海藻糖代谢及其调控昆虫几丁质合成研究进展

doi:10.3864/j.issn.0578-1752.2018.04.009

摘要/Abstract

摘要： 海藻糖为一种非还原性糖，广泛存在于细菌、藻类、真菌、植物和无脊椎动物中。海藻糖被称为昆虫“血糖”，源于该糖为昆虫血淋巴中的主要糖类物质，在昆虫生长、发育、蜕皮等正常生理活动中有着重要的作用。昆虫的海藻糖先由海藻糖合成酶（trehalose-6-phosphate synthase，TPS）生成海藻糖-6-磷酸，然后通过海藻糖磷酸脂酶（trehalose-6-phosphate phosphatase，TPP）最终合成海藻糖，在能量需求时通过海藻糖酶（trehalase，TRE）降解为葡萄糖，用于能量供给。几丁质为昆虫表皮、中肠围食膜和气管系统的主要组成成分，昆虫在发育过程中需要蜕掉旧表皮，形成新的表皮，该过程一直是害虫控制的重要靶标途径。海藻糖酶为昆虫几丁质合成途径的第一个酶，在几丁质合成通路中有着重要的功能。那么海藻糖代谢又是如何调控几丁质合成途径来控制昆虫的蜕皮及几丁质代谢的呢？随着国内外海藻糖代谢相关基因功能研究的深入开展，研究结果表明昆虫海藻糖供给在几丁质合成中具有重要的作用，海藻糖酶分为可溶性和膜结合型两类，可溶性TRE和TPS在不同昆虫种类中具有多个同源基因，表明昆虫海藻糖代谢进化途径多样化。其次，海藻糖代谢直接调控几丁质合成途径，不论是海藻糖合成酶还是海藻糖酶基因的低表达，均能控制海藻糖使其供给不平衡，从而导致几丁质合成途径受阻，特别是几丁质合成酶基因表达降低而造成几丁质含量下降，该调控作用可进一步引起昆虫蜕皮困难、翅发育畸形等，甚至大量死亡。再次，海藻糖酶抑制剂能够抑制可溶性和膜结合型两类海藻糖酶活性、引起几丁质合成通路相关基因及几丁质酶基因表达的显著下降，导致几丁质含量显著降低，产生高比例的昆虫个体死亡。这些结果充分表明，一旦昆虫海藻糖代谢的供给平衡被打破，会直接影响到昆虫的几丁质合成乃至昆虫的蜕皮与发育过程。本文综述前人在海藻糖代谢调控几丁质合成方面的最新研究成果，为将来开发和利用海藻糖酶抑制剂及海藻糖合成酶抑制剂等绿色农药防治害虫提供理论依据。

关键词: 海藻糖代谢, 海藻糖合成酶, 海藻糖酶, 几丁质合成, RNA干扰

Abstract: Trehalose as a non-reducing disaccharide is widely found in bacteria, algae, fungi, plants, and invertebrates. Moreover, trehalose is regarded as ‘blood sugar’, since it is the primary carbohydrate substances in insects, which plays a key role in normal physiological processes, such as growth, development, moulting and so on. The trehalose in insects is synthesized by trehalose-6-phosphate synthase (TPS) and trehalose-6-phosphatase (TPP). Trehalase (TRE) can hydrolyze trehalose into glucose rapidly and provide energy when energy is needed. Chitin is the main component of insect epidermis, midgut peritrophic membrane and tracheal system. During developmental stages, insects need to shed old epidermis for forming new epidermis. This process has always been an important target for pest control. TRE is the first enzyme in the chitin biosynthesis pathway, which has significant functions of influencing the chitin metabolism by regulating chitin synthesis pathway. So how does trehalose metabolism regulate chitin synthesis pathways to control insect molt and chitin metabolism? With further research on the function of trehalose metabolism related genes over the world, these results showed that the providing of trehalose in insects plays a pivotal role in chitin synthesis. In addition, trehalase can be divided into soluble and membrane-bound types. The soluble TRE and TPS have multiple homologous genes in different insect species, indicating that the trehalose metabolic evolution of insects is diversified. Second, trehalose metabolism can regulate the chitin synthesis directly. Whether the low expression of TPS or TRE can break the supply balance of trehalose, resulting in chitin synthesis pathway blocked, especially the expression of chitin synthase gene decreased which lead to low chitin content, and further cause molting difficulties, developmental deformities, even death. Furthermore, trehalase inhibitors can inhibite the activities between soluble and membrane-bound TRE, resulting in a significant decrease in chitin synthesis pathway-related genes and chitinase gene expression, low chitin content and high proportion of death. These results indicate that once the supply balance of insect trehalose metabolism is broken, it will directly affect the chitin synthesis of insects which related to the process of molting and development. In this report, the research progress on trehalose metabolism and the regulation of chitin biosynthesis are introduced and summarized, in the desire to provide a theoretical basis for the development of green pesticides represented by trehalase inhibitor and trehalose-6-phosphate synthase pathway inhibitor aimed at pest control.

