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Characterization of carotenoid biosynthetic pathway genes in the pea aphid(Acyrthosiphon pisum)revealed by heterologous complementation and RNA interference assays

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Insect Science 2022年第3期29卷 645-656页

作者： Bi-Yue Ding Xiu-Cheng Xie Feng Shang Guy Smagghe Jin-Zhi Niu Jin-Jun Wang Key Laboratory of Entomology and Pest Control Engineering College of Plant ProtectionSouthwest UniversityChongqingChina International Joint Laboratory of China-Belgium on Sustainable Crop Pest ControlAcademy of Agricultural SciencesSouthwest UniversityChongqingChina Department of Plants and Crops Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

Carotenoids are involved in many essential physiological functions and are produced from geranylgeranyl pyrophosphate through synthase,desaturase,and cyclase activities.In the pea aphid(Acyrthosiphon pisum),the duplication of carotenoid biosynthetic genes,including carotenoid synthases/cyclases(ApCscA-C)and desaturases(ApCdeA-D),through horizontal gene transfer from fungi has been detected,and ApCdeB has known dehydrogenation functions.However,whether other genes contribute to aphid carotenoid biosynthesis,and its specific regulatory pathway,remains unclear.In the current study,functional analyses of seven genes were performed using heterologous complementation and RNA interference assays.The bifunctional enzymes ApCscA-C were responsible for the synthase of phytoene,and ApCscC may also have a cyclase activity.ApCdeA,ApCdeC,and ApCdeD had diverse dehydrogenation functions.ApCdeA catalyzed the enzymatic conversion of phytoene to neurosporene(three-step product),ApCdeC catalyzed the enzymatic conversion of phytoene to ζ-carotene(two-step product),and ApCdeD catalyzed the enzymatic conversion of phytoene to lycopene(four-step product).Silencing of ApCscs reduced the expression levels of ApCdes,and silencing these carotenoid biosynthetic genes reduced the α-,β-,and γ-carotene levels,as well as the total carotenoid level.The results suggest that these genes were activated and led to carotenoid biosynthesis in the pea aphid.

关键词： carotenoid biosynthesis heterologous complementary pea aphid RNA interference

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Hosting certain facultative symbionts modulates the phenoloxidase activity and immune response of the pea aphid Acyrthosiphon pisum

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Insect Science 2021年第6期28卷 1780-1799页

作者： Chen Luo Maya Belghazi Antonin Schmitz Severine Lemauf Nicolas Desneux Jean-Christophe Simon Marylene Poirie Jean-Luc Gatti Universite Cote d'Azur INRAECNRSUMR Institut Sophia Agrobiotech(ISA)Sophia AntipolisFrance INP UMR7051CNRSAix Marseille UniversiteMarseille13015France Universite Cote d'Azur INRAECNRSUMR Institut Sophia Agrobiotech(ISA)06000 NiceFrance INRAE UMR IGEPP Domaine de la MotteLe RheuFrance Present address:State Key Laboratory of Crop Stress Biology for Arid Areas College of Plant ProtectionNorthwest A&F UniversityYanglingShaanxi Province712100China

The pea aphid Acyrthosiphon pisum hosts different facultative symbionts(FS)which provide it with various benefits,such as tolerance to heat or protection against natural enemies(e.g.,fungi,parasitoid wasps).Here,we investigated whether and how the presence of certain FS could affect phenoloxidase(PO)activity,a key component of insect innate immunity,under normal and stressed conditions.For this,we used clones of A.pisum of difTerent genetic backgrounds(LLOl,YR2 and T3-8V1)lacking FS or harboring one or two(Regiella insecticola,Hamiltonella defensa,Serratia symbiotica Rickettsiella viridis).Gene expression and proteomics analyses of the aphid hemolymph indicated that the two A.pisum POs,PPOl and PP02,are expressed and translated into proteins.The level of PPO genes expression as well as the amount of PPO proteins and phenoloxidase activity in the hemolymph depended on both the aphid genotype and FS species.In particular,H.defensa and R.insecticola,but not S.symbiotica-h R.viridis,caused a sharp decrease in PO activity by interfering with both transcription and translation.The microinjection of different types of stressors(yeast,Escherichia coli,latex beads)in the YR2 lines hosting different symbionts affected the survival rate of aphids and,in most cases,also decreased the expression of PPO genes after 24 h.The amount and activity of PPO proteins varied according to the type of FS and stressor,without clear corresponding changes in gene expression.These data demonstrate that the presence of certain FS influences an important component of pea aphid immunity.

