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A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches

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A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches HIGHLIGHTED ARTICLE | INVESTIGATION A Crucial Caste Regulation Gene Detected by Comparing Termites and Sister Group Cockroaches Yudai Masuoka,*,†,1 Kouhei Toga,‡ Christine A. Nalepa,§ and Kiyoto Maekawa*,1 *Graduate School of Science and Engineering, University of Toyama, 930-8555, Japan, †Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, 305-8634, Japan, ‡Department of Integrated Sciences in Physics and Biology, Nihon University, Tokyo 156-8550, Japan, and §Department of Entomology, North Carolina State University, Raleigh, North Carolina 27695-7613 ORCID IDs: 0000-0001-9164-5178 (Y.M.); 0000-0002-2354-1059 (K.M.) ABSTRACT Sterile castes are a defining criterion of eusociality; investigating their evolutionary origins can critically advance theory. In termites, the soldier caste is regarded as the first acquired permanently sterile caste. Previous studies showed that juvenile hormone (JH) is the primary factor inducing soldier differentiation, and treatment of workers with artificial JH can generate presoldier differentiation. It follows that a shift from a typical hemimetabolous JH response might be required for soldier formation during the course of termite evolution within the cockroach clade. To address this possibility, analysis of the role of JH and its signaling pathway was performed in the termite Zootermopsis nevadensis and compared with the wood roach Cryptocercus punctulatus, a member of the sister group of termites. Treatment with a JH analog (JHA) induced a nymphal molt in C. punctulatus. RNA interference (RNAi) of JH receptor Methoprene tolerant (Met) was then performed, and it inhibited the presoldier molt in Z. nevadensis and the nymphal molt in C. punctulatus. Knockdown of Met in both species inhibited expression of 20-hydroxyecdysone (20E; the active form of ecdysone) synthesis genes. However, in Z. nevadensis, several 20E signaling genes were specifically inhibited by Met RNAi. Consequently, RNAi of these genes were performed in JHA-treated termite individuals. Knockdown of 20E signaling and nuclear receptor gene, Hormone receptor 39 (HR39/FTZ-F1b) resulted in newly molted individuals with normal worker phenotypes. This is the first report of the JH–Met signaling feature in termites and Cryptocercus. JH-dependent molting activation is shared by both taxa and mediation between JH receptor and 20E signalings for soldier morphogenesis is specific to termites. KEYWORDS 20-hydroxyecdysone; Cryptocercus; juvenile hormone; soldier differentiation; termites HE complex eusocial society of one-piece termites (those sterile caste (Nalepa 2011). The molecular basis of termite Tusing a single log as food and nest) consists of a repro- soldier evolution, however, is still far from fully understood. ductive caste (queen and king) and temporarily or per- Increasing juvenile hormone (JH) titers triggers soldier dif- manently sterile castes (workers—also known as helpers, ferentiation in workers via an intermediate presoldier stage pseudergates, or alloparents—and soldiers, respectively). (Noirot 1985; Roisin 1996) which can be induced in many Termites are a monophyletic group within cockroaches (Lo termite species by treating workers with JH or JH analogs et al. 2000; Inward et al. 2007; Bourguignon et al. 2017) and (JHA) (Watanabe et al. 2014; Scharf 2015). This is in con- the soldier caste is regarded as the first acquired permanently trast to other insects in which JH maintains larval traits and has an inhibitory function on molting via suppression of pro- Copyright © 2018 by the Genetics Society of America thoracicotropic hormone (PTTH) release (Gilbert 2012). It is doi: https://doi.org/10.1534/genetics.118.301038 Manuscript received April 17, 2018; accepted for publication June 21, 2018; published also known that treatment with JHA can inhibit or delay Early Online June 22, 2018. 20-hydroxyecdysone (20E; the active form of ecdysone) syn- Supplemental material available at Figshare: https://doi.org/10.25386/genetics. thesis and suppress expression of the 20E signaling genes 6564572. 