TY - JOUR
T1 - Control of Pem protein level by localized maternal factors for transcriptional regulation in the germline of the ascidian, Halocynthia roretzi
AU - Miyaoku, Kaori
AU - Nakamoto, Ayaki
AU - Nishida, Hiroki
AU - Kumano, Gaku
N1 - Funding Information:
This study was supported by Grant-in-Aid for Scientific Research (KAKENHI) 23570252 and 15K07071, Japan Society for the promotion of Sciences (https://www.jsps.go.jp/english/index. html) and by Grant-in-Aid for Scientific Research (KAKENHI) on Innovative Areas, ‘Mechanisms regulating gamete formation in animals’ (16H01250), the Ministry of Education, Culture, Sports, Science and Technology (http://www.mext. go.jp/en/), to Gaku Kumano. Also, this study was supported by Grant-in-Aid for Scientific Research (KAKENHI) 22370078, Japan Society for the Promotion of Sciences (https://www.jsps.go.jp/ english/index.html), to Hiroki Nishida. These funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. We thank the staff members from Otsuchi International Coastal Research Center and Asamushi Research Center for Marine Biology for their assistance in collecting live ascidian adults and from Seto Marine Biological Laboratory for their help in maintaining them. We are also grateful to Dr. T. Numakunai for his advices for maintaining adult ascidians, and Mr. T. Zheng for reading the manuscript.
Publisher Copyright:
© 2018 Miyaoku et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2018/4
Y1 - 2018/4
N2 - Localized maternal mRNAs play important roles in embryogenesis, e.g. the establishment of embryonic axes and the developmental cell fate specification, in various animal species. In ascidians, a group of maternal mRNAs, called postplasmic/PEM RNAs, is localized to a subcellular structure, called the Centrosome-Attracting Body (CAB), which contains the ascidian germ plasm, and is inherited by the germline cells during embryogenesis. Posterior end mark (Pem), a postplasmic/PEM RNAs member, represses somatic gene expression in the germline during cleavage stages by inhibition of RNA polymerase II activity. However, the functions of other postplasmic/ PEM RNAs members in germline formation are largely unknown. In this study, we analyzed the functions of two postplasmic/PEM RNAs, Popk-1 and Zf-1, in transcriptional regulation in the germline cells. We show that Popk-1 contributes to transcriptional quiescence by controlling the size of the CAB and amount of Pem protein translated at the CAB. Our studies also indicated that zygotic expression of a germline gene starts around the onset of gastrulation and that the decrease of Pem protein is necessary and sufficient for the zygotic germline gene expression. Finally, further studies showed that the decrease of the Pem protein level is facilitated by Zf-1. Taken together, we propose that postplasmic/PEM RNAs such as Popk-1 and Zf-1 control the protein level of the transcriptional repressor Pem and regulate its transcriptional state in the ascidian germline.
AB - Localized maternal mRNAs play important roles in embryogenesis, e.g. the establishment of embryonic axes and the developmental cell fate specification, in various animal species. In ascidians, a group of maternal mRNAs, called postplasmic/PEM RNAs, is localized to a subcellular structure, called the Centrosome-Attracting Body (CAB), which contains the ascidian germ plasm, and is inherited by the germline cells during embryogenesis. Posterior end mark (Pem), a postplasmic/PEM RNAs member, represses somatic gene expression in the germline during cleavage stages by inhibition of RNA polymerase II activity. However, the functions of other postplasmic/ PEM RNAs members in germline formation are largely unknown. In this study, we analyzed the functions of two postplasmic/PEM RNAs, Popk-1 and Zf-1, in transcriptional regulation in the germline cells. We show that Popk-1 contributes to transcriptional quiescence by controlling the size of the CAB and amount of Pem protein translated at the CAB. Our studies also indicated that zygotic expression of a germline gene starts around the onset of gastrulation and that the decrease of Pem protein is necessary and sufficient for the zygotic germline gene expression. Finally, further studies showed that the decrease of the Pem protein level is facilitated by Zf-1. Taken together, we propose that postplasmic/PEM RNAs such as Popk-1 and Zf-1 control the protein level of the transcriptional repressor Pem and regulate its transcriptional state in the ascidian germline.
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U2 - 10.1371/journal.pone.0196500
DO - 10.1371/journal.pone.0196500
M3 - Article
C2 - 29709000
AN - SCOPUS:85046280953
SN - 1932-6203
VL - 13
JO - PLoS ONE
JF - PLoS ONE
IS - 4
M1 - e0196500
ER -