Research progress on heat shock transcription factors in insects

doi:10.3785/j.issn.1008-9209.2022.04.061

Journal of Zhejiang University (Agriculture and Life Sciences)

2022, Vol. 48

Issue (6): 701-708 DOI: 10.3785/j.issn.1008-9209.2022.04.061

Reviews

Research progress on heat shock transcription factors in insects

Chao ZHANG^1,²(

),Ni WANG^1,²,Zheyi SHI^1,²,Min CHEN^1,²,Wenwu ZHOU^1,²,Ying ZHOU²,Zengrong ZHU^1,²(

)

^1.Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China
^2.Hainan Institute of Zhejiang University, Sanya 572025, Hainan, China

Download:

HTML

HTML ( )

PDF(1514KB)
Export: BibTeX | EndNote (RIS)

Abstract

Insects are capable of inducing the production of heat shock proteins when exposed to environmental stresses or under specific physiological conditions such as diapause. The transcriptional activation of heat shock proteins is usually controlled by the heat shock transcription factor (HSF), a class of transcription factors that are widely present in the organism. There are numerous HSF genes in plants and mammalian species, while previous studies suggested that many insects only had single HSF gene. Under normal conditions, HSF proteins are often present in the inactive form in cells, and they are activated upon shock, and then transferred to the nucleus, where they bind to specific functional domains of target genes and eventually activate the transcription of target genes to improve the tolerance of the whole organism. This paper reviewed the research progress on the basic structure, transcriptional regulation, and biological function of HSF in insects to deepen the understanding of the regulatory role of HSF in stress response mechanisms of insects, and provide new ideas for agroforestry pest control.

Key words： heat shock response heat shock transcription factor insect stress response function

Received: 06 April 2022 Published: 27 December 2022

CLC:

Q 966

Corresponding Authors: Zengrong ZHU E-mail: chaozh@zju.edu.cn;zrzhu@zju.edu.cn

	Service
	E-mail this article
	Add to my bookshelf
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors
	Chao ZHANG
	Ni WANG
	Zheyi SHI
	Min CHEN
	Wenwu ZHOU
	Ying ZHOU
	Zengrong ZHU

Cite this article:

Chao ZHANG,Ni WANG,Zheyi SHI,Min CHEN,Wenwu ZHOU,Ying ZHOU,Zengrong ZHU. Research progress on heat shock transcription factors in insects. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(6): 701-708.

URL:

https://www.zjujournals.com/agr/10.3785/j.issn.1008-9209.2022.04.061 OR https://www.zjujournals.com/agr/Y2022/V48/I6/701

昆虫热激转录因子的研究进展

昆虫在遭受环境胁迫或在滞育等生理状态下能够诱导机体产生热激蛋白，这些热激蛋白的转录激活通常由热激转录因子（heat shock transcription factor, HSF）控制。HSF是生物体内广泛存在的一类转录因子，其在植物和哺乳动物中数量众多，但据报道许多昆虫体内只有HSF的单个基因。在正常条件下，HSF常以非活性蛋白的形态存在，但在机体应激时HSF被激活，然后转移到细胞核内与靶基因中的特定结构域序列结合，最终激活靶基因的转录，从而提高机体耐受性。本文综述了昆虫HSF的基本结构、转录调控以及功能的研究进展，以加深对HSF在昆虫胁迫响应机制中调控作用的认识，并为农林害虫防治提供新的思路。

关键词： 热激反应, 热激转录因子, 昆虫, 胁迫反应, 功能

Fig. 1 General structure of HSF in insectsDBD: DNA-binding domain; HR-A/B: Heptad repeat regions A and B; HR-C: Heptad repeat region of C end; TAD: Transactivation domain.

