海洋国家实验室在扇贝基因组精细图谱绘制和动物宏观进化领域取得重要进展 | Nature Ecology & Evolution

题目 Scallop genome provides insights into evolution of bilaterian karyotype and development

作者 Shi Wang, Jinbo Zhang, Wenqian Jiao, et al

期刊 Nature Ecology & Evolution 1, Article number: 0120 (2017)

doi:10.1038/s41559-017-0120

在线发表日期 03 April 2017

摘要 Reconstructing the genomes of bilaterian ancestors is central to our understanding of animal evolution, where knowledge from ancient and/or slow-evolving bilaterian lineages is critical. Here we report a high-quality, chromosome-anchored reference genome for the scallop Patinopecten yessoensis, a bivalve mollusc that has a slow-evolving genome with many ancestral features. Chromosome-based macrosynteny analysis reveals a striking correspondence between the 19 scallop chromosomes and the 17 presumed ancestral bilaterian linkage groups at a level of conservation previously unseen, suggesting that the scallop may have a karyotype close to that of the bilaterian ancestor. Scallop Hox gene expression follows a new mode of subcluster temporal co-linearity that is possibly ancestral and may provide great potential in supporting diverse bilaterian body plans. Transcriptome analysis of scallop mantle eyes finds unexpected diversity in phototransduction cascades and a potentially ancient Pax2/5/8-dependent pathway for noncephalic eyes. The outstanding preservation of ancestral karyotype and developmental control makes the scallop genome a valuable resource for understanding early bilaterian evolution and biology.

The nature of Urbilateria, the last common ancestor of all bilaterians, is enigmatic due to the lack of a plausible candidate in the fossil records 1 . The earliest unambiguous fossil of a bilaterian, Kimberella, shows remarkable resemblance to a mollusc, albeit its relationship with Urbilateria remains uncertain 2,3 . In the absence of definitive fossil records, genomic reconstruction by comparing extant bilaterian genomes becomes essential to our understanding of early bilaterian ancestors and their subsequent evolution 4,5 . However, reconstructing the genome of the bilaterian ancestor is challenging due to the paucity of high-order genome assemblies from ancient and/or slow-evolving lineages. Early genome sequencing efforts have mostly focused on two of the three major bilaterian groups, that is, protostome ecdysozoans and deuterostomes. Limited sequencing in the third group of protostome lophotrochozoans, a large superclade that includes molluscs, annelids and brachiopods, has revealed that their genomes are less derived from the ancestral bilaterian state than those of many ecdysozoans 5 . Unfortunately, none of these less-derived lophotrochozoan genomes were assembled to a degree that permits chromosome-level genome comparison.

Mollusca is the most speciose phylum of Lophotrochozoa and among the first bilaterians to appear in fossil records 6 . Many molluscan lineages including bivalves showed little change in shell morphology and life style over several hundred million years, and yet extant molluscs are abundant and thriving in diverse marine, freshwater and terrestrial environments, providing key ecological services and significant economic benefits to humans. Molluscs are highly diverse in form, making them excellent subjects to study body plan evolution and in particular its patterning by Hox genes 7 . Molluscs also have the greatest diversity in eye morphology, ranging from simple cupped to chambered or compound eyes, as well as in the number and placement of their eyes 8 , providing good subjects to study the origin and evolution of the eye, or Darwin’s ‘organ of extreme perfection’. Despite the great evolutionary and biological significance of molluscs, our sampling of their genomes remains limited to a few species 5,9,10,11 and without high-order assemblies.

Here we report a high-quality, chromosome-anchored reference genome of the scallop Patinopecten yessoensis (Jay, 1857), a bivalve mollusc from the large Pectinidae family that contains ~270 living species and thousands of fossil species (dating back to ~320–340 million years ago, Ma 12 ). Scallops are widely distributed in world oceans. They are mostly free-living and have multiple eyes scattering along the mantle edge. Many scallops are important fishery and aquaculture species. P. yessoensis is a large scallop living on cold and stable ocean bottoms of the northwestern Pacific. It has a conserved 19-chromosome karyotype that is common to diverse bivalves and may represent the ancient karyotype of bivalves 13 . Analysis of the scallop genome and extensive transcriptomes reveals outstanding preservation of ancestral bilaterian linkage groups, an intact Hox gene cluster under new expression control and diverse phototransduction cascades with a potentially ancient Pax2/5/8-dependent pathway for noncephalic eye formation, providing insights into the evolution of genome organization and developmental control during the emergence of bilaterians.

链接 https://www.nature.com/articles/s41559-017-0120