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Heat Shock Protein 83 Plays Pleiotropic Roles in Embryogenesis, Longevity, and Fecundity of the Pea Aphid Acyrthosiphon Pisum

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Heat Shock Protein 83 Plays Pleiotropic Roles in Embryogenesis, Longevity, and Fecundity of the Pea Aphid Acyrthosiphon Pisum Dev Genes Evol DOI 10.1007/s00427-016-0564-1 ORIGINAL ARTICLE Heat shock protein 83 plays pleiotropic roles in embryogenesis, longevity, and fecundity of the pea aphid Acyrthosiphon pisum Torsten Will1,2 & Henrike Schmidtberg1 & Marisa Skaljac3 & Andreas Vilcinskas1,3 Received: 5 June 2016 /Accepted: 27 September 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Heat shock protein 83 (HSP83) is homologous to attenuate its expression and studied the impact on complex the chaperone HSP90. It has pleiotropic functions in parameters. The RNA interference (RNAi)-mediated deple- Drosophila melanogaster, including the control of longevity tion of HSP83 expression in A. pisum reduced both longevity and fecundity, and facilitates morphological evolution by and fecundity, suggesting this chaperone has an evolutionarily buffering cryptic deleterious mutations in wild populations. conserved function in insects. Surprisingly, HSP83 depletion In the pea aphid Acyrthosiphon pisum, HSP83 expression is reduced the number of viviparous offspring while simulta- moderately induced by bacterial infection but upregulated neously increasing the number of premature nymphs develop- more strongly in response to heat stress and fungal infection. ing in the ovaries, suggesting an unexpected role in aphid Stress-inducible heat shock proteins are of considerable evo- embryogenesis and eclosion. The present study indicates lutionary and ecological importance because they are known that reduced HSP83 expression in A. pisum reveals both to buffer environmental variation and to influence fitness un- functional similarities and differences compared with its der non-optimal conditions. To investigate the functions of reported roles in holometabolous insects. Its impact on HSP83 in viviparous aphids, we used RNA interference to aphid lifespan, fecundity, and embryogenesis suggests a function that determines their fitness. This could be achieved by targeting different client proteins, recruiting Communicated by Claude Desplan distinct co-chaperones or transposon activation. Electronic supplementary material The online version of this article (doi:10.1007/s00427-016-0564-1) contains supplementary material, . which is available to authorized users. Keywords Acyrthosiphon pisum HSP83 HSP90 Longevity . Fecundity . Development . Viviparous . * Andreas Vilcinskas reproduction Epigenetics [email protected] Torsten Will [email protected] Abbreviations dsRNA double-stranded RNA Henrike Schmidtberg [email protected] HSP heat shock protein RNAi RNA interference dai Marisa Skaljac [email protected] 1 Institute of Insect Biotechnology, Justus-Liebig-University of Introduction Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany 2 Institute of Phytopathology, Justus-Liebig-University of Giessen, Heat shock proteins (HSPs) are evolutionarily conserved chap- Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany erones whose predominant function is to prevent the misfolding 3 Fraunhofer-Institute for Molecular Biology and Applied Ecology and denaturation of proteins caused by environmental stressors (IME) Project Group ‘Bioresources’, Winchesterstraße 2, such as heat, toxins, or pathogens (Johnson 2012). Their func- 35394 Giessen, Germany tions in Drosophila melanogaster are associated with the Dev Genes Evol buffering of environmental variations, determining fitness un- unusual (autosome-like) inheritance of the X chromosome der non-optimal conditions, and are therefore of significant (The International Aphid Genomic Consortium 2010). evolutionary and ecological relevance (Sorensen et al. 2003). The attenuation of gene expression by RNA interference HSPs have been assigned to five families based on homology (RNAi) is a powerful method for the functional analysis of and molecular mass. The HSP90 family is particularly relevant genes in A. pisum (Mutti et al. 2006; Jaubert-Possamai et al. in the context of evolutionary biology because one member 2007; Will and Vilcinskas 2013). We therefore attenuated (HSP90) acts as a capacitor for morphological evolution in HSP83 expression in viviparous A. pisum by microinjecting D. melanogaster (Rutherford and Lindquist 1998) by buffering the aphids with the corresponding double-stranded RNA phenotypic variance producing altered phenotypes in response (dsRNA). Several fitness parameters were observed in the to environmental stressors. The silencing of HSP90 generates injected insects to determine the effect of HSP83 attenuation variation by transposon-mediated Bcanonical^ mutagenesis on longevity, fecundity, and