Transcriptomic analysis of the testicular fusion in Spodoptera litura

Abstract Background Lepidoptera is one group of the largest plant-feeding insects and Spodoptera litura (Lepidoptera: Noctuidae) is one of the most serious agricultural pests in Asia countries. An interesting and unique phenomenon for gonad development of Lepidoptera is the testicular fusion. Two se...

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Main Authors: Yaqing Chen, Jun Ou, Yucheng Liu, Qiong Wu, Liang Wen, Sichun Zheng, Sheng Li, Qili Feng, Lin Liu
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-6494-3
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author Yaqing Chen
Jun Ou
Yucheng Liu
Qiong Wu
Liang Wen
Sichun Zheng
Sheng Li
Qili Feng
Lin Liu
author_facet Yaqing Chen
Jun Ou
Yucheng Liu
Qiong Wu
Liang Wen
Sichun Zheng
Sheng Li
Qili Feng
Lin Liu
author_sort Yaqing Chen
collection DOAJ
description Abstract Background Lepidoptera is one group of the largest plant-feeding insects and Spodoptera litura (Lepidoptera: Noctuidae) is one of the most serious agricultural pests in Asia countries. An interesting and unique phenomenon for gonad development of Lepidoptera is the testicular fusion. Two separated testes fused into a single one during the larva-to-pupa metamorphosis, which is believed to contribute to sperm production and the prevalence in field. To study the molecular mechanism of the testicular fusion, RNA sequencing (RNA-seq) experiments of the testes from 4-day-old sixth instar larvae (L6D4) (before fusion), 6-day-old sixth instar larvae (L6D6, prepupae) (on fusing) and 4-day-old pupae (P4D) (after fusion) of S. litura were performed. Results RNA-seq data of the testes showed that totally 12,339 transcripts were expressed at L6D4, L6D6 and P4D stages. A large number of differentially expressed genes (DEGs) were up-regulated from L6D4 to L6D6, and then more genes were down-regulated from L6D6 to P4D. The DEGs mainly belongs to the genes related to the 20E signal transduction pathway, transcription factors, chitin metabolism related enzymes, the families of cytoskeleton proteins, extracellular matrix (ECM) components, ECM-related protein, its receptor integrins and ECM-remodeling enzymes. The expression levels of these genes that were up-regulated significantly during the testicular fusion were verified by qRT-PCR. The matrix metalloproteinases (MMPs) were found to be the main enzymes related to the ECM degradation and contribute to the testicular fusion. The testis was not able to fuse if MMPs inhibitor GM6001 was injected into the 5th abdomen region at L6D6 early stage. Conclusions The transcriptome and DEGs analysis of the testes at L6D4, L6D6 and P4D stages provided genes expression information related to the testicular fusion in S. litura. These results indicated that cytoskeleton proteins, ECM-integrin interaction genes and ECM-related proteins were involved in cell migration, adhesion and fusion during the testicular fusion. The ECM degradation enzymes MMPs probably play a critical role in the fusion of testis.
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spelling doaj.art-96f27042c4eb45e7b82bca2c3b8a93fb2022-12-22T01:18:38ZengBMCBMC Genomics1471-21642020-02-0121111510.1186/s12864-020-6494-3Transcriptomic analysis of the testicular fusion in Spodoptera lituraYaqing Chen0Jun Ou1Yucheng Liu2Qiong Wu3Liang Wen4Sichun Zheng5Sheng Li6Qili Feng7Lin Liu8Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityGuangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal UniversityAbstract Background Lepidoptera is one group of the largest plant-feeding insects and Spodoptera litura (Lepidoptera: Noctuidae) is one of the most serious agricultural pests in Asia countries. An interesting and unique phenomenon for gonad development of Lepidoptera is the testicular fusion. Two separated testes fused into a single one during the larva-to-pupa metamorphosis, which is believed to contribute to sperm production and the prevalence in field. To study the molecular mechanism of the testicular fusion, RNA sequencing (RNA-seq) experiments of the testes from 4-day-old sixth instar larvae (L6D4) (before fusion), 6-day-old sixth instar larvae (L6D6, prepupae) (on fusing) and 4-day-old pupae (P4D) (after fusion) of S. litura were performed. Results RNA-seq data of the testes showed that totally 12,339 transcripts were expressed at L6D4, L6D6 and P4D stages. A large number of differentially expressed genes (DEGs) were up-regulated from L6D4 to L6D6, and then more genes were down-regulated from L6D6 to P4D. The DEGs mainly belongs to the genes related to the 20E signal transduction pathway, transcription factors, chitin metabolism related enzymes, the families of cytoskeleton proteins, extracellular matrix (ECM) components, ECM-related protein, its receptor integrins and ECM-remodeling enzymes. The expression levels of these genes that were up-regulated significantly during the testicular fusion were verified by qRT-PCR. The matrix metalloproteinases (MMPs) were found to be the main enzymes related to the ECM degradation and contribute to the testicular fusion. The testis was not able to fuse if MMPs inhibitor GM6001 was injected into the 5th abdomen region at L6D6 early stage. Conclusions The transcriptome and DEGs analysis of the testes at L6D4, L6D6 and P4D stages provided genes expression information related to the testicular fusion in S. litura. These results indicated that cytoskeleton proteins, ECM-integrin interaction genes and ECM-related proteins were involved in cell migration, adhesion and fusion during the testicular fusion. The ECM degradation enzymes MMPs probably play a critical role in the fusion of testis.http://link.springer.com/article/10.1186/s12864-020-6494-3Transcriptomic analysisTesticular fusionSpodoptera lituraExtracellular matrix (ECM)Matrix metalloproteinase (MMP)
spellingShingle Yaqing Chen
Jun Ou
Yucheng Liu
Qiong Wu
Liang Wen
Sichun Zheng
Sheng Li
Qili Feng
Lin Liu
Transcriptomic analysis of the testicular fusion in Spodoptera litura
BMC Genomics
Transcriptomic analysis
Testicular fusion
Spodoptera litura
Extracellular matrix (ECM)
Matrix metalloproteinase (MMP)
title Transcriptomic analysis of the testicular fusion in Spodoptera litura
title_full Transcriptomic analysis of the testicular fusion in Spodoptera litura
title_fullStr Transcriptomic analysis of the testicular fusion in Spodoptera litura
title_full_unstemmed Transcriptomic analysis of the testicular fusion in Spodoptera litura
title_short Transcriptomic analysis of the testicular fusion in Spodoptera litura
title_sort transcriptomic analysis of the testicular fusion in spodoptera litura
topic Transcriptomic analysis
Testicular fusion
Spodoptera litura
Extracellular matrix (ECM)
Matrix metalloproteinase (MMP)
url http://link.springer.com/article/10.1186/s12864-020-6494-3
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