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研究生:陳倢蓁
研究生(外文):Chieh-Jhen Chen
論文名稱:台灣北部石珊瑚有性生殖及Dmrt基因家族在珊瑚生殖的角色
論文名稱(外文):Sexual reproduction of scleractinian corals in northern Taiwan and roles of Dmrt gene family in coral reproduction
指導教授:陳韋仁陳韋仁引用關係張清風張清風引用關係識名信也
指導教授(外文):Wei-Jen ChenChing-Fong ChangShinya Shikina
口試日期:2017-04-28
學位類別:博士
校院名稱:國立臺灣大學
系所名稱:海洋研究所
學門:自然科學學門
學類:海洋科學學類
論文種類:學術論文
論文出版年:2017
畢業學年度:105
語文別:英文
論文頁數:126
中文關鍵詞:台灣北部有性生殖地衣微孔珊瑚腎型針葉珊瑚Dmrt基因家族
外文關鍵詞:Northern Taiwansexual reproductionPorites lichenEuphyllia ancoraDmrt gene family
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珊瑚礁生態系因為受到許多不可逆轉的天然災害、人為及全球暖化的因素而面臨嚴重的威脅。台灣的珊瑚群聚在熱帶及亞熱帶地區皆有分布,大約有317個物種, 也受到威脅。受到干擾的珊瑚群聚主要依靠成功的生殖來維持及回復。因此,為執行有效的策略來管理珊瑚礁生態系,珊瑚生殖的研究乃為重要。過去關於石珊瑚的有性生殖之研究主要集中在熱帶區產之物種。在台灣,目前有56種石珊瑚其包括一模式物種 - 腎型真葉珊瑚的有性生殖之特徵曾被描述過。 對其它珊瑚物種於此方面的認知還顯不足。因此本論文的研究目標為 1)以深入的野外潛水採樣 (2013年至2016年間進行)、觀察及組織切片的方式來紀錄在台灣北部地區的珊瑚群聚物種之有性生殖; 2)利用組織切片的方式和水族缸飼養方式來確認台灣北部地衣微孔珊瑚的有性生殖的特徵,包括性別,受精方式及生殖腺發育過程,3)利用腎型真葉珊瑚當模式物種來了解Dmrt基因家族的在珊瑚有性生殖過程中扮演的角色。
從第一個研究(2013年到2016收集的資料)的結果顯示, 排放精卵珊瑚的物種及數量在年間有顯著的差異。這四年內一共觀察到六科19屬43種珊瑚排放精卵。而排放精卵在七月及/或八月的晚上八點到十點之間 。而且同一株珊瑚不同步排放精卵的現象也很顯著。
從第二個研究結合組織切片和水族養殖觀察之結果,我確認了微孔地衣珊瑚是雌雄異體及孵育型。生殖腺發育及受精時間有季節性。在組織切片的觀察過程,發現兩個從未發現的生殖型態特微:在早期生殖腺發育時,雌雄同體的個體,其卵和精細胞在精巢內一起發育,以及在精巢內發現黑色素顆粒細胞。
從第三個研究中, 我成功在腎型針葉珊瑚找到並描述七個Dmrt基因(EaDmrtA, EaDmrtB, EaDmrtC, EaDmrtE, EaDmrtF, EaDmrtG, 和 EaDmrtH) ,基因表現分析結果只有EaDmrtE具在卵發育時具專一性的表現。根據演化分析結果,此在卵發育過程具專一性表現的EaDmrtE,和在多孔軸孔珊瑚的DM1 (目前鑑定為DmrtA; 可能也和有性生殖有關),及脊椎動物性別決定基因Dmrt1的其親源關係並不相近。EaDmrtE的基因表現在未受精的卵及初期受精卵維持高度的表現,但是在受精的後期顯著下降,因此推測EaDmrtE為母性因子在卵細胞發育過程及初期受精卵發育時扮演重要的角色。而在早期動物演化的過程中, 就有和生殖有關的Dmrt基因的存在,且這樣的基因可能經過多次的演化。雌性專一性表現的EaDmrtE 除了可能應用在鑑定珊瑚的性別,且提供一個分子生物研究的基因材料,來研究並建立生殖基因調控的機制。
Coral reef ecosystem is now facing severe threats due to irreversible disturbances caused by natural disasters, anthropogenic effects and global warming. Coral communities in Taiwan are found in both subtropical and tropical regions and contain about 317 species that are also under threats. The persistence and recovery of coral communities depend partly on the success of reproduction after the disturbances. It is, therefore, important to study their reproductive biology in order to propose the effective strategy for the management of the coral reef ecosystem. Most of the previous studies documenting the sexual reproduction in scleractinian corals, however, concerned mainly the tropical-living species. To date, among the reported species in Taiwan, only 56 species including a model species, Euphyllia ancora, have been investigated. Little was known from other species. The objectives of this dissertation are 1) to study the coral spawning in the subtropical coral communities in northern Taiwan by comprehensive field samplings and