Key words: trehalose metabolism, trehalose-6-phosphate synthase (TPS), trehalase, chitin biosynthesis, RNA interference

唐斌，张露，熊旭萍，汪慧娟，王世贵. 海藻糖代谢及其调控昆虫几丁质合成研究进展[J]. 中国农业科学, 2018, 51(4): 697-707.

TANG Bin, ZHANG Lu, XIONG XuPing, WANG HuiJuan, WANG ShiGui . Advances in Trehalose Metabolism and Its Regulation of Insect Chitin Synthesis[J]. Scientia Agricultura Sinica, 2018, 51(4): 697-707.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2018.04.009

https://www.chinaagrisci.com/CN/Y2018/V51/I4/697

参考文献

[1] ELBEIN A D, PAN Y T, PASTUSZAK I, CARROLL D. New insights on trehalose: a multifunctional molecule. Glycobiology, 2003, 13(4): 17R-27R.

[2] 唐斌, 魏苹, 陈洁, 王世贵, 张文庆. 昆虫海藻糖酶的基因特性及功能研究进展. 昆虫学报, 2012, 55(11): 1315-1321.

Tang B, Wei P, Chen J, Wang S G, Zhang W Q. Progress in gene features and functions of insect trehalases. Acta Entomologica Sinica, 2012, 55(11):1315-1321. (in Chinese)

[3] TANG B, QIN Z, SHI Z K, WANG S, GUO X J, WANG S G, ZHANG F. Trehalase in Harmonia axyridis (Coleoptera: Coccinellidae): effects on beetle locomotory activity and the correlation with trehalose metabolism under starvation conditions. Applied Entomology and Zoology, 2014, 49(2): 255-264.

[4] IORDACHESCU M,IMAI R. Trehalose biosynthesis in response to abiotic stresses. Journal of Integrative Plant Biology, 2008, 50(10): 1223-1229.

[5] TANG B, CHEN X, LIU Y, TIAN H, LIU J, HU J, XU W H, ZHANG W Q. Characterization and expression patterns of a membrane-bound trehalase from Spodoptera exigua. BMC Molecular Biology, 2008, 9: 51.

[6] SHUKLA E, THORAT L J, NATH B B, GAIKWAD S M. Insect trehalase: physiological significance and potential applications. Glycobiology, 2015, 25(4): 357-367.

[7] LIU J H,SHANG X D,LIU J Y,TAN Q. Changes in trehalose content, enzyme activity and gene expression related to trehalose metabolism in Flammulina velutipes under heat shock. Microbiology, 2016, 162(8): 1274-1285.

[8] ZHU K Y, MERZENDORFER H, ZHANG W Q, ZHANG J Z, MUTHUKRISHNAN S. Biosynthesis, turnover, and functions of chitin in insects. Annual Review of Entomology, 2016, 61: 177-196.

[9] CHEN J, TANG B, CHEN H X, YAO Q, HUANG X F, CHEN J, ZHANG D W, ZHANG W Q. Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by RNA interference. PLoS One, 2010, 5(4): e10133.

[10] ZHAO L N, YANG M M, SHEN Q D, SHI Z K, WANG S G, TANG B. Functional characterization of three trehalase genes regulating the chitin metabolism pathway in rice brown planthopper using RNA interference. Scientific Reports, 2016, 6: 27841.

[11] YANG M M, ZHAO L N, SHEN Q D, XIE G Q, WANG S G, TANG B. Knockdown of two trehalose-6-phosphate synthases severely affects chitin metabolism gene expression in the brown planthopper Nilaparvata lugens. Pest Management Science, 2017, 73(1): 206-216.

[12] ARGüELLES J C. Why can’t vertebrates synthesize trehalose? Journal of Molecular Evolution, 2014, 79(3/4): 111-116.

[13] TANG B, WANG S, WANG S G, WANG H J, ZHANG J Y, CUI S Y. Invertebrate trehalose-6-phosphate synthase gene: genetic architecture, biochemistry, physiological function, and potential applications. Frontiers in Physiology, 2018, 9: 30.

[14] TANG B, CHEN J, YAO Q, PAN Z Q, XU W H, WANG S G, ZHANG W Q. Characterization of a trehalose-6-phosphate synthase gene from Spodoptera exigua and its function identification through RNA interference. Journal of Insect Physiology, 2010, 56(7): 813-821.

[15] TANG B, WEI P, ZHAO L N, SHI Z K, SHEN Q D, YANG M M, XIE G Q, WANG S G. Knockdown of five trehalase genes using RNA interference regulates the gene expression of the chitin biosynthesis pathways in Tribolium castaneum. BMC Biotechnology, 2016, 16: 67.

