Evolution of Biomineralization Genes in the Prismatic Layer of the Pen Shell Atrina pectinata

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ORIGINAL ARTICLE

Evolution of Biomineralization Genes in the Prismatic Layer of the Pen Shell Atrina pectinata Keisuke Shimizu1 · Hiroyuki Kintsu1,2 · Masahiko Awaji3 · Toshie Matumoto3 · Michio Suzuki1 Received: 1 September 2020 / Accepted: 18 November 2020 / Published online: 24 November 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Molluscan shells are composed of calcium carbonates, with small amounts of extracellular matrices secreted from mantle epithelial cells. Many types of shell matrix proteins (SMPs) have been identified from molluscan shells or mantle cells. The pen shell Atrina pectinata (Pinnidae) has two different shell microstructures, the nacreous and prismatic layers. Nacreous and prismatic layer-specific matrix proteins have been reported in Pteriidae bivalves, but remain unclear in Pinnidae. We performed transcriptome analysis using the mantle cells of A. pectinata to screen the candidate transcripts involved in its prismatic layer formation. We found Asprich and nine highly conserved prismatic layer-specific SMPs encoding transcript in P. fucata, P. margaritifera, and P. maxima (Tyrosinase, Chitinase, EGF-like proteins, Fibronectin, valine-rich proteins, and prismatic uncharacterized shell protein 2 [PUSP2]) using molecular phylogenetic analysis or multiple alignment. We confirmed these genes were expressed in the epithelial cells of the mantle edge (outer surface of the outer fold) and the mantle pallium. Phylogenetic character mapping of these SMPs was used to infer a possible evolutionary scenario of them in Pteriomorphia. EGF-like proteins, Fibronectin, and valine-rich proteins encoding genes each evolved in the linage leading to four Pteriomorphia (Mytilidae, Pinnidae, Ostreidae, and Pteriidae), PUSP2 evolved in the linage leading to three Pteriomorphia families (Pinnidae, Ostreidae, and Pteriidae), and chitinase was independently evolved as SMPs in Mytilidae and in other Pteriomorphia (Pinnidae, Ostreidae, and Pteriidae). Our results provide a new dataset for A. pectinata SMP annotation, and a basis for understanding the evolution of prismatic layer formation in bivalves. Keywords  Atrina pectinata · Biomineralization · Evolution · Prismatic layer · Transcriptome

Introduction Handling editor: John Bracht. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0023​9-020-09977​-7) contains supplementary material, which is available to authorized users. * Michio Suzuki [email protected]‑tokyo.ac.jp; [email protected]‑tokyo.ac.jp 1



Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1‑1‑1 Yayoi, Bunkyo, Tokyo 113‑8657, Japan

2



Center for Health and Environmental Risk Research, National Institute for Environmental Studies, 16‑2 Onogawa, Tsukuba, Ibaraki 305‑8506, Japan

3

Fisheries Technology Institute, Japan Fisheries Research and Education Agency, 422‑1 Nakatsuhama, Minami‑Ise, Watarai, Mie 516‑0193, Japan



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