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Dr. Shengzhang Dong
Johns Hopkins Bloomberg School of Public Health

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0 Aedes aegypti
0 Mosquito gene silencing
0 Mosquito biology
0 Mosquito-arbovirus interactions
0 insect transgenesis

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Review
Published: 14 January 2021 in Viruses
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Mosquito-borne arthropod-borne viruses (arboviruses) such as the dengue virus (DENV), Zika virus (ZIKV), and chikungunya virus (CHIKV) are important human pathogens that are responsible for significant global morbidity and mortality. The recent emergence and re-emergence of mosquito-borne viral diseases (MBVDs) highlight the urgent need for safe and effective vaccines, therapeutics, and vector-control approaches to prevent MBVD outbreaks. In nature, arboviruses circulate between vertebrate hosts and arthropod vectors; therefore, disrupting the virus lifecycle in mosquitoes is a major approach for combating MBVDs. Several strategies were proposed to render mosquitoes that are refractory to arboviral infection, for example, those involving the generation of genetically modified mosquitoes or infection with the symbiotic bacterium Wolbachia. Due to the recent development of high-throughput screening methods, an increasing number of drugs with inhibitory effects on mosquito-borne arboviruses in mammalian cells were identified. These antivirals are useful resources that can impede the circulation of arboviruses between arthropods and humans by either rendering viruses more vulnerable in humans or suppressing viral infection by reducing the expression of host factors in mosquitoes. In this review, we summarize recent advances in small-molecule antiarboviral drugs in mammalian and mosquito cells, and discuss how to use these antivirals to block the transmission of MBVDs.

ACS Style

Shengzhang Dong; George Dimopoulos. Antiviral Compounds for Blocking Arboviral Transmission in Mosquitoes. Viruses 2021, 13, 108 .

AMA Style

Shengzhang Dong, George Dimopoulos. Antiviral Compounds for Blocking Arboviral Transmission in Mosquitoes. Viruses. 2021; 13 (1):108.

Chicago/Turabian Style

Shengzhang Dong; George Dimopoulos. 2021. "Antiviral Compounds for Blocking Arboviral Transmission in Mosquitoes." Viruses 13, no. 1: 108.

Research article
Published: 24 April 2020 in PLOS Pathogens
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Malaria, caused by the protozoan parasite Plasmodium and transmitted by Anopheles mosquitoes, represents a major threat to human health. Plasmodium’s infection cycle in the Anopheles vector is critical for transmission of the parasite between humans. The midgut-stage bottleneck of infection is largely imposed by the mosquito’s innate immune system. microRNAs (miRNAs, small noncoding RNAs that bind to target RNAs to regulate gene expression) are also involved in regulating immunity and the anti-Plasmodium defense in mosquitoes. Here, we characterized the mosquito’s miRNA responses to Plasmodium infection using an improved crosslinking and immunoprecipitation (CLIP) method, termed covalent ligation of endogenous Argonaute-bound RNAs (CLEAR)-CLIP. Three candidate miRNAs’ influence on P. falciparum infection and midgut microbiota was studied through transgenically expressed miRNA sponges (miR-SPs) in midgut and fat body tissues. MiR-SPs mediated conditional depletion of aga-miR-14 or aga-miR-305, but not aga-miR-8, increased mosquito resistance to both P. falciparum and P. berghei infection, and enhanced the mosquitoes’ antibacterial defenses. Transcriptome analysis revealed that depletion of aga-miR-14 or aga-miR-305 resulted in an increased expression of multiple immunity-related and anti-Plasmodium genes in mosquito midguts. The overall fitness cost of conditionally expressed miR-SPs was low, with only one of eight fitness parameters being adversely affected. Taken together, our results demonstrate that targeting mosquito miRNA by conditional expression of miR-SPs may have potential for the development of malaria control through genetically engineered mosquitoes.

ACS Style

Shengzhang Dong; Xiaonan Fu; Yuemei Dong; Maria L. Simões; Jinsong Zhu; George Dimopoulos. Broad spectrum immunomodulatory effects of Anopheles gambiae microRNAs and their use for transgenic suppression of Plasmodium. PLOS Pathogens 2020, 16, e1008453 .

AMA Style

Shengzhang Dong, Xiaonan Fu, Yuemei Dong, Maria L. Simões, Jinsong Zhu, George Dimopoulos. Broad spectrum immunomodulatory effects of Anopheles gambiae microRNAs and their use for transgenic suppression of Plasmodium. PLOS Pathogens. 2020; 16 (4):e1008453.

Chicago/Turabian Style

Shengzhang Dong; Xiaonan Fu; Yuemei Dong; Maria L. Simões; Jinsong Zhu; George Dimopoulos. 2020. "Broad spectrum immunomodulatory effects of Anopheles gambiae microRNAs and their use for transgenic suppression of Plasmodium." PLOS Pathogens 16, no. 4: e1008453.

Journal article
Published: 27 March 2020 in Insects
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The white-backed planthopper (WBPH) Sogatella furcifera is one of the most harmful pests of rice in Southeast Asia. The fat body of WBPH harbors intracellular yeast-like symbionts (YLS). YLS are vertically transmitted to WBPH offspring by transovarial infection. YLS play an important role in the WBPH life cycle. YLS diversity and function have been extensively studied in the brown planthopper (BPH) and small brown planthopper but not in WBPH, even though a novel strategy for controlling the BPH based on suppressing YLS has been proposed. Here, using denaturing gradient gel electrophoresis, we identified 12 unique fungal sequences among YLS of WBPH, and five of them represented uncultured fungi. We then fed WBPH with rice plants treated with different fungicides [70% propineb wettable powder (WP) (PR), 70% propamocarb hydrochloride aqueous solution (AS) (PH), 25% trifloxystrobin and 50% tebuconazole water-dispersible granules (WG) (TT), 40% pyrimethanil suspension concentrate (SC) (PY), and 50% iprodione SC (IP)] and evaluated their effects on YLS abundance and WBPH survival rate. Both YLS abundance and adult WBPH survival rate were significantly decreased upon feeding fungicide-treated rice plants, and exposure to 50% IP resulted in the strongest reduction. The abundance of two Sf-YLS species (Ascomycetes symbiotes and Cla-like symbiotes) was significantly reduced upon exposure to 50% IP. The counts of Ascomycetes symbiotes, the most abundant YLS species, were also suppressed by the other fungicides tested. In conclusion, 50% IP was the most effective fungicide, reducing YLS abundance and WBPH survival rate under controlled conditions, suggesting its potential use to control WBPH.