Fig. 2 Simplified model for activation and transcriptional regulation of HSF in insects

Table 1 Identified HSFs in insects and their biological functions


[1]	MA C S, MA G, PINCEBOURDE S. Survive a warming climate: insect responses to extreme high temperatures[J]. Annual Review of Entomology, 2021, 66(1): 163-184. DOI:10.1146/annurev-ento-041520-074454 doi: 10.1146/annurev-ento-041520-074454

[2]	YANG L, HUANG L F, WANG W L, et al. Effects of temperature on growth and development of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae)[J]. Environmental Entomology, 2021, 50(1): 1-11. DOI:10.1093/ee/nvaa144 doi: 10.1093/ee/nvaa144

[3]	KING A M, MACRAE T H. Insect heat shock proteins during stress and diapause[J]. Annual Review of Entomology, 2015, 60(1): 59-75. DOI:10.1146/annurev-ento-011613-162107 doi: 10.1146/annurev-ento-011613-162107

[4]	ROOS-MATTJUS P, SISTONEN L. Interplay between mammalian heat shock factors 1 and 2 in physiology and pathology[J]. The FEBS Journal, 2021.

[5]	FUJIKAKE N, NAGAI Y, POPIEL H A, et al. Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress[J]. FEBS Letters, 2005, 579(17): 3842-3848. DOI:10.1016/j.febslet.2005.05.074 doi: 10.1016/j.febslet.2005.05.074

[6]	NEUDEGGER T, VERGHESE J, HAYER-HARTL M, et al. Structure of human heat-shock transcription factor 1 in complex with DNA[J]. Nature Structural & Molecular Biology, 2016, 23(2): 140-146. DOI:10.1038/nsmb.3149 doi: 10.1038/nsmb.3149

[7]	VUISTER G W, KIM S J, OROSZ A, et al. Solution structure of the DNA-binding domain of Drosophila heat shock transcription factor[J]. Nature Structural Biology, 1994, 1(9): 605-614. DOI:10.1038/nsb0994-605 doi: 10.1038/nsb0994-605

[8]	FENG N, FENG H, WANG S, et al. Structures of heat shock factor trimers bound to DNA[J]. iScience, 2021, 24(9): 102951. DOI:10.1016/j.isci.2021.102951 doi: 10.1016/j.isci.2021.102951

[9]	CICERO M P, HUBL S T, HARRISON C J, et al. The wing in yeast heat shock transcription factor (HSF) DNA-binding domain is required for full activity[J]. Nucleic Acids Research, 2001, 29(8): 1715-1723. DOI:10.1093/nar/29.8.1715 doi: 10.1093/nar/29.8.1715

[10]	DONG B S, JAEGER A M, THIELE D J. Inhibiting heat shock factor 1 in cancer: a unique therapeutic opportunity[J]. Trends in Pharmacological Sciences, 2019, 40(12): 986-1005. DOI:10.1016/j.tips.2019.10.008 doi: 10.1016/j.tips.2019.10.008

[11]	WANG G, CAO P X, FAN Y M, et al. Emerging roles of HSF1 in cancer: cellular and molecular episodes[J]. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer, 2020, 1874(1): 188390. DOI:10.1016/j.bbcan.2020.188390 doi: 10.1016/j.bbcan.2020.188390

[12]	WISNIEWSKI J, OROSZ A, ALLADA R, et al. The C-terminal region of Drosophila heat shock factor (HSF) contains a constitutively functional transactivation domain[J]. Nucleic Acids Research, 1996, 24(2): 367-374. DOI:10.1093/nar/24.2.367 doi: 10.1093/nar/24.2.367

[13]	KMIECIK S W, BRETON L L, MAYER M P. Feedback regulation of heat shock factor 1 (Hsf1) activity by Hsp70-mediated trimer unzipping and dissociation from DNA[J]. The EMBO Journal, 2020, 39(14): e104096. DOI:10.15252/embj.2019104096 doi: 10.15252/embj.2019104096

[14]	ANDRÁSI N, PETTKÓ-SZANDTNER A, SZABADOS L. Diversity of plant heat shock factors: regulation, interactions, and functions[J]. Journal of Experimental Botany, 2021, 72(5): 1558-1575. DOI:10.1093/jxb/eraa576 doi: 10.1093/jxb/eraa576

[15]	ÅKERFELT M, MORIMOTO R I, SISTONEN L. Heat shock factors: integrators of cell stress, development and lifespan[J]. Nature Reviews-Molecular Cell Biology, 2010, 11(8): 545-555. DOI:10.1038/nrm2938 doi: 10.1038/nrm2938

[16]	ZHONG M, KIM S J, WU C. Sensitivity of Drosophila heat shock transcription factor to low pH[J]. The Journal of Biological Chemistry, 1999, 274(5): 3135-3140. DOI:10.1074/jbc.274.5.3135 doi: 10.1074/jbc.274.5.3135