[16] CHEN J, ZHANG D W, YAO Q, ZHANG J Q,DONG X L,TIAN H G,CHEN J, ZHANG W Q. Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology, 2010, 19(6): 777-786.

[17] KERN C,WOLF C,BENDER F,BERGER M,NOACK S,SCHMALZ S,ILG T. Trehalose-6-phosphate synthase from the cat flea Ctenocephalides felis and Drosophila melanogaster: gene identification, cloning, heterologous functional expression and identification of inhibitors by high throughput screening. Insect Molecular Biology, 2012, 21(4): 456-471.

[18] TANG B, YANG M M, SHEN Q D, XU Y X, WANG H J, WANG S G. Suppressing the activity of trehalase with validamycin disrupts the trehalose and chitin biosynthesis pathways in the rice brown planthopper, Nilaparvata lugens. Pesticide Biochemistry and Physiology, 2017, 137: 81-90.

[19] SNELLING E P, SEYMOUR R S, RUNCIMAN S. Molting of insect tracheae captured by light and electron-microscopy in the metathoracic femur of a third instar locust Locusta migratoria. Journal of Insect Physiology, 2011, 57(9): 1312-1316.

[20] ZHONG H Y, WEI C, ZHANG Y L. Gross morphology and ultrastructure of salivary glands of the mute cicada Karenia caelatata Distant (Hemiptera: Cicadoidea). Micron, 2013, 45: 83-91.

[21] 张建珍. 昆虫几丁质代谢与植物保护. 中国农业科学, 2014, 47(7): 1301-1302.

ZHANG J Z. Insect chitin metabolism and plant protection. Scientia Agricultura Sinica, 2014, 47(7): 1301-1302. (in Chinese)

[22] KRAMER K J, HOPKINS T L, SCHAEFER J. Applications of solids NMR to the analysis of insect sclerotized structures. Insect Biochemistry and Molecular Biology, 1995, 25(10): 1067-1080.

[23] 张文庆, 陈晓菲, 唐斌, 田宏刚, 陈洁, 姚琼. 昆虫几丁质合成及其调控研究前沿. 应用昆虫学报, 2011, 48(3): 475-479.

ZHANG W Q, CHEN X F, TANG B, TIAN H G, CHEN J, YAN Q. Insect chitin biosynthesis and its regulation. Chinese Journal of Applied Entomology, 2011, 48(3): 475-479. (in Chinese)

[24] 刘晓健, 崔淼, 李大琪, 张欢欢, 杨美玲, 张建珍. 飞蝗几丁质合成酶2基因的表达特性、功能及调控. 中国农业科学, 2014, 47(7): 1330-1340.

LIU X J, CUI M, LI D Q, ZHANG H H, YANG M L, ZHANG J Z. Expression, function and regulation of chitin synthase 2 gene in Locusta migratoria. Scientia Agricultura Sinica, 2014, 47(7): 1330-1340. (in Chinese)

[25] 余志涛, 刘晓健, 马恩波, 郭亚平, 张建珍. 中华稻蝗几丁质合成酶1基因的mRNA表达及功能. 中国农业科学, 2012, 45(5): 877-884.

YU Z T, LIU X J, MA E B, GUO Y P, ZHANG J Z. mRNA expression and physiological function of chitin synthase1 from Oxya chinensis (Thunberg). Scientia Agricultura Sinica, 2012, 45(5): 877-884. (in Chinese)

[26] 李大琪, 杜建中, 张建琴, 郝耀山, 刘晓健, 王亦学, 马恩波, 张建珍, 孙毅. 东亚飞蝗几丁质酶家族基因的表达特性与功能研究. 中国农业科学, 2011, 44(3): 485-492.

LI D Q, DU J Z, ZHANG J Q, HAO Y S, LIU X J, WANG Y X, MA E B, ZHANG J Z, SUN Y. Study on expression characteristics and functions of chitinase family genes from Locusta migratoria manilensis (Meyen). Scientia Agricultura Sinica, 2011, 44(3): 485-492. (in Chinese)

[27] 李大琪, 王燕, 张建琴, 李涛, 孙毅, 张建珍. 中华稻蝗几丁质酶基因10 (OcCht10)的分子特性及功能. 中国农业科学, 2014, 47(7): 1313-1320.

LI D Q, WANG Y, ZHANG J Q, LI T, SUN Y, ZHANG J Z. Molecular characterization and function of chitinase 10 gene (OcCht10) from Oxya chinensis. Scientia Agricultura Sinica, 2014, 47(7): 1313-1320. (in Chinese)

[28] 张欢欢, 张学尧, 刘晓健, 马恩波, 张建珍. 飞蝗葡萄糖胺-6-磷酸-N-乙酰转移酶的特性及生物学功能. 中国农业科学, 2012, 45(12): 2393-2403.