ACS Style

Kun Pang; Shengzhang Dong; Peiying Hao; Tongtong Chen; Xinlong Wang; Xiaoping Yu; Huafeng Lin. Fungicides Reduce the Abundance of Yeast-like Symbionts and Survival of White-Backed Planthopper Sogatella furcifera (Homoptera: Delphacidae). Insects 2020, 11, 209 .

AMA Style

Kun Pang, Shengzhang Dong, Peiying Hao, Tongtong Chen, Xinlong Wang, Xiaoping Yu, Huafeng Lin. Fungicides Reduce the Abundance of Yeast-like Symbionts and Survival of White-Backed Planthopper Sogatella furcifera (Homoptera: Delphacidae). Insects. 2020; 11 (4):209.

Chicago/Turabian Style

Kun Pang; Shengzhang Dong; Peiying Hao; Tongtong Chen; Xinlong Wang; Xiaoping Yu; Huafeng Lin. 2020. "Fungicides Reduce the Abundance of Yeast-like Symbionts and Survival of White-Backed Planthopper Sogatella furcifera (Homoptera: Delphacidae)." Insects 11, no. 4: 209.

Preprint content
Published: 27 February 2020
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SUMMARY Dietary sugar is the major energy source for mosquitoes, but its influence on mosquitoes’ capability to transmit malaria parasite remains unclear. Here we show thatPlasmodium bergheiinfection changes global metabolism ofAnopheles stephensiwith the most significant impact on glucose metabolism. Supplementation of glucose or trehalose (the main hemolymph sugar) to mosquito increasesPlasmodiuminfection by alkalizing the mosquito midgut. The glucose/trehalose diets promote rapid growth of a commensal bacterium,Asaia bogorensis, which remodels glucose metabolism and consequently increases midgut pH. The pH increase in turn promotesPlasmodiumgametogenesis. We also demonstrate the sugar composition from different natural plants influencesA. bogorensisgrowth andPlasmodiuminfection is associated with their capability to expandA. bogorensis. Altogether, our results demonstrate that dietary glucose is an important factor that determines mosquito’s competency to transmitPlasmodiumand further highlight a key role for mosquito-microbiota metabolic interactions in regulating development of malaria parasite.

ACS Style

Mengfei Wang; Yanpeng An; Shengzhang Dong; Yuebiao Feng; Li Gao; Penghua Wang; George Dimopoulus; Huiru Tang; Jingwen Wang. Glucose-mediated expansion of a gut commensal bacterium promotesPlasmodiuminfection through alkalizing mosquito midgut. 2020, 1 .

AMA Style

Mengfei Wang, Yanpeng An, Shengzhang Dong, Yuebiao Feng, Li Gao, Penghua Wang, George Dimopoulus, Huiru Tang, Jingwen Wang. Glucose-mediated expansion of a gut commensal bacterium promotesPlasmodiuminfection through alkalizing mosquito midgut. . 2020; ():1.

Chicago/Turabian Style

Mengfei Wang; Yanpeng An; Shengzhang Dong; Yuebiao Feng; Li Gao; Penghua Wang; George Dimopoulus; Huiru Tang; Jingwen Wang. 2020. "Glucose-mediated expansion of a gut commensal bacterium promotesPlasmodiuminfection through alkalizing mosquito midgut." , no. : 1.

Research article
Published: 20 August 2019 in PLOS Neglected Tropical Diseases
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Zika virus (ZIKV), an emerging arbovirus belonging to the genus Flavivirus, is transmitted by Aedes mosquitoes. ZIKV infection can cause microcephaly of newborn babies and Guillain–Barré syndrome in adults. Because no licensed vaccine or specific antiviral treatment is available for ZIKV infection, the most commonly used approach to control the spread of ZIKV is suppression of the mosquito vector population. A novel proposed strategy to block arthropod virus (arbovirus) transmission is based on the chemical inhibition of virus infection in mosquitoes. However, only a few drugs and compounds have been tested with such properties. Here we present a comprehensive screen of 55 FDA-approved anti-flaviviral drugs for potential anti-ZIKV and mosquitocidal activity. Four drugs (auranofin, actinomycin D (Act-D), bortezomib and gemcitabine) were toxic to C6/36 cells, and two drugs (5-fluorouracil and mycophenolic acid (MPA)) significantly reduced ZIKV production in C6/36 cells at 2 μM and 0.5 μM, respectively. Three drugs (Act-D, cyclosporin A, ivermectin) exhibited a strong adulticidal activity, and six drugs (U18666A, retinoic acid p-hydroxyanilide (4-HPR), clotrimazole, bortezomib, MPA, imatinib mesylate) significantly suppressed ZIKV infection in mosquito midguts. Some of these FDA-approved drugs may have potential for use for the development of ZIKV transmission-blocking strategies. Zika virus (ZIKV) is a human threat with a global health burden. As many as 86 countries and territories have reported evidence of mosquito-transmitted Zika infection, and there is no effective means of control. Recently, several studies have identified FDA-approved drugs exerting anti-ZIKV activity in mammalian cells. Here, we have screened such drugs for the ability to reduce mosquito viability or suppress ZIKV infection of mosquito cells. We identified three drugs that significantly increased mosquito mortality and six that significantly suppressed ZIKV infection in mosquito midguts. Altogether, our study provides a list of candidate agents for potential use to block ZIKV transmission in mosquitoes by chemical inhibition.

ACS Style

Shengzhang Dong; Seokyoung Kang; George Dimopoulos. Identification of anti-flaviviral drugs with mosquitocidal and anti-Zika virus activity in Aedes aegypti. PLOS Neglected Tropical Diseases 2019, 13, e0007681 .

AMA Style

Shengzhang Dong, Seokyoung Kang, George Dimopoulos. Identification of anti-flaviviral drugs with mosquitocidal and anti-Zika virus activity in Aedes aegypti. PLOS Neglected Tropical Diseases. 2019; 13 (8):e0007681.

Chicago/Turabian Style

Shengzhang Dong; Seokyoung Kang; George Dimopoulos. 2019. "Identification of anti-flaviviral drugs with mosquitocidal and anti-Zika virus activity in Aedes aegypti." PLOS Neglected Tropical Diseases 13, no. 8: e0007681.