[17]	GUERTIN M J, LIS J T. Chromatin landscape dictates HSF binding to target DNA elements[J]. PLoS Genetics, 2010, 6(9): e1001114. DOI:10.1371/journal.pgen.1001114 doi: 10.1371/journal.pgen.1001114

[18]	JAEGER A M, MAKLEY L N, GESTWICKI J E, et al. Genomic heat shock element sequences drive cooperative human heat shock factor 1 DNA binding and selectivity[J]. The Journal of Biological Chemistry, 2014, 289(44): 30459-30469. DOI:10.1074/jbc.M114.591578 doi: 10.1074/jbc.M114.591578

[19]	ACUNZO J, KATSOGIANNOU M, ROCCHI P. Small heat shock proteins HSP27 (HspB1), αB-crystallin (HspB5) and HSP22 (HspB8) as regulators of cell death[J]. The International Journal of Biochemistry & Cell Biology, 2012, 44(10): 1622-1631. DOI:10.1016/j.biocel.2012.04.002 doi: 10.1016/j.biocel.2012.04.002

[20]	ZHAO Y M, SUN H, LU J, et al. Lifespan extension and elevated hsp gene expression in Drosophila caused by histone deacetylase inhibitors[J]. Journal of Experimental Biology, 2005, 208(4): 697-705. DOI:10.1242/jeb.01439 doi: 10.1242/jeb.01439

[21]	BOEHM A K, SAUNDERS A, WERNER J, et al. Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock[J]. Molecular and Cellular Biology, 2003, 23(21): 7628-7637. DOI:10.1128/mcb.23.21.7628-7637.2003 doi: 10.1128/mcb.23.21.7628-7637.2003

[22]	KUROP M K, HUYEN C M, KELLY J H, et al. The heat shock response and small molecule regulators[J]. European Journal of Medicinal Chemistry, 2021, 226: 113846. DOI:10.1016/j.ejmech.2021.113846 doi: 10.1016/j.ejmech.2021.113846

[23]	SARGE K D, MURPHY S P, MORIMOTO R I. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress[J]. Molecular and Cellular Biology, 1993, 13(3): 1392-1407.

[24]	WESTWOOD J T, CLOS J, WU C. Stress-induced oligomerization and chromosomal relocalization of heat-shock factor[J]. Nature, 1991, 353(6347): 822-827. DOI:10.1038/353822a0 doi: 10.1038/353822a0

[25]	OROSZ A, WISNIEWSKI J, WU C. Regulation of Drosophila heat shock factor trimerization: global sequence requirements and independence of nuclear localization[J]. Molecular and Cellular Biology, 1996, 16(12): 7018-7030.

[26]	HUANG C, WU J J, XU L, et al. Regulation of HSF1 protein stabilization: an updated review[J]. European Journal of Pharmacology, 2018, 822: 69-77. DOI:10.1016/j.ejphar.2018.01.005 doi: 10.1016/j.ejphar.2018.01.005

[27]	FRITSCH M, WU C. Phosphorylation of Drosophila heat shock transcription factor[J]. Cell Stress & Chaperones, 1999, 4(2): 102-117.

[28]	SOLOMON J M, ROSSI J M, GOLIC K, et al. Changes in hsp70 alter thermotolerance and heat-shock regulation in Drosophila [J]. The New Biologist, 1991, 3(11): 1106-1120.

[29]	MARCHLER G, WU C. Modulation of Drosophila heat shock transcription factor activity by the molecular chaperone DROJ1[J]. The EMBO Journal, 2001, 20(3): 499-509. DOI:10.1093/emboj/20.3.499 doi: 10.1093/emboj/20.3.499

[30]	JIN J S, LI Y Z, ZHOU Z S, et al. Heat shock factor is involved in regulating the transcriptional expression of two potential Hsps (AhHsp70 and AhsHsp21) and its role in heat shock response of Agasicles hygrophila [J]. Frontiers in Physiology, 2020, 11: 562204. DOI:10.3389/fphys.2020.562204 doi: 10.3389/fphys.2020.562204

