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      Seminal fluid protein genes of the brown planthopper, Nilaparvata lugens

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          Abstract

          Background

          Seminal fluid proteins (SFPs) are produced mainly in the accessory gland of male insects and transferred to females during mating, in which they induce numerous physiological and post-mating behavioral changes. The brown plant hopper (BPH), Nilaparvata lugens, is an economically important hemipterous pest of rice. The behavior and physiology of the female of this species is significantly altered by mating. SFPs in hemipteran species are still unclear.

          Results

          We applied high-throughput mass spectrometry proteomic analyses to characterize the SFP composition in N. lugens. We identified 94 putative secreted SFPs, and the expression levels of these proteins was determined from the male accessory gland digital gene expression database. The 94 predicted SFPs showed high expression in the male accessory gland. Comparing N. lugens and other insect SFPs, the apparent expansion of N. lugens seminal fluid trypsins and carboxylesterases was observed. The number of N. lugens seminal fluid trypsins (20) was at least twice that in other insects. We detected 6 seminal fluid carboxylesterases in N. lugens seminal fluid, while seminal fluid carboxylesterases were rarely detected in other insects. Otherwise, new insect SFPs, including mesencephalic astrocyte–derived neurotrophic factor, selenoprotein, EGF (epidermal growth factor) domain–containing proteins and a neuropeptide ion transport-like peptide were identified.

          Conclusion

          This work represents the first characterization of putative SFPs in a hemipeteran species. Our results provide a foundation for future studies to investigate the functions of SFPs in N. lugens and are an important addition to the available data for comparative studies of SFPs in insects.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12864-016-3013-7) contains supplementary material, which is available to authorized users.

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          Most cited references41

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          Male accessory gland secretions: modulators of female reproductive physiology and behavior.

          Secretions of male accessory glands contain a variety of bioactive molecules. When transferred during mating, these molecules exert wide-ranging effects on female reproductive activity and they improve the male's chances of siring a significant proportion of the female's offspring. The accessory gland secretions may affect virtually all aspects of the female's reproductive activity. The secretions may render her unwilling or unable to remate for some time, facilitating sperm storage and ensuring that any eggs laid will be fertilized by that male's sperm. They may stimulate an increase in the number and rate of development of eggs and modulate ovulation and/or oviposition. Antimicrobial agents in the secretions ensure that the female reproductive tract is a hospitable environment during sperm transfer. In a few species the secretions include noxious chemicals. These are sequestered by developing eggs that are thereby protected from predators and pathogens when laid.
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            Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation

            Background The brown planthopper, Nilaparvata lugens, the most destructive pest of rice, is a typical monophagous herbivore that feeds exclusively on rice sap, which migrates over long distances. Outbreaks of it have re-occurred approximately every three years in Asia. It has also been used as a model system for ecological studies and for developing effective pest management. To better understand how a monophagous sap-sucking arthropod herbivore has adapted to its exclusive host selection and to provide insights to improve pest control, we analyzed the genomes of the brown planthopper and its two endosymbionts. Results We describe the 1.14 gigabase planthopper draft genome and the genomes of two microbial endosymbionts that permit the planthopper to forage exclusively on rice fields. Only 40.8% of the 27,571 identified Nilaparvata protein coding genes have detectable shared homology with the proteomes of the other 14 arthropods included in this study, reflecting large-scale gene losses including in evolutionarily conserved gene families and biochemical pathways. These unique genomic features are functionally associated with the animal’s exclusive plant host selection. Genes missing from the insect in conserved biochemical pathways that are essential for its survival on the nutritionally imbalanced sap diet are present in the genomes of its microbial endosymbionts, which have evolved to complement the mutualistic nutritional needs of the host. Conclusions Our study reveals a series of complex adaptations of the brown planthopper involving a variety of biological processes, that result in its highly destructive impact on the exclusive host rice. All these findings highlight potential directions for effective pest control of the planthopper. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0521-0) contains supplementary material, which is available to authorized users.
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              Complexity of seminal fluid: a review

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                Author and article information

                Contributors
                yubing19861114@sina.com
                lidanting040122@163.com
                lujiabao10@163.com
                zhangwenxin@sibs.ac.cn
                +86-571-88982991 , chxzhang@zju.edu.cn
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                18 August 2016
                18 August 2016
                2016
                : 17
                : 654
                Affiliations
                State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Hangzhou, 310058 China
                Author information
                http://orcid.org/0000-0002-7784-1188
                Article
                3013
                10.1186/s12864-016-3013-7
                4990865
                27538518
                231f48f0-6629-4ed4-978b-14b1cfafbc82
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 22 January 2016
                : 12 August 2016
                Funding
                Funded by: the National Natural Science Foundation of China
                Award ID: 31471765; 31272374
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Genetics
                nilaparvata lugens,seminal fluid protein,proteome,uplc/ms/ms
                Genetics
                nilaparvata lugens, seminal fluid protein, proteome, uplc/ms/ms

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