observations conducted from 2013 and 2016, and by the assessments from histological analyses of the collected samples; 2) to characterize the sexual system, mode of reproduction as well as gametogenesis of Porites lichen living in Pitoujiiao, northern Taiwan by histological analyses and in situ aquarium observations; 3) to investigate the possible roles of the Dmrt gene family in coral reproduction by using Euphyllia ancora as a model.
First, field observations and histological examinations revealed a large annual variation of spawning pattern among species and individuals. Forty-three species classified into 19 genera and six families spawned asynchronously in the nights (between 8 pm to 10 pm) July and/or August from 2013 to 2014. In addition, corals spawned asynchronously within the same colony.
Second, the combined results from the histological examinations and others revealed that the gonochoric P. lichen is a polygamodioecious brooder that displays a seasonal pattern of sexual reproduction in gametogenesis and embryogenesis. In addition, I also reported two new morphological configurations during the early stage of gametogenesis with oocytes being developed within spermaries in bisexual polyps and melanin granular cells being clustered into spermaries.
Third, I successfully isolated and characterized seven paralogous Dmrt genes (EaDmrtA, EaDmrtB, EaDmrtC, EaDmrtE, EaDmrtF, EaDmrtG, and EaDmrtH) from the gonochoric E. ancora. I found that EaDmrtE is predominantly expressed in oocytes. This oocyte-specific DmrtE is not closely related to neither the DM1 gene (i.e. currently known as DmrtA; its function is possibly related to sexual reproduction) of Acropora millepora nor to Dmrt1 of vertebrates based on the result of phylogenetic analysis; these two genes are involved in sexual reproduction, especially in sex determination (e.g. vertebrate Dmrt1 gene). High levels of EaDmrtE transcripts were detected in unfertilized mature eggs, and that were retained in newly formed zygotes and, then, the levels of expression decreased during embryonic development. I suggest that this newly discovered gene possibly plays an important role during oogenesis and early embryogenesis in corals as a maternal factor. These results strongly support a complex evolutionary history for the sexual reproduction-associated Dmrt genes with the possibility that such kinds of the genes have originated multiple times early in the evolution of metazoans. The identification of female-specific genes (E. ancora DmrtE) not only provides useful biomarkers to determine the sex of gonochoric corals, but also provide materials for molecular studies on the characterization of the genetic pathways underlying the sexual reproduction in corals.
