烟粉虱MED隐种中温度胁迫相关microRNAs的特征和功能分析

doi:10.1016/j.jia.2024.09.021

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (7): 2719-2731.DOI: 10.1016/j.jia.2024.09.021

烟粉虱MED隐种中温度胁迫相关microRNAs的特征和功能分析

收稿日期:2024-07-02 修回日期:2024-09-24 接受日期:2024-08-23 出版日期:2025-07-20 发布日期:2025-06-17

Characterization and functions of temperature stress-associated microRNAs in invasive insect Bemisia tabaci Mediterranean cryptic species

Xiaona Shen^{1, 2}, Jianyang Guo², Fanghao Wan², Zhichuang Lü^2#, Jianying Guo^2#, Wanxue Liu²

¹Department of Basic Medicine, Changzhi Medical College, Changzhi 046000, China
²State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

Received:2024-07-02 Revised:2024-09-24 Accepted:2024-08-23 Online:2025-07-20 Published:2025-06-17
About author:#Correspondence Zhichuang Lü, E-mail: lvzhichuang@caas.cn; Jianying Guo, E-mail: guojianying@caas.cn
Supported by:
This work was funded by the National Natural Science Foundation of China (32072494), the Fundamental Research Program of Shanxi Province, China (202203021212165) and the Shanxi Province Higher Education Technology Innovation Project, China (2022L363).

摘要/Abstract

摘要：

随着当前国际贸易的发展和人员的频繁交流，生物入侵在全球范围内正呈现快速增长趋势。昆虫是变温动物，它们的地理分布很大程度上取决于温度耐受性的强弱。为了研究入侵种烟粉虱MED隐种的温度响应机制，我们采用miRNA-seq技术分别对三个具有不同环境温度条件的烟粉虱田间种群（吐鲁番、哈尔滨和海口市）进行sRNA高通量测序。结果表明在烟粉虱MED隐种中存在12个响应温度胁迫并发生差异表达的miRNA，其中Bta-miR-998和Bta-miR-129与温度耐受性相关。此外，我们预测并验证了Bta-miR-998和Bta-miR-129靶基因中与耐温性相关的靶基因。该结果显示高温种群中Bta-miR-129表达量降低，靶基因BtMGAT3表达增加并导致其耐热性显著提升。而低温种群中Bta-miR-129表达量增加，靶基因BtRGS7表达显著下调并使其耐寒性显著提升。本研究结果表明miRNA调控基因表达的调节方式是烟粉虱MED隐种中重要的温度响应机制，揭示了miRNA在昆虫温度响应中的重要调节作用，为研究miRNA对昆虫基因表达的调节提供了新的途径。

Abstract:

With the development of international trade and frequent personnel exchanges, biological invasion is showing a rapidly growing trend worldwide. Insects are ectothermic animals, so their geographical distribution is due largely to their high and low temperature tolerances. To study the temperature response mechanisms of Bemisia tabaci Mediterranean cryptic species (MED), miRNA-seq technology was used to unravel the miRNA library of B. tabaci MED in three field populations (TP, HB, and HK) from cities with different environmental temperatures. We identified 12 differentially expressed miRNAs in response to temperature stress, and Bta-miR-998 and Bta-miR-129 were shown to be associated with temperature tolerance. In addition, we predicted and verified the target genes associated with the temperature tolerance imparted by Bta-miR-998 and Bta-miR-129. The results showed that the down-regulated target gene of Bta-miR-129, BtMGAT3, significantly reduced the heat tolerance and another down-regulated target gene, BtRGS7, affected the cold tolerance of B. tabaci MED. These results indicate that gene expression regulated by miRNAs is an important temperature response mechanism in B. tabaci MED. This study reveals the important regulatory role of miRNA in insect temperature adaptation and provides a new avenue for studying the regulation of insect gene expression by miRNA

Key words: miRNA , invasive insects , temperature stress , response mechanisms

Xiaona Shen, Jianyang Guo, Fanghao Wan, Zhichuang Lü, Jianying Guo, Wanxue Liu. 烟粉虱MED隐种中温度胁迫相关microRNAs的特征和功能分析[J]. Journal of Integrative Agriculture, 2025, 24(7): 2719-2731.

Xiaona Shen, Jianyang Guo, Fanghao Wan, Zhichuang Lü, Jianying Guo, Wanxue Liu. Characterization and functions of temperature stress-associated microRNAs in invasive insect Bemisia tabaci Mediterranean cryptic species[J]. Journal of Integrative Agriculture, 2025, 24(7): 2719-2731.

参考文献

Barro P, Dinsdale A. 2009. Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56, 1–19.

