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De Novo Transcriptome Analysis for Examination of the Nutrition

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De Novo Transcriptome Analysis for Examination of the Nutrition Sakamoto et al. BMC Res Notes (2021) 14:182 https://doi.org/10.1186/s13104-021-05600-0 BMC Research Notes RESEARCH NOTE Open Access De novo transcriptome analysis for examination of the nutrition metabolic system related to the evolutionary process through which stick insects gain the ability of fight (Phasmatodea) Takuma Sakamoto1,2, Shunya Sasaki2, Nobuki Yamaguchi2, Miho Nakano2, Hiroki Sato2, Kikuo Iwabuchi2, Hiroko Tabunoki1,2, Richard J. Simpson1,3 and Hidemasa Bono4,5* Abstract Objective: Insects are the most evolutionarily successful groups of organisms, and this success is largely due to their fight ability. Interestingly, some stick insects have lost their fight ability despite having wings. To elucidate the shift from wingless to fying forms during insect evolution, we compared the nutritional metabolism system among fight- winged, fightless-winged, and fightless-wingless stick insect groups. Results: Here, we report RNA sequencing of midgut transcriptome of Entoria okinawaensis, a prominent Japanese fightless-wingless stick insect, and the comparative analysis of its transcriptome in publicly available midgut tran- scriptomes obtained from seven stick insect species. A gene enrichment analysis for diferentially expressed genes, including those obtained from winged vs wingless and fight vs fightless genes comparisons, revealed that carbo- hydrate metabolic process-related genes were highly expressed in the winged stick insect group. We also found that the expression of the mitochondrial enolase superfamily member 1 transcript was signifcantly higher in the winged stick insect group than in the wingless stick insect group. Our fndings could indicate that carbohydrate metabolic processes are related to the evolutionary process through which stick insects gain the ability of fight. Keywords: Stick insect, RNA sequencing, Transcriptome assembly, Transcriptome database, Enolase, Glycolytic pathway Introduction insects exist worldwide, and some females have lost the Te evolutionary success of insects has been attributed ability of fight [4]. Interestingly, wingless insects tend to their fight ability and small size. Specifcally, insects to exhibit higher female fecundity [5]. In addition, some are able to expand to new environmental niches due to stick insects lost their fight ability despite having wings, their fight ability [1–3]. More than 3000 species of stick and this feature might play an important role in evolu- tionary diversifcation [6]. Te loss of fight ability could be involved in nutrient metabolism to produce energy, *Correspondence: [email protected] 5 Program of Biomedical Science, Graduate School of Integrated Sciences but the diferences in the nutrient metabolic system for Life, Hiroshima University, 3-10-23 Kagamiyama, Higashi-Hiroshima, between fight and fightless insects and between winged Hiroshima 739-0046, Japan and wingless insects have not been examined. Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Sakamoto et al. BMC Res Notes (2021) 14:182 Page 2 of 7 Te midgut is a main organ that contributes to food Te midguts and fat body were weighed, homogenized digestion and nutrient metabolism [7]. It has been sug- with lysis bufer from a PureLink® RNA extraction kit gested that the insect midgut physiology is strongly (Termo Fisher Scientifc Inc., Valencia, CA, USA) and afected by the presence of unique cell types that confer then centrifuged at 13,000×g for 10 min. Te superna- peculiar features to this organ, and these midgut cells tants were then collected and processed for RNA puri- might support species-specifc nutrient metabolism [8]. fcation according to the manufacturer’s instructions. Te stick insect Entoria okinawaensis has the larg- Purifed total RNA (1 μg) samples were processed for est body size among Japanese stick insect species and is RNA sequencing or quantitative RT-PCR (qRT-PCR). wingless, which resulted in the loss of its fying ability. E. okinawaensis is both male and female and undergoes RNA sequencing sexual reproduction [9]. We are interested in why stick Te RNA quality was assessed using Bioanalyzer 2100 insects lost their fight ability during the process of evolu- (Agilent Technologies, Santa Clara, CA, USA). Libraries tion and the relationship between nutrition metabolism for cDNA sequencing were constructed using the Illu- and fight ability in stick insects. mina TruSeq