Acknowledgments

中文摘要……………………………………………………………………………...I
Abstract………………………………………………………………..…………….III
Chapter 1 General Introduction…………………………………………………….1
1.1 Sexual reproduction in scleractinian corals……………………………………..1
1.2 Gametogenesis and spawning in corals…………………………………………3
1.3 Coral communities in Taiwan…………………………………………………..4
1.4 Studies of sexual reproduction in corals in Taiwan…………………………….6
1.5 Molecular mechanisms of sexual reproduction in scleractinian corals………...7
1.6 Objectives of this dissertation…………….…………………………………….8
Chapter 2 Multi-species Spawning of Scleractinian Corals in Pitoujiiao and Longdong, Northern Taiwan……………………………………………………….13
2.1 Introduction…………….…………………..……………………………...…..13
2.2 Materials and methods……..……………..………………………………..….14
2.2.1 Study sites……………………………………………………………...14
2.2.2 Coral spawning by field survey………………….……………………..14
2.2.3 Multiple spawning among conspecific colonies……………………….15
2.2.4 Inference of spawning period by histological analysis………………...15
2.2.5 Seawater temperatures and typhoon occurrence……………………….16
2.2.6 Analytical methods……………………………………….…………….16
2.2.6.1 Species identification……………………………………………...16
2.2.6.2 Histological analysis………………………………………………16
2.2.6.3 Seawater temperature...……………………………………………17
2.3 Results and Discussion………………………….....………………………...17
2.3.1 Spawning time window and related to the full moon from 2013 to 2016…………………………………………………………………..………17
2.3.2 Annual variation in spawning pattern from 2014 to 2016…………….18
2.3.3 Multiple spawning in conspecific species and within colony……....…19
2.3.4 Spawning periods inferred by histological analyses…………...….…..19
2.3.5 Temperature…………………………………………………….……..20
2.3.6 Typhoon disturbance during spawning and post-spawning…….…..…21
Chapter 3 Characterization of sexual reproduction of a scleractinian, Porites lichen Pitoujiiao, northern Taiwan……………………….……………………...31
3.1 Introduction….……………………………………….……..………..……….31
3.2 Materials and methods….………………………………………..……….…..31
3.2.1 Sample collections……………………………………………….……31
3.2.2 Histological analysis…………………………………..………………32
3.2.3 In situ observation of coral reproduction in aquarium………….……..32
3.3 Analytic methods…………………………………………………...…………33
3.4 Results and Discussion………………………...…………………….…….….33
3.4.1 Sexual system …………………….…………..……………………….33
3.4.2 Gametogenesis of P. lichen……………………………………………34
3.4.3 Germ cell development in bisexual colonies………………….……….36
3.4.4 mode of reproduction and reproductive cycle in P. lichen………….....37
3.4.5 Melanin granular cells…………………………………………….……37
Chapter 4 A novel female-specific and sexual reproduction-associated Dmrt gene discovered in the stony coral, Euphyllia ancora (Cnidarian, Anthozoa)…..46
4.1 Introduction…………………………………………….……………………..46
4.2 Materials and Methods……………………………………….……………….48
4.2.1 Coral collection in the field and different time points from adult colony……………………………………………………………………..….48
4.2.2 Collection for specific tissues……………………………...…………..49
4.2.3 Analytical methods……………………………………….…………….49
4.2.3.1 cDNA synthesis, polymerase chain reaction amplification, cloning and sequencing …………………………..………………………..49
4.2.3.2 Quantitative RT-PCR analysis……………………………………51
4.2.3.3 Phylogenetic analyses and comparison of sequence similarity…...53
4.2.3.4 Northern Bloting and in situ hybridization……….…………...…..54
4.3 Results………………………………………………………………………...55
4.3.1 Isolation and characterization of EaDmrt paralogs……………...……..55
4.3.2 Phylogeny of metazoan Dmrt genes…………………………….……..56
4.3.3 Temporal gene expression of EaDmrts………………………………..56
4.3.4 Spatial gene expression for EaDmrts……………………….…………57
4.3.5 Northern blot analysis and in situ hybridization of EaDmrtE transcripts…………………………………………………………………….57
