Comparative genomics highlight the importance of lineage-specific gene families in evolutionary divergence of the coral genus, Montipora

Abstract

Background Scleractinian corals of the genus Montipora (Anthozoa, Cnidaria) possess some unusual biological traits, such as vertical transmission of algal symbionts; however, the genetic bases for those traits remain unknown. We performed extensive comparative genomic analyses among members of the family Acroporidae (Montipora, Acropora, and Astreopora) to explore genomic novelties that might explain unique biological traits of Montipora using improved genome assemblies and gene predictions for M. cactus, M. efflorescens and Astreopora myriophthalma. Results We obtained genomic data for the three species of comparable high quality to other published coral genomes. Comparative genomic analyses revealed that the gene families restricted to Montipora are significantly more numerous than those of Acropora and Astreopora, but their functions are largely unknown. The number of gene families specifically expanded in Montipora was much lower than the number specifically expanded in Acropora. In addition, we found that evolutionary rates of the Montipora-specific gene families were significantly higher than other gene families shared with Acropora and/or Astreopora. Of 40 gene families under positive selection (Ka/Ks ratio > 1) in Montipora, 30 were specifically detected in Montipora-specific gene families. Comparative transcriptomic analysis of early life stages of Montipora, which possesses maternally inherited symbionts, and Acropora, which lacks them, revealed that most gene families continuously expressed in Montipora, but not expressed in Acropora do not have orthologs in Acropora. Among the 30 Montipora-specific gene families under positive selection, 27 are expressed in early life stages. Conclusions Lineage-specific gene families were important to establish the genus Montipora, particularly genes expressed throughout early life stages, which under positive selection, gave rise to biological traits unique to Montipora. Our findings highlight evolutionarily acquired genomic bases that may support symbiosis in these stony corals and provide novel insights into mechanisms of coral-algal symbiosis, the physiological foundation of coral reefs.

A genome and tissue-specific transcriptomes of the large-polyp coral,Fimbriaphyllia(Euphyllia)ancora: Recipe for a coral polyp

“…Combining this, tissue-specific transcriptomics of 6 tissues, i.e., tentacles, mesenterial filaments, body wall, mouth with pharynx, testes, and ovary, are now available for F. ancora. To the best of our knowledge, although genomes of more than 25 coral species have been reported so far (Shinzato et al, 2011; Voolstra et al, 2017; Cunning et al, 2018; Ying et al, 2019; Shinzato et al, 2021a; Shinzato et al, 2021b; Yoshioka et al, 2022), global classification of genes with regard to spatial expression patterns across tissues has not been undertaken in those species. Tissue-specific transcriptomic datasets of F. ancora in this study not only shed light on unexplored functions of coral tissues, but provide a useful foundation for better understanding of gene functions, as well as biological and physiological characteristics of corals.…”

“…Predicted gene models were BLASTed against the Uniprot/Swissprot (UniProt Consortium 2018) database and were analyzed with InterProScan 5 with cutoff of e -5 (Jones et al, 2014). For clustering orthologous genes in scleractinian genomes, we used four species of Acroporidae ( A. millepora , A. tenuis , Montipora cactus, and Astreopora myriophthalma ) (Shinzato et al, 2011; Ying et al, 2019; Shinzato et al, 2021a; Yoshioka et al, 2022), Porites australiensis (Shinzato et al, 2021b), Stylophora pistillata (Voolstra et al, 2017), Pocillopora damicornis (Cunning et al, 2018) and Orbicella faveolata (Prada et al, 2016). For the A. millepora , S. pistillata , O. faveolata , and P. damicornis genomes, we downloaded data from the NCBI RefSeq database.…”

Genes possibly related to symbiosis in early life stages of Acropora tenuis inoculated with Symbiodinium microadriaticum

“…Publicly available RNA-seq data of A. tenuis in various samples, including eggs, blastulae, gastrulae, early planula larvae, planula larvae, polyps, and an adult colony (Accession number: DRA011820 94 ) were used. Data processing was performed as in Yoshioka et al 94 . Briefly, low-quality reads and sequencing adaptors were trimmed, and cleaned reads were mapped to A. tenuis gene models.…”

Genomic Data Reveal Diverse Biological Characteristics of Scleractinian Corals and Promote Effective Coral Reef Conservation

“…Interestingly, the genus Astreopora , phylogenetically the basal clade of the Acroporidae, acquires algal symbionts horizontally, like Acropora , suggesting that the vertical transmission mode of symbionts may have originated after the divergence of Acropora and Montipora . Following this hypothesis, an extensive comparative genomic analysis among Acroporidae ( Acropora , Montipora , and Astreopora ) was performed to explore genomic novelties that might explain biological traits unique to Montipora ( Yoshioka et al 2022a ). The Montipora genome contains more gene families not shared with other acroporid lineages than Acropora or Astreopora .…”