] HKM Dweck, JR Carlson. (2020). Molecular logic and evolution of bitter taste in. Current Biology.30:17-30. DOI: 10.1007/s11103-008-9435-0.
[47] J Wang, D Wu, Y Wang, D Xie. et al.(2019). Jasmonate action in plant defense against insects. Journal of Experimental Botany.70:3391-3400. DOI: 10.1007/s11103-008-9435-0.
[48] J Wu, IT Baldwin. (2010). New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics.44:1-24. DOI: 10.1007/s11103-008-9435-0.
[49] P Engsontia, U Sangket, W Chotigeat, C Satasook. et al.(2014). Molecular evolution of the odorant and gustatory receptor genes in lepidopteran insects: implications for their adaptation and speciation. Journal of Molecular Evolution.79:21-39. DOI: 10.1007/s11103-008-9435-0.
[50] J Sang, S Rimal, Y Lee. (2019). is necessary for avoiding saponin in. EMBO Reports.20. DOI: 10.1007/s11103-008-9435-0.
[51] LM Schoonhoven, JJA van Loon, M Dicke. (2005). Insect-Plant Biology. DOI: 10.1007/s11103-008-9435-0.
[52] JJA van Loon, CZ Wang, JK Nielsen, R Gols. et al.(2002). Flavonoids from cabbage are feeding stimulants for diamondback moth larvae additional to glucosinolates: Chemoreception and behaviour. Entomologia Experimentalis et Applicata.104:27-34. DOI: 10.1007/s11103-008-9435-0.
[53] WC Ma. (1969). Some properties of gustation in larva of. Entomologia Experimentalis et Applicata.12:584-590. DOI: 10.1007/s11103-008-9435-0.
[54] MP Zalucki, A Shabbir, R Silva, D Adamson. et al.(2012). Estimating the economic cost of one of the world's major insect pests, (Lepidoptera: plutellidae): just how long is a piece of string?. Journal of Economic Entomology.105:1115-1129. DOI: 10.1007/s11103-008-9435-0.
[55] DG Harcourt. (1957). Biology of the diamondback moth, (Curt.) (Lepidoptera: Plutellidae), in Eastern Ontario. II. Life-history, behaviour, and host relationships. The Canadian Entomologist.89:554-564. DOI: 10.1007/s11103-008-9435-0.
[56] LM Schoonhoven, JJA van Loon. (2002). An inventory of taste in caterpillars: each species its own key. Acta Zoologica Academiae Scientiarum Hungaricae.48:215-263. DOI: 10.1007/s11103-008-9435-0.
[57] Y Lv, S Liu. (2005). Effects of exogenous jasmonic acid-induced plant responses on development and growth of. Chinese Journal of Applied Ecology.16:193-195. DOI: 10.1007/s11103-008-9435-0.
[58] T Jermy. (1966). Feeding inhibitors and food preference in chewing phytophagous insects. Entomologia Experimentalis et Applicata.9:1-12. DOI: 10.1007/s11103-008-9435-0.
[59] S Ishikawa. (1966). Electrical response and function of a bitter substance receptor associated with the maxillary sensilla of the larva of the silkworm, L. Journal of Cellular Physiology.67:1-11. DOI: 10.1007/s11103-008-9435-0.
[60] M You, F Ke, S You, Z Wu. et al.(2020). Variation among 532 genomes unveils the origin and evolutionary history of a global insect herbivore. Nature Communications.11. DOI: 10.1007/s11103-008-9435-0.
[61] JW Fahey, AT Zalcmann, P Talalay. (2001). The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry.56:5-51. DOI: 10.1007/s11103-008-9435-0.
[62] JW Mitchell, N Mandava, JF Worley, JR Plimmer. et al.(1970). Brassins--a new family of plant hormones from rape pollen. Nature.225:1065-1066. DOI: 10.1007/s11103-008-9435-0.
[63] ES Hodgson, JY Lettvin, KD Roeder. (1955). Physiology of a primary chemoreceptor unit. Science.122:417-418. DOI: 10.1007/s11103-008-9435-0.
[64] M You, Z Yue, W He, X Yang. et al.(2013). A heterozygous moth genome provides insights into herbivory and detoxification. Nature Genetics.45:220-225. DOI: 10.1007/s11103-008-9435-0.
[65] EG Freeman, A Dahanukar. (2015). Molecular neurobiology of taste. Current Opinion in Neurobiology.34:140-148. DOI: 10.1007/s11103-008-9435-0.
[66] S Yang, D Cao, G Wang, Y Liu. et al.(2017). Identification of genes involved in chemoreception in by antennal transcriptome analysis. Scientific Reports.7. DOI: 10.1007/s11103-008-9435-0.
[67] R Bari, JDG Jones. (2009). Role of plant hormones in plant defence responses. Plant Molecular Biology.69:473-488. DOI: 10.1007/s11103-008-9435-0.
[68] MJ Furlong, DJ Wright, LM Dosdall. (2013). Diamondback moth ecology and management: problems, progress, and prospects. Annual Review of Entomology.58:517-541. DOI: 10.1007/s11103-008-9435-0.
[69] DA Yarmolinsky, CS Zuker, NJP Ryba. (2009). Common sense about taste: from mammals to insects. Cell.139:234-244. DOI: 10.1007/s11103-008-9435-0.
[70] S Fujioka, A Sakurai. (1997). Brassinosteroids. Natural Product Reports.14:1-10. DOI: 10.1007/s11103-008-9435-0.
[71] G Smagghe, L Decombel, B Carton, B Voigt. et al.(2002). Action of brassinosteroids in the cotton leafworm. Insect Biochemistry and Molecular Biology.32:199-204. DOI: 10.1007/s11103-008-9435-0.
[72] J Shim, Y Lee, YT Jeong, Y Kim. et al.(2015). The full repertoire of gustatory receptors for detecting an aversive compound. Nature Communications.6. DOI: 10.1007/s11103-008-9435-0.
[73] W Xu, A Papanicolaou, HJ Zhang, A Anderson. et al.(2016). Expansion of a bitter taste receptor family in a polyphagous insect herbivore. Scientific Reports.6. DOI: 10.1007/s11103-008-9435-0.
[74] JJB Smith, BK Mitchell, BM Rolseth, AT Whitehead. et al.(1990). SAPID tools: microcomputer programs for analysis of multi-unit nerve recordings. Chemical Senses.15:253-270. DOI: 10.1007/s11103-008-9435-0.
文献评价指标
浏览 163次
下载全文 6次
评分次数 0次
用户评分 0.0分
分享 0次