The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties
Abstract Background Coleoid cephalopods have distinctive neural and morphological characteristics compared to other invertebrates. Early studies reported massive genomic rearrangements occurred before the split of octopus and squid lineages (Proc Natl Acad Sci U S A 116:3030-5, 2019), which might be...
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01500-2 |
| _version_ | 1797863570581487616 |
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| author | Dianhang Jiang Qun Liu Jin Sun Shikai Liu Guangyi Fan Lihua Wang Yaolei Zhang Inge Seim Shucai An Xin Liu Qi Li Xiaodong Zheng |
| author_facet | Dianhang Jiang Qun Liu Jin Sun Shikai Liu Guangyi Fan Lihua Wang Yaolei Zhang Inge Seim Shucai An Xin Liu Qi Li Xiaodong Zheng |
| author_sort | Dianhang Jiang |
| collection | DOAJ |
| description | Abstract Background Coleoid cephalopods have distinctive neural and morphological characteristics compared to other invertebrates. Early studies reported massive genomic rearrangements occurred before the split of octopus and squid lineages (Proc Natl Acad Sci U S A 116:3030-5, 2019), which might be related to the neural innovations of their brain, yet the details remain elusive. Here we combine genomic and single-nucleus transcriptome analyses to investigate the octopod chromosome evolution and cerebral characteristics. Results We present a chromosome-level genome assembly of a gold-ringed octopus, Amphioctopus fangsiao, and a single-nucleus transcriptome of its supra-esophageal brain. Chromosome-level synteny analyses estimate that the chromosomes of the ancestral octopods experienced multiple chromosome fission/fusion and loss/gain events by comparing with the nautilus genome as outgroup, and that a conserved genome organization was detected during the evolutionary process from the last common octopod ancestor to their descendants. Besides, protocadherin, GPCR, and C2H2 ZNF genes are thought to be highly related to the neural innovations in cephalopods (Nature 524:220–4, 2015), and the chromosome analyses pinpointed several collinear modes of these genes on the octopod chromosomes, such as the collinearity between PCDH and C2H2 ZNF, as well as between GPCR and C2H2 ZNF. Phylogenetic analyses show that the expansion of the octopod protocadherin genes is driven by a tandem-duplication mechanism on one single chromosome, including two separate expansions at 65 million years ago (Ma) and 8–14 Ma, respectively. Furthermore, we identify eight cell types (i.e., cholinergic and glutamatergic neurons) in the supra-esophageal brain of A. fangsiao, and the single-cell expression analyses reveal the co-expression of protocadherin and GPCR in specific neural cells, which may contribute to the neural development and signal transductions in the octopod brain. Conclusions The octopod genome analyses reveal the dynamic evolutionary history of octopod chromosomes and neural-related gene families. The single-nucleus transcriptomes of the supra-esophageal brain indicate their cellular heterogeneities and functional interactions with other tissues (i.e., gill), which provides a foundation for further octopod cerebral studies. |
| first_indexed | 2024-04-09T22:37:38Z |
| format | Article |
| id | doaj.art-e23020acbb5840678296a0b623e531a2 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T22:37:38Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-e23020acbb5840678296a0b623e531a22023-03-22T12:23:15ZengBMCBMC Biology1741-70072022-12-0120111510.1186/s12915-022-01500-2The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural noveltiesDianhang Jiang0Qun Liu1Jin Sun2Shikai Liu3Guangyi Fan4Lihua Wang5Yaolei Zhang6Inge Seim7Shucai An8Xin Liu9Qi Li10Xiaodong Zheng11Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Ocean University of ChinaBGI-QingDao, BGI-ShenzhenInstitute of Evolution & Marine Biodiversity (IEMB)Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Ocean University of ChinaBGI-QingDao, BGI-ShenzhenKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Ocean University of ChinaBGI-QingDao, BGI-ShenzhenIntegrative Biology Laboratory, College of Life Sciences, Nanjing Normal UniversityThe Affiliated Hospital of Qingdao UniversityBGI-QingDao, BGI-ShenzhenKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Ocean University of ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Ocean University of ChinaAbstract Background Coleoid cephalopods have distinctive neural and morphological characteristics compared to other invertebrates. Early studies reported massive genomic rearrangements occurred before the split of octopus and squid lineages (Proc Natl Acad Sci U S A 116:3030-5, 2019), which might be related to the neural innovations of their brain, yet the details remain elusive. Here we combine genomic and single-nucleus transcriptome analyses to investigate the octopod chromosome evolution and cerebral characteristics. Results We present a chromosome-level genome assembly of a gold-ringed octopus, Amphioctopus fangsiao, and a single-nucleus transcriptome of its supra-esophageal brain. Chromosome-level synteny analyses estimate that the chromosomes of the ancestral octopods experienced multiple chromosome fission/fusion and loss/gain events by comparing with the nautilus genome as outgroup, and that a conserved genome organization was detected during the evolutionary process from the last common octopod ancestor to their descendants. Besides, protocadherin, GPCR, and C2H2 ZNF genes are thought to be highly related to the neural innovations in cephalopods (Nature 524:220–4, 2015), and the chromosome analyses pinpointed several collinear modes of these genes on the octopod chromosomes, such as the collinearity between PCDH and C2H2 ZNF, as well as between GPCR and C2H2 ZNF. Phylogenetic analyses show that the expansion of the octopod protocadherin genes is driven by a tandem-duplication mechanism on one single chromosome, including two separate expansions at 65 million years ago (Ma) and 8–14 Ma, respectively. Furthermore, we identify eight cell types (i.e., cholinergic and glutamatergic neurons) in the supra-esophageal brain of A. fangsiao, and the single-cell expression analyses reveal the co-expression of protocadherin and GPCR in specific neural cells, which may contribute to the neural development and signal transductions in the octopod brain. Conclusions The octopod genome analyses reveal the dynamic evolutionary history of octopod chromosomes and neural-related gene families. The single-nucleus transcriptomes of the supra-esophageal brain indicate their cellular heterogeneities and functional interactions with other tissues (i.e., gill), which provides a foundation for further octopod cerebral studies.https://doi.org/10.1186/s12915-022-01500-2CephalopodOctopodaChromosomeGenomeSingle cellSupra-esophageal brain |
| spellingShingle | Dianhang Jiang Qun Liu Jin Sun Shikai Liu Guangyi Fan Lihua Wang Yaolei Zhang Inge Seim Shucai An Xin Liu Qi Li Xiaodong Zheng The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties BMC Biology Cephalopod Octopoda Chromosome Genome Single cell Supra-esophageal brain |
| title | The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| title_full | The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| title_fullStr | The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| title_full_unstemmed | The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| title_short | The gold-ringed octopus (Amphioctopus fangsiao) genome and cerebral single-nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| title_sort | gold ringed octopus amphioctopus fangsiao genome and cerebral single nucleus transcriptomes provide insights into the evolution of karyotype and neural novelties |
| topic | Cephalopod Octopoda Chromosome Genome Single cell Supra-esophageal brain |
| url | https://doi.org/10.1186/s12915-022-01500-2 |
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