4.3.6 EaDmrtE as a maternal factor…………………………….……………57
4.4 Discussion………………………………...………………………………….58
4.4.1 Female-specific Dmrt genes in metazoans……………………………..58
4.4.2 Transcriptional regulations in oogenesis……………………………….59
4.4.3 Maternal inheritance of Dmrts…………………………………………60
4.4.4 Homology of cnidarian sexual reproduction-associated Dmrt genes..…61
Chapter 5 Conclusion and perspectives……………………………………..…..77
References……………………………………………………….…………………..80
Appendix I. Coral species studied in Taiwan in Chapter 2…………………………..98
Appendix II. Primers used for the classical PCR amplification, 5'' and 3'' RACE, and q-PCR in chapter 4……………………………………………………………………105
Appendix III. NCBI sequences and reference for chapter 4………………..………110
Appendix IV. References for Fig. 4.1 in Chapter 4…………………………..…….120 
Figure content
Figure 2.1 Study sites……………………………………………………………..….24
Figure 2.2.1 Abundance of spawning corals in Merulinidae in July and August from 2014 to 2016………………………………………………………………..….25
Figure 2.2.2 Abundance of spawning corals in Poritidae, Agaricidae, Fungiidae, Psammocoridae, and Lobophyllidae in July and August from 2014 to 2016……………………………………………………………………………26
Figure 2.3 Multiple spawning in Favites pentagona, Astrea curta, Favites stylifera and Favites halicora from 20 to 28 July 2016…………………………..…….27
Figure 2.4 Inference of the coral spawning by histological analyses in 2014…….…28
Figure 2.5 Sea water temperature from January 2014 to September 2016 in Pitoujiiao, northern Taiwan……………………………………………………………….29
Figure 2.6 Typhoon occurrences in July, August (during spawning) and September (after spawning) from 2014 to 2016…………………….…………….……….30
Figure 3.1 Study sites and a colony of Porites lichen………………………..………40
Figure 3.2 Histological examinations of the sexual system of P. lichen………….…41
Figure 3.3 Spermatogenesis in male colonies in 2015……………………………….42
Figure 3.4 Oogenesis in female colonies in 2015……………………………………43
Figure 3.5 Germ cell development in bisexual colonies…………………….……….44
Figure 3.6 Melanin granular cells in P. lichen………………………………...……..45
Figure 4.1 Summary of the available data on the diversity, tissue-specific expression patterns, and functions of the Dmrt members in metazoan adults and embryos………………………………………………………………………..64
Figure 4.2 The schematic diagrams of the Euphyllia ancora Dmrt transcripts…………………………………..……………………………….…66
Figure 4.3 The 50% majority-rule consensus tree is resulted from the Bayesian phylogenetic analysis with best-fit JTT+Gamma model based on the amino-acid sequences from the DM domains o the metazoan Dmrts……………..……….67
Figure 4.4 The 50% majority-rule consensus tree resulting from the Bayesian phylogenetic analysis with best-fit JTT+Gamma model based on the amino-acid sequences from the DM domains of the cnidarian Dmrts………………….….69
Figure 4.5 Quantification of the relative expression of EaDmrts in gonad tissues during spermatogenesis and oogenesis of gonad tissues by quantitative RT-PCR analysis………………………………………………………………….…….71
Figure 4.6 Quantification of the relative expression of EaDmrts in the male and female tissues that were collected in March…………………….…………….73
Figure 4.7 Expression of EaDmrtE in ovarian tissues……………………..………..75
Figure 4.8 Relative expression of EaDmrtE during E. ancora embryonic development …………………………………………………………………….…………...76

Table content
Table 1.1 Coral species studied in Taiwan……………………………………………9
Table 2.1 Numbers of spawning colony and species from 2014 to 2016………..…..23
Table 3.1 Criteria for oogenic and spermatogenic stages for P. lichen…………...…39
Table 4.1 Comparison of similarity of E. ancora Dmrt amino acid sequences (full sequence and DM/DMA domains)………………………………………………..….63
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