1Corresponding authors: Institute of Agrobiological Sciences, National Agriculture and (Berger et al. 1992; Zufelato et al. 2000; Aribi et al. 2006). Food Research Organization, 1-2 Owashi, Tsukuba 305-8634, Japan. E-mail: In the German cockroach, Blattella germanica, JHA treatment [email protected]; and Graduate School of Science and Engineering, University of Toyama, 3190 Gofuku, Toyama 930-8555, Japan. E-mail: kmaekawa@ of young instars inhibited 20E synthesis and resulted in de- sci.u-toyama.ac.jp velopmental arrest in the nymphal stage (Hangartner and Genetics, Vol. 209, 1225–1234 August 2018 1225 Masner 1973; Masner et al. 1975). Furthermore, JH inhibits Japan, in May 2015 and 2016 and kept at 25° in constant expression levels of the 20E-induced heat shock protein gene darkness until the following experiments were performed. in Drosophila melanogaster (Berger et al. 1992), but in D. mela- Young instar nymphs [head width = 1.31–1.57 mm, class nogaster and Manduca sexta JH activates expression level of the 1 (third or fourth instars); and head width = 1.91–2.12 mm, 20E-inducible nuclear receptor gene E75 (Dubrovskaya et al. class 2 (probably fifth instars) (Nalepa 1984, 1990)] of 2004). There is therefore a possibility that one or more uniden- C. punctulatus were collected at Mountain Lake Biological tified JH signaling pathways related to the involvement of 20E Station, Giles County, VA, in April 2015–2017. These individ- in both molting (from worker to presoldier) and morphological uals were kept at 15° in constant darkness until use. modification (formation of weapons such as enlarged mandi- JHA treatment bles) were acquired during the course of termite evolution. To clarify this hypothesis, it is necessary to analyze the role of JH in In Z. nevadensis, according to the methods of Saiki et al. nymphal development in additional cockroaches, particularly (2014), filter paper was treated with 0 (for control) or those of the sister group of termites, cockroaches in the family 10 mg JHA (pyriproxyfen; Wako, Osaka, Japan) dissolved Cryptocercidae (wood roaches; Cryptocercus spp.). in 400 ml acetone and placed in a 90-mm petri dish with Recently,the presence of JH signaling genes has been estab- 10 individual seventh instars. In C. punctulatus, filter paper lished in some model insect species (Jindra et al. 2015). In both and 200 mg cellulose powder (Wako) was treated with 0 (for hemimetabolous (without pupal stage, including termites and control) or 100 mg pyriproxyfen dissolved in 200 ml acetone cockroaches) and holometabolous (with pupal stage) insects, a and placed in a 60-mm petri dish with 10 class-1 or -2 JH receptor, Methoprene tolerant (Met) and a steroid receptor nymphs. All petri dishes were kept in an incubator at 25° coactivator (SRC; taiman; FISC) induce the expression of (Z. nevadensis)or15° (C. punctulatus) in constant darkness Krüppel homolog 1 (Kr-h1), which is necessary for JH to func- for 30 days. Dishes were checked for dead and newly molted tion in maintaining developmental status quo (Riddiford 2013; individuals every 24 hr. Molting rates in each species were Jindra et al. 2015). Met and Kr-h1 knockdown inhibited molts compared between JHA and acetone control treatments. in the penultimate instar and induced precocious metamor- Fisher’s exact test was performed using Mac Statistical Anal- phosis in Tribolium castaneum (Konopova and Jindra 2007; ysis version 2.0 (Esumi, Tokyo, Japan). Minakuchi et al. 2009) and B. germanica (Lozano and Bellés RNAi experiment 2011, 2014). On the other hand, although Met is generally involved in insect ovarian development, Kr-h1 function dif- Each double-strand RNA (dsRNA) was generated by the fered somewhat among species (Konopova et al. 2011; Song partial complementary DNA (cDNA) sequences amplified et al. 2014). Specifically, Kr-h1 was not required for ovarian by the gene-specific primers (Supplemental Material, Table development in the linden bug, Pyrrhocoris apterus (Smykal S1) using T7 RNA polymerase with a MEGAscript T7 Tran- et al. 2014). In termites, a previous study demonstrated that scription Kit (Ambion, Austin, TX). As in previous studies RNA interference (RNAi) of Met suppressed soldier-specific (Masuoka et al. 2015, 2018; Masuoka and Maekawa morphogenesis in Zootermopsis nevadensis (Masuoka et al. 2016a,b), GFP was selected as a control gene, and dsRNA 2015). Roles of other JH signaling genes, including Kr-h1, was generated using GFP vector pQBI-polII (Wako). Specific for termite soldier differentiation, however,have not been clar- primers of the following genes of Z. nevadensis were designed ified. Moreover, in Cryptocercus cockroaches, no studies have from genome sequence data using Primer3Plus software focused on the function of JH signaling genes during molting. (Untergasser et al. 2007): ZnMet (gene identifier Znev_09571; To determine potential differences in the role of JH during Terrapon et al. 2014), ZnSRC (Znev_05083), ZnKr-h1 molting in C. punctulatus and termites, JHA treatment of (Znev_04171), ZnShr (Znev_16529), ZnSpo (Znev_04417), young nymphs was performed in C. punctulatus. To further ZnEcR (Znev_13925), ZnE74 (Znev_00833), ZnE75 clarify the function of JH signaling genes in these taxa, RNAi (Znev_11406), ZnHR3 (Znev_14707), and ZnHR39 knockdown of Met and Kr-h1 was conducted in both Z. neva- (Znev_00332). Specific primers of the following genes of densis and C. punctulatus. Furthermore, expression and func- C. punctulatus
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