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Insect Seminal Fluid Proteins: Identification and Function EN56CH02-Wolfner ARI 14 October 2010 9:49 Insect Seminal Fluid Proteins: Identification and Function Frank W. Avila, Laura K. Sirot, Brooke A. LaFlamme, C. Dustin Rubinstein, and Mariana F. Wolfner Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853; email: [email protected], [email protected], [email protected], [email protected], [email protected] Annu. Rev. Entomol. 2011. 56:21–40 Key Words First published online as a Review in Advance on egg production, mating receptivity, sperm storage, mating plug, sperm September 24, 2010 by University of California - San Diego on 08/13/13. For personal use only. competition, feeding, reproduction, Acp Annu. Rev. Entomol. 2011.56:21-40. Downloaded from www.annualreviews.org The Annual Review of Entomology is online at ento.annualreviews.org Abstract This article’s doi: Seminal fluid proteins (SFPs) produced in reproductive tract tissues 10.1146/annurev-ento-120709-144823 of male insects and transferred to females during mating induce nu- Copyright c 2011 by Annual Reviews. merous physiological and behavioral postmating changes in females. All rights reserved These changes include decreasing receptivity to remating; affecting 0066-4170/11/0107-0021$20.00 sperm storage parameters; increasing egg production; and modulating sperm competition, feeding behaviors, and mating plug formation. In addition, SFPs also have antimicrobial functions and induce expression of antimicrobial peptides in at least some insects. Here, we review re- cent identification of insect SFPs and discuss the multiple roles these proteins play in the postmating processes of female insects. 21 EN56CH02-Wolfner ARI 14 October 2010 9:49 INTRODUCTION SFPs provide intriguing targets for the control of disease vectors and agricultural pests. As we In many insect species, mating initiates a be- discuss below, SFPs alter reproductive and/or Seminal fluid protein havioral and physiological switch in females, feeding behaviors in a number of arthropods, (SFP): protein triggering responses in several processes related including insects that cause economic damage expressed from tissues to fertility. Receipt of seminal fluid—a mix- of the male or spread disease. In many of these species, ture of proteins and other molecules—by the reproductive tract and there are no approved and effective methods to female is a major component of this switch. likely transferred to control the damage they cause. For example, females during mating Insect seminal fluid proteins (SFPs) are the vaccines for tick-borne pathogens have been products of male reproductive tract (RT) se- RT: reproductive developed for a limited number of tick anti- tract cretory tissues—accessory glands (AGs), semi- gens (35) and the principal vectors of malaria nal vesicles, ejaculatory duct, ejaculatory bulb, AG: accessory gland and dengue fever—the mosquitoes and testes. SFPs are transferred to females with Aedes ae- and , respectively—have sperm during mating. They are major effectors gypti Anopheles gambiae been notoriously difficult to control. Thus, the of a wide range of female postmating responses, best current method of limiting these diseases including changing female likelihood of remat- is to control the spread of their insect vectors. ing, increasing ovulation and egg-laying rates, In another area, increased resistance to pesti- changing female flight and feeding behavior, cides has made population control by conven- inducing antimicrobial activities, and modulat- tional means difficult for pests such as the cotton ing sperm storage parameters. Absence of SFPs bollworm/corn earworm from the ejaculate adversely affects the repro- , Helicoverpa armigera (61); the bed bug, (80, 143); ductive success of both sexes. SFPs identified Cimex lectularius and ticks (57). As more is learned about the to date represent numerous protein classes, in- reproductive biology of specific arthropods, cluding proteases/protease inhibitors, lectins, their SFPs may provide tools or targets for prohormones, peptides, and protective pro- the control of disease vectors and agricultural teins such as antioxidants; these protein classes pests. are present in the ejaculate of organisms from The study of SFPs also provides insight into arthropods to mammals (121). While nonpro- the evolutionary patterns of reproductive traits. tein molecules are also present in seminal fluid Although the functional classes of SFPs are con- (e.g., prostaglandins in crickets: 86; steroid hor- served, a significant fraction of individual SFPs mones in mosquitoes: 124), research on the ef- show signs of unusual, often rapid, evolution at fects of seminal fluid receipt has focused largely the primary sequence level. The forces driving on the action of SFPs. Although the focus of this this pattern are not understood, and the study review is on insect SFPs, progress on the iden- of SFPs may allow for their identification and tification and function of SFPs in tick species is by University of California - San Diego on 08/13/13. For personal use only. dissection. Comparative studies of SFPs, indi- also included. Annu. Rev. Entomol. 