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Functional analysis of small RNAs in the pearl oyster, Pinctada fucata

黄, 松銭 東京大学 DOI:10.15083/0002004935

2022.06.22

概要

Based on the biogenesis mechanism and the type of Argonaute partners, animal species express three types of endogenous silencing inducting small RNAs, which are microRNAs (miRNAs), endogenous short interfering RNAs (endo-siRNAs), and PIWI-interacting RNAs (piRNAs). miRNAs and endo-siRNAs are generated from double-stranded precursors by Dicer into 20-23 nt length, while piRNAs are generated from single-stranded precursors with a length of 26-31 nt independently of RNase III enzymes, which are, in contrast, necessary for miRNAs and endo-siRNAs biogenesis. piRNAs are associated with PIWI subfamily members of the Argonaute family of proteins, while miRNAs and endo-siRNAs are associated with AGO subfamily members. These three small RNAs play crucial roles in development, differentiation, biological processes, and genomic protection. miRNAs negatively regulate gene expression at the post-transcriptional level, especially for signaling pathways involved in cellular development, proliferation, apoptosis, oncogenesis, and differentiation; endo-siRNA are involved in genome protection and gene regulation; piRNAs silence transposons to safeguard the genome integrity in animals. For that, recently studies related to the functions of these small RNAs have been increasingly carried out.

The Akoya pearl oyster Pinctada fucata, is a well-studied organism, owing to the economic potential of pearl production as well as the fascinating biology of mollusks. Pearl oyster P. fucata is also a representative marine species for biomineralization analysis. Mollusk shells consist of about 95% calcium carbonate (CaCO3) and 5% organic components. The fracture toughness of composite shell is 3,000 times greater than that of the crystals themselves. Mollusk shell is a biosynthetic composite material that has been the subject of much interest in the field of materials science because of the extraordinary properties and model characteristics of biomineralization.

Biomineralization process is a very complex process involving many biological and environmental factors are involved. The fabulous and diverse formation of mollusk shells has been widely recognized and has drawn great attention from the scientific and breeding communities. Over recent decades, a larger number of omics analysis such as transcriptomics, proteomics, genomics and gene interference techniques have been used to investigate the genetic components of biomineralization in mollusks. Small RNAs, however, are still indistinct in mollusks. Small RNA sequencing was used to explore small RNA expression in the pearl oyster P. fucata and thus abundant small RNAs, including miRNAs and piRNAs, were expressed in somatic and gonad tissues in P. fucata. In that respect, in this study, separate analyses were conducted on these two different sets of small RNAs in this study. Transcriptomic analysis was conducted to research piRNA biogenesis factors in P. fucata. To explore the piRNA function in this species, locked-nucleic-acid modified oligonucleotide (LNA) was used to silencing single piRNA (piRNA0001) expression. We also examined the endogenous genes expression profiles after piRNA0001 silencing in P. fucata by RNA-seq, and predicted the potential target genes of piRNA0001.

1. miRNAs expression and their predicted functions in biomineralization
To obtain various miRNAs and explore their potential functions in biomineralization, we constructed and sequenced eight small RNA libraries prepared from adductor muscle, gill, mantle, and ovary tissues of two adult P. fucata. miRNA identification was performed by comparing the sequences with the known mature miRNAs and miRNA precursors in miRBase 22.0. All unannotated sequences that failed to match with the sequences in the databases were analyzed by miRDeep2 to predict novel miRNA candidates. The expression profiles of identified miRNAs were clarified in all examined tissues according to the reads per million reads (RPM) method. Furthermore, biomineralization-related genes were used for miRNA target prediction in biomineralization process

A total of 186 known and 42 novel miRNAs were identified in the pearl oyster P. fucata, 165, 198, 159 and 185 miRNAs were found in adductor muscle, gill, ovary, and mantle tissues, respectively. Of these, 119 miRNAs were ubiquitously expressed in all examined tissues. Novel miRNAs demonstrate weaker expression than previously known miRNAs. Clustering analysis showed that the expression patterns of miRNAs were similar among the somatic tissues, but they differed significantly between the somatic and ovary tissues. We screened out 105 biomineralization-related genes with complete sequences from Pinctada genus for miRNA target prediction. Hundreds of potential target sites were detected among these biomineralization-related genes using multiple software tools. miR-1990c-3p, miR-876, miR-9a-3p, and novel-3, which were highly expressed in mantle tissues, may play a core role in biomineralization by regulating the formation of matrix proteins or protein kinase and transcription factor genes. Furthermore, stem-loop RT-PCR was employed to validate the existence of the identified miRNAs in the pearl oyster P. fucata.