Research article
Published: 29 September 2017 in PLOS Neglected Tropical Diseases
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In the mosquito, the midgut epithelium is the initial tissue to become infected with an arthropod-borne virus (arbovirus) that has been acquired from a vertebrate host along with a viremic bloodmeal. Following its replication in midgut epithelial cells, the virus needs to exit the midgut and infect secondary tissues including the salivary glands before it can be transmitted to another vertebrate host. The viral exit mechanism from the midgut, the midgut escape barrier (MEB), is poorly understood although it is an important determinant of mosquito vector competence for arboviruses. Using chikungunya virus (CHIKV) as a model in Aedes aegypti, we demonstrate that the basal lamina (BL) of the extracellular matrix (ECM) surrounding the midgut constitutes a potential barrier for the virus. The BL, predominantly consisting of collagen IV and laminin, becomes permissive during bloodmeal digestion in the midgut lumen. Bloodmeal digestion, BL permissiveness, and CHIKV dissemination are coincident with increased collagenase activity, diminished collagen IV abundance, and BL shredding in the midgut between 24–32 h post-bloodmeal. This indicates that there may be a window-of-opportunity during which the MEB in Ae. aegypti becomes permissive for CHIKV. Matrix metalloproteinases (MMPs) are the principal extracellular endopeptidases responsible for the degradation/remodeling of the ECM including the BL. We focused on Ae. aegypti (Ae)MMP1, which is expressed in midgut epithelial cells, is inducible upon bloodfeeding, and shows collagenase (gelatinase) activity. However, attempts to inhibit AeMMP activity in general or specifically that of AeMMP1 did not seem to affect its function nor produce an altered midgut escape phenotype. As an alternative, we silenced and overexpressed the Ae. aegypti tissue inhibitor of metalloproteinases (AeTIMP) in the mosquito midgut. AeTIMP was highly upregulated in the midgut during bloodmeal digestion and was able to inhibit MMP activity in vitro. Bloodmeal-inducible, midgut-specific overexpression of AeTIMP or its expression via a recombinant CHIKV significantly increased midgut dissemination rates of the virus. Possibly, AeTIMP overexpression affected BL degradation and/or restoration thereby increasing the midgut dissemination efficiency of the virus. The biological nature of the midgut escape barrier in insects for arthropod-borne viruses has been a mystery for decades. Here we show that the basal lamina (BL) surrounding the mosquito midgut acts as a barrier for chikungunya virus, an alphavirus, which has emerged in the New World hemisphere around three years ago. The barrier became permissive for the virus during digestion of a viremic bloodmeal inside the midgut lumen. Concurrent with BL permissiveness, we observed that collagen IV, a major component of the BL became temporally degraded while the BL was visibly damaged. Based on previous findings, we hypothesized that matrix metalloproteinases such as Ae. aegypti (Ae)MMP1 may be involved in BL degradation. We confirmed that recombinant AeMMP1 exhibited strong gelatinase activity, which was profoundly reduced when recombinant AeMMP1 interacted in vitro with the recombinant Ae. aegypti tissue inhibitor of metalloproteinases (AeTIMP). When transgenically overexpressing AeTIMP in an attempt to temporally inhibit general MMP activity in the mosquito midgut, we observed that the dissemination efficiency of chikungunya virus became significantly increased, while its midgut infection was not affected. It is possible that AeTIMP overexpression affected BL degradation/restoration permitting increased quantities of virus to escape from the midgut.

ACS Style

Shengzhang Dong; Velmurugan Balaraman; Asher M. Kantor; Jingyi Lin; Deana G. Grant; Nicole L. Held; Alexander W. E. Franz. Chikungunya virus dissemination from the midgut of Aedes aegypti is associated with temporal basal lamina degradation during bloodmeal digestion. PLOS Neglected Tropical Diseases 2017, 11, e0005976 .

AMA Style

Shengzhang Dong, Velmurugan Balaraman, Asher M. Kantor, Jingyi Lin, Deana G. Grant, Nicole L. Held, Alexander W. E. Franz. Chikungunya virus dissemination from the midgut of Aedes aegypti is associated with temporal basal lamina degradation during bloodmeal digestion. PLOS Neglected Tropical Diseases. 2017; 11 (9):e0005976.

Chicago/Turabian Style

Shengzhang Dong; Velmurugan Balaraman; Asher M. Kantor; Jingyi Lin; Deana G. Grant; Nicole L. Held; Alexander W. E. Franz. 2017. "Chikungunya virus dissemination from the midgut of Aedes aegypti is associated with temporal basal lamina degradation during bloodmeal digestion." PLOS Neglected Tropical Diseases 11, no. 9: e0005976.

Journal article
Published: 15 May 2017 in BMC Genomics
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The mosquito Aedes aegypti is the primary vector for medically important arthropod-borne viruses, including chikungunya virus (CHIKV). Following oral acquisition, an arbovirus has to persistently infect several organs in the mosquito before becoming transmissible to another vertebrate host. A major obstacle an arbovirus has to overcome during its infection cycle inside the mosquito is the midgut escape barrier, representing the exit mechanism arboviruses utilize when disseminating from the midgut. To understand the transcriptomic basis of midgut escape and to reveal genes involved in the process, we conducted a comparative transcriptomic analysis of midgut samples from mosquitoes which had received a saline meal (SM) or a protein meal (PM) (not) containing CHIKV. CHIKV which was orally acquired by a mosquito along with a SM or PM productively infected the midgut epithelium and disseminated to secondary tissues. A total of 27 RNA-Seq libraries from midguts of mosquitoes that had received PM or SM (not) containing CHIKV at 1 and 2 days post-feeding were generated and sequenced. Fewer than 80 genes responded differentially to the presence of CHIKV in midguts of mosquitoes that had acquired the virus along with SM or PM. SM feeding induced differential expression (DE) of 479 genes at day 1 and 314 genes at day 2 when compared to midguts of sugarfed mosquitoes. By comparison, PM feeding induced 6029 DE genes at day 1 and 7368 genes at day 2. Twenty-three DE genes encoding trypsins, metalloproteinases, and serine-type endopeptidases were significantly upregulated in midguts of mosquitoes at day 1 following SM or PM ingestion. Two of these genes were Ae. aegypti late trypsin (AeLT) and serine collagenase 1 precursor (AeSP1). In vitro, recombinant AeLT showed strong matrix metalloproteinase activity whereas recombinant AeSP1 did not. By substituting a bloodmeal for SM, we identified midgut-expressed genes not involved in blood or protein digestion. These included genes coding for trypsins, metalloproteinases, and serine-type endopeptidases, which could be involved in facilitating midgut escape for arboviruses in Ae. aegypti. The presence of CHIKV in any of the ingested meals had relatively minor effects on the overall gene expression profiles in midguts.

