The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis
Temperature is a crucial environmental factor that affects embryonic development, particularly for marine organisms with long embryonic development periods. However, the sensitive period of embryonic development and the role of autophagy/apoptosis in temperature regulation in cephalopods remain uncl...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2023-10-01
|
Series: | International Journal of Molecular Sciences |
Subjects: | |
Online Access: | https://www.mdpi.com/1422-0067/24/20/15365 |
_version_ | 1797573608542830592 |
---|---|
author | Yifan Liu Long Chen Fang Meng Tao Zhang Jun Luo Shuang Chen Huilai Shi Bingjian Liu Zhenming Lv |
author_facet | Yifan Liu Long Chen Fang Meng Tao Zhang Jun Luo Shuang Chen Huilai Shi Bingjian Liu Zhenming Lv |
author_sort | Yifan Liu |
collection | DOAJ |
description | Temperature is a crucial environmental factor that affects embryonic development, particularly for marine organisms with long embryonic development periods. However, the sensitive period of embryonic development and the role of autophagy/apoptosis in temperature regulation in cephalopods remain unclear. In this study, we cultured embryos of <i>Sepiella japonica</i>, a typical species in the local area of the East China Sea, at different incubation temperatures (18 °C, 23 °C, and 28 °C) to investigate various developmental aspects, including morphological and histological characteristics, mortality rates, the duration of embryonic development, and expression patterns of autophagy-related genes (<i>LC3</i>, <i>BECN1</i>, <i>Inx4</i>) and apoptosis marker genes (<i>Cas3</i>, <i>p53</i>) at 25 developmental stages. Our findings indicate that embryos in the high-temperature (28 °C) group had significantly higher mortality and embryonic malformation rates than those in the low-temperature (18 °C) group. Furthermore, high temperature (28 °C) shortened the duration of embryonic development by 7 days compared to the optimal temperature (23 °C), while low temperature (18 °C) caused a delay of 9 days. Therefore, embryos of <i>S. japonica</i> were more intolerant to high temperatures (28 °C), emphasizing the critical importance of maintaining an appropriate incubation temperature (approximately 23 °C). Additionally, our study observed, for the first time, that the Early blastula, Blastopore closure, and Optic vesicle to Caudal end stages were the most sensitive stages. During these periods, abnormalities in the expression of autophagy-related and apoptosis-related genes were associated with higher rates of mortality and malformations, highlighting the strong correlation and potential interaction between autophagy and apoptosis in embryonic development under varying temperature conditions. |
first_indexed | 2024-03-10T21:11:31Z |
format | Article |
id | doaj.art-219b41a3a39d4ab090a56ef13a151a82 |
institution | Directory Open Access Journal |
issn | 1661-6596 1422-0067 |
language | English |
last_indexed | 2024-03-10T21:11:31Z |
publishDate | 2023-10-01 |
publisher | MDPI AG |
record_format | Article |
series | International Journal of Molecular Sciences |
spelling | doaj.art-219b41a3a39d4ab090a56ef13a151a822023-11-19T16:45:37ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-10-0124201536510.3390/ijms242015365The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and ApoptosisYifan Liu0Long Chen1Fang Meng2Tao Zhang3Jun Luo4Shuang Chen5Huilai Shi6Bingjian Liu7Zhenming Lv8National Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaMarine Science and Technical College, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaZhejiang Province Key Lab of Mariculture and Enhancement, Marine Fisheries Research Institute of Zhejiang, Zhoushan 316021, ChinaMarine Science and Technical College, Zhejiang Ocean University, Zhoushan 316022, ChinaMarine Science and Technical College, Zhejiang Ocean University, Zhoushan 316022, ChinaZhejiang Province Key Lab of Mariculture and Enhancement, Marine Fisheries Research Institute of Zhejiang, Zhoushan 316021, ChinaNational Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaTemperature is a crucial environmental factor that affects embryonic development, particularly for marine organisms with long embryonic development periods. However, the sensitive period of embryonic development and the role of autophagy/apoptosis in temperature regulation in cephalopods remain unclear. In this study, we cultured embryos of <i>Sepiella japonica</i>, a typical species in the local area of the East China Sea, at different incubation temperatures (18 °C, 23 °C, and 28 °C) to investigate various developmental aspects, including morphological and histological characteristics, mortality rates, the duration of embryonic development, and expression patterns of autophagy-related genes (<i>LC3</i>, <i>BECN1</i>, <i>Inx4</i>) and apoptosis marker genes (<i>Cas3</i>, <i>p53</i>) at 25 developmental stages. Our findings indicate that embryos in the high-temperature (28 °C) group had significantly higher mortality and embryonic malformation rates than those in the low-temperature (18 °C) group. Furthermore, high temperature (28 °C) shortened the duration of embryonic development by 7 days compared to the optimal temperature (23 °C), while low temperature (18 °C) caused a delay of 9 days. Therefore, embryos of <i>S. japonica</i> were more intolerant to high temperatures (28 °C), emphasizing the critical importance of maintaining an appropriate incubation temperature (approximately 23 °C). Additionally, our study observed, for the first time, that the Early blastula, Blastopore closure, and Optic vesicle to Caudal end stages were the most sensitive stages. During these periods, abnormalities in the expression of autophagy-related and apoptosis-related genes were associated with higher rates of mortality and malformations, highlighting the strong correlation and potential interaction between autophagy and apoptosis in embryonic development under varying temperature conditions.https://www.mdpi.com/1422-0067/24/20/15365embryonic developmenttemperatureautophagyapoptosis<i>Sepiella japonica</i> |
spellingShingle | Yifan Liu Long Chen Fang Meng Tao Zhang Jun Luo Shuang Chen Huilai Shi Bingjian Liu Zhenming Lv The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis International Journal of Molecular Sciences embryonic development temperature autophagy apoptosis <i>Sepiella japonica</i> |
title | The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis |
title_full | The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis |
title_fullStr | The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis |
title_full_unstemmed | The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis |
title_short | The Effect of Temperature on the Embryo Development of Cephalopod <i>Sepiella japonica</i> Suggests Crosstalk between Autophagy and Apoptosis |
title_sort | effect of temperature on the embryo development of cephalopod i sepiella japonica i suggests crosstalk between autophagy and apoptosis |
topic | embryonic development temperature autophagy apoptosis <i>Sepiella japonica</i> |
url | https://www.mdpi.com/1422-0067/24/20/15365 |
work_keys_str_mv | AT yifanliu theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT longchen theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT fangmeng theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT taozhang theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT junluo theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT shuangchen theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT huilaishi theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT bingjianliu theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT zhenminglv theeffectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT yifanliu effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT longchen effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT fangmeng effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT taozhang effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT junluo effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT shuangchen effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT huilaishi effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT bingjianliu effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis AT zhenminglv effectoftemperatureontheembryodevelopmentofcephalopodisepiellajaponicaisuggestscrosstalkbetweenautophagyandapoptosis |