ZHANG H H, ZHAGN X Y, LIU X J, MA E B, ZHANG J Z. The characteristics and biological fuction of glucosamine-6-phosphate-N- acetyltransferase in Locusta migratoria. Scientia Agricultura Sinica, 2012, 45(12): 2393-2403. (in Chinese)

[29] 陈洁, 陈宏鑫, 姚琼, 张文庆. 甜菜夜蛾UAP的克隆、时空表达及RNAi研究. 中国农业科学, 2014, 47(7): 1351-1361.

CHEN J, CHEN H X, YAO Q, ZHANG W Q. Molecular cloning, expression patterns and RNAi of UDP-N-acetylglucosamine pyrophosphorylase in Spodoptera exigua. Scientia Agricultura Sinica, 2014, 47(7): 1351-1361. (in Chinese)

[30] 于荣荣, 丁国伟, 郭亚平, 马恩波, 张建珍. 中华稻蝗几丁质脱乙酰基酶2基因的分子特性和生物学功能. 中国农业科学, 2014, 47(7): 1321-1329.

YU R R, DING G W, GUO Y P, MA E B, ZHANG J Z. Molecular characterization and functional analysis of chitin deacetylase 2 gene in Oxya chinensis. Scientia Agricultura Sinica, 2014, 47(7): 1321-1329. (in Chinese)

[31] 闫晓平, 赵丹, 郭巍, 王伟, 张雅昆, 郝玉杰, 赵坤莉. 美国白蛾几丁质脱乙酰酶的克隆、表达及酶学性质. 中国农业科学, 2017, 50(5): 849-858.

YAN X P, ZHAO D, GUO W, WANG W, ZHANG Y K, HAO Y J, ZHAO K L. Cloning, expression and enzymatic characterization of chitin deacetylases from Hyphantria cunea. Scientia Agricultura Sinica, 2017, 50(5): 849-858. (in Chinese)

[32] 赵盼, 张学尧, 刘晓健, 赵小明, 于荣荣, 董玮, 马恩波, 张建珍, 张敏. 飞蝗几丁质脱乙酰基酶的真核表达、亲和纯化及酶活性. 中国农业科学, 2017, 50(6): 1057-1066.

ZHAO P, ZHANG X Q, LIU X J, ZHAO X M, YU R R, DONG W, MA E B, ZHANG J Z, ZHANG M. Eukaryotic expression, affinity purification and enzyme activity of chitin deacetylase in Locusta migratoria. Scientia Agricultura Sinica, 2017, 50(6): 1057-1066. (in Chinese)

[33] 王燕, 李大琪, 刘晓健, 李涛, 马恩波, 范仁俊, 张建珍. 飞蝗表皮蛋白Obstructor家族基因的分子特性及基于RNAi的功能分析. 中国农业科学, 2015, 48(1): 73-82.

WANG Y, LI D Q, LIU X J, MA E B, FAN R J, ZHANG J Z. Molecular characterization and RNAi-based functional analysis of Obstructor family genes in Locusta migratoria. Scientia Agricultura Sinica, 2015, 48(1): 73-82. (in Chinese)

[34] 赵小明, 贾盼, 勾昕, 刘卫敏, 马恩波, 张建珍. 飞蝗内表皮蛋白基因LmAbd-5的表达与功能分析. 中国农业科学, 2017, 50(10): 1817-1826.

ZHAO X M, JIA P, GOU X, LIU W M, MA E B, ZHANG J Z. Expression and functional analysis of endocuticle structural glycoprotein gene LmAbd-5 in Locusta migratoria. Scientia Agricultura Sinica, 2017, 50(10): 1817-1826. (in Chinese)

[35] 张薇薇, 董照明, 张艳, 赵晓璐, 张守亚, 赵萍. 家蚕表皮蛋白BmCPAP3-G的表达特征及其与几丁质的结合特性. 中国农业科学, 2017, 50(9): 1723-1733.

ZHANG W W, DONG Z M, ZHANG Y, ZHAO X L, ZHANG S Y, ZHAO P. Expression pattern and chitin-binding mode analyses of cuticle protein BmCPAP3-G in the silkworm (Bombyx mori). Scientia Agricultura Sinica, 2017, 50(9): 1723-1733. (in Chinese)

[36] Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G. Insights on the evolution of trehalose biosynthesis. BMC Evolutionary Biology, 2006, 6: 109.

[37] STRøM A R, KAASEN I. Trehalose metabolism in Escherichia coli: stress protection and stress regulation of gene expression. Molecular Microbiology, 1993, 8(2): 205-210.

[38] THOMPSON S N. Trehalose – The insect ‘blood’ sugar. Advances in Insect Physiology, 2003, 31: 205-285.