ACS Style

Shengzhang Dong; Susanta K. Behura; Alexander W. E. Franz. The midgut transcriptome of Aedes aegypti fed with saline or protein meals containing chikungunya virus reveals genes potentially involved in viral midgut escape. BMC Genomics 2017, 18, 382 .

AMA Style

Shengzhang Dong, Susanta K. Behura, Alexander W. E. Franz. The midgut transcriptome of Aedes aegypti fed with saline or protein meals containing chikungunya virus reveals genes potentially involved in viral midgut escape. BMC Genomics. 2017; 18 (1):382.

Chicago/Turabian Style

Shengzhang Dong; Susanta K. Behura; Alexander W. E. Franz. 2017. "The midgut transcriptome of Aedes aegypti fed with saline or protein meals containing chikungunya virus reveals genes potentially involved in viral midgut escape." BMC Genomics 18, no. 1: 382.

Journal article
Published: 22 February 2017 in Scientific Reports
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Bursicon is a neuropeptide hormone consisting of two cystine-knot proteins (burs α and burs β), responsible for cuticle tanning and other developmental processes in insects. Recent studies show that each bursicon subunit forms homodimers that induce prophylactic immunity in Drosophila melanogaster. Here, we investigated the hypothesis that bursicon homodimers act in prophylactic immunity in insects, and possibly arthropods, generally, using the mosquito, Aedes aegypti. We found that burs α and burs β are expressed in larvae, pupae and newly emerged adults. Treating newly emerged Ae. aegypti and D. melanogaster adults with recombinant bursicon (r-bursicon) heterodimer led to cuticle tanning in both species. Treating larvae and adults with r-bursicon homodimers led to up-regulation of five anti-microbial peptide (AMP) genes, noting the possibility that bursicon heterodimers also lead to up-regulation of these genes can not been excluded. The induced AMPs effectively suppressed the growth of bacteria in vitro. RNAi knock-down of the transcriptional factor Relish2 abolished the influence of r-bursicon homodimers on AMP production. We infer the bursicon homodimers induce expression of AMP genes via Relish2 in Ae. aegypti, as prophylactic immunity to protect mosquitoes during the vulnerable stages of each molt.

ACS Style

Hongwei Zhang; Shengzhang Dong; Xi Chen; David Stanley; Brenda Beerntsen; Qili Feng; Qisheng Song. Relish2 mediates bursicon homodimer-induced prophylactic immunity in the mosquito Aedes aegypti. Scientific Reports 2017, 7, 43163 .

AMA Style

Hongwei Zhang, Shengzhang Dong, Xi Chen, David Stanley, Brenda Beerntsen, Qili Feng, Qisheng Song. Relish2 mediates bursicon homodimer-induced prophylactic immunity in the mosquito Aedes aegypti. Scientific Reports. 2017; 7 (1):43163.

Chicago/Turabian Style

Hongwei Zhang; Shengzhang Dong; Xi Chen; David Stanley; Brenda Beerntsen; Qili Feng; Qisheng Song. 2017. "Relish2 mediates bursicon homodimer-induced prophylactic immunity in the mosquito Aedes aegypti." Scientific Reports 7, no. 1: 43163.

Original article
Published: 07 November 2016 in Insect Molecular Biology
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Aedes aegypti is a major vector for arboviruses such as dengue, chikungunya and Zika viruses. During acquisition of a viremic bloodmeal, an arbovirus infects mosquito midgut cells before disseminating to secondary tissues, including the salivary glands. Once virus is released into the salivary ducts it can be transmitted to another vertebrate host. The midgut is surrounded by a basal lamina (BL) in the extracellular matrix, consisting of a proteinaceous mesh composed of collagen IV and laminin. BL pore size exclusion limit prevents virions from passing through. Thus, the BL probably requires remodelling via enzymatic activity to enable efficient virus dissemination. Matrix metalloproteinases (MMPs) are extracellular endopeptidases that are involved in remodelling of the extracellular matrix. Here, we describe and characterize the nine Ae. aegypti encoded MMPs, AeMMPs 1−9, which share common features with other invertebrate and vertebrate MMPs. Expression profiling in Ae. aegypti revealed that Aemmp4 and Aemmp6 were upregulated during metamorphosis, whereas expression of Aemmp1 and Aemmp2 increased during bloodmeal digestion. Aemmp1 expression was also upregulated in the presence of a bloodmeal containing chikungunya virus. Using polyclonal antibodies, AeMMP1 and AeMMP2 were specifically detected in tissues associated with the mosquito midgut.

ACS Style

Asher M. Kantor; Shengzhang Dong; Nicole L. Held; Egide Ishimwe; A. Lorena Passarelli; Rollie J. Clem; Alexander W.E. Franz. Identification and initial characterization of matrix metalloproteinases in the yellow fever mosquito,Aedes aegypti. Insect Molecular Biology 2016, 26, 113 -126.

AMA Style

Asher M. Kantor, Shengzhang Dong, Nicole L. Held, Egide Ishimwe, A. Lorena Passarelli, Rollie J. Clem, Alexander W.E. Franz. Identification and initial characterization of matrix metalloproteinases in the yellow fever mosquito,Aedes aegypti. Insect Molecular Biology. 2016; 26 (1):113-126.

Chicago/Turabian Style

Asher M. Kantor; Shengzhang Dong; Nicole L. Held; Egide Ishimwe; A. Lorena Passarelli; Rollie J. Clem; Alexander W.E. Franz. 2016. "Identification and initial characterization of matrix metalloproteinases in the yellow fever mosquito,Aedes aegypti." Insect Molecular Biology 26, no. 1: 113-126.

Journal article
Published: 22 April 2016 in Scientific Reports
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Chikungunya virus (CHIKV) is an emerging mosquito-borne virus belonging to the Togaviridae, which is transmitted to humans by Aedes aegypti and Ae. albopictus. We describe the infection pattern of CHIKV in two New World Ae. aegypti strains, HWE and ORL. Both mosquito strains were susceptible to the virus but showed different infection patterns in midguts and salivary glands. Even though acquisition of a bloodmeal showed moderate levels of apoptosis in midgut tissue, there was no obvious additional CHIKV-induced apoptosis detectable during midgut infection. Analysis of expression of apoptosis-related genes suggested that CHIKV infection dampens rather than promotes apoptosis in the mosquito midgut. In both mosquito strains, the virus was present in saliva within two days post-oral infection. HWE and ORL mosquitoes exhibited no salivary gland infection barrier; however, only 60% (HWE) to 65% (ORL) of the females had released the virus in their saliva at one week post-oral acquisition, suggesting a salivary gland escape barrier. CHIKV induced an apoptotic response in salivary glands of HWE and ORL mosquitoes, demonstrating that the virus caused pathology in its natural vector.