De Barro P J, Liu S S, Boykin L M, Dinsdale A B. 2011. Bemisia tabaci: A statement of species status. Annual Review of Entomology, 56, 1–19.

Biswanath M, Adele S, Yunxia O, Askeland R W, Sugg S L, Fisher R A. 2020. Identification of MT1E as a novel tumor suppressor in hepatocellular carcinoma. Pathology Research and Practice, 216, 153213.

Byrne D N, Bellows T S J. 1991. Whitefly biology. Annual Review of Entomology, 36, 431–457.

Chakraborty A K, Pawelek J M. 2003. GnT-V, macrophage and cancer metastasis: A common link. Clinical and Experimental Metastasis, 20, 365–373.

Chu D, Zhang Y J, Cong B, Xu B Y, Wu Q J. 2005. Identification for Yunnan Q-biotype Bemisia tabaci population. Entomology Knowledge, 42, 54–56. (in Chinese)

Dai T M, Lü Z C, Liu W X, Wan F H, Hong X Y. 2017. The homology gene BtDnmt1 is essential for temperature tolerance in Invasive Bemisia tabaci Mediterranean cryptic species. Science Reports, 7, 3040.

Dai T M, Lü Z C, Wang Y S, Liu W X, Hong X Y, Wan F H. 2018. Molecular characterizations of DNA methyltransferase 3 and its roles in temperature tolerance in the whitefly, Bemisia tabaci Mediterranean. Insect Molecular Biology, 27, 123–132.

Deng Q, Liu X, Yang Z, Xie L. 2019. Expression of N-Acetylglucosaminyltransferase III promotes trophoblast invasion and migration in early human placenta. Reproductive Sciences, 26, 1373–1381.

Dinsdale A, Cook L, Riginos C, Buckley Y M, De Barro P. 2010. Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America, 103, 196–208.

Ekuni A, Miyoshi E, Ko J H, Noda K, Kitada T, Ihara S, Endo T, Hino A, Honke K, Taniguchi N. 2002. A glycomic approach to hepatic tumors in N-acetylglucosaminyltransferase III (GnT-III) transgenic mice induced by diethylnitrosamine (DEN): Identification of haptoglobin as a target molecule of GnT-III. Free Radical Research, 36, 827–833.

Enright A J, John B, Gaul U, Tuschl T, Sander C, Marks D S. 2003. MicroRNA targets in Drosophila. Genome Biology, 5, R1.

Fast I, Rosenkranz D. 2018. Temperature-dependent small RNA expression in Drosophila melanogaster. RNA Biology, 15, 308–313.

Friedlander M R, Mackowiak S D, Li N, Chen W, Rajewsky N. 2012. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Research, 40, 37–52.

Hu J, De Barro P, Zhao H, Wang J, Nardi F, Liu S S. 2011. An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE, 6, e16061.

Huang J, Stewart A, Maity B, Hagen J, Fisher R A. 2014. RGS6 suppresses Ras-induced cellular transformation by facilitating Tip60-mediated Dnmt1 degradation and promoting apoptosis. Oncogene, 33, 3604–3611.

Ji S X, Wang X D, Shen X N, Liang L, Liu W X, Wan F H, Lu Z C. 2020. Using RNA interference to reveal the function of chromatin remodeling factor ISWI in temperature tolerance in Bemisia tabaci Middle East-Asia Minor 1 cryptic species. Insects, 11, 113.

Krol J, Loedige I, Filipowicz W. 2010. The widespread regulation of microRNA biogenesis, function and decay. Nature Reviews Genetics, 11, 597–610.

Langmead B, Trapnell C, Pop M, Salzberg S L. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25.

Lee R C, Feinbaum R L, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.

HuennekeL F. 1997. Outlook for plant invasions: Interactions with other agents of global change. Assessment and Management of Plant Invasions, 8, 95–103.

Li J J, Shi Y, Lin G L, Yang C H, Liu T X. 2020. Genome-wide identification of neuropeptides and their receptor genes in Bemisia tabaci and their transcript accumulation change in response to temperature stresses. Insect Science, 28, 35–46.

Lü Z C, Wan F H. 2008. Differential gene expression in whitefly (Bemisia tabaci) B-biotype females and males under heat-shock condition. Comparative Biochemistry and Physiology (D: Genomics & Proteomics), 3, 257–262.

Lyons P J, Govaere L, Crapoulet N, Storey K B, Morin P J. 2016. Characterization of cold-associated microRNAs in the freeze-tolerant gall fly Eurosta solidaginis using high-throughput sequencing. Comparative Biochemistry and Physiology (D: Genomics & Proteomics), 20, 95–100.