[39] GOU Q,HAO Y J,LI Y,ZHANG, Y J,REN S,SI F L, CHEN B. Gene cloning, characterization and expression and enzymatic activities related to trehalose metabolism during diapauses of the onion maggot Delia antique (Diptera: Anthomyiidae). Gene,2015, 565(1): 106-115.

[40] CHENQ,MA E,BEHAR K L,XU T,HADDAD G G. Role of trehalose phosphate synthase in anoxia tolerance and development in Drosophila melanogaster. Journal of Biological Chemistry, 2002, 277(5): 3274-3279.

[41] CHEN Q, BEHAR K L, XU T, FAN C, HADDAD G G. Expression of Drosophila trehalose-phosphate synthase in HEK-293 cells increases hypoxia tolerance. Journal of Biological Chemistry, 2003, 278(49): 49113-49118.

[42] XU J, BAO B, ZHANG Z F, YI Y Z, XU W H. Identification of a novel gene encoding the trehalose phosphate synthase in the cotton bollworm, Helicoverpa armigera. Glycobiology, 2009, 19(3): 250-257.

[43] MATSUDA H, YAMADA T, YOSHIDA M, NISHIMURA T. Flies without trehalose. Journal of Biological Chemistry2015, 290(2): 1244-1255.,

[44] YASUGI T,YAMADA T,NISHIMURA T. Adaptation to dietary conditions by trehalose metabolism in Drosophila. Scientific Reports, 2017, 7: 1619.

[45] 陈静, 张道伟. 德国小蠊两个海藻糖合成酶基因的克隆、组织分布及诱导表达分析. 昆虫学报, 2015, 58(10): 1046-1053.

CHEN J, ZHANG D W. Molecular cloning, tissue distribution and temperature-induced expression of two trehalose-6-phosphate synthase genes in Blattella germanica (Blattodea: Blattellidae). Acta Entomology Sinica, 2015, 58(10): 1046-1053. (in Chinese)

[46] CHEN Q W, JIN S, ZHANG L, SHEN Q D, WEI P, WEI C M, WANG S G, TANG B. Regulatory functions of trehalose-6-phosphate synthase in the chitin biosynthesis pathway in Tribolium castaneum (Coleoptera: Tenebrionidae) revealed by RNA interference. Bulletin of Entomological Research, 2017, 18: 1-12.

[47] 沈祺达. 褐飞虱TPS3基因特性、功能鉴定与调控分析[D]. 杭州: 杭州师范大学, 2017.

SHEN Q D. Genetic characteristics, functional identification and regulation analysis of trehalose-6-phosphate synthase 3 in Nilaparvata lugens[D]. Hangzhou: Hangzhou Normal University, 2017. (in Chinese)

[48] PELLERONE F I, ARCHER S K, BEHM C A, GRANT W N, LACERY M J, SOMERVILLE A C. Trehalose metabolism genes in Caenorhabditis elegans and filarial nematodes. International Journal for Parasitology, 2003, 33(11): 1195-1206.

[49] GOYAL K, BROWNE J A, BURNELL A M, TUNNACLIFFE A. Dehydration-induced tps gene transcripts from an anhydrobiotic nematode contain novel spliced leaders and encode atypical GT-20 family proteins. Biochimie, 2005, 87: 565-574.

[50] 王军娥, 刘静. 昆虫海藻糖酶的研究进展. 贵州农业科学, 2009, 37(4): 88-90.

WANG J E, LIU J. Research progress of insect trehalase. Guizhou Agricultural Sciences, 2009, 37(4): 88-90. (in Chinese)

[51] UJITA M, YAMANAKA M, MAENO Y, YOSHIDA K, OHSHIO W, UENO Y, BANNO Y, FUJII H, OKUMURA H. Expression of active and inactive recombinant soluble trehalase using baculovirus- silkworm expression system and their glycan structures. Journal of Bioscience and Bioengineering, 2011, 111(1): 22-25.

[52] 褚亚平. 氟铃脲对斜纹夜蛾海藻糖酶活性及基因表达的影响[D]. 泰安: 山东农业大学, 2013.

ZHU Y P. Effects of hexaflumuron on trehalase activity and expression of trehalase gene from Spodoptera litura Fabricius[D]. Taian: Shandong Agricultural University, 2013. (in Chinese)

[53] 魏苹. 赤拟谷盗海藻糖酶基因调控几丁质合成及能量代谢的功能研究[D]. 杭州: 杭州师范大学, 2013.

WEI P. Regulating functions of trehalase in the pathway of energy metabolism and chitin biosynthesis in Tribolium castaneum revealed by RNA interference[D]. Hangzhou: Hangzhou Normal University, 2013. (in Chinese)

[54] CLEGG J S, Evans D R. Blood trehalose and flight metabolism in the blowfly. Science, 1961, 134(3741): 54-55.