v2 kit (Illumina Inc., San Diego, CA, USA) In this study, we compared the nutrient metabolic according to the manufacturer’s protocol. RNA sequenc- systems of fight-winged, fightless-winged and fight- ing of three biological replicates of E. okinawaensis mid- less-wingless stick insect groups using our midgut tran- gut samples was performed using HiSeq 2500. scriptome data and those from public database and found the expression of transcripts related to the production Functional annotation pipeline of energy in carbohydrate metabolic processes in the Trinity software (v2.5.1) was used to construct de novo winged stick insect groups. transcriptomes [10], and TransDecoder (v5.2.0) was used to fnd coding regions within transcripts [11]. Te tran- Main text scriptome sequences were compared through successive Methods execution of BLASTP program (v2.7.1 ) [12] against Insects + protein datasets described below. We obtained Entoria okinawaensis from Amami- Ohshima in Kagoshima, Japan, in 2011 and Ishigaki Meta‑analysis of public data Island in Okinawa, Japan, in 2013 and maintained the We utilized transcriptome assemblies available in Tran- insects in an insectary room at Tokyo University of Agri- scriptome Shotgun Assembly (TSA) database. If unavail- culture and Technology prior to collecting their eggs for able in TSA, transcriptomes were constructed locally this study. Te eggs were maintained at 25 °C under 70% using Trinity. A program (align_and_estimate_abun- humidity and a 16-h light/8-h dark cycle. After hatch- dance.pl) in Trinity software with Kallisto (v0.43.1) was ing, the frst-instar nymphs were maintained on young used to estimate the abundance of reads [13]. rose leaves, and the insects at the second-instar nymph to adult stages were maintained on Quercus myrsinifolia or Gene enrichment and pathway analyses rose (Rosa multifora) leaves under 70% humidity and a 16-h light/8-h dark cycle. Metascape was used for the gene set enrichment analysis Sipyloidea sipylus eggs were gifted by Dr. Takeshi [14]. Using EC numbers from our functional annotation Yokoyama at Tokyo University of Agriculture and Tech- pipeline, those genes related to carbohydrate metabolic nology. Te eggs were maintained at 25 °C under 70% processes in E. okinawaensis were mapped to refer- humidity and a 16-h light/8-h dark cycle. After hatching, ence pathway maps in Kyoto Encyclopedia of Genes and the frst-instar nymphs were maintained on young rose Genomes (KEGG) [15]. leaves, and the insects from the second-instar nymph to the adult stage were maintained on rose (Rosa multifora) Data visualization leaves under 70% humidity and a 16-h light/8-h dark A heatmap of the hierarchical clustering and a scatter cycle. plot with gene IDs were generated using TIBCO Spotfre Desktop version 7.6.0 (TIBCO Software Inc., Palo Alto, Sample collection and purifcation of total RNA CA, USA) with TIBCO Software’s “Better World” pro- gram license. Te midguts (n = 3; samples 1 and 2 were females, and sample 3 was male) and fat bodies (n = 3) were dissected Analysis of enolase‑coding sequences from adult E. okinawaensis, and the midguts (n = 3) and fat bodies (n = 3) from adult S. sipylus were also dis- HMMsearch program (v3.2.1) [16] was used to detect sected. Tese tissues were stored at − 80 °C until use. enolase candidates using profles of enolase N-terminal Sakamoto et al. BMC Res Notes (2021) 14:182 Page 3 of 7 domain (Enolase_N, PF03952) and C-terminal domain expression levels. All the data were calibrated against (Enolase_C, PF00113) in Pfam database (v32.0) [17]. universal reference data, and relative quantifcation (RQ) values of three biological replicates were used to rep- qRT‑PCR resent the relative expression level against a reference We used 0.5 μg of total RNA purifed from the midgut sample. of male and female adults of fight (S. sipylus) and fight- less (E. okinawaensis) stick insects for cDNA synthesis. Results and discussion cDNA synthesis was performed using a PrimeScript™ In this study, we developed functional annotation pipe- First-strand cDNA Synthesis Kit (Takara Co. Ltd., Tokyo, line for E. okinawaensis midgut transcriptome (Fig. 1). Japan) according to the manufacturer’s instructions. qRT- First, we generated more than 100 million 100-bp PCR was performed with a Step One plus Real-Time PCR paired-end reads from each of three biological replicate System (Applied Biosystems, Foster City, CA, USA) using RNA libraries of the E. okinawaensis midgut (Addi- the delta-delta Ct method. Te 20-μL reaction volumes tional fle 1: Table S2).
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