关键词： Acyrthosiphon pisum facultative symbionts hemolymph immune response pea aphid phenoloxidases

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Lipophorin receptor regulates the cuticular hydrocarbon accumulation and adult fecundity of the pea aphid Acyrthosiphon pisum

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Insect Science 2021年第4期28卷 1018-1032页

作者： Jian-Wen Qiao Yong-Liang Fan Tian-Tian Bai Bing-Jin Wu Xiao-Jin Pei Dun Wang Tong-Xian Liu State Key Laboratory of Crop Stress Biology for Arid Areas and Key Laboratory of Integrated Pest Management on Crops in Northwestern Loess Plateau Ministry of AgricultureNorthwest A&F UniversityYanglingShaanxiChina

Cuticular hydrocarbons form a barrier that protects terrestrial insects from water loss via the epicuticle.Lipophorin loads and transports lipids,including hydrocarbons,from one tissue to another.In some insects,the lipophorin receptor(LpR),which binds to lipophorin and accepts its lipid cargo,is essential for female fecundity because it mediates the incorporation of lipophorin by developing oocytes.However,it is unclear whether LpR is involved in the accumulation of cuticular hydrocarbons and its precise role in aphid reproduction remains unknown.We herein present the results of our molecular characterization,phylogenetic analysis,and functional annotation of the pea aphid(Acyrthosiphon pisum)LpR gene(ApLpR).This gene was transcribed throughout the A.pisum life cycle,but especially during the embryonic stage and in the abdominal cuticle.Furthermore,we optimized the RHA interference(RNAi)parameters by determining the ideal dose and duration for gene silencing in the pea aphid.We observed that the RNAi-based ApLpR suppression significantly decreased the internal and cuticular hydrocarbon contents as well as adult fecundity.Additionally,a deficiency in cuticular hydrocarbons increased the susceptibility of aphids to desiccation stress,with decreased survival rates under simulated drought conditions.Moreover,ApLpR expression levels significantly increased in response to the desiccation treatment.These results confirm that ApLpR is involved in transporting hydrocarbons and protecting aphids from desiccation stress.Furthermore,this gene is vital for aphid reproduction.Therefore,the ApLpR gene of A.pisum may be a novel RNAi target relevant for insect pest management.

关键词： desiccation resistance fecundity hydrocarbon lipophorin receptor pea aphid

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Identification of two clip domain serine proteases involved in the pea aphid's defense against bacterial and fungal infection

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Insect Science 2020年第4期27卷 735-744页

作者： Li Ma Feng Chen Wen Wang Lu Xu Zhi-Qiang Lu Department of Entomology College of Plant ProtectionNorthwest A&F UniversityYanglingShaanxiChina Key Laboratory of Plant Protection Resources and Pest Management Ministry of EducationNorthwest A&F UniversityYanglingShaanxiChina

Phenoloxidases(POs)are required for the pea aphid s defense against bacterial and fungal infection.Prophenoloxidases(PPOs)are protcolytically converted to its active form PO through a clip domain serine protease cascade.In this study,we identified five clip domain serine proteases in the pea aphids.The messenger RNA levels of two of them,Ap.SPLP and Ap_VP,were upregulated by Gram-positive bacterium Staphylococcus aureus and fungus Beauveha bassiana infections.Double-stranded RNA-based expression knockdown of these two genes resulted in reduced PO activity of the aphid hemolymph,higher loads of S.aureus and B.bassiana in the aphids,and lower survival rates of the aphids after infections.Our data suggest that Ap.SPLP and Ap_VP are involved in PPO activation pathway in the pea aphid.

