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

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.

Identifying genes associated with genetic control of color polymorphism in the pearl oyster Pinctada margaritifera var. cumingii (Linnaeus 1758) using a comparative whole genome pool‐sequencing approach

“…They also have SNPs impacting pigments from the pterin pathway, a pathway previously identified in Stenger et al (2021aStenger et al ( , 2021b. However, the present results identified a new pathway that was not described before: indeed, we found multiple SNPs impacting genes of the carotenoid pathways.…”

“…PurH controls the synthesis of FAICAR molecule (5′‐Phosphoribosyl‐5‐formamido‐4‐imidazolecarboxamide) and can also use PurH as a substrate to produce IMP (Inosine 5′‐monophosphate), the final molecule in the de novo purine nucleotide pathway (Beardsley et al, 1998 ). IMP molecule is the direct precursor to Guanosine 5′ triphosphate (GTP) (Ng et al, 2009 ) and was identified as differentially methylated and potentially involved in the coloration process in the pearl oyster P. margaritifera (Stenger, Ky, Reisser, Cosseau, et al, 2021 ). This specific GTP is involved in the synthesis of yellow pigments in the pterins pathways (xanthopterins and sepiapterins) and in pheomelanin or in eumelanin in the Raper–Mason pathway (Stenger, Ky, Reisser, Cosseau, et al, 2021 ; Stenger, Ky, Reisser, Duboisset, et al, 2021 ).…”

“…More recently, the black‐lipped pearl oyster Pinctada margaritifera var. cumingii (Linnaeus, 1758) emerged as a model to study pigmentation pathways (Ky et al, 2016 , 2018 ; Ky, Le Pabic, et al, 2017 ; Stenger et al, 2019 ; Stenger, Ky, Reisser, Cosseau, et al, 2021 ; Stenger, Ky, Reisser, Duboisset, et al, 2021 ). While color has been studied in scallops and oysters because of the importance of their appearance and visual flesh and shell quality for the food industry (Ding et al, 2015 ), the color of the black‐lipped pearl oyster inner shell is of importance for pearl production.…”

“…These results suggest that the red phenotype is likely controlled by a few genes, with high impact alleles, whereas the control of yellow and green phenotype likely depends on multiple genes with low impact alleles (polygenic). Recently, transcriptomic (Stenger, Ky, Reisser, Duboisset, et al, 2021 ) and epigenomic (Stenger, Ky, Reisser, Cosseau, et al, 2021 ) studies have for the first time identified pathways leading to color variability in this species, and some key genes. However, putative genomic variants that could control those phenotypes have not yet been described.…”

DNA Methylation Analyses Unveil a Regulatory Landscape in the Formation of Nacre Color in Pearl Oyster Pinctada fucata martensii

“… Yuan et al (2021) identified differently methylated regions related to shell color between brown and white shells, which were primarily enriched in GO functions and pathways relevant to melanin and porphyrin biosynthesis ( Yuan et al, 2021 ). In pearl oyster Pinctada margaritifera , Stenger et al (2021) explored how methylation modifies the color change of the nacre under the change of depth at which an oyster is grown. It is found that the methylation patterns of the four different patterns of clams are different, which may be related to the shell color patterns.…”