[31]	CLOS J, WESTWOOD J T, BECKER P B, et al. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation[J]. Cell, 1990, 63(5): 1085-1097. DOI:10.1016/0092-8674(90)90511-c doi: 10.1016/0092-8674(90)90511-c

[32]	靳继苏.热激转录因子(Hsf)与热激蛋白基因(Hsp70、Hsp21、sHsp21)在莲草直胸跳甲高温耐受性中的作用[D].北京:中国农业科学院,2017. JIN J S. The roles of heat shock transcription factor (Hsf) and heat shock protein gene (Hsp70, Hsp21, sHsp21) on the high temperature tolerance of Agasicles hygrophila Selman and Vogt (Coleoptera: Cheysomelidae)[D]. Beijing: Chinese Academy of Agricultural Sciences, 2017. (in Chinese with English abstract)

[33]	HE F J, ZHU F, LU M X, et al. Molecular characterization of heat-induced HSP11.0 and master-regulator HSF from Cotesia chilonis and their consistent response to heat stress[J]. Insects, 2021, 12(4): 322. DOI:10.3390/insects12040322 doi: 10.3390/insects12040322

[34]	SONODA S, TSUMUKI H. Characterization of alternatively spliced transcripts encoding heat shock transcription factor in cultured cells of the cabbage armyworm, Mamestra brassicae [J]. Archives of Insect Biochemistry and Physiology, 2010, 73(1): 49-60. DOI:10.1002/arch.20339 doi: 10.1002/arch.20339

[35]	宋杰.热休克转录因子对水稻二化螟小分子量热激蛋白的调控研究[D].江苏,扬州:扬州大学,2020. DOI:10.1016/s2095-3119(19)62808-x SONG J. Regulation of heat shock transcription factor on small heat shock protein of Chilo suppressalis (Walker)[D]. Yangzhou, Jiangsu: Yangzhou University, 2020. (in Chinese with English abstract) doi: 10.1016/s2095-3119(19)62808-x

[36]	CHEN W, GENG S L, SONG Z, et al. Alternative splicing and expression analysis of HSF1 in diapause pupal brains in the cotton bollworm, Helicoverpa armigera [J]. Pest Management Science, 2019, 75(5): 1258-1269. DOI:10.1002/ps.5238 doi: 10.1002/ps.5238

[37]	覃富健,李玉娟,施静雯,等.棉铃虫中HSF1的分子克隆、选择性剪接及亚细胞定位研究[J].环境昆虫学报,2018,40(5):1078-1086. DOI:10.3969/j.issn.1674-0858.2018.05.15 QIN F J, LI Y J, SHI J W, et al. Molecular characterization, alternative splicing and subcellular localization of HSF1 in the cotton bollworm, Helicoverpa armigera [J]. Journal of Environmental Entomology, 2018, 40(5): 1078-1086. (in Chinese with English abstract) doi: 10.3969/j.issn.1674-0858.2018.05.15

[38]	KIHARA F, NIIMI T, YAMASHITA O, et al. Heat shock factor binds to heat shock elements upstream of heat shock protein 70a and Samui genes to confer transcriptional activity in Bombyx mori diapause eggs exposed to 5 ℃[J]. Insect Biochemistry and Molecular Biology, 2011, 41(11): 843-851. DOI:10.1016/j.ibmb.2011.06.006 doi: 10.1016/j.ibmb.2011.06.006

[39]	郭莉莉.入侵粉虱热激调控因子Hsf1对Hsp60表达的影响[D].河南,新乡:河南科技学院,2013. GUO L L. Heat shock regulatory factor Hsf1’s influence on Hsp60’s expression in invasion whiteflies[D]. Xinxiang, Henan: Henan Institute of Science and Technology, 2013. (in Chinese with English abstract)

[40]	CHANG Y W, WANG Y C, ZHANG X X, et al. Transcriptional regulation of small heat shock protein genes by heat shock factor 1 (HSF1) in Liriomyza trifolii under heat stress[J]. Cell Stress Chaperones, 2021, 26(5): 835-843. DOI:10.1007/s12192-021-01224-2 doi: 10.1007/s12192-021-01224-2

[41]	常亚文.三叶斑潜蝇的种间竞争优势和温度耐受性的分子机制[D].江苏,扬州:扬州大学,2021. CHANG Y W. Molecular mechanism of interspecific competitive advantage and temperature tolerance of Liriomyza trifolii [D]. Yangzhou, Jiangsu: Yangzhou University, 2021. (in Chinese with English abstract)

