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Smurf participates in Helicoverpa armigera diapause by regulating the transforming growth factor-βsignaling pathway

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Insect Science 2022年第5期29卷 1251-1261页

作者： Haiyin Li Qin Lu Yan Li Yufang Yan Zhiyong Yin Jianjun Guo Weihua Xu Guizhou Provincial Key Laboratory for Agricultural Pest Management of the Mountainous Region Institute of EntomologyGuizhou UniversityGuiyangChina State Key Laboratory of Biocontrol School of Life SciencesSun Yat-sen UniversityGuangzhouChina

diapause,an important strategy used by insects to avoid adverse environments,is regulated by various cell signaling pathways.The results of our previous studies demonstrated that the transforming growth factor-β(TGF-β)signaling pathway regulated pupal diapause in Helicoverpa armigera,which was accompanied by downregulation of proteins in TGF-βsignaling.However,to date the mechanism underlying this phenomenon remains unknown.Here,we cloned the E3 ubiquitin ligases gene Smurf.In vitro experiments showed that Smurf directly bound to TGF-βreceptor type I(TGFβRI)and Smad2.Overexpressing Smurf promoted ubiquitination of TGFβRI and Smad2,thereby downregulating their protein levels.Conversely,silencing of the Smurf gene suppressed ubiquitination of TGFβRI and Smad2 thereby increasing their protein levels.Results from in vivo co-immunoprecipitation assays revealed that the binding of Smurf to TGFβRI or Smad2 was stronger in diapause pupae than in nondiapause pupae.Injection of Smurf inhibitor A01 into diapause pupae markedly upregulated expression of TGFβRI and Smad2 proteins,leading to resumption of development in diapause pupae.Taken together,these findings suggested that ubiquitin ligase E3 Smurf participated in H.armigera diapause by regulating TGF-βsignaling,and thus could be playing a crucial role in insect diapause.

关键词： degradation diapause Helicoverpa armigera Smurf TGF-βsignaling ubiquitination

Physiological mitochondrial ROS regulate diapause by enhancing HSP60/Lon complex stability in Helicoverpa armigera

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Journal of Integrative Agriculture 2022年第6期21卷 1703-1712页

作者： ZHANG Xiao-shuai SU Xiao-long GENG Shao-lei WANG Zheng-hao School of Life Sciences Sun Yat-Sen UniversityGuangzhou 510006P.R.China

diapause is a long-lived stage which has evolved into an important strategy for insects to circumvent extreme environments.In the pupal stage,Helicoverpa armigera can enter diapause,a state characterized by significantly decreased metabolic activity and enhanced stress resistance,to survive cold winters.Previous studies have shown that reactive oxygen species(ROS)can promote the diapause process by regulating a distinct insulin signaling pathway.However,the source of ROS in the diapause-destined pupal brains and mechanisms by which ROS regulate diapause are still unknown.In this study,we showed that diapause-destined pupal brains accumulated high levels of mitochondrial ROS(mtROS)and total ROS during the diapause process,suggesting that mitochondria are the main source of ROS in diapause-destined pupal brains.In addition,injection of 2-deoxy-D-glucose(DOG),a glucose metabolism inhibitor,could delay pupal development by elevating mtROS levels in the nondiapause-destined pupal brains.Furthermore,the injection of a metabolite mixture to increase metabolic activity could avert the diapause process in diapause-destined pupae by decreasing mtROS levels.We also found that ROS could activate HSP60 expression and promote the stability of the HSP60-Lon complex,increasing its ability to degrade mitochondrial transcription factor A(TFAM)and decreasing mitochondrial activity or biogenesis under oxidative stress.Thus,this study illustrated the beneficial function of ROS in diapause or lifespan extension by decreasing mitochondrial activity.