ACS Style

Shengzhang Dong; Asher M. Kantor; Jingyi Lin; A. Lorena Passarelli; Rollie J. Clem; Alexander W. E. Franz. Infection pattern and transmission potential of chikungunya virus in two New World laboratory-adapted Aedes aegypti strains. Scientific Reports 2016, 6, 24729 .

AMA Style

Shengzhang Dong, Asher M. Kantor, Jingyi Lin, A. Lorena Passarelli, Rollie J. Clem, Alexander W. E. Franz. Infection pattern and transmission potential of chikungunya virus in two New World laboratory-adapted Aedes aegypti strains. Scientific Reports. 2016; 6 (1):24729.

Chicago/Turabian Style

Shengzhang Dong; Asher M. Kantor; Jingyi Lin; A. Lorena Passarelli; Rollie J. Clem; Alexander W. E. Franz. 2016. "Infection pattern and transmission potential of chikungunya virus in two New World laboratory-adapted Aedes aegypti strains." Scientific Reports 6, no. 1: 24729.

Journal article
Published: 27 March 2015 in Archives of Insect Biochemistry and Physiology
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Bursicon is a heterodimeric neuropeptide formed of bursicon α (burs α) and bursicon β (burs β) that controls cuticle tanning and wing expansion in insects. Burs α-α and burs β-β homodimers are also formed; they act via an unknown receptor to induce expression of prophylactic immune and stress genes during molting. Based on the hypothesis that burs β-β and/or bursicon influence expression of additional genes acting after the molt, we prepared and sequenced six Drosophila cDNA libraries from groups of flies separately injected with burs β-β, bursicon, or blank control. Compared to the control, the burs β-β treatments led to upregulation (by at least 1.5-fold) of 262 genes at 0.5 h postinjection (PI) and 298 genes at 1 h PI; 323 genes at 0.5 h PI and 269 genes at 1h PI were downregulated (by at least 0.67). Similar changes were recorded following bursicon injections. Of these genes, expression of seven transcripts encoding cuticle proteins was upregulated and three downregulated by burs β-β; expression of nine transcripts encoding cuticle proteins were upregulated and four downregulated following bursicon treatments. Expression of dozens of genes involved in chitin metabolism was altered by the experimental treatments. We recorded parallel changes in expression of selected genes by transcriptome and qPCR analysis. These findings support our hypothesis that burs β-β and bursicon influence expression of additional genes acting after the molt. We report that burs β-β and bursicon act in cuticle synthesis and degradation by regulating the expression of cuticular protein and chitin metabolizing related genes.

ACS Style

Shengzhang Dong; Hongwei Zhang; Xi Chen; David Stanley; Xiaoping Yu; Qisheng Song. THE NEUROPEPTIDE BURSICON ACTS IN CUTICLE METABOLISM. Archives of Insect Biochemistry and Physiology 2015, 89, 87 -97.

AMA Style

Shengzhang Dong, Hongwei Zhang, Xi Chen, David Stanley, Xiaoping Yu, Qisheng Song. THE NEUROPEPTIDE BURSICON ACTS IN CUTICLE METABOLISM. Archives of Insect Biochemistry and Physiology. 2015; 89 (2):87-97.

Chicago/Turabian Style

Shengzhang Dong; Hongwei Zhang; Xi Chen; David Stanley; Xiaoping Yu; Qisheng Song. 2015. "THE NEUROPEPTIDE BURSICON ACTS IN CUTICLE METABOLISM." Archives of Insect Biochemistry and Physiology 89, no. 2: 87-97.

Research article
Published: 27 March 2015 in PLOS ONE
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In vivo targeted gene disruption is a powerful tool to study gene function. Thus far, two tools for genome editing in Aedes aegypti have been applied, zinc-finger nucleases (ZFN) and transcription activator-like effector nucleases (TALEN). As a promising alternative to ZFN and TALEN, which are difficult to produce and validate using standard molecular biological techniques, the clustered regularly interspaced short palindromic repeats/CRISPR-associated sequence 9 (CRISPR/Cas9) system has recently been discovered as a "do-it-yourself" genome editing tool. Here, we describe the use of CRISPR/Cas9 in the mosquito vector, Aedes aegypti. In a transgenic mosquito line expressing both Dsred and enhanced cyan fluorescent protein (ECFP) from the eye tissue-specific 3xP3 promoter in separated but tightly linked expression cassettes, we targeted the ECFP nucleotide sequence for disruption. When supplying the Cas9 enzyme and two sgRNAs targeting different regions of the ECFP gene as in vitro transcribed mRNAs for germline transformation, we recovered four different G1 pools (5.5% knockout efficiency) where individuals still expressed DsRed but no longer ECFP. PCR amplification, cloning, and sequencing of PCR amplicons revealed indels in the ECFP target gene ranging from 2-27 nucleotides. These results show for the first time that CRISPR/Cas9 mediated gene editing is achievable in Ae. aegypti, paving the way for further functional genomics related studies in this mosquito species.

ACS Style

Shengzhang Dong; Jingyi Lin; Nicole L. Held; Rollie J. Clem; A. Lorena Passarelli; Alexander W. E. Franz. Heritable CRISPR/Cas9-Mediated Genome Editing in the Yellow Fever Mosquito, Aedes aegypti. PLOS ONE 2015, 10, e0122353 -e0122353.

AMA Style

Shengzhang Dong, Jingyi Lin, Nicole L. Held, Rollie J. Clem, A. Lorena Passarelli, Alexander W. E. Franz. Heritable CRISPR/Cas9-Mediated Genome Editing in the Yellow Fever Mosquito, Aedes aegypti. PLOS ONE. 2015; 10 (3):e0122353-e0122353.

Chicago/Turabian Style

Shengzhang Dong; Jingyi Lin; Nicole L. Held; Rollie J. Clem; A. Lorena Passarelli; Alexander W. E. Franz. 2015. "Heritable CRISPR/Cas9-Mediated Genome Editing in the Yellow Fever Mosquito, Aedes aegypti." PLOS ONE 10, no. 3: e0122353-e0122353.

