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A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora - morphology, transcriptome, and developmental gene expression.

ABSTRACT: Research into various aspects of coral biology has greatly increased in recent years due to anthropogenic threats to coral health including pollution, ocean warming and acidification. However, knowledge of coral early development has lagged. The present paper describes the embryonic development of two previously uncharacterized robust corals, Favia lizardensis (a massive brain coral) and Ctenactis echinata (a solitary coral) and compares it to that of the previously characterized complex coral, Acropora millepora, both morphologically and in terms of the expression of a set of key developmental genes.Illumina sequencing of mixed age embryos was carried out, resulting in embryonic transcriptomes consisting of 40605 contigs for C.echinata (N50?=?1080 bp) and 48536 contigs for F.lizardensis (N50?=?1496 bp). The transcriptomes have been annotated against Swiss-Prot and were sufficiently complete to enable the identification of orthologs of many key genes controlling development in bilaterians. Developmental series of images of whole mounts and sections reveal that the early stages of both species contain a blastocoel, consistent with their membership of the robust clade. In situ hybridization was used to examine the expression of the developmentally important genes brachyury, chordin and forkhead. The expression of brachyury and forkhead was consistent with that previously reported for Acropora and allowed us to confirm that the pseudo-blastopore sometimes seen in robust corals such as Favia spp. is not directly associated with gastrulation. C.echinata chordin expression, however, differed from that seen in the other two corals.Embryonic transcriptomes were assembled for the brain coral Favia lizardensis and the solitary coral Ctenactis echinata. Both species have a blastocoel in their early developmental stages, consistent with their phylogenetic position as members of the robust clade. Expression of the key developmental genes brachyury, chordin and forkhead was investigated, allowing comparison to that of their orthologs in Acropora, Nematostella and bilaterians and demonstrating that even within the Anthozoa there are significant differences in expression patterns.

SUBMITTER: Okubo N

PROVIDER: S-EPMC4770532 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora - morphology, transcriptome, and developmental gene expression.

Okubo Nami N Hayward David C DC Forêt Sylvain S Ball Eldon E EE

BMC evolutionary biology 20160229

<h4>Background</h4>Research into various aspects of coral biology has greatly increased in recent years due to anthropogenic threats to coral health including pollution, ocean warming and acidification. However, knowledge of coral early development has lagged. The present paper describes the embryonic development of two previously uncharacterized robust corals, Favia lizardensis (a massive brain coral) and Ctenactis echinata (a solitary coral) and compares it to that of the previously characteri ...[more]

PMID: 26924819

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Project description:BackgroundCorals, like many other marine invertebrates, lack a mature allorecognition system in early life history stages. Indeed, in early ontogeny, when corals acquire and establish associations with various surface microbiota and dinoflagellate endosymbionts, they do not efficiently distinguish between closely and distantly related individuals from the same population. However, very little is known about the molecular components that underpin allorecognition and immunity responses or how they change through early ontogeny in corals.Methodology/principal findingsPatterns in the expression of four putative immune response genes (apextrin, complement C3, and two CELIII type lectin genes) were examined in juvenile colonies of Acropora millepora throughout a six-month post-settlement period using quantitative real-time PCR (qPCR). Expression of a CELIII type lectin gene peaked in the fourth month for most of the coral juveniles sampled and was significantly higher at this time than at any other sampling time during the six months following settlement. The timing of this increase in expression levels of putative immune response genes may be linked to allorecognition maturation which occurs around this time in A. millepora. Alternatively, the increase may represent a response to immune challenges, such as would be involved in the recognition of symbionts (such as Symbiodinium spp. or bacteria) during winnowing processes as symbioses are fine-tuned.Conclusions/significanceOur data, although preliminary, are consistent with the hypothesis that lectins may play an important role in the maturation of allorecognition responses in corals. The co-expression of lectins with apextrin during development of coral juveniles also raises the possibility that these proteins, which are components of innate immunity in other invertebrates, may influence the innate immune systems of corals through a common pathway or system. However, further studies investigating the expression of these genes in alloimmune-challenged corals are needed to further clarify emerging evidence of a complex innate immunity system in corals.

Project description:Purpose: Corals are major sources of dimethylsulphoniopropionate (DMSP), a compound that plays a central role in the global sulphur cycle. While DMSP biosynthesis pathways have been investigated in plants and algae, the molecular basis for its production by corals is unknown. Given its potential role as an osmolyte, the effect of salinity stress on levels of DMSP was investigated in both adults and juveniles (lacking photosynthetic symbionts) of the coral Acropora millepora. This study used transcriptomic data to analyse the effects of salinity over the coral A. millepora and to identify coral genes likely to be involved in DMSP biosynthesis. Methods: Adults coral transcriptomic libraries were constructed from samples exposed during 1 and 24 hours of salinity treatment (25 PSU) and control (35 PSU) conditions (n=5 per condition). Juveniles coral transcriptomic libraries were constructed from samples exposed to 24 and 48 hours of salinity treatment (28 PSU) and control (35 PSU) conditions (n=6 per condition). All libraries were sequenced by 100 bp paired-end in a HiSeq 2000. Reads were mapped onto the Acropora millepora genome using TopHat2 to produce a count data gene expression matrix for subsequent gene expression analysis using DESeq2 package. Results: In adult coral samples, 5.5 - 10.2 million RNAseq reads were obtained for each treatment sampling time while 3.4 - 8.8 million reads were obtained for each juvenile coral sample. The count matrix of the 26,622 A. millepora gene predictions were generated using htseq-count workflow. BlastP analysis of the A. millepora gene predictions led to the identification of coral members of gene families implicated in DMSP biosynthesis in other organisms, while RNA-seq data was used to identify the differentially expressed ones in response to hyposaline stress and on this basis were considered to be candidates for roles in DMSP biosynthesis in corals. Conclusions: Hyposaline stress increased DMSP production in both adults and aposymbiotic juvenile corals, and transcriptomic analyses highlighted the potential involvement of specific candidate genes in the production of DMSP via an alga-like pathway. The biochemistry of DMSP production is not well established for any eukaryotic system and, as the first animals in which it has been demonstrated, this is particularly true in the case of corals. Our RNA-seq results enabled the identification of candidates for roles in DMSP biosynthesis in corals but, given its critical roles in diverse biological processes, a thorough investigation of the molecular mechanisms leading to its production by corals is required.

Dataset Information

A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora - morphology, transcriptome, and developmental gene expression.

Publications

A comparative view of early development in the corals Favia lizardensis, Ctenactis echinata, and Acropora millepora - morphology, transcriptome, and developmental gene expression.

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