[55] TATUN N, SINGTRIPOP T, TUNGJITAYAKUL J, SAKURAI S. Regulation of soluble and membrane-bound trehalase activity and expression of the enzyme in the larval midgut of the bamboo borer Omphisa fuscidentalis. Insect Biochemistry and Molecular Biology, 2008, 38(8): 788-795.

[56] 张露, 朱世城, 郑好, 沈祺达, 王世贵, 唐斌. 褐飞虱海藻糖酶基因在表皮几丁质代谢中的调控作用. 中国农业科学, 2017, 50(6): 1047-1056.

ZHANG L, ZHU S C, ZHENG H, SHEN Q D, WANG S G, TANG B. Regulatory function of trehalase genes on chitin metabolism in the cuticle of Nilaparvata lugens. Scientia Agricultura Sinica, 2017, 50(6): 1047-1056. (in Chinese)

[57] 刘晓健, 张欢欢, 李大琪, 崔淼, 马恩波, 张建珍. 飞蝗可溶型海藻糖酶基因的序列分析及mRNA表达特性. 昆虫学报, 2012, 55(11): 1264-1271.

LIU X J, ZHANG H H, LI D Q, CUI M, MA E B, ZHANG J Z. Sequence characterization and mRNA expression profiling of a soluble trehalase gene in Locusta migratoria (Orthoptera: Acrididae). Acta Entomologica Sinica, 2012, 55(11): 1264-1271. (in Chinese)

[58] TAKIGUCHI M, NIIMI T, SU Z H, YAGINUMA T. Trehalase from male accessory gland of an insect, Tenebrio molitor. cDNA sequencing and developmental profile of the gene expression. The Biochemical Journal, 1992, 288(1): 19-22.

[59] MITSUMASU K, AZUMA M, NIIMI T, YAMASHITA O, YAGINUMA T. Membrane-penetrating trehalase from silkworm Bombyx mori. Molecular cloning and localization in larval midgut. Insect Molecular Biology, 2005, 14(5): 501-508.

[60] BECKER A, SCHLöDER P, STEELE J E, WEGENER G. The regulation of trehalose metabolism in insects. Experientia, 1996, 52(5): 433-439.

[61] MüLLER J, AESCHBACHER R A, WINGLER A, BOLLER T, WIEMKEN A. Trehalose and trehalase in Arabidopsis. Plant Physiology, 2001, 125(2): 1086-1093.

[62] SILVA M C, TERRA W R, FERREIRA C. The role of carboxyl, guanidine and imidazole groups in catalysis by a midgut trehalase purified from an insect larvae. Insect Biochemistry and Molecular Biology, 2004, 34(10): 1089-1099.

[63] DE ALMEIDA F M, BONINI B M, BETON D, JORGE J A, TERENZI A M, DA SILVA A M. Heterologous expression in Escherichia coli of Neurospora crassa neutral trehalase as an active enzyme. Protein expression and purification, 2009, 65(2): 185-189.

[64] 马龙. 棉铃虫几丁质合成相关基因特性及昆虫生长调节剂对其影响研究[D]. 杨凌: 西北农林科技大学, 2014.

MA L. Characterization of genes related to chitin biosynthesis and influence of insect growth regulators on genes in cotton bollworm, Helicoverpa armigera[D]. Yangling: Northwest A&F University, 2014. (in Chinese)

[65] 赵丽娜. 海藻糖酶和海藻糖合成酶基因对褐飞虱海藻糖代谢途径关键基因的调控研究[D]. 杭州: 杭州师范大学, 2014.

ZHAO L N. Regulating effects of trehalase and TPS on the key genes in the pathway of trehalose metabolic in Nilaparvata lugens[D]. Hangzhou: Hangzhou Normal University, 2014. (in Chinese)

[66] SHI Z K, LIU X, XU Q, QIN Z, WANG S, ZHANG F, WANG S G, TANG B. Two novel soluble trehalase genes cloned from Harmonia axyridis and regulation of the enzyme in a rapid changing temperature. Comparative Biochemistry and Physiology, 2016, 198: 10-18.

[67] PARKINSON N M, CONYERS C M, KEEN J N, MACNICOLL A D, SMITH I, WEAVER R J. cDNAs encoding large venom proteins from the parasitoid wasp Pimpla hypochondriaca identified by random sequence analysis. Comparative Biochemistry and Physiology, 2003, 134(4): 513-520.

[68] LEE J H, SAITO S, MORI H, NISHIMOTO M, OKUYAMA M, KIM D, WONGCHAWALIT J, KIMURA A, CHIBA S. Molecular cloning of cDNA for trehalase from the European honeybee, Apis mellifera L. and its heterologous expression in Pichia pastoris. Bioscience, Biotechnology and Biochemistry, 2007, 71(9): 2256-2265.