2. piRNA expression patterns in P. fucata
piRNA and their partner PIWI proteins play an essential role in fertility, germline stem cell development, as well as the basic control of the integrity of animal genome. Abundant piRNA-sized small RNAs were detected in P. fucata somatic and gonad tissues by conducting separate analyses of piRNA. Reads were blasted against identified miRNAs, non-coding RNA database, Rfam, and reference genome to separate out miRNA, tRNA, snRNA, snoRNA, and rRNA sequences from the dataset. Reads within the size range of 26-31 nt were selected as putative piRNAs. The reads per million (RPM) value was used to compare the relative expression of unique piRNA among tissues. Putative piRNA sequences were mapped with reference genome. Neighboring piRNA loci with a distance of < 1 kb were merged for piRNA cluster analysis. Normalized expression of piRNA cluster was calculated using the measure reads per kilobase per million mapped reads (RPKM), and edgeR package was employed to identify differently expressed piRNA clusters among tissues. We also examined the 2-O-methylation of piRNA using βelimination reaction, detected putative piRNA expression in somatic tissues by northern blotting and in situ hybridization.

A total of 18.0 million reads united into 2.8 million unique sequences were considered valid putative piRNAs, which opt to begin with a uridine (U) at 5’ terminal. Among these unique piRNAs, 25% of the unique piRNAs mapped to multiple tandem loci on the scaffold. piRNA0001 with a sequence of 5′-UACUUUAACAUGGCACA GAUAUAAUGACCU-3’ was the most highly expressed in all examined somatic tissues. A total of 35,848 piRNA clusters were identified in P. fucata genome with a length range from 30 bp (single piRNA) to 60.9 kb. Moreover, a principal component analysis (PCA) of piRNA cluster expression patterns from all libraries clustered those of the somatic tissues together and differentiated the somatic and ovary tissues. As a result, differently expressed piRNA cluster analysis showed no difference in the expression patterns of piRNA clusters among the somatic tissues. However, 127, 30, and 377 piRNA clusters were significantly differently expressed in the mantle, adductor muscle, and gill tissues than in the ovary tissues, respectively. Furthermore, β-elimination reaction verified the 2- O-methylation at 3’ terminal of piRNA. Northern blotting showed piRNA expression in all examined somatic tissues, especially in gill. In situ hybridization of small RNA also revealed the expression of piRNAs in mantle tissue.

3. piRNA biogenesis factors in P. fucata
piRNAs biogenesis is associated with PIWI subfamily members of the Argonaute family of proteins and multiple factor complexes. Two models of piRNA biogenesis pathway have been demonstrated in various animals, which are the primary piRNA biogenesis pathway and the amplification loop or ping-pong cycle. Concerning the primary piRNA biogenesis pathway, long piRNA precursors are transcribed from piRNA clusters, cleaved and modified by complicated factors in cytoplasm, and then transported into the nucleus with complex factors. Primary piRNAs are also subjected to an amplification system to enforce the high expression of piRNA. Although piRNAs were ubiquitously expressed in P. fucata somatic and gonad tissues, the biogenesis factors are not clear. We preformed RNA sequencing to identify the homologous piRNA biogenesis factors in P. fucata. Relative expression of piRNA biogenesis factors were calculated by transcripts per million reads (TPM) method and RT-PCR. The characteristics of these factors were analyzed based on the deduced amino acid sequences; homologous sequences were also compared within diverse animals. A comprehensive computational analysis of piRNA populations among tissues were employed to clarify piRNA biogenesis pathway in the pearl oyster P. fucata.

piRNA biogenesis factors, including PIWI, AGO, Zuc and HEN1, are assembled based on the annotated transcripts by RNA sequencing. PIWI and AGO have the conserved PAZ and PIWI domain as homologues in other organisms, Zuc protein contain a PLDc domain. Although these factors were ubiquitously expressed in all examined tissues, Piwil1 and Piwil2 were highly expressed in male and female gonad tissues; Zuc and HEN1 were highly expressed in female gonad at three-year old. AGO2 was highly expressed in female tissues. AGO1, however, have a wellbalanced expression in all examined tissues. Bioinformatic analysis of piRNA population among different tissues showed that a Piwil1-Piwil1 is dependent to homotypic ping-pong amplification in somatic tissues, while a preponderant Piwil1-Piwil1 dependent homotypic and an unpredominant Piwil1-Piwil2 dependent heterotypic ping-pong amplification were both displayed in gonad tissues. In support to these findings, 29/30 nt piRNAs presumably bound to Piwil1, are heavily biased for a 5’ uridine (U), whereas 25/26 nt piRNAs presumably bound to Piwil2, have shown a stronger bias for an adenine (A) at position 10.