[42]	SANDALTZOPOULOS R, MITCHELMORE C, BONTE E, et al. Dual regulation of the Drosophila hsp26 promoter in vitro [J]. Nucleic Acids Research, 1995, 23(13): 2479-2487. DOI:10.1093/nar/23.13.2479 doi: 10.1093/nar/23.13.2479

[43]	WANG Z, LINDQUIST S. Developmentally regulated nuclear transport of transcription factors in Drosophila embryos enable the heat shock response[J]. Development, 1998, 125(23): 4841-4850.

[44]	SALAMANCA H H, FUDA N, SHI H, et al. An RNA aptamer perturbs heat shock transcription factor activity in Drosophila melanogaster [J]. Nucleic Acids Research, 2011, 39(15): 6729-6740. DOI:10.1093/nar/gkr206 doi: 10.1093/nar/gkr206

[45]	KUCHAR J, MCDONOUGH C, SACKERSON C. Heat shock factor controls expression of a non-heat shock protein gene in Drosophila embryos[J]. BioOne Complete, 2007, 78(2): 62-68. DOI:10.1893/0005-3155(2007)78 [62:RAHSFC]2.0.CO;2 doi: 10.1893/0005-3155(2007)78

[46]	JEDLICKA P, MORTIN M A, WU C. Multiple functions of Drosophila heat shock transcription factor in vivo [J]. The EMBO Journal, 1997, 16(9): 2452-2462. DOI:10.1093/emboj/16.9.2452 doi: 10.1093/emboj/16.9.2452

[47]	MERKLING S H, OVERHEUL G J, VAN MIERLO J T, et al. The heat shock response restricts virus infection in Drosophila [J]. Scientific Reports, 2015, 5: 12758. DOI:10.1038/srep12758 doi: 10.1038/srep12758

[48]	HERCUS M J, LOESCHCKE V, RATTAN S I S. Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress[J]. Biogerontology, 2003, 4(3): 149-156. DOI:10.1023/a:1024197806855 doi: 10.1023/a:1024197806855

[49]	SIRIGINEEDI S, VIJAYAGOWRI E, MURTHY G N, et al. Molecular characterization of DnaJ 5 homologs in silkworm Bombyx mori and its expression during egg diapause[J]. Insect Science, 2014, 21(6): 677-686. DOI:10.1111/1744-7917.12048 doi: 10.1111/1744-7917.12048

[50]	BAIRD N A, TURNBULL D W, JOHNSON E A. Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1[J]. The Journal of Biological Chemistry, 2006, 281(50): 38675-38681. DOI:10.1074/jbc.M608013200 doi: 10.1074/jbc.M608013200

[51]	WANG L J, ZHOU L J, ZHU Z H, et al. Differential temporal expression profiles of heat shock protein genes in Drosophila melanogaster (Diptera: Drosophilidae) under ultraviolet a radiation stress[J]. Environmental Entomology, 2014, 43(5): 1427-1434. DOI:10.1603/en13240 doi: 10.1603/en13240

[52]	AKIYAMA H, SASAKI N, HANAZAWA S, et al. Novel sterol glucosyltransferase in the animal tissue and cultured cells: evidence that glucosylceramide as glucose donor[J]. Biochimica et Biophysica Acta, 2011, 1811(5): 314-322. DOI:10.1016/j.bbalip.2011.02.005 doi: 10.1016/j.bbalip.2011.02.005

[53]	AKIYAMA H, IDE M, NAGATSUKA Y, et al. Glucocerebrosidases catalyze a transgalactosylation reaction that yields a newly-identified brain sterol metabolite, galactosylated cholesterol[J]. The Journal of Biological Chemistry, 2020, 295(16): 5257-5277. DOI:10.1074/jbc.RA119.012502 doi: 10.1074/jbc.RA119.012502

[54]	FRANCO R, SÁNCHEZ-ARIAS J A, NAVARRO G, et al. Glucocerebrosidase mutations and synucleinopathies. Potential role of sterylglucosides and relevance of studying both GBA1 and GBA2 genes[J]. Frontiers in Neuroanatomy, 2018, 12: 52. DOI:10.3389/fnana.2018.00052 doi: 10.3389/fnana.2018.00052

[55]	BARNA J, CSERMELY P, VELLAI T. Roles of heat shock factor 1 beyond the heat shock response[J]. Cellular and Molecular Life Sciences, 2018, 75(16): 2897-2916. DOI:10.1007/s00018-018-2836-6 doi: 10.1007/s00018-018-2836-6

[1]	Yudong QUAN,Kongming WU. Research progress of vegetative insecticidal protein Vip3 insect-resistant transgenic crops[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(6): 672-682.