[69] TATUN N, SINGTRIPOP T, SAKURAI S. Dual control of midgut trehalase activity by 20-hydroxyecdysone and an inhibitory factor in the bamboo borer Omphisa fuscidentalis Hampson. Journal of Insect Physiology, 2008, 54(2): 351-357.

[70] 张倩, 鲁鼎浩, 蒲建, 吴敏, 韩召军. 灰飞虱海藻糖酶基因的克隆及RNA干扰效应. 昆虫学报, 2012, 55(8): 911-920.

Zhang Q, Lu D H, Pu J, Wu M, Han Z J. Cloning and RNA interference effects of trehalase genes in Laodelphax striatellus (Homoptera: Delphacidae). Acta Entomologica Sinica, 2012, 55(8): 911-920.(in Chinese)

[71] 刘晓健, 孙亚文, 崔淼, 马恩波, 张建珍. 飞蝗海藻糖酶基因的分子特性及功能. 中国农业科学, 2016, 49(22): 4375-4386.

LIU X J, SUN Y W, CUI M, MA E B, ZHANG J Z. Molecular characteristics and functional analysis of trehalase genes in Locusta migratoria. Scientia Agricultura Sinica, 2016, 49(22): 4375-4386. (in Chinese)

[72] CHEN X F, TIAN H G, ZOU L Z, TANG B, HU J, ZHANG W Q. Disruption of Spodoptera exigua larval development by silencing chitin synthase gene A with RNA interference. Bulletin of Entomological Research, 2008, 98(6): 613-619.

[73] CHEN X F, YANG X, KUMAR N S, TANG B, SUN X J, QIU X M, HU J, ZHANG W Q. The class A chitin synthase gene of Spodoptera exigua: Molecular cloning and expression patterns. Insect Biochemistry and Molecular Biology, 2007, 37(5): 409-417.

[74] WANG Y, FAN H W, HUANG H J, XUE J, WU W J, BAO Y Y, XU H J, ZHU Z R, CHENG J A, ZHANG C X. Chitin synthase 1 gene and its two alternative splicing variants from two sap-sucking insects, Nilaparvata lugens and Laodelphax striatellus (Hemiptera: Delphacidae). Insect Biochemistry and Molecular Biology, 2012, 42(9): 637-646.

[75] MERZENDORFER H, ZIMOCH L. Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinase. The Journal of Experimental Biology, 2005, 206(24): 4393-4412.

[76] ARAKANE Y, HOGENKAMP D G, ZHU Y C, KRAMER K J, SPECHT C A, BEEMAN R W, KANOST MR, MUTHUKRISHNAN S. Characterization of two chitin synthase genes of the red ?our beetle, Tribolium castaneum, and alternate exon usage in one of the genes during development. Insect Biochemistry and Molecular Biology, 2004, 34(3): 291-304.

[77] CANDY D J, KILBY B A. Studies on chitin synthesis in the desert locust. Journal of Experimental Biology, 1962, 39: 129-140.

[78] KRAMER K J, DZIADIK-TURNER C, KOGA D. Chitin metabolism in insects. Comprehensive Insect PhysiologyBiochemistry Pharmacology, 1985, 3: 75-115.

[79] KRAMER K J, MUTHUKRISHNAN S. Chitin metabolism in insects//Gilbert L I, Iatrou K, Gill S S. Comprehensive Molecular Insect Science. Elsevier, Oxford, 2005, 4: 111-144.

[80] ZHANG L, WANG H J, CHEN, J Y, SHEN Q D, WANG S G, XU H X, TANG B. Glycogen phosphorylase and glycogen synthase: gene cloning and expression analysis reveal their role in trehalose metabolism in the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Journal of Insect Science, 2017, 17(2): 42.

[81] XIONG K C,WANG J,LI J H,DENG Y Q,PU P,FAN H,LIU Y H. RNA interference of a trehalose-6-phosphate synthase gene reveals its role during larval-pupal metamorphosis in Bactrocera minax (Diptera: Tephritidae). Journal of Insect Physiology, 2016, 91/92: 84-92.

[82] TIAN H G, PENG H, YAO Q, CHEN H X, XIE Q, TANG B, ZHANG W Q. Developmental regulation of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-midgut gene. PLoS One, 2009, 4(7): e6225.

[83] ARAKANE Y, SPECHT C A, KRAMER K J, MUTHUKRISHNAN S, BEEMAN R W. Chitin synthases are required for survival, fecundity and egg hatch in the red ?our beetle, Tribolium castaneum. InsectBiochemistry and Molecular Biology, 2008, 38(10): 959-962.

[84] 杨艳, 陈玲玲, 曾宪垠, 张红雨. 海藻糖酶抑制剂 —— 一种新型农药先导结构. 生命的化学, 2005, 25(3): 196-198.

