Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen

Bumblebee queens have remarkable spermathecae that store sperm for year-round reproduction. The spermathecal gland is regarded as a secretory organ that could benefit sperm storage. Queen mating provokes substantial physiological, behavioral, and gene expression changes. Here, the transcriptomes of...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Yueqin Guo, Qi Zhang, Xiao Hu, Chunxiu Pang, Jilian Li, Jiaxing Huang
Formato: article
Lenguaje:EN
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://doaj.org/article/10276f1cca8e4a409925c6876c1d9c30
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:10276f1cca8e4a409925c6876c1d9c30
record_format dspace
spelling oai:doaj.org-article:10276f1cca8e4a409925c6876c1d9c302021-12-01T06:32:48ZMating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen1664-802110.3389/fgene.2021.795669https://doaj.org/article/10276f1cca8e4a409925c6876c1d9c302021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fgene.2021.795669/fullhttps://doaj.org/toc/1664-8021Bumblebee queens have remarkable spermathecae that store sperm for year-round reproduction. The spermathecal gland is regarded as a secretory organ that could benefit sperm storage. Queen mating provokes substantial physiological, behavioral, and gene expression changes. Here, the transcriptomes of spermathecae were compared between virgins and mated queens of the bumblebee, Bombus terrestris L., at 24 h post mating. Differentially expressed genes were further validated by real time quantitative PCR and immunofluorescence assay. In total, the expression of 11, 069 and 10, 862 genes were identified in virgins and mated queens, respectively. We identified that 176 differentially expressed genes between virgin and mated queen spermathecae: 110 (62.5%) genes were upregulated, and 66 (37.5%) genes were downregulated in mated queens. Most of the differentially expressed genes validated by RT-qPCR were concentrated on immune response [i.e., leucine-rich repeat-containing protein 70 (35.8-fold), phenoloxidase 2 (41.9-fold), and defensin (4.9-fold)] and sperm storage [i.e., chymotrypsin inhibitor (6.2-fold), trehalose transporter Tret1 (1.7-, 1.9-, 2.4-, and 2.4-fold), and heterogeneous nuclear ribonucleoprotein A3 (1.2-, and 2.6-fold)] functions in the spermathecae of mated queens. Procollagen-lysine, 2-oxoglutarate 5-dioxygenase 1 (PLOD1) was hypothesized to promote the mating behavior according to RT-qPCR and immunofluorescence assay. The expression levels of most upregulated immune genes were decreased significantly at 3 days post mating. In conclusion, the external sperm transfer into spermathecae led to the significantly upregulated immune response genes in bumblebees. These gene expression differences in queen spermathecae contribute to understanding the bumblebee post mating regulatory network.Yueqin GuoQi ZhangQi ZhangXiao HuChunxiu PangChunxiu PangJilian LiJiaxing HuangFrontiers Media S.A.articlebumblebeeBombus terrestrisspermathecaetranscriptomeRT-qPCRgene expressionGeneticsQH426-470ENFrontiers in Genetics, Vol 12 (2021)
institution DOAJ
collection DOAJ
language EN
topic bumblebee
Bombus terrestris
spermathecae
transcriptome
RT-qPCR
gene expression
Genetics
QH426-470
spellingShingle bumblebee
Bombus terrestris
spermathecae
transcriptome
RT-qPCR
gene expression
Genetics
QH426-470
Yueqin Guo
Qi Zhang
Qi Zhang
Xiao Hu
Chunxiu Pang
Chunxiu Pang
Jilian Li
Jiaxing Huang
Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
description Bumblebee queens have remarkable spermathecae that store sperm for year-round reproduction. The spermathecal gland is regarded as a secretory organ that could benefit sperm storage. Queen mating provokes substantial physiological, behavioral, and gene expression changes. Here, the transcriptomes of spermathecae were compared between virgins and mated queens of the bumblebee, Bombus terrestris L., at 24 h post mating. Differentially expressed genes were further validated by real time quantitative PCR and immunofluorescence assay. In total, the expression of 11, 069 and 10, 862 genes were identified in virgins and mated queens, respectively. We identified that 176 differentially expressed genes between virgin and mated queen spermathecae: 110 (62.5%) genes were upregulated, and 66 (37.5%) genes were downregulated in mated queens. Most of the differentially expressed genes validated by RT-qPCR were concentrated on immune response [i.e., leucine-rich repeat-containing protein 70 (35.8-fold), phenoloxidase 2 (41.9-fold), and defensin (4.9-fold)] and sperm storage [i.e., chymotrypsin inhibitor (6.2-fold), trehalose transporter Tret1 (1.7-, 1.9-, 2.4-, and 2.4-fold), and heterogeneous nuclear ribonucleoprotein A3 (1.2-, and 2.6-fold)] functions in the spermathecae of mated queens. Procollagen-lysine, 2-oxoglutarate 5-dioxygenase 1 (PLOD1) was hypothesized to promote the mating behavior according to RT-qPCR and immunofluorescence assay. The expression levels of most upregulated immune genes were decreased significantly at 3 days post mating. In conclusion, the external sperm transfer into spermathecae led to the significantly upregulated immune response genes in bumblebees. These gene expression differences in queen spermathecae contribute to understanding the bumblebee post mating regulatory network.
format article
author Yueqin Guo
Qi Zhang
Qi Zhang
Xiao Hu
Chunxiu Pang
Chunxiu Pang
Jilian Li
Jiaxing Huang
author_facet Yueqin Guo
Qi Zhang
Qi Zhang
Xiao Hu
Chunxiu Pang
Chunxiu Pang
Jilian Li
Jiaxing Huang
author_sort Yueqin Guo
title Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
title_short Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
title_full Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
title_fullStr Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
title_full_unstemmed Mating Stimulates the Immune Response and Sperm Storage-Related Genes Expression in Spermathecae of Bumblebee (Bombus terrestris) Queen
title_sort mating stimulates the immune response and sperm storage-related genes expression in spermathecae of bumblebee (bombus terrestris) queen
publisher Frontiers Media S.A.
publishDate 2021
url https://doaj.org/article/10276f1cca8e4a409925c6876c1d9c30
work_keys_str_mv AT yueqinguo matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT qizhang matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT qizhang matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT xiaohu matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT chunxiupang matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT chunxiupang matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT jilianli matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
AT jiaxinghuang matingstimulatestheimmuneresponseandspermstoragerelatedgenesexpressioninspermathecaeofbumblebeebombusterrestrisqueen
_version_ 1718405457205264384