[2]	Hongji TAN,Yanming GAO,Jianshe LI,Wenlu WEI. Effects of different functional fertilizers on quality, yield and substrate environment of substrate-grown cherry tomatoes[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(4): 434-442.

[3]	Shuai TANG,Zhe XU,Wuyun Lü,Qi TONG,Yu XIAO,Zhengyi WANG. Functional analysis of the putative ribosome biogenesis factor MoRei1in Magnaporthe oryzae[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(4): 443-452.

[4]	Yueliang BAI,Wenwu ZHOU,Zengrong ZHU. Effects of globa l warming on insect natural enemies[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(3): 269-278.

[5]	Hyunuk KANG,Hui ZHOU,Yushan YE,Zhonghua LIU,Yuede WEI,Jiangfan YANG,Eunhye KIM,Puming HE,Bo LI,Yuanyuan WU,Youying TU. Effects and mechanisms of Tieguanyin on the behavior of Alzheimer’s disease APP/PS1 mice[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2022, 48(1): 68-77.

[6]	Hui LI,Wei FENG,Junjie YU,Mingyin ZHANG,Chunmiao ZHOU,Yongkai TANG. Research progress of peroxiredoxingene in crustaceans[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2021, 47(3): 284-294.

[7]	Shudi ZHAO,Xiaofeng WU. Research advance of N⁶-methyladenosine (m⁶A) in insect[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2021, 47(3): 295-302.

[8]	Yunrui CHEN,Zhijun MAO,Zhaowei LI,Kai FAN. Research status and progress in structure and function of protein phosphatase 2C in plants[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2021, 47(1): 11-20.

[9]	Caiwang PENG,Songlin SUN,Xi HE,Daojun XU,Peng ZHANG. *Design and experiment of bidirectional spiral collecting device for Hermetia illucens* insect sand**[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(5): 637-646.

[10]	Xiaolian CHEN,Wenjing SONG,Quanyong ZHOU,Qiongli SONG,Zhiheng ZOU,Linxiu LIU,Lizhen HU,Qipeng WEI,Jingsheng YAN, Dalieya?AHEMAITI. *Effects of Callicarpa kwangtungensis* Chun. extract on reproductive performance, immune function, antioxidant capacity and intestinal flora of sows**[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2020, 46(3): 360-368.

[11]	Xin LIU,Yong CHEN,Lirong SHEN. Protective effects of major royal jelly proteins on reproductive function of mice during perimenopausal period[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(6): 751-759.

[12]	Elmon CHINDUDZI,Bangrong SU,Yi GUO,Zhentao ZHONG,Jane MAKONI,Shuijin ZHU,Jinhong CHEN. [J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(6): 647-656.

[13]	Fanfan WANG,Shaoxuan QU,Jinsheng LIN,Huiping LI,Lijuan HOU,Ning JIANG,Xin LUO,Lin MA,Jucai HAN. *Screening of Bacillus thuringiensis* and identification of insecticidal crystal protein gene against Bradysia difformis in mushroom cultivation**[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(2): 189-195.

[14]	Zhigang WANG,Chao XU,Xiahui LI,Shiyu LIN,Xiaxia DU,Chonglin RAN,Gang SHU. *Effects of Moringa oleifera* leaf powder on production performance, immune function and antioxidant capacity of quails**[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(2): 243-250.

[15]	Xu WEN,Xuzhou MA,Wei FAN,Xingxing LI,Yingliang ZHONG. Structural characteristics of phytoplankton functional groups in the young crab pond with different reed type rice acreages[J]. Journal of Zhejiang University (Agriculture and Life Sciences), 2019, 45(1): 85-94.

Viewed

Full text

Abstract

Cited

Shared

Discussed