2011.56:21-40. Downloaded from www.annualreviews.org vidually and in aggregate, are important be- The past few years have witnessed an explo- cause ( ) lineage-specific SFPs may be involved sion in the identification and functional analyses a in the reproductive isolation between species; of SFPs in insects due to new proteomic and ( ) highly conserved SFPs or SFP classes may RNA interference technologies. Because ear- b be essential for reproduction; and ( ) SFP di- lier results in this field were reviewed by Gillott c vergence between closely related species may (56), Chen (29), and Leopold (84), we focus illuminate selective pressures underlying SFP here primarily on recent developments, refer- evolution. Recent reviews have focused on the ring readers to those comprehensive reviews for evolutionary dynamics of SFPs (49, 53, 120, details on earlier studies. 148); therefore, we refer the reader to those re- Dissection of the nature and function of in- views and focus here on the nature and function sect SFPs has relevance beyond understanding of SFPs. insect reproductive molecules and their actions. 22 Avila et al. EN56CH02-Wolfner ARI 14 October 2010 9:49 IDENTIFICATION OF SEMINAL females during mating (Table 1). For the pur- FLUID PROTEINS poses of this review, proteins within the seminal fluid and transferred to females are called SFPs. The identification of proteins produced in se- Accessory gland Proteins synthesized in male AGs are called cretory tissues of the male RT and demon- protein (Acp): Acps. strated to be, or likely to be, transferred to protein made by, and Most of the Acp/SFP identification stud- expected to be secreted females during mating is the primary step in ies in Table 1 examined RNA or proteins from, the accessory SFP identification. Transcriptomic [expressed found in tissues of the male RT, but did gland of male insect sequence tag (EST), microarray; 5, 16, 20, 30, reproductive tracts not demonstrate SFP transfer during mating. 34, 41, 112, 130, 151, 158, 161, 165] and pro- A novel proteomic method directly identified teomic (6, 10, 32, 48, 50, 75, 136, 140, 149, 153, 146 SFPs (39 previ- 160, 162) methods have given a global view of Drosophila melanogaster ously unannotated), 126 SFPs, and proteins produced in arthropod male RT glands D. simulans 116 SFPs that are transferred to and, in some cases, of proteins transferred to D. yakuba Table 1 Recently identified SFPs and RT-expressed genes in insects No. identified (Ref.) Order Family Genus sp. Method (Ref.) In RT Transferred Diptera Drosophilidae Drosophila simulans EST screen (151), proteomic (48) 57a (151) 3 (48) Drosophila Cumulative review (130), EST 112a (130), 138 (50), 8 (48), melanogaster screen (151), peptide purification 46 (30, 130), 14 (130), (91, 137), proteomic (48, 104, 153, 440 (153), 3 (91, 137, 160), microarray (30, 130) 13a (160), 34a 169) (104, 151) Drosophila yakuba EST screen (16), proteomic (48, 50) 119 (16) 107 (50), 8 (48) Drosophila erecta EST screen (16) 114 (16) — Drosophila EST screen (158), proteomic (75) 54 (158), — mojavensis 786 (75) Tephritidae Ceratitis capitata EST screen (34) 13 (34) — Culicidae Aedes aegypti Bioinf. candidates/RT-PCR (149), 63a (149) 56 (147) proteomic (147) Anopheles gambiae Bioinf. candidates/RT-PCR (41), 46 (41), 25 (140) 15 (140) proteomic (140) Lepidoptera Nymphalidae Heliconius erato EST screen/bioinf. filter/RT-PCR 371 (161) 25 (162) by University of California - San Diego on 08/13/13. For personal use only. (161), proteomic (162) Annu. Rev. Entomol. 2011.56:21-40. Downloaded from www.annualreviews.org Heliconius EST screen/bioinf. filter/RT-PCR 340 (161) 10 (162) melpomene (161), proteomic (162) Hymenoptera Apidae Apis mellifera Proteomic (10, 32) 69 (32) 33 (32), 57 (10) Coleoptera Tenebrionidae Tribolium castaneum Microarray (112) 112 (112) — Orthoptera Gryllidae Allonebrius EST screen (20) 183 (20) — Gryllus firmus EST screen (5, 20) 247 (5, 20) — Gryllus EST screen (5), proteomic (6) 277 (5) 22 (6) pennsylvanicus Arachnida: Ixodidae Amblyomma EST screen (165) 35 (165) — Ixodida hebraeum aCandidate SFPs were based on criteria of accessory gland–specific or –enriched expression and/or presence of a predicted secretion signal sequence. Abbreviations: Acp, accessory gland protein; EST, expressed sequence tag; RT, reproductive tract; RT-PCR, reverse transcriptase–polymerase chain reaction; SFP, seminal fluid protein. www.annualreviews.org • Reproductive Gland Proteins 23 EN56CH02-Wolfner ARI 14 October 2010 9:49 females during mating (48, 50). Findlay et al. diction of SFPs by sequence comparison much (50) fed females a diet enriched in 15Nsothat easier. For example, comparative structural the females produced isotopically heavy pro- modeling suggested the structure/function of teins. After these females were mated to un- 28 predicted Acps of D. melanogaster males labeled males, only proteins transferred from (105). FlyBase annotations to D. melanogaster males were detected when the female RTs were genes were used to predict the functional analyzed by mass spectrometry. This method classes of 240 candidate SFPs in D.
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