Dynamic transcriptome analysis reveals the gene network of gonadal development from the early history life stages in dwarf surfclam Mulinia lateralis

Abstract

Background Gonadal development is driven by a complex genetic cascade in vertebrates. However, related information remains limited in molluscs owing to the long generation time and the difficulty in maintaining whole life cycle in the lab. The dwarf surfclam Mulinia lateralis is considered an ideal bivalve model due to the short generation time and ease to breed in the lab. Results To gain a comprehensive understanding of gonadal development in M. lateralis, we conducted a combined morphological and molecular analysis on the gonads of 30 to 60 dpf. Morphological analysis showed that gonad formation and sex differentiation occur at 35 and 40–45 dpf, respectively; then the gonads go through gametogenic cycle. Gene co-expression network analysis on 40 transcriptomes of 35–60 dpf gonads identifies seven gonadal development-related modules, including two gonad-forming modules (M6, M7), three sex-specific modules (M14, M12, M11), and two sexually shared modules (M15, M13). The modules participate in different biological processes, such as cell communication, glycan biosynthesis, cell cycle, and ribosome biogenesis. Several hub transcription factors including SOX2, FOXZ, HSFY, FOXL2 and HES1 are identified. The expression of top hub genes from sex-specific modules suggests molecular sex differentiation (35 dpf) occurs earlier than morphological sex differentiation (40–45 dpf). Conclusion This study provides a deep insight into the molecular basis of gonad formation, sex differentiation and gametogenesis in M. lateralis, which will contribute to a comprehensive understanding of the reproductive regulation network in molluscs.

Gonadal Transcriptome Sequencing Analysis Reveals the Candidate Sex-Related Genes and Signaling Pathways in the East Asian Common Octopus, Octopus sinensis

“…Based on the transcriptome analysis, at least 21 DEGs involved in sex determination/differentiation were identified. These genes included Dmrt1 , Foxn5 , Foxj1 , Sox14 , Sox30 , Fem1 , Tssk6 , Tssk1 , Tssk3 and other potential candidates that have been reported previously in vertebrates and in mollusks [ 21 , 22 , 23 , 24 , 25 , 26 , 27 ].…”

“…Currently, a number of sex-related genes have been identified from diverse mollusks based on a gonadal transcriptome analysis. These include transcription factor Sox2 ( Sox2 ), forkhead box protein Z ( Foxz ), heat shock transcription factor, Y-linked ( Hsfy ), forkhead box protein L2 ( Foxl2 ) and transcription factor HES-1 ( Hes1 ) in dwarf surf clam ( M. lateralis ) [ 21 ]; Foxl2 , beta-catenin ( β-catenin ) and sex-lethal ( Sxl ) in blood clam ( Tegillarca granosa ) [ 22 ]; FoxL2 and doublesex- and mab-3-related transcription factor A2 ( Dmrta2 ) in Pacific abalone ( Haliotis discus hannai ) [ 23 ]; transcription factor SoxH ( SoxH ), FoxL2 , doublesex ( Dsx ), feminization ( Fem ), GATA binding protein 4 ( Gata4 ), wnt family member 4 ( Wnt4 ) and β-catenin in Pacific oyster ( C. gigas ) [ 24 , 25 ]; testis-specific serine/threonine-protein kinase 1 ( Tssk1 ), testis-specific serine/threonine-protein kinase 4 ( Tssk4 ), testis-specific serine/threonine-protein kinase 5 ( Tssk5 ), doublesex- and mab-3-related transcription factor 1 ( Dmrt1 ), sperm protein 17 ( Sp17 ) and feminization-1 ( Fem1 ) in fluted giant clam ( Tridacna squamosa ) [ 26 ]; DmrtA2 , transcription factor Sox9 ( Sox9 ), Fem-1b , Fem-1c , vitellogenin ( Vg ), cytochrome P450 family 17 subfamily A member 1 ( Cyp17a1 ) and spermatogenesis- and oogenesis-specific basic Helix-Loop-Helix 2 ( Sohlh2 ) in razor clam ( Sinonovacula constricta ) [ 27 ]; and Dmrt1 , transcription factor Sox30 ( Sox30 ), testis-specific serine/threonine-protein kinase ( Tssk ), Gata1 and Vg in yesso scallop ( Patinopecten yessoensis ) [ 17 ]. The sex-determination genes in vertebrates, such as Foxl2 , Dmrt1 and sry , were also identified in mollusks, which suggests that the sex-determination mechanisms in animals may be conserved.…”

Signatures of selection in Mulinia lateralis underpinning its rapid adaptation to laboratory conditions

“…After quality control, high‐quality reads were mapped to the M. lateralis genome using STAR (Dobin et al., 2013 ), and the expression level was calculated in transcripts per million (TPM) using the RNA‐Seq by Expectation Maximization (RSEM) method. Meanwhile, the transcriptome data for G6 has been previously published (PRJNA862073; Li et al., 2022 ), while the transcriptome data of the G0 generation will be released with the genome article (as shown in Supplementary Sheet 6 ). Three transcriptome samples from each sex per generation were used for differential expression analysis.…”

Development of a non-programmable sperm cryopreservation technique in dwarf surfclams Mulinia lateralis–a potential model species for bivalve research

“…The dwarf surfclam Mulinia lateralis is a dioecious marine bivalve species and has all the characters as a model species: a short generation interval (approximately three months), well established laboratory cultivation technique, and accessibility of genomic information (Yang and Guo, 2006;Li et al, 2022;Guo et al, 2023). In fact, this species has already been used as a model species in some studies, such as the optimization of tetraploid production methods (Yang and Guo, 2006) and the elucidation of shell formation mechanisms for bivalves (Guo et al, 2023).…”