embryogenesis. (Specchia et al. 2010). The pleiotropic roles of HSP90 family members in D. melanogaster are associated with spermatogenesis, oogen- Material and methods esis, and embryogenesis (Ding et al. 1993; Yue et al. 1999; Song et al. 2007; Pisa et al. 2009) as well as the buffering of Aphid and plant rearing cryptic deleterious mutations in wild populations, longevity, and fecundity (Chen and Wagner 2012). In the beetle The rearing of A. pisum clone LL01 and the cultivation of the Tribolium castaneum, another holometabolous model insect, host plant Vicia faba var. minor were carried out as previously HSP83, which belongs to the HSP90 family, is expressed in described (Will and Vilcinskas 2015). During the experi- the whole body as well as in the oocytes where it is specifically ments, aphids were kept on detached, mature V. faba leaves located in the follicle cells. There it is differently expressed under controlled environmental conditions (Mutti et al. 2006; during different stages of oogenesis (Xu et al. 2010)andin Will and Vilcinskas 2015). response to heat shock (Xu et al. 2009). The latter suggests that HSP90 family members may regulate physiological pro- RNAi-mediated attenuation of HSP83 expression cesses in response to, e.g., environmental signals (Erlejman et al. 2014). In the whole body of T. castaneum, the expression The RNAi-mediated suppression of HSP83 expression was of HSP90 reaches its highest levels during the larval and pre- carried out as previously described (Will and Vilcinskas pupal phases and the attenuation of its expression negatively 2015). Briefly, the Ambion MEGAscript T7 Kit (Applied affects compound eye development in larvae, suggesting that Biosystems, Austin, TX) was used to prepare dsRNA according members of the HSP90 family are essential for normal post- to the manufacturer’s protocol. Gene-specific primers including embryonic development (Knorr and Vilcinskas 2011). A phy- the T7 polymerase promoter sequence at the 5′ end were used to logenetic analysis of arthropod HSP90 genes reveals that the synthesize a 530-bp HSP83 (GenBank XM_001943137.3) sequences cluster according to their taxonomic order, with ho- dsRNA template (forward primer 5′-TAA TAC GAC TCA lometabolous and hemimetabolous species showing clear sep- CTA TAG GGA GAG TGA GCC GCA TCA AGC CTA aration (Knorr and Vilcinskas 2011). AC-3′, reverse primer 5′-TAA TAC GAC TCA CTA TAG In response to heat shock, the hemimetabolous whitefly GGA GAT ATC AGC CTC GGC CTT CTG TC-3′). We ex- Bemisia tabaci shows no differential expression of members cluded the presence of sequence overlaps >19 bp with other of the HSP90 family (Lü and Wan 2011). In the aphid species A. pisum genes to avoid off-target effects. The QIAquick PCR Acyrthosiphon pisum, the first hemimetabolous insect with a Purification Kit (Quiagen, Hilden, Germany) was used for tem- completely sequenced genome (The International Aphid plate preparation, and dsRNA was produced using the Ambion Genomic Consortium 2010), Gerardo et al. (2010) demon- MEGAscript RNAi kit (Applied Biosystems). Primers were strated that HSP83 expression is induced fivefold in response designed with Primer3 (Rozen and Skaletsky 2000)andwere to heat stress. The latter study also showed only minor differ- purchased from Sigma-Aldrich (Taufkirchen, Germany). ences in expression levels between untreated controls and Control aphids were injected with equivalent concentrations aphids exposed to environmental stress or pathogens. To de- of dsRNA encoding the insect metalloproteinase inhibitor termine whether HSP90 family members show overlapping or IMPI (GenBank gbAY330624.1) from the greater wax moth diverse functions in holometabolous and hemimetabolous in- Galleria mellonella (Clermontetal.2004; Wedde et al. sects, we investigated the direct impact of HSP83 expression 2007). This sequence is not present in insects other than the on reproduction in the pea aphid A. pisum, as previously Lepidoptera (Mylonakis et al. 2016). shown for HSP90 in D. melanogaster (Chen and Wagner We injected 8-day-old apterous L4 nymphs with ∼50 ng 2012). Aphids have evolved complex life cycles including dsRNA in a total volume of 6.9 nl under a stereomicroscope the alternation of sexual and asexual reproduction, with an using a Nanoliter 2000 injector with a Sys-Micro4 controller Dev Genes Evol (World Precision Instruments, Berlin, Germany). Glass Image analysis for coloring and body plan area microcapillaries for injection were prepared using a PN- 30 puller (Narishige International Limited, London, UK). The quality of images of whole animals and dissected ovaries Prior to injection, aphids were immobilized with their was improved for brightness and contrast using Photoshop CS dorsal thorax on a vacuum holder (van Helden and v5.1 (Adobe Systems Inc., San Jose, CA, USA). Images Tjallingii 2000). The dsRNA was
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