Comparative study
Published: 01 December 2014 in Fish & Shellfish Immunology
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The golden apple snail, Pomacea canaliculata, has strong tolerance to high temperature, facilitating its invasion in East and Southeast Asia. In the present study, three cDNAs encoding heat shock proteins (PocaHSP60, PocaHSP70, PocaHSP90) in P. canaliculata were cloned and characterized. The PocaHSP60 cDNA was 2447 bp, containing an ORF encoding a polypeptide of 574 amino acids. The PocaHSP70 cDNA was 2644 bp, containing an ORF encoding a polypeptide of 643 amino acids. The PocaHSP90 cDNA was 2546 bp, containing an ORF encoding a polypeptide of 726 amino acids. Genomic DNA analysis showed that PocaHSP60 had 11 introns in the coding region and PocaHSP90 had 7 introns but PocaHSP70 had no one. The expression changes of these three PocaHSPs in the gill, digestive gland, kidney and foot muscle of P. canaliculata exposed to high and low temperature were investigated. The results of quantitative PCR and western blotting showed that the expression level of PocaHSP90 was much higher than PocaHSP60 and PocaHSP70 at room temperature, and PocaHSP70 expression level was the lowest among them. Afterheat shock, PocaHSP70 expression increased rapidly, much more significantly than PocaHSP90 expression, and the effect of heat shock on the expression of PocaHSP70 and PocaHSP90 in the different tissues of P. canaliculata was not the same. Unlike PocaHSP70 and PocaHSP90, PocaHSP60 expression seemed not to be affected by heat shock, because its expression was moderately induced only in the foot muscle. However, cool shock had little effect on the expression change of above three PocaHSPs. These results indicated that HSPs might be related to the thermal resistance of P. canaliculata.

ACS Style

Yipeng Xu; Guowan Zheng; Shengzhang Dong; Guangfu Liu; Xiaoping Yu. Molecular cloning, characterization and expression analysis of HSP60, HSP70 and HSP90 in the golden apple snail, Pomacea canaliculata. Fish & Shellfish Immunology 2014, 41, 643 -653.

AMA Style

Yipeng Xu, Guowan Zheng, Shengzhang Dong, Guangfu Liu, Xiaoping Yu. Molecular cloning, characterization and expression analysis of HSP60, HSP70 and HSP90 in the golden apple snail, Pomacea canaliculata. Fish & Shellfish Immunology. 2014; 41 (2):643-653.

Chicago/Turabian Style

Yipeng Xu; Guowan Zheng; Shengzhang Dong; Guangfu Liu; Xiaoping Yu. 2014. "Molecular cloning, characterization and expression analysis of HSP60, HSP70 and HSP90 in the golden apple snail, Pomacea canaliculata." Fish & Shellfish Immunology 41, no. 2: 643-653.

Research article
Published: 27 November 2013 in PLOS ONE
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To assess the safety of transgenic rice expressing Cry1Ab protein to vertebrates, the effect of Cry1Ab rice on broad health indicators in blood and various organs of Swiss rats were analyzed. The 30 and 90 day safety studies of Cry1Ab rice on female Swiss rats revealed that Cry1Ab rice had no significant effect on the several elements of blood lymph including hemogram, calcium ion concentration and apoptosis rate of lymphocytes, indicating that Cry1Ab protein could not affect the blood lymph of Swiss rat. Similarly, Cry1Ab rice had no effect on enzyme activities in a variety of organs of Swiss rat. However, Cry1Ab rice did have significant effects on the blood biochemistry indexes including urea, triglyceride (TG), glutamic oxalacetic transaminase (AST) and alkaline phosphatase (ALP) after the rats were fed with Cry1Ab rice for 30 days, but not after 90 days, indicating that Cry1Ab protein may influence blood metabolism for a short duration. Quantitative real-time PCR (qPCR) analysis of the 6 genes encoding enzymes responsible for the major detoxification functions of liver revealed that Cry1Ab rice exerted no influences on the levels of these transcripts in liver of Swiss rat, indicating that significant differences registered in part of the blood biochemical parameters in the 30 day study might result from other untested organs or tissues in response to the stress of exogenous Cry1Ab protein. The results suggest that Cry1Ab protein has no significant long-term (90 day) effects on female Swiss rat.

ACS Style

Yang Wang; Baoyang Wei; Yixing Tian; Zhi Wang; Yun Tian; Shuduan Tan; Shengzhang Dong; Qisheng Song. Evaluation of the Potential Effect of Transgenic Rice Expressing Cry1Ab on the Hematology and Enzyme Activity in Organs of Female Swiss Rats. PLOS ONE 2013, 8, e80424 .

AMA Style

Yang Wang, Baoyang Wei, Yixing Tian, Zhi Wang, Yun Tian, Shuduan Tan, Shengzhang Dong, Qisheng Song. Evaluation of the Potential Effect of Transgenic Rice Expressing Cry1Ab on the Hematology and Enzyme Activity in Organs of Female Swiss Rats. PLOS ONE. 2013; 8 (11):e80424.

Chicago/Turabian Style

Yang Wang; Baoyang Wei; Yixing Tian; Zhi Wang; Yun Tian; Shuduan Tan; Shengzhang Dong; Qisheng Song. 2013. "Evaluation of the Potential Effect of Transgenic Rice Expressing Cry1Ab on the Hematology and Enzyme Activity in Organs of Female Swiss Rats." PLOS ONE 8, no. 11: e80424.

Evaluation study
Published: 03 April 2013 in Current Microbiology
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Yeast-like symbiotes (YLS) are endosymbionts that are intimately associated with the growth, development, reproduction of their host, the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). However, it is unclear how many species of YLS are found within N. lugens, and how they are related to each other. Traditional methods or simple amplification based on 18S rDNA sequence does not reliably identify new species quickly and efficiently. Therefore, a novel nested PCR-denaturing gradient gel electrophoresis (DGGE) strategy was developed in this article to analyze the YLS of brown planthopper using a nested PCR protocol that involved the 18S rDNA gene and the 5.8S–ITS gene using fungal universal primers. The nested PCR protocol was developed as follows: firstly, the 18S rDNA gene, and 5.8S–ITS gene were amplified using fungal universal primers. Subsequently, these products were used as a template in a second PCR with primers ITS1GC–ITS2, ITS1FGC–ITS2, and NFGC-NR, which was suitable for DGGE. Using this highly specific molecular approach, we found several previously detected fungi: Noda, Pichia guilliermondii, Candida sp., and some previously undetected fungi, such as Saccharomycetales sp., Debaryomyces hansenii, and some uncultured fungi. In conclusion, the nested PCR system developed in this study, coupled with DGGE fingerprinting, offers a new tool for uncovering fungal endosymbiont diversity within planthoppers.