关键词： mtROS diapause HSP60 Helicoverpa armigera

diapause affects cuticular hydrocarbon composition and mating behavior of both sexes in Drosophila montana

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Insect Science 2020年第2期27卷 304-316页

作者： Outi Ala-Honkola Hannele Kauranen Venera Tyukmaeva Fabian A.Boetzl Anneli Hoikkala Thomas Schmitt Department of Biological and Environmental Science University of JyvaskylaJyvaskylaFinland Department of Animal Ecology and Tropical Biology BiocenterUniversity of WurzburgWurzburgGermany

Envipnmental cues,mainly photoperiod and temperature,are known to control female adult reproductive diapause in several insect species.diapause enhances female survival during adverse conditions and postpones progeny production to the favorable season.Male diapause(a reversible inability to inseminate receptive females)has been studied much less than female diapause.However,if the males maximized their chances to fertilize females while minimizing their energy expenditure,they would be expected to be in diapause at the same time as females.We investigated Drosophila montana male mating bchavior under short-day conditions that induce diapause in females and found the males to be reproductively inactive.We also found that males reared under long-day conditions(reproducing individuals)court reproducing postdiapause fermales,but not diapausing ones.The diapausing fies of both sexes had more long-chain and less short-chain hydrocarbons on their cuticle than the reproducing ones,which presumably increase their survival under stressful conditions,but at the same time decrease their attractiveness.Our study shows that the mating behavior of females and males is well coordinated during and afier overwintering and it also gives support to the dual role of insect cuticular hydrocarbons in adaptation and mate choice.

关键词： cuticular hydrocarbon diapause Drosophila male choice male reproduction

Changes in glutathione redox cycle during diapause determination and termination in the bivoltine silkworm, Bombyx moil

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Insect Science 2014年第1期21卷 39-46页

作者： Lin-Chuan Zhao Yi-Sheng Hou Yang-Hu Sima College of Biological and Basic Medicine Sciences Soochow University Suzhou Jiangsu Province China

To explore whether glutathione regulates diapause determination and termina tion in the bivoltine silkworm Bombyx mori, we monitored the changes in glutathione redox cycle in the ovary of both diapanse and nondiapauseegg producers, as well as those in dia pause eggs incubated at different temperatures. The activity ofthioredoxin reductase （TrxR） was detected in ovaries but not in eggs, while neither ovaries nor eggs showed activity of glutathione peroxidase. A lower reduced glutathione/oxidized glutathione （GSH/GSSG） ratio was observed in the ovary of diapauseegg producers, due to weaker reduction of oxidized glutathione （GSSG） to the reduced glutathione （GSH） catalyzed by glutathione reductase （GR） and TrxR. This indicates an oxidative shift in the glutathione redox cy cle during diapause determination. Compared with the 25℃treated diapause eggs, the 5℃treated diapause eggs showed lower GSH/GSSG ratio, a result of stronger oxidation of GSH catalyzed by thioredoxin peroxidase and weaker reduction of GSSG catalyzed by GR. Our study demonstrated the important regulatory role of glutathione in diapause determination and termination of the bivoltine silkworm.

关键词： Bombyx mori determination diapause glutathione redox cycle termination

diapause induction and termination in a commonly univoltine leaf beetle （ Phratora vulgatissima）

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Insect Science 2011年第4期18卷 443-450页

作者： Peter Dalin Department of Ecology Swedish University of Agricultural Sciences Uppsela Sweden

TheleafbeetlePhratoravulgatissima（Linnaeus 1758）iscommonlyunivoltine in south-central Sweden but may sometimes initiate a partial second generation. The current study was set out to investigate under what abiotic conditions the beetles initiate a second generation. Using climate chamber experiments, the beetles were shown to have a facultative reproductive diapause induced by declining day-length. The critical day-length （CDL） for diapause induction was estimated to be 18 h and 10 min. In the field, firstgeneration beetles developing to adulthood before August in 2009 became reproductively active and produced a second generation, but most individuals emerged later and were in reproductive diapause. P vulgatissima overwinter as adults and diapause was shown to be maintained until mid-winter in 2008/2009. The cumulative temperature requirement for oviposition after diapause termination was estimated to be 222 day-degrees with a 5.5℃ temperature threshold. Three different day-degree models that were developed to predict the phenology of female oviposition in the spring were validated by comparing model results with field data on the timing of oviposition in previous years. The study suggests that P vulgatissima may initiate a second generation in Sweden if development of the first generation is completed before August. Warmer spring and summer temperatures due to ongoing climate change may cause advanced insect phenology and faster completion of insect life-cycles at northern latitudes, which will affect the proportion of insects that initiate a second generation.

