Environmentally Driven Color Variation in the Pearl Oyster Pinctada margaritifera var. cumingii (Linnaeus, 1758) Is Associated With Differential Methylation of CpGs in Pigment- and Biomineralization-Related Genes

Type Article
Date 2021-03
Language English
Author(s) Stenger Pierre-Louis1, 2, Ky Chin-Long1, 2, Reisser CelineORCID1, 3, Cosseau Céline4, Grunau Christoph4, Mege Mickael1, 5, Planes Serge6, Vidal-Dupiol Jeremie2
Affiliation(s) 1 : IFREMER, UMR 241 Écosystèmes Insulaires Océaniens, Labex Corail, Centre du Pacifique, Tahiti, French Polynesia
2 : IHPE, Université de Montpellier, CNRS, IFREMER, Université de Perpignan Via Domitia, Montpellier, France
3 : MARBEC, Université de Montpellier, CNRS, IFREMER, IRD, Montpellier, France
4 : IHPE, Université de Montpellier, CNRS, IFREMER, Université de Perpignan Via Domitia, Perpignan, France
5 : IFREMER, PDG-RBE-SGMM-LGPMM, La Tremblade, France
6 : EPHE-UPVD-CNRS, USR 3278 CRIOBE, Labex Corail, PSL Research University, Université de Perpignan, Perpignan, France
Source Frontiers in Genetics (1664-8021) (Frontiers Media SA), 2021-03 , Vol. 12 , P. 630290 (18p.)
DOI 10.3389/fgene.2021.630290
Keyword(s) pearl oyster, environmental pressure, depth, color change, pigmentation, DNA methylation, methylome characterization
Abstract

Today, it is common knowledge that environmental factors can change the color of many animals. Studies have shown that the molecular mechanisms underlying such modifications could involve epigenetic factors. Since 2013, the pearl oyster Pinctada margaritifera var. cumingii has become a biological model for questions on color expression and variation in Mollusca. A previous study reported color plasticity in response to water depth variation, specifically a general darkening of the nacre color at greater depth. However, the molecular mechanisms behind this plasticity are still unknown. In this paper, we investigate the possible implication of epigenetic factors controlling shell color variation through a depth variation experiment associated with a DNA methylation study performed at the whole genome level with a constant genetic background. Our results revealed six genes presenting differentially methylated CpGs in response to the environmental change, among which four are linked to pigmentation processes or regulations (GART, ABCC1, MAPKAP1, and GRL101), especially those leading to darker phenotypes. Interestingly, the genes perlucin and MGAT1, both involved in the biomineralization process (deposition of aragonite and calcite crystals), also showed differential methylation, suggesting that a possible difference in the physical/spatial organization of the crystals could cause darkening (iridescence or transparency modification of the biomineral). These findings are of great interest for the pearl production industry, since wholly black pearls and their opposite, the palest pearls, command a higher value on several markets. They also open the route of epigenetic improvement as a new means for pearl production improvement.

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Publisher's official version 18 4 MB Open access
Supplementary Table 1 | FastQC results for raw and trimmed data. 14 KB Open access
Supplementary Table 2 | Average values by category (control/depth treatment) and sampling time for: the number of read pairs, ... 9 KB Open access
Supplementary Table 3 | All significantly differentially methylated positions (q value < 0.05) for the controls. Scaffold name: scaffold ... 14 KB Open access
Supplementary Figure 1 | Treemaps of biological processes obtained from the GO terms significantly enriched from the lowly methylated genes (A) (data from Figure 2C – “1” part) and the highly ... 1 MB Open access
Supplementary Figure 2 | Treemaps of biological processes and molecular functions obtained from the GO terms significantly enriched from the genes with differentially methylated positions in ... 1 MB Open access
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How to cite 

Stenger Pierre-Louis, Ky Chin-Long, Reisser Celine, Cosseau Céline, Grunau Christoph, Mege Mickael, Planes Serge, Vidal-Dupiol Jeremie (2021). Environmentally Driven Color Variation in the Pearl Oyster Pinctada margaritifera var. cumingii (Linnaeus, 1758) Is Associated With Differential Methylation of CpGs in Pigment- and Biomineralization-Related Genes. Frontiers in Genetics, 12, 630290 (18p.). Publisher's official version : https://doi.org/10.3389/fgene.2021.630290 , Open Access version : https://archimer.ifremer.fr/doc/00685/79667/