4. Potential piRNA-mediated gene regulation in the somatic tissues of P. fucata
Recent decade studies have showed additional targets and functions of piRNA that do not map to transposons in various animals. Although piRNAs are ubiquitously expressed in somatic tissues, the role of somatic piRNAs was not well characterized in the pearl oyster P. fucata. To gain insight into piRNA targeting mechanism, we identified the targets of piRNA and examined the endogenous genes expression profiles by single piRNA silence in P. fucata. Locked-nucleic-acid modified oligonucleotide (LNA-antagonist) was injected into body cavity to silence single piRNA (piRNA0001) expression in P. fucata. Somatic tissues, including adductor muscle, gill, and mantle tissues, were collected for RNA extraction. Stem-loop RT-PCR was employed for piRNA0001 determination. Therefore, twenty-four libraries of somatic tissues were constructed for RNA sequencing. Differently expressed genes were analyzed for target sites prediction using miRanda. The predicted target sites were also determined by RT-PCR.

piRNA0001 was silenced by LNA-antagonist in P. fucata. Transcriptomic analysis of 24 somatic tissues showed that 456, 900, and 699 genes were differently expressed in adductor muscle, gill and mantle tissues, respectively. Moreover, 16 and 15 genes were commonly up-regulated and down-regulated in three examined somatic tissues after LNA-antagonist injection. Target site prediction was performed on differently expressed genes 3’ UTR. FHOD3, SRS10, VINC, and ZNF622 were predicted to be targeted by piRNA0001 in adductor muscle. ART2, EF1A, EMC7, ESI1L, NAC2, PA2HB, SYWC, TM87A, and ZNF622 were predicted to be targeted by piRNA0001 in gill tissue, while CAH14, CBF, CDC42, FRRS1, GOLI4, KAT3, NBR1, PA2HB, TYR1, TYR2 and ZNF622 in mantle tissues. Among these predicted target genes, ZNF622 was up-regulated in all examined somatic tissues after piRNA0001 silencing. The alignment pairing from 2nd to 8th nucleotide, which considered as seed region of piRNA, were prefect complementarities. Furthermore, base-pairing outside of the seed was also important for piRNA target prediction. Up-regulated and down-regulated genes were both potentially targeted by piRNA0001, demonstrating the mystery of piRNA-mediated gene regulation in P. fucata.

Conclusion
This study has identified small RNAs, including miRNAs and piRNAs, in somatic and gonad tissues in the pearl oyster P. fucata using next generation sequencing technology. A total of 186 known and 42 novel miRNAs were identified in P. fucata. We figured out the characteristics and expression patterns of these miRNAs in P. fucata somatic and gonad tissues. We also collected hundreds of biomineralization-related genes for miRNA target prediction that helps to understand better the biomineralization understanding in mollusks.

Except for miRNAs expression and function analysis, piRNA and the potential gene silencing in somatic tissues are the most attractive findings in this study. We established a set of piRNA analysis procedures for non-model animals, including piRNA and piRNA cluster identification, expression pattern analysis, comparative analysis of differences, and differentiation of piRNA primary and second biogenesis pathway, and target genes prediction etc. We described the key factors for piRNA biogenesis, which further promotes the understanding of piRNA biogenesis and function in the pearl oyster P. fucata. We also predicted the potential targeted genes of a single piRNA in somatic tissues that provide insight into the increased understanding of additional target and function of piRNAs in P. fucata.

The improved understanding of biomineralization process under miRNA guidance from this study will provide a basis for future research towards upgrading the pearl culture and pearl quality. This study also gives more valuable information about piRNA biogenesis and piRNA-mediated gene regulation outside of germline in mollusk. However, further functional analyses are needed to verify the functions of somatic piRNA in this species.

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