关键词： defense pea aphid prophenoloxidase RNA interference serine proteases

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Discovery of a widespread presence bunyavirus that may have symbiont-like relationships with different species of aphids

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Insect Science 2022年第4期29卷 1120-1134页

作者： Xin An Wei Zhang Chao Ye Guy Smagghe Jin-Jun Wang Jinzhi Niu Key Laboratory of Entomology and Pest Control Engineering College of Plant ProtectionSouthwest UniversityChongqingChina International Joint Laboratory of China–Belgium on Sustainable Crop Pest Control Academy of Agricultural SciencesSouthwest UniversityChongqingChina Department of Plants and Crops Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

aphids are important agricultural pests,vectors of many plant viruses and have sophisticated relationships with symbiotic microorganisms.Abundant asymptomatic RNA viruses have been reported in aphids due to the application of RNA-seq,but aphid-virus interactions remain unclear.Bunyavirales is the most abundant RNA virus order,which can infect mammals,arthropods,and plants.However,many bunyaviruses have specific hosts,such as insects.Here,we discovered 18 viruses from 10 aphid species by RNA-seq.Importantly,a widespread presence bunyavirus,aphid bunyavirus 1(ABV-1),was determined to have a wide host range,infecting and replicating in all 10 tested aphid species.ABV-1 may be transmitted horizontally during feeding on plant leaves and vertically through reproduction.In a comparison of the physiological parameters of ABV-1high and ABV-1low strains of pea aphid,higher ABV-1 titers reduced the total nymphal duration and induced the reproduction.Moreover,viral titer significantly affected the lipid and protein contents in pea aphids.In summary,we proposed that ABV-1 may have stable symbiont-like relationships with aphids,and these observations may provide a new direction for studying bunyaviruses in aphids and establishing a model for virus-aphid interactions.

关键词： insec-specific virus pea aphid Phasmaviridae RNA virus RNAi

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Diversity, frequency, and geographic distribution of facultative bacterial endosymbionts in introduced aphid pests

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Insect Science 2017年第3期24卷 511-521页

作者： Daniela A. Sepulvedat Francisca Zepeda-Paulo Claudio C. Ramfrez Bias Lavandero Christian C. Figueroa Facultad de Ciencias Agrarias Universidad de Talca Instituto de Ciencias BiolSgicas Universidad de Talca Millennium Nucleus Centre in Molecular Ecology and Evolutionary Applications in the Agroecosystems Universidad de Talca 2 Norte 685 Talca Chile

Facultative bacterial endosymbionts in insects have been under intense study during the last years. Endosymbionts can modify the insect＇s phenotype, conferring adap- tive advantages under environmental stress. This seems particularly relevant for a group of worldwide agricultural aphid pests, because endosymbionts modify key fitness-related traits, including host plant use, protection against natural enemies and heat tolerance. Aimed to understand the role of facultative endosymbionts on the success of introduced aphid pests, the distribution and abundance of 5 facultative endosymbionts （Hamiltonella defensa, Regiella insecticola, Serratia symbiotica, Rickettsia and Spiroplasma） were stud- ied and compared in 4 cereal aphids （Sitobion avenae, Diuraphis noxia, Metopolophium dirhodum and Schizaphis graminium） and in the pea aphid Acyrthosiphon pisum complex from 2 agroclimatic zones in Chile. Overall, infections with faeultative endosymbionts exhibited a highly variable and characteristic pattern depending on the aphid species/host race and geographic zone, which could explain the success of aphid pest populations after their introduction. While S. symbiotica and H. defensa were the most frequent endosym- bionts carried by the A. pisum pea-race and A. pisum alfalfa-race aphids, respectively, the most frequent facultative endosymbiont carried by all cereal aphids was R. insecticola. Interestingly, a highly variable composition of endosymbionts carried by S. avenae was also observed between agroclimatic zones, suggesting that endosymbionts are responding differentially to abiotic variables （temperature and precipitations）. In addition, our findings constitute the first report of bacterial endosymbionts in cereal aphid species not screened before, and also the first report of aphid endosymbionts in Chile.

关键词： cereal aphids facultative bacterial endosymbionts grain aphid introduced aphids pea aphid

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