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Molecular approaches underlying the oogenic cycle of the scleractinian coral, Acropora tenuis.

ABSTRACT: This study aimed to elucidate the physiological processes of oogenesis in Acropora tenuis. Genes/proteins related to oogenesis were investigated: Vasa, a germ cell marker, vitellogenin (VG), a major yolk protein precursor, and its receptor (LDLR). Coral branches were collected monthly from coral reefs around Sesoko Island (Okinawa, Japan) for histological observation by in situ hybridisation (ISH) of the Vasa (AtVasa) and Low Density Lipoprotein Receptor (AtLDLR) genes and immunohistochemistry (IHC) of AtVasa and AtVG. AtVasa immunoreactivity was detected in germline cells and ooplasm, whereas AtVG immunoreactivity was detected in ooplasm and putative ovarian tissues. AtVasa was localised in germline cells located in the retractor muscles of the mesentery, whereas AtLDLR was localised in the putative ovarian and mesentery tissues. AtLDLR was detected in coral tissues during the vitellogenic phase, whereas AtVG immunoreactivity was found in primary oocytes. Germline cells expressing AtVasa are present throughout the year. In conclusion, Vasa has physiological and molecular roles throughout the oogenic cycle, as it determines gonadal germline cells and ensures normal oocyte development, whereas the roles of VG and LDLR are limited to the vitellogenic stages because they act in coordination with lipoprotein transport, vitellogenin synthesis, and yolk incorporation into oocytes.

SUBMITTER: Tan ES

PROVIDER: S-EPMC7303178 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Scleractinian corals are colonial organisms comprising multiple physiologically integrated polyps and branches. Colonialism in corals is highly beneficial, and allows a single colony to undergo several life processes at once through physiological integration and compartmentalised functioning. Elucidating differences in the biochemical composition of intra-colonial branch positions will provide valuable insight into the nutritional reserves underlying different regions in individual coral colonies. This will also ascertain prudent harvesting strategies of wild donor-colonies to generate coral stock with high survival and vigour prospects for reef-rehabilitation efforts and captive husbandry. This study examined the effects of colony branch position on the nutritional profile of two different colony sizes of the common scleractinian, Acropora millepora. For smaller colonies, branches were sampled at three locations: the colony centre (S-centre), 50% of the longitudinal radius length (LRL) (S-50), and the colony edge (S-edge). For larger colonies, four locations were sampled: the colony centre (L-centre), 33.3% of the LRL (L-33), 66.6% of the LRL (L-66), and the edge (L-edge). Results demonstrate significant branch position effects, with the edge regions containing higher protein, likely due to increased tissue synthesis and calcification. Meanwhile, storage lipid and total fatty acid concentrations were lower at the edges, possibly reflecting catabolism of high-energy nutrients to support proliferating cells. Results also showed a significant effect of colony size in the two classes examined. While the major protein and structural lipid sink was exhibited at the edge for both sizes, the major sink for high-energy lipids and fatty acids appeared to be the L-66 position of the larger colonies and the S-centre and S-50 positions for the smaller colonies. These results confirm that the scleractinian coral colony is not nutritionally homogeneous, and while different regions of the coral colony are functionally specialised, so too are their nutritional profiles geared toward meeting specific energetic demands.

Project description:BackgroundSexual reproduction of scleractinians has captured the attention of researchers and the general public for decades. Although extensive ecological data has been acquired, underlying molecular and cellular mechanisms remain largely unknown. In this study, to better understand mechanisms underlying gametogenesis, we isolated ovaries and testes at different developmental phases from a gonochoric coral, Euphyllia ancora, and adopted a transcriptomic approach to reveal sex- and phase-specific gene expression profiles. In particular, we explored genes associated with oocyte development and maturation, spermiogenesis, sperm motility / capacitation, and fertilization.Results1.6 billion raw reads were obtained from 24 gonadal samples. De novo assembly of trimmed reads, and elimination of contigs derived from symbiotic dinoflagellates (Symbiodiniaceae) and other organisms yielded a reference E. ancora gonadal transcriptome of 35,802 contigs. Analysis of 4 developmental phases identified 2023 genes that were differentially expressed during oogenesis and 678 during spermatogenesis. In premature/mature ovaries, 631 genes were specifically upregulated, with 538 in mature testes. Upregulated genes included those involved in gametogenesis, gamete maturation, sperm motility / capacitation, and fertilization in other metazoans, including humans. Meanwhile, a large number of genes without homology to sequences in the SWISS-PROT database were also observed among upregulated genes in premature / mature ovaries and mature testes.ConclusionsOur findings show that scleractinian gametogenesis shares many molecular characteristics with that of other metazoans, but it also possesses unique characteristics developed during cnidarian and/or scleractinian evolution. To the best of our knowledge, this study is the first to create a gonadal transcriptome assembly from any scleractinian. This study and associated datasets provide a foundation for future studies regarding gametogenesis and differences between male and female colonies from molecular and cellular perspectives. Furthermore, our transcriptome assembly will be a useful reference for future development of sex-specific and/or stage-specific germ cell markers that can be used in coral aquaculture and ecological studies.

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Molecular approaches underlying the oogenic cycle of the scleractinian coral, Acropora tenuis.

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