关键词： climate change diapause insect pests population dynamics seasonal adaptations voltinism

Molecular characterization of DnaJ 5 homologs in silkworm Bombyx mori and its expression during egg diapause

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Insect Science 2014年第6期21卷 677-686页

作者： Sasibhushan Sirigineedi Esvaran Vijayagowri Geetha N. Murthy Guruprasada Rao Kangayam M. Ponnuvel Genomics Division Seribiotech Research Laboratory Carmelaram Post Kodathi Bangalore 560035 Karnataka India

A comparison of the cDNA sequences （1 056 bp） of Bombyx mori DnaJ 5 homolog with B. mori genome revealed that unlike in other Hsps, it has an intron of 234 bp. The DnaJ 5 homolog contains 351 amino acids, of which 70 contain the conserved DnaJ domain at the N-terminal end. This homolog orB. mori has all desirable functional domains similar to other insects, and the 13 different DnaJ homologs identified in B. mori genome were distributed on different chromosomes. The expressed sequence tag database analysis of Hsp40 gene expression revealed higher expression in wing disc followed by diapause-induced eggs. Microarray analysis revealed higher expression of DnaJ 5 homolog at 18th h after oviposition in diapause-induced eggs. Further validation of DnaJ 5 expression through qPCR in diapause-induced and nondiapause eggs at different time intervals revealed higher expression in diapause eggs at 18 and 24 h after oviposition, which coincided with the expression of Hsp70 as the Hsp 40 is its co-chaperone. This study thus provides an outline of the genome organization of lisp40 gene, and its role in egg diapause induction in B. mori.

关键词： Bombyx mori diapause DnaJ exon Hsp40 intron

Seasonal and geographical variation in diapause and cold hardiness of the Asian corn borer, Ostrinia furnacalis

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Insect Science 2015年第4期22卷 578-586页

作者： Hai-Cui Xie Dun-Song Li Hong-Gang Zhang Charles E. Mason Zhen-Ying Wang Xin Lu Wan-Zhi Cai Kang-Lai He The State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection Chinese Academy of Agricultural Sciences Beijing 100193 Department of Entomology China Agriculture University Beijing 100193 The Plant Protection Research Institute Guangdong Academy of Agricultural Sciences Guangzhou 510640 China Department of Entomology and Wildlife Ecology University of Delaware 531 S College Ave Rm 250 Newark DE 19716-2160 USA Institute of Plant Protection Jilin Academy of Agricultural Sciences Gongzhuling 136100 Jilin China

Asian corn borer, Ostrinia furnacalis （Guenee）, is a key corn pest in the Asian-Western Pacific countries. It overwinters as flail-grown larvae in plant stalks or in a spun-silk covering located in the plant debris in the temperate regions of China. Supercooling point （SCP） and survival rate after low sub-zero temperature treatment were assessed for field-collected populations in the laboratory using a cool bath with a 1 ℃/min cooling rate until -40℃. Mean SCPs were varied among geographical populations, with a significant decline from -22.7℃ of Haikou, the multivoltine tropical population in the south, to -28.5℃ of Gongzhuling, the univoltine temperate population in the northeast of China. In addition, there was more than 1℃ difference in SCP between Gongzhuling univoltine and bivoltine populations that were from the same geographic origin. Mean SCPs of the Guangzhou population fluctuated over the year, with significantly lower SCPs in winter than in other seasons, which correlated with a significantly higher proportion of diapausing larvae in winter than in other seasons. Over 41% of overwintering larvae from the northeast population could withstand to be supercooled for a few minutes to the low sub-zero temperature of-40℃, but only 6.7% of their southern counterparts did so. The findings from this study suggest that O. furnacalis mostly takes advantage of freeze avoidance as diapausing larvae for overwintering in the southern region, whereas it exhibits freeze tolerance in diapause in the northeastern region.

关键词： cold hardiness diapause geographical population Ostriniafurnacalis overwintering seasonality

Identification of diapause-associated proteins in migratory locust, Locusta migratoria L.(Orthoptera: Acridoidea) by label-free quantification analysis

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Journal of Integrative Agriculture 2019年第11期18卷 2579-2588页

作者： CUI Dong-nan TU Xiong-bing HAO Kun Aftab Raza CHEN Jun Mark McNeill ZHANG Ze-hua State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant ProtectionChinese Academy of Agricultural SciencesBeijing 100193P.R.China AgResearch Ltd. Christchurch 8140New Zealand

Maternal photoperiodic response is a key factor that affects offspring diapause in migratory locust,Locusta migratoria L.(Orthoptera:Acridoidea).Although many aspects of insect diapause have been studied,little is known about the molecular mechanisms of maternal photoperiodic response that influence diapause regulation.To gain insight into the possible mechanisms of maternal photoperiod influence on diapause regulation,proteomics data by label-free quantification analysis were generated from non-diapause and diapause eggs.A total of 175 proteins were differentially expressed between diapause and non-diapause eggs.Among them,24 proteins were upregulated,and 151 proteins were downregulated.Gene Ontology(GO)analysis and Kyoto Encyclopedia of Genes and Genomes(KEGG)pathway enrichments were performed on all differentially expressed proteins(DEPs)and showed that peroxisome,insect hormone biosynthesis,and longevity regulating pathway may be related to diapause of migratory locust.Furthermore,we used qRT-PCR to verify some results of the proteomic analysis.Proteins such as hexamerin-like protein 4,juvenile hormone epoxide hydrolase 1(JHEH1),cytochrome P450 and heat shock protein(HSP)20.7 were predicted to be involved in diapause.This study provides an important reference for future research that will explore the mechanisms of diapause induced by maternal effects in migratory locust.

关键词： diapause proteome maternal effect molecular mechanism

Transcriptomic and proteomic analysis of Locusta migratoria eggs at different embryonic stages: Comparison for diapause and non-diapause regimes

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Journal of Integrative Agriculture 2017年第8期16卷 1777-1788页

作者： HAO Kun WANG Jie TU Xiong-bing Douglas W.Whitman ZHANG Ze-hua State Key Laboratory for Biology of Plant Diseases and Insect Pests Institute of Plant Protection Chinese Academy of Agricultural Sciences School of Biological Sciences Illinois State University

Temperate-zone insects typically survive winter by entering diapause. Although many aspects of insect diapause have been studied, the underlying molecular mechanism of insect diapause is not well understood. Here we report the results of the transcriptional and translational differences of migratory locust eggs at different embryonic states using diapause （low temperature） and non-diapause （high temperature） regimes. Compared with non-diapause eggs at 100 degree-days （N2） treatment, 29671 transcripts and 296 proteins were differentially expressed at the diapause maintenance stage （D2）. While compared with 150 degree-days （N3） treatment, 45 922 transcripts and 404 proteins were differentially expressed in the post-diapause stage （D3）. Among them, 51 and 102 transcripts had concurrent transcription and translation profiles in D2 vs. N2 and D3 vs. N3 treatments, respectively. Analysis of Gene Ontology categorized these genes and proteins into three categories： biological processes, cellular components, and molecular functions. Biological pathway analysis indicat- ed that three pathways：（1） insect hormone biosynthesis （KEGG： Map 00981）, （2） the insulin signaling pathway （KEGG： Map 04910）, and （3） the peroxisome proliferator-activated receptor （PPAR） signaling pathway （KEGG： Map 03320） play an important role in locust diapause regulation. Most of these transcripts and proteins were up-regulated in the diapause treatments, and were highly linked to juvenile hormone biosynthesis, insulin and PPAR signaling pathways, suggesting these three pathways may be Jnvolved Jn diapause and development regulation. This study demonstrates the applicability of high-throughput omics tools to identify biochemical pathways linked to diapause in locust egg development. In addition, it reveals that cellular metabolism in diapause eggs is more inactive than in non-diapause eggs, and most of the down-reg- ulated enzymes and pathways are related to reduce energy loss.

关键词： Locusta migratoria diapause transcriptome proteome molecular mechanism