Ma F Z, Lu Z C, Wang R, Wan F H. 2014. Heritability and evolutionary potential in thermal tolerance traits in the invasive Mediterranean cryptic species of Bemisia tabaci (Hemiptera: Aleyrodidae). PLoS ONE, 9, e103279.

Mahadav A, Kontsedalov S, Czosnek H, Ghanim M. 2009. Thermotolerance and gene expression following heat stress in the whitefly Bemisia tabaci B and Q biotypes. Insect Biochemistry and Molecular Biology, 39, 668–676.

Mooney H A, Cleland E E. 2001. The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences of the United States of America, 98, 5446–5451.

Peng W, Yu S, Handler A M, Tu Z, Saccone G, Xi Z, Zhang H. 2020. miRNA-1-3p is an early embryonic male sex-determining factor in the Oriental fruit fly Bactrocera dorsalis. Nature Communications, 11, 932.

Sailaja B, Voleti S R, Subrahmanyam D, Sarla N, Prasanth V V, Bhadana V P, Mangrauthia S K. 2014. Prediction and expression analysis of miRNAs associated with heat stress in Oryza sativa. Rice Science, 21, 3–12.

Shen X N, Wang X D, Wan F H, Lü Z C, Liu W X. 2023. Gene expression analysis reveals potential regulatory factors response to temperature stress in Bemisia tabaci Mediterranean. Genes, 14, 1013.

Simberloff D. 2000. Nonindigenous Species: A Global Threat to Biodiversity and Stability. National Academy Press, Washington, D.C. pp. 325–334.

Storey J D. 2003. The positive false discovery rate: A Bayesian interpretation and the q-value. Annals of Statistics, 31, 2013–2035.

Tay Y, Zhang J, Thomson A M, Lim B, Rigoutsos I. 2008. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature, 455, 1124–1128.

Truscott M, Islam A B, Lightfoot J, López-Bigas N, Frolov M V. 2014. An intronic microRNA links Rb/E2F and EGFR signaling. PLoS Genetics, 24, e1004493.

Tseng M. 2003. A simple parafilm M-based method for blood-feeding Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology, 40, 588–589.

Varki A. 1993. Biological roles of oligosaccharides: All of the theories are correct. Glycobiology, 3, 97–130.

Wang L, Feng Z, Wang X, Wang X, Zhang X. 2010. DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26, 136–138.

Wu L, Belasco J G. 2008. Let me count the ways: Mechanisms of gene regulation by miRNAs and siRNAs. Molecular Cell, 29, 1–7.

Xue Y T. 2018. Geographical distribution, genetic Structure of Bemisia tabaci (Hemiptera: Aleyrodidae) in China, and diversity of its secondary endosymbionts. Ph D thesis, Southwest University, China. (in Chinese)

Yang J, Platt L T, Maity B, Ahlers K E, Fisher R A. 2016. RGS6 is an essential tumor suppressor that prevents bladder carcinogenesis by promoting p53 activation and DNMT1 downregulation. Oncotarget, 7, 69159–69172.

Zhang L P, Zhang Y J, Zhang W J, Wu Q J, Xu B Y, Chu D. 2005. Analysis of genetic diversity among different geographical populations and determination of biotypes of Bemisia tabaci in China. Journal of Applied Entomology, 129, 121–128.

Zhao S, Liu M F. 2009. New progress in the research of microRNA’s mechanism of action. Scientia Sinica Vitae, 30, 109–113. (in Chinese)

Zheng Y X, Jiao B H. 2010. The biological formation of MiRNA and the mechanism of regulating gene expression. Chemistry Life, 30, 821–826.

Zhou L, Chen J, Li Z, Li X, Hu X, Yi H, Zhao X K, Liang C Z, Wang Y, Sun L, Shi M, Xu X H, Shen F, Chen M S, Han Z J, Peng Z Y, Zhai Q N, Chen J, Zhang Z F, Yang R L, et al. 2010. Integrated profiling of microRNAs and mRNAs: MicroRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS ONE, 5, e15224.

Zhu B, Sun X, Nie X, Liang P, Gao X. 2020. MicroRNA-998-3p contributes to Cry1Ac-resistance by targeting ABCC2 in lepidopteran insects. Insect Biochemistry Molecular Biology, 117, 103283.

烟粉虱MED隐种中温度胁迫相关microRNAs的特征和功能分析

Characterization and functions of temperature stress-associated microRNAs in invasive insect Bemisia tabaci Mediterranean cryptic species

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics