Comparative Analysis of the Transcriptome in Tissues Secreting Purple and White Nacre in the Pearl Mussel Hyriopsis cumingii

Bai, Zhiyi; Zheng, Hanfeng; Lin, Jing-Yun; Wang, Guiling; Li, Jiale

doi:10.1371/journal.pone.0053617

Cited by 84 publications

(60 citation statements)

References 65 publications

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“…Metabolism of chitin, a biopolymer that has been detected in molluscan shells, involves chitin synthase, chitin deacetylase and chitinase [79,87,88], which have all been found to be differentially expressed in the S. glomerata of this study (Fig. 2).…”

Section: Biomineralisation and Cytoskeletonmentioning

confidence: 63%

Molecular analysis of the Sydney rock oyster (Saccostrea glomerata) CO2 stress response

Ertl

O’Connor

Wiegand

et al. 2016

Clim Chang Responses

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Background: Human activities have led to a substantial increase in carbon dioxide (CO 2 ) emission, with further increases predicted. A RNA-Seq study on adult Saccostrea glomerata was carried out to examine the molecular response of this bivalve species to elevated pCO 2 . Results: A total of 1626 S. glomerata transcripts were found to be differentially expressed in oysters exposed to elevated pCO 2 when compared to control oysters. These transcripts cover a range of functions, from immunity (e.g. pattern recognition receptors, antimicrobial peptides), to respiration (e.g. antioxidants, mitochondrial respiratory chain proteins) and biomineralisation (e.g. carbonic anhydrase). Overall, elevated levels of CO 2 appear to have resulted in a priming of the immune system and in producing countermeasures to potential oxidative stress. CO 2 exposure also seems to have resulted in an increase in the expression of proteins involved in protein synthesis, whereas transcripts putatively coding for proteins with a role in cilia and flagella function were down-regulated in response to the stressor. In addition, while some of the transcripts related to biomineralisation were up-regulated (e.g. carbonic anhydrase 2, alkaline phosphatase), a small group was down-regulated (e.g. perlucin). Conclusions: This study highlighted the complex molecular response of the bivalve S. glomerata to expected near-future ocean acidification levels. While there are indications that the oyster attempted to adapt to the stressor, gauged by immune system priming and the increase in protein synthesis, some processes such cilia function appear to have been negatively affected by the elevated levels of CO 2 .

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Section: Biomineralisation and Cytoskeletonmentioning

confidence: 63%

Molecular analysis of the Sydney rock oyster (Saccostrea glomerata) CO2 stress response

Ertl

O’Connor

Wiegand

et al. 2016

Clim Chang Responses

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“…A partial cDNA sequence was harvested via high-throughput transcriptome sequencing using the mRNA extracted from pooled mantle tissue (Bai et al, 2013). To amplify the 5'-end of the HcCS1 ORF sequence, one pair of primers (RaceF: 5'-TAC GGC TGC GAG AAG ACG ACA GAA G-3' and RaceR: CAC TGG ATG CCC TCA AAC TCA TAG TC) was subsequently designed and synthesized.…”

Section: Cloning the Hccs1 Open-reading Frame (Orf)mentioning

confidence: 99%

“…In contrast to the seawater pearl oyster, the triangle sail mussel has a different evolutionary position, and its shell and nacre contain aragonite prisms instead of the calcite prisms found in seawater oysters (Bai et al, 2013). To date, the mechanisms of shell and nacre formation, especially chitin-mediated shell and nacre formation, in the triangle sail mussel remain largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Characterization and functional analysis of a chitin synthase gene (HcCS1) identified from the freshwater pearlmussel Hyriopsis cumingii

Lin

et al. 2015

Genet. Mol. Res.

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ABSTRACT. The triangle sail mussel, Hyriopsis cumingii, is the most important freshwater pearl mussel in China. However, the mechanisms underlying its chitin-mediated shell and nacre formation remain largely unknown. Here, we characterized a chitin synthase (CS) gene (HcCS1) in H. cumingii, and analyzed its possible physiological function. The complete ORF sequence of HcCS1 contained 6903 bp, encoding a 2300-amino acid protein (theoretical molecular mass = 264 kDa; isoelectric point = 6.22), and no putative signal peptide was predicted. A myosin motor head domain, a CS domain, and 12 transmembrane domains were found. The predicted spatial structures of the myosin head and CS domains were similar to the electron microscopic structure of the heavy meromyosin subfragment 19264-19274 (2015) of chicken smooth muscle myosin and the crystal structure of bacterial cellulose synthase, respectively. This structural similarity indicates that the functions of these two domains might be conserved. Quantitative reverse transcription PCR results showed that HcCS1 was present in all detected tissues, with the highest expression levels detected in the mantle. The HcCS1 transcripts in the mantle were upregulated following shell damage from 12 to 24 h post-damage, and they peaked (approximately 1.5-fold increase) at 12 h after shell damage. These findings suggest that HcCS1 was involved in shell regeneration, and that it might participate in shell and nacre formation in this species via chitin synthesis. HcCS1 might also dynamically regulate chitin deposition during the process of shell and nacre formation with the help of its conserved myosin head domain.

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“…To gain a broader understanding of the molecular mechanisms that underlie shell formation, mantle transcriptomes have been obtained for a number of molluscs (Jackson et al 2006, Bai et al 2010, Clark et al 2010, Jackson et al 2010, Gardner et al 2011, Jones et al 2011, Kinoshita et al 2011, de Wit and Palumbi 2012, Zhang et al 2012, Bai et al 2013, Shi et al 2013a, Shi et al 2013b, Werner et al 2013, Artigaud et al 2014, Freer et al 2014. These allowed for the rapid identification and classification of hundreds of genes encoding potential SMPs and gene products that are not necessarily incorporated into the shell, but are, nonetheless, expressed in the mantle and appear essential for calcium carbonate deposition.…”

Section: The Mantle Appears To Use Conserved Developmental Regulatorsmentioning

confidence: 99%

“…Publicly available 454 adult mantle transcriptome data from previous studies (Clark et al 2010, Kinoshita et al 2011, Bai et al 2013 (Grabherr et al 2011), using default settings and a minimum transcript length of 200 bp. ESTs from L. gigantea were assembled by CAP3 software (Huang and Madan 1999), using a sequence identity of 95%.…”

Section: Mantle Transcriptome Data Collectionmentioning

confidence: 99%

Investigation of gene family evolution and the molecular basis of shell formation in molluscs

Aguilera¹

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Since the emergence of shell-bearing molluscs in the Early Cambrian, diverse shell forms have evolved. Modern molluscs are renowned for a highly complex and robust shell, which is the product of the orchestrated expression of genes and secretion of a large number of proteins and other macromolecules from the epithelium of a specialised organ called the mantle. Molluscan shells display remarkable morphological diversity, structure and ornamentation, however the molecular mechanisms underlying the evolution and formation of the shell remain largely unknown. In this thesis, I seek to investigate the nature of the mantle transcriptome focussing on the timing of origin of genes expressed in the mantle and the evolutionary history of gene families that encode secreted proteins in representatives of bivalve and gastropod species.First, by comparative transcriptomics of the mantle, I determined the origin and evolution of gene families expressed in this organ. Gene origin analyses show that most genes expressed in the mantle are taxon-restricted innovations (i.e. unique to a particular species), although a large number of genes arose along the stems leading to the bilaterian and molluscan last common ancestors. Focussing on gene families that encode secreted proteins that are likely to be embedded within the shell and/or to regulate shell construction, I found that these are comprised of both ancient and lineage-specific gene families. The evolution of these gene families is highly dynamic with prolific gene family gains and losses over evolutionary time. By comparing sequences, I also detected indications of positively selected gene families over molluscan evolution. These gene families show unique patterns of enrichment of protein domains, and presumably molecular functions, that are taxa-specific, suggesting that bivalves and gastropods use almost completely different secretory repertoire to construct their shells.I then focused on an ancient gene family expressed in the molluscan mantles -the tyrosinase gene family -to understand how a conserved gene family has been co-opted into the biomineralisation pathway. I found no evidence of large-scale expansion of tyrosinase genes in gastropods, whereas tyrosinase genes in bivalves have undergone substantial independent gene expansions in at least two lineages (Pinctada spp. and Crassostrea gigas), and that the resulting gene duplicates have been co-opted into the mantle gene regulatory network. Many of the tyrosinase genes are found in clusters within the genomes and are expressed at relatively high levels in the mantle. Detailed 3 comparisons of tyrosinase gene expression in different regions of the mantle in two closely related pearl oysters, P. maxima and P. margaritifera, reveal that recently evolved orthologous genes have unique expression profiles across the mantle with high expression levels at the distal mantle edge, suggesting roles in colouration and/or prismatic shell layer construction. Differences in expression levels are consistent with the rapid evo...

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Comparative Analysis of the Transcriptome in Tissues Secreting Purple and White Nacre in the Pearl Mussel Hyriopsis cumingii

Cited by 84 publications

References 65 publications

Molecular analysis of the Sydney rock oyster (Saccostrea glomerata) CO2 stress response

Molecular analysis of the Sydney rock oyster (Saccostrea glomerata) CO2 stress response

Characterization and functional analysis of a chitin synthase gene (HcCS1) identified from the freshwater pearlmussel Hyriopsis cumingii

Investigation of gene family evolution and the molecular basis of shell formation in molluscs

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