YANG Y, CHEN L L, ZENG X G, ZHANG H Y. Trehalose inhibitor - A new pesticide pilot structure. Chemistry of Life, 2005, 25(3): 196-198. (in Chinese)

[85] 席羽. 褐飞虱几丁质降解酶系基因家族分析[D]. 杭州: 浙江大学, 2014.

Xi Y. Analyses of chitinolytic enzyme gene families in Nilaparata lugens[D]. Hangzhou: Zhejiang University, 2014. (in Chinese)

[86] ARAKANE Y, DIXIT R, BEGUM K, PARK Y, SPECHT C A, MERZENDORFER H, KRAMER K J, MUTHUKRISHNAN S, BEEMAN R W. Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. InsectBiochemistry and Molecular Biology, 2009, 39(5/6): 355-365.

[87] XI Y, PAN P L, ZHANG C X. The β-N-acetylhexosaminidase gene family in the brown planthopper, Nilaparvata lugens. Insect Molecular Biology, 2015, 24(6): 601-610.

[88] ARAKANE Y, MUTHUKRISHNAN S, KRAMER K J, SPECHT C A, TOMOYASU Y, LORENZEN M D, KANOST M, BEEMAN R W. The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Molecular Biology, 2005, 14(5): 453-463.

[89] DEVINE W P, LUBARSKY B, SHAW K, LUSCHNIG S, MESSINA L, KRASNOW M A. Requirement for chitin biosynthesis in epithelial tube morphogenesis. Proceedings of the National Academy of Sciences United States of America, 2005, 102(47): 17014-17019.

[90] QU M, YANG Q. A novel alternative splicing site of class A chitin synthase from the insect Ostrinia furnacalise-gene organization, expression pattern and physiological signi?cance. InsectBiochemistry and Molecular Biology, 2011, 41(12): 923-931.

[91] ZHANG L, QIU L Y, YANG H L, WANG H J, ZHOU M, WANG S G, TANG B. Study on the effect of wing bud chitin metabolism and its developmental network genes in the brown planthopper, Nilaparvata lugens by knockdown TRE gene. Frontiers in Physiology, 2017, 8: 750.

[92] IWASA T, YAMAAMOTO H, SHIBATA M. Studies on validamycins, new antibiotics. I. Streptomyces hygroscopicus var. limoneus nov. var., validamycin-producing organism. The Japanese Journal of Antibiotics, 1970, 23(6): 595-602.

[93] ASANO N, YAMAGUCHI T, KAMEDA Y, MATSUI K. Effect of validamycins on glycohydrolases of Rhizoctonia solania. The Journal of Antibiotics, 1987, 40(4): 526-532.

[94] KAMEDA Y, ASANO N, YAMAGUCHI T, MATSUI K. Validoxylamines as trehalase inhibitor. The Journal of Antibiotics, 1987, 40(4): 563-565.

[95] 申屠旭萍, 俞晓平, 吕仲贤, 陈建明, 郑许松, 徐红星, 张珏锋, 陈列忠. 海藻糖酶抑制剂——井冈霉亚基胺A的研究进展//当代昆虫学研究—中国昆虫学会成立60周年纪念大会暨学术讨论会论文集, 2004.

SHENTu X P, YU X P, LÜ Z X, CHEN J M, ZHENG X S, XU H X, ZHANG J F, CHEN L Z. Research progress of trehalosidase inhibitors – validoxylamine A//Contemporary Entomological Research - The 60th Anniversary of the Chinese Entomological Society and the Proceedings of the Symposium, 2004. (in Chinese)

[96] 池明姬. 海藻糖酶—杀虫剂的作用靶标. 世界农药, 2003, 25(5): 34-36.

CHI M J. Trehalase-insecticide target. World Pesticides, 2003, 25(5): 34-36. (in Chinese)

[97] RHINEHART B L, ROBINSON K M, LIU P S, PAYNE A J, WHEATLEY M E, WAGNER S R. Inhibition of intestinal disaccharidases and suppression of blood glucose by a new alpha- glucohydrolase inhibitor-MDL 25,637. The Journal of Pharmacology and Experimental Therapeutics, 1987, 241(3): 915-920.

[98] ANDO O, SATAKE H, ITOIi K, SATO A, NAKAJIMA M, TAKAHASHI S, HARUYAMA H, OHKUMA Y, KINOSHITA T, ENOKITA R. Trehazolin, a new trehalase inhibitor. The Journal of Antibiotics, 1991, 44(10): 1165-1168.

[99] LIU C L, DUNAWAY-MARIANO D, MARIANO P S. Rational design of reversible inhibitors for trehalose-6-phosphate phosphatases. European Journal of Medicinal Chemistry, 2017, 128: 274-286.