ACS Style

Yun Hou; Zheng Ma; Shengzhang Dong; Yolanda H. Chen; Xiaoping Yu. Analysis of Yeast-Like Symbiote Diversity in the Brown Planthopper (BPH), Nilaparvata lugens Stål, Using a Novel Nested PCR-DGGE Protocol. Current Microbiology 2013, 67, 263 -270.

AMA Style

Yun Hou, Zheng Ma, Shengzhang Dong, Yolanda H. Chen, Xiaoping Yu. Analysis of Yeast-Like Symbiote Diversity in the Brown Planthopper (BPH), Nilaparvata lugens Stål, Using a Novel Nested PCR-DGGE Protocol. Current Microbiology. 2013; 67 (3):263-270.

Chicago/Turabian Style

Yun Hou; Zheng Ma; Shengzhang Dong; Yolanda H. Chen; Xiaoping Yu. 2013. "Analysis of Yeast-Like Symbiote Diversity in the Brown Planthopper (BPH), Nilaparvata lugens Stål, Using a Novel Nested PCR-DGGE Protocol." Current Microbiology 67, no. 3: 263-270.

Research article
Published: 24 August 2012 in PLOS ONE
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The MEAM1 (B biotype) Bemisia tabaci (Gennadius) is one of the most widespread and damaging whitefly cryptic species. Our previous studies discovered that the MEAM1 whitefly indirectly benefits from interactions with the tomato yellow leaf curl China virus (TYLCCNV) via accelerated ovarian development and increased fecundity. However, the physiological mechanism of begomoviruse-infected plants acting on the reproduction of the insect vector was unknown. Biochemical and molecular properties of vitellogenin (Vg) and vitellin (Vt) were characterized in the MEAM1 whitefly. In addition, kinetics of Vt levels in ovary and Vg levels in hemolymph in different stages were detected using a sandwich ELISA. The level of hemolymph Vg increased rapidly after eclosion. A significantly higher level of hemolymph Vg and ovary Vt were observed in whiteflies feeding on virus-infected tobacco plants than those feeding on uninfected plants. In order to detect the levels of Vg mRNA transcription, complete vitellogenin (Vg) mRNA transcripts of 6474 bp were sequenced. Vg mRNA level in whiteflies feeding on virus-infected plants was higher than those feeding on uninfected plants. However, virus-infection of the whiteflies per se, as demonstrated using an artificial diet system, did not produce significant changes in Vg mRNA level. In MEAM1 whitefly, increased levels of both vitellin and vitellogenin as well as increased transcription of Vg mRNA are associated with feeding on begomovirus-infected plants, thus providing a mechanism for accelerated vitellogenesis. We conclude that MEAM1 whitefly profits from feeding on begomovirus-infected plants for yolk protein synthesis and uptake, and thereby increases its fecundity. These results not only provide insights into the molecular and physiological mechanisms underlying the elevated reproduction of a whitefly species through its association with a begomovirus-infected plant, but also provide a better understanding of the molecular mechanisms related to whitefly reproduction.

ACS Style

Jian-Yang Guo; Shengzhang Dong; Xiuling Yang; Lu Cheng; Fang-Hao Wan; Shu-Sheng Liu; Xue-Ping Zhou; Gong-Yin Ye. Enhanced Vitellogenesis in a Whitefly via Feeding on a Begomovirus-Infected Plant. PLOS ONE 2012, 7, e43567 .

AMA Style

Jian-Yang Guo, Shengzhang Dong, Xiuling Yang, Lu Cheng, Fang-Hao Wan, Shu-Sheng Liu, Xue-Ping Zhou, Gong-Yin Ye. Enhanced Vitellogenesis in a Whitefly via Feeding on a Begomovirus-Infected Plant. PLOS ONE. 2012; 7 (8):e43567.

Chicago/Turabian Style

Jian-Yang Guo; Shengzhang Dong; Xiuling Yang; Lu Cheng; Fang-Hao Wan; Shu-Sheng Liu; Xue-Ping Zhou; Gong-Yin Ye. 2012. "Enhanced Vitellogenesis in a Whitefly via Feeding on a Begomovirus-Infected Plant." PLOS ONE 7, no. 8: e43567.

Book chapter
Published: 14 June 2012 in Advanced Technologies for Managing Insect Pests
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Bursicon is an insect heterodimeric neuropeptide hormone which binds to a specific G protein-coupled receptor, Drosophila leucine-rich repeats-containing G-protein-coupled receptor 2 (DLGR2) and regulates various aspects of cuticle tanning (sclerotization and melanization) and wing expansion in diverse insect orders. Bursicon was discovered 50 years ago by Gottfried Fraenkel using the blowfly Calliphora erythrocephala in a neck-ligated fly assay. Over the last few years, there has been a tremendous increase in our knowledge of bursicon molecular structure and signaling pathway due to recent advances in genomics, proteomics and genetic analysis, combined with physiological and behavior analysis. Insect neuropeptides, which are released from neurosecretory cells in the insect central nervous system (CNS), regulate virtually all aspects of insect life and would appear to be excellent candidates for development of new methods for pest control. As a critical neuropeptide during the process of insect molting cycle, bursicon could also be used for the design of novel, safe and selective compounds to control pests. Here, we will review recent advances in bursicon research and developments of neuropeptides for pest control, and then discuss the possibilities of bursicon as a target for pest control.

ACS Style

Shengzhang Dong; Qisheng Song. Bursicon as a Potential Target for Insect Control. Advanced Technologies for Managing Insect Pests 2012, 83 -105.

AMA Style

Shengzhang Dong, Qisheng Song. Bursicon as a Potential Target for Insect Control. Advanced Technologies for Managing Insect Pests. 2012; ():83-105.

Chicago/Turabian Style

Shengzhang Dong; Qisheng Song. 2012. "Bursicon as a Potential Target for Insect Control." Advanced Technologies for Managing Insect Pests , no. : 83-105.

