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Developmental Characteristics of Pearl Oyster Pinctada Fucata Martensii

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Developmental Characteristics of Pearl Oyster Pinctada Fucata Martensii Zheng et al. BMC Genomics (2019) 20:122 https://doi.org/10.1186/s12864-019-5505-8 RESEARCH ARTICLE Open Access Developmental characteristics of pearl oyster Pinctada fucata martensii: insight into key molecular events related to shell formation, settlement and metamorphosis Zhe Zheng1,2, Ruijuan Hao1,2, Xinwei Xiong1,2, Yu Jiao1,2, Yuewen Deng1,2* and Xiaodong Du1,2* Abstract Background: Marine bivalves undergo complex development processes, such as shell morphology conversion and changes of anatomy and life habits. In this study, the transcriptomes of pearl oyster Pinctada fucata martensii and Pacific oyster Crassostrea gigas at different development stages were analyzed to determine the key molecular events related to shell formation, settlement and metamorphosis. Result: According to the shell matrix proteome, biomineralization-related genes exhibited a consensus expression model with the critical stages of shell formation. Differential expression analysis of P. f. martensii, revealed the negative regulation and feedback of extracellular matrixs as well as growth factor pathways involved in shell formation of larvae, similar to that in C. gigas. Furthermore, neuroendocrine pathways in hormone receptors, neurotransmitters and neuropeptide receptors were involved in shell formation, settlement and metamorphosis. Conclusion: Our research demonstrated the main clusters of regulation elements related to shell formation, settlement and metamorphosis. The regulation of shell formation and metamorphosis could be coupled forming the neuroendocrine- biomineralization crosstalk in metamorphosis. These findings could provide new insights into the regulation in bivalve development. Keywords: Shell formation, Settlement, Metamorphosis, Molecular events Backgrounds (the dissoconch), even with different calcium carbonate Bivalves comprise millions of species that are widely crystal products, could function on mechanical stability, distributed in the world as common benthic community physical protection and even chemical defence [2, 3]. As in coastal areas. Marine bivalves undergo complex life the shells of bivalves undergo the big change in the de- development processes, such as shell morphology con- velopment stage, such as the crystal polymorph transi- version as well as changes of anatomy and life habits [1]. tion that happens need special physical conditions in At these stages, larvae are sensitive and perishable. Many nature, the formation and regulation mechanisms of bi- endogenous physiological processes and exogenous valve shells are important to the development of bioma- physical and chemical elements could affect their terials. And the mechanisms by which larvae shells are survival. fabricated and conversed in the development processes Bivalve shells are the typical biomineralization prod- along with the morphological metamorphosis are im- ucts, with multiple morphological structure and special portant to understand the evolution and regulation of stress. The symbolic bivalves’ shells covering the body mineralization in biological organisms [4]. Complex or- surface in both larvae (the protoconch) and adults stages ganic macromolecules compounded by mantle tissue cells harnessing the processes of nucleation along with haemocyte have been developed for mediating the * Correspondence: [email protected]; [email protected] 1Fishery College, Guangdong Ocean University, Zhanjiang 524088, China process of shell formation [5, 6]. Recently, the main Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zheng et al. BMC Genomics (2019) 20:122 Page 2 of 11 biomolecular components in several shellfish, such as from GigaDB (http://gigadb.org/search/new?keyword=Pinc- bivalves and gastropods species, have been identified [7– tada+fucata+martensii). The transcriptome and genome 11]. Some regulation pathways and transcriptional fac- data of C. gigas at different development stages and tors involved in shell formation have been elucidated its shell matrix proteome data were downloaded from [12–14]. Most of them are homologues of regulators in https://www.nature.com/articles/nature11413,supplementary the operation of endoskeleton system construction. tables [21]. However, the vital regulation factors in shell morphology construction remain unclear. Different expression analysis and function enrichment of Metamorphosis of bivalve species is a significant physio- P. f. martensii at different development stages logical process from free-living larva to sessile juvenile that Target genes (TGs) that differently expressed with the includes loss of the velum, development of tissues, such as condition (|log2 Ratio| > 1, FDR < 0.001) were selected gills and foot, and production of adult shell [15]. The grad- for the function enrichment at different development ual covering of protoconch accompanied with the veliger stages. We performed functional enrichment analysis of stage, which represents the changes of digestive and swim- our TGs with the commonly used Gene Ontology (GO) ming behaviors. Adult dissoconch is one of the indicators and KEGG databases. GO provides three ontologies: mo- of the transition of free-swimming larvae to benthic and lecular function, cellular component and biological often sessile and attached juveniles. And larvae at this stage process. By comparing with the background of all genes, aresensitivetotheenvironmentandeasytodie.Inbivalves, enrichment analysis provides all terms (GO term, path- larval responses to environmental cues, including salinity, way ID) that are significantly enriched in the TGs. We depth, temperature and light, and the main biophysical developed a strict algorithm for the analysis, with cues, such as neuroendocrine compounds and appropriate p-value defined as: ion concentrations, influence their subsequent settlement and metamorphosis. Recently, specific neurotransmitters ÀÁÀÁ Xm−1 M N−M and chemicals have been found to induce specific responses − P ¼ 1− i ÀÁn i in initiating bivalve metamorphosis [16–18]. As many of bi- N i¼0 n valvespeciesaretheimportanteconomicspeciessuchas oysters, finding the regulation mechanisms of metamor- Where N is the count of all genes with functional an- phosis in bivalves could contribute to improve the rate of notation; n is the count of TGs in N; M is the count of survival and promote relative industries. In addition, several all genes that are annotated to certain functional terms; neuroendocrine factors and pathways across invertebrate and m represents the count of TGs in M. The calculated and vertebrate species are evolutionarily conserved and an- p-value was subjected to Bonferroni Correction, taking cient origins [19]. While, recently, a series of artificial in- corrected p-value ≤0.05 as the significantly enriched. ducers, such as neurotransmitters and analogues used as Functional terms fulfilling this condition were defined as pesticide or anticorrosive paint, act as marine pollutants significantly enriched functional terms in TGs. and influence larval settlement and metamorphosis of mar- ine invertebrates [20]. Therefore, exploring the intrinsic Identification of specifically expressed genes in mantle neuroendocrine pathways in bivalves could contribute to edge (ME) and mantle pallial (MP) marine environmental protection and species conservation. According to the published transcriptome data [22], we In this study, we selected pearl oyster Pinctada fucata mar- selected the specifically expressed genes that were highly tensii as well as Pacific oyster Crassostrea gigas with high pre- expressed in one tissue (ME or MP), compared to all cision genomic data, intact developmental transcriptome data other tissues including in the adductor muscle, hemo- and shell matrix proteome [21, 22].Thesedatawerereana- cyte, foot, gill, gonad, hepatopancreas, with criteria that lyzed to explore the key molecular events related to shell for- reads per kilobase of exon per million fragments mapped mation, settlement and metamorphosis. We also determined (RPKM) ratio of ≥4 fold (upregulated) and false discov- the important molecular events involved in shell formation ery rate (FDR) of ≤0.05. and proposed the neuroendocrine-biomineralization crosstalk in metamorphosis. Identification of gene expression patterns Given that the expression of different genes in the differ- Methods ent samples showed considerable difference, we normal- Collection of supported data of the pearl oyster P. f. ized each gene in all samples. Based on normalized martensii and the Pacific oyster C. gigas expressed values of genes, we used hierarchical cluster- The genome data and transcriptome of P. f. martensii at ing of R package with default parameters to identify the different development stages and in different tissues, as gene families with the same expression patterns, and well as the shell matrix proteome data were downloaded then divided the gene tree into a series of sub-trees Zheng et al. BMC
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