Journal article
Published: 13 June 2012 in Aquaculture
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The heat shock cognate 70 (PHSC70) gene of the golden apple snail, Pomacea canaliculata, was cloned and characterized, which was 2275 base pairs (bp) containing a single 1950 bp open reading frame (ORF) that encoded a polypeptide of 650 amino acids. Genomic DNA of PHSC70 in P. canaliculata confirmed the presence of nine introns located at the coding region as well as the 5′-terminal untranslated region (UTR). BLAST analysis revealed that the PHSC70 gene shared high similarity with other known HSC70 genes. The phylogenetic analysis demonstrated a separate clustering of the PHSC70 with constitutive members from other mollusk species. Expression of PHSC70 in different tissues (gill, digestive gland, kidney and foot muscle) of the snails exposed to high (36 °C) and low (9 °C) temperatures was investigated. The results showed that PHSC70 transcript levels were constitutively modulated in non-stressed condition in above tissues. After the cold treatment, PHSC70 transcript levels decreased significantly in the gill, but had no obvious changes in the digestive gland, kidney and foot muscle. However, PHSC70 transcript levels increased significantly in all the tissues under the heat shock condition. In addition, PHSC70 protein was detected in different tissues from both young and adult snails by a Western blot. The result of quantitative immunofluorescence indicated that a large amount of PHSC70 proteins localize in the gill lamella cells. These results strongly suggested that PHSC70 may play an important role in mediating the physiological responses to the high temperature.

ACS Style

Guowan Zheng; Shengzhang Dong; Yun Hou; Ke Yang; Xiaoping Yu. Molecular characteristics of HSC70 gene and its expression in the golden apple snails, Pomacea canaliculata (Mollusca: Gastropoda). Aquaculture 2012, 358-359, 41 -49.

AMA Style

Guowan Zheng, Shengzhang Dong, Yun Hou, Ke Yang, Xiaoping Yu. Molecular characteristics of HSC70 gene and its expression in the golden apple snails, Pomacea canaliculata (Mollusca: Gastropoda). Aquaculture. 2012; 358-359 ():41-49.

Chicago/Turabian Style

Guowan Zheng; Shengzhang Dong; Yun Hou; Ke Yang; Xiaoping Yu. 2012. "Molecular characteristics of HSC70 gene and its expression in the golden apple snails, Pomacea canaliculata (Mollusca: Gastropoda)." Aquaculture 358-359, no. : 41-49.

Journal article
Published: 01 April 2012 in Scientia Agricola
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The wild rice, Zizania latifolia Turcz, used to be one of the important aquatic vegetables cultivated in China. Recently, the golden apple snail - GAS (Pomacea canaliculata (Lamarck)) was found to be a major invasive pest attacking Z. latifolia. To control efficiently GAS, predation by the Chinese soft-shelled turtles (Pelodiscus sinensis) on GAS was evaluated in laboratory and field trials. P. sinensis had a strong predatory capacity and selectivity for GAS both in laboratory and field conditions. All the sizes of P. sinensis prefer to capture smaller snails. The optimum number of P. sinensis released in Z. latifolia field was dependent on the density of over-wintered GAS, and varied between 30 and 50 turtles per 666.7 m². The number of GAS declined in the fields with turtles as compared to turtle-free field. A pattern of releasing P. sinensis in Z. latifolia fields was developed and widely adopted by farmers because of much more benefit besides biologically controlling GAS.

ACS Style

Shengzhang Dong; Guowan Zheng; Xiaoping Yu; Changhuan Fu. Biological control of golden apple snail, Pomacea canaliculata by Chinese soft-shelled turtle, Pelodiscus sinensis in the wild rice, Zizania latifolia field. Scientia Agricola 2012, 69, 142 -146.

AMA Style

Shengzhang Dong, Guowan Zheng, Xiaoping Yu, Changhuan Fu. Biological control of golden apple snail, Pomacea canaliculata by Chinese soft-shelled turtle, Pelodiscus sinensis in the wild rice, Zizania latifolia field. Scientia Agricola. 2012; 69 (2):142-146.

Chicago/Turabian Style

Shengzhang Dong; Guowan Zheng; Xiaoping Yu; Changhuan Fu. 2012. "Biological control of golden apple snail, Pomacea canaliculata by Chinese soft-shelled turtle, Pelodiscus sinensis in the wild rice, Zizania latifolia field." Scientia Agricola 69, no. 2: 142-146.

Original article
Published: 01 April 2012 in Insect Science
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The brown planthopper (BPH), Nilaparvata lugens Stål, which is one of the most destructive pests of rice, has been confirmed to harbor yeast‐like symbiotes (YLS) in the fat body. Several morphologically different YLS have been previously isolated and cultured in vitro from BPH, but direct evidence is lacking to further clarify whether the cultured YLS were from BPH. In this study, one species of YLS was successfully cultured in vitro and simultaneously verified to exist in the fat body of BPH by sequence analysis and nested polymerase chain reaction (PCR). The cultured YLS isolate in vitro was identified as a member of the genus Candida on the basis of 18S rDNA (ribosomal DNA) and 5.8S‐ITS (internal transcribed spacer) rDNA sequence and a phylogenetic analysis of ITS sequences from yeast. Therefore, this yeast isolate was named as Candida‐like symbiotes. Candida‐like symbiotes was found to exist in fat bodies, ovaries and newly laid eggs of the BPH, but not in the heads, thoraxes and mid‐guts. In addition, the number of Candida‐like symbiotes in 1 × 106 of purified YLS from BPH fat bodies was speculated to be (5.32 ± 0.22) × 104 on the basis of a quantitative PCR analysis.

ACS Style

Kun Pang; Sheng-Zhang Dong; Yun Hou; Ya-Lin Bian; Ke Yang; Xiao-Ping Yu. Cultivation, identification and quantification of one species of yeast-like symbiotes, Candida, in the rice brown planthopper, Nilaparvata lugens. Insect Science 2012, 19, 477 -484.

AMA Style

Kun Pang, Sheng-Zhang Dong, Yun Hou, Ya-Lin Bian, Ke Yang, Xiao-Ping Yu. Cultivation, identification and quantification of one species of yeast-like symbiotes, Candida, in the rice brown planthopper, Nilaparvata lugens. Insect Science. 2012; 19 (4):477-484.

Chicago/Turabian Style

Kun Pang; Sheng-Zhang Dong; Yun Hou; Ya-Lin Bian; Ke Yang; Xiao-Ping Yu. 2012. "Cultivation, identification and quantification of one species of yeast-like symbiotes, Candida, in the rice brown planthopper, Nilaparvata lugens." Insect Science 19, no. 4: 477-484.