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研究生:陳建勳
研究生(外文):Chienhsun Chen
論文名稱:鹿角珊瑚科珊瑚的粒線體基因組
論文名稱(外文):Mitochondrial Genome of the Pocilloporid Scleractinian
指導教授:戴昌鳳戴昌鳳引用關係
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:2008
畢業學年度:96
語文別:英文
論文頁數:150
中文關鍵詞:石珊瑚鹿角珊瑚科粒線體基因組
外文關鍵詞:ScleractinianPocilloporidaeMitogenome
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本論文利用鹿角珊瑚科石珊瑚的粒線體基因組來探討 (1)珊瑚蟲綱生物粒線體序列慢速演化假說是否適合所有石珊瑚,(2)確立鹿角珊瑚科在石珊瑚中的親緣演化關係。
首先,實驗藉由列孔珊瑚(Seriatopora)粒線體基因組序列分析和不同粒線體DNA片段在族群內、族群間及種間的遺傳變異分析來驗證珊瑚蟲綱生物的粒線體序列慢速演化假說。由粒線體基因組序列顯示列孔珊瑚與其他的石珊瑚除了有類似的粒線體基因組成外,它具有3個明顯的分子特徵,一個特殊的atp8基因、重複的trnW基因及一個位於atp6及nad4基因之間的控制區域。另外在種間與種內的遺傳變異分析結果中顯示,許多蛋白質基因及基因間隔區的DNA序列可作為判定近緣種及族群晚近分歧的親緣分析資料;其中atp6基因及控制區的分子演化速率大約是其他石珊瑚的2~7倍。利用親緣關係分析印度西太平洋的族群,結果說明過去3百萬年來因為歷史事件而隔離於安達曼海的族群是一個單系群;本實驗成功地以粒線體DNA建構西太平洋鈍枝列孔(Se. caliendrum)及尖枝列孔(Se. hystrix)的親緣關係,並顯示出列孔珊瑚的粒線體內高度變異DNA序列可用來作為族群遺傳分析的分子標誌。由此說明珊瑚蟲綱生物的粒線體序列可能在基因之間、基因間隔區之間,或是系群之間有不同的演化速率,慢速演化的假說並不適合所有石珊瑚。
在論文第二部分說明鹿角珊瑚科的成員同樣具有列孔珊瑚粒線體基因組的特性。由該科其他屬珊瑚包括Madracis formosa、細枝鹿角珊瑚(Pocillopora damicornis)及萼柱珊瑚(Stylophora pistillata)的粒線體基因組序列分析的結果顯示,鹿角珊瑚科石珊瑚與其他的石珊瑚也擁有同樣類似的粒線體基因組,序列的長度大多介於16,951~17,426個鹼基對,編碼股的A+T鹼基組成介於68.3~70.1%之間。利用反轉錄聚合鏈鎖反應及北方墨點分析的結果顯示此科石珊瑚粒線體基因組上的atp8基因會表現。另外,其atp6及nad4基因間隔區也發現具有相連重複序列、保守序列區及形成可能具有功能的二級結構,此部份區域可能是鹿角珊瑚科石珊瑚粒線體的控制區。重複的trnW基因目前僅在列孔珊瑚及柱珊瑚(Stylophora)發現。由於鹿角珊瑚科在所有石珊瑚中是唯一同時具有此3項分子特徵的珊瑚,說明其親緣演化關係值得進一步探討。
為了說明鹿角珊瑚科在石珊瑚內的親緣演化關係,本研究從粒線體蛋白質基因的氨基酸使用率(codon usage)及其分子親緣關係來釐清鹿角珊瑚科在傳統分類及分子親緣關係之間的歧見。結果顯示現生的石珊瑚是一個多系群,包括複雜骨骼系群(complex clade)、結實骨骼系群(robust clade)及鹿角珊瑚科等三個系群,其中,由鹿角珊瑚科與結實骨骼系群的姊妹系群關係來看,二者間有最近起源的共同祖先,此結果支持前人利用rDNA所建構的分子親緣關係。
另外,本研究亦利用分子定年的分析方法來估計鹿角珊瑚科系群的分歧時間,並檢視現生石珊瑚演進的時程。結果顯示鹿角珊瑚科系群大約出現在330百萬年前,比最古老的星珊瑚亞目化石(三疊紀中葉)還要早100百萬年;此結果支持”裸珊瑚"假說,根據該假說,我們推測不具有骨骼的鹿角珊瑚(或星珊瑚)系群大約自石炭紀與結實骨骼系群分歧(約330百萬年前),直到三疊紀才衍生出外骨骼的特徵。
我們總結(1)珊瑚蟲綱物種粒線體序列慢速演化假說,並不適用於所有石珊瑚;(2)根據粒線體基因組分析的證據,現生的石珊瑚可以區分成3個系群,(3)確立鹿角珊瑚科在石珊瑚中的親緣演化關係,為獨立的另一石珊瑚系群。
In this dissertation, I focus on the study of mitochondrial genome (mitogenome) of the scleractinian family Pocilloporidae to address two main evolutionary issues. Firsty, the slow-evolution hypothesis of anthozoan mitochondrial (mt) DNA was evaluated by comparing mitogenomes of 2 sibling (sister) coral species. Secondly, the evolutionary phylogeny of the Pocilloporidae was investigated by mitogenomic analyses.
The complete mitochondrial genomes of 2 sibling (sister) Seriatopora species were first sequenced and determined in order to verify the slow evolution of anthozoan mtDNA (Chapter 3). Afterward different mtDNA regions were evaluated by analyzing variations and divergences within and between populations of the same species and by comparisons between 2 Seriatopora species. Gene arrangement of the Seriatopora mitogenomes is similar to the currently published scleractinian mitogenomes with the exception of three eclusive features, including gene atp8, a duplicated trnW (tRNATRP), and a putative control region located between atp6 and nad4. The significances of a highest value in between-species variation and a lowest one in within-population comparison showed several protein-coding genes and intergenic spacers could provide phylogenetic information in discerning among recently-diverged populations or boundaries of delineating species. Phylogenetic analyses of the hypervariable regions for the Indo-West Pacific populations also revealed a monophyly of the Andaman-Sea Seriatopora, which is suggested to be separated geographically since 3 million years ago. Evaluation of the molecular evolution of atp6 and the putative control region showed 2- to 7-fold higher divergence rates among populations or between species than those published for scleractinian mitogenomes. This study not only successfully reveals the phylogenies of Se. hystrix and Se. caliendrum from the West Pacific Ocean by mtDNA of the 9th intergenic spacer, putative control region, atp6, and the cox1 genes, but also highlights the potential utility of hypervariable regions of mt phylogenetic tree construction for Seriatopora below the species level. The hypothesis of slow evolution of anthozoan mtDNA should be treated with caution, since the evolutionary rate of the mitogenomes could be highly variable among different genes and intergenic spacers, and even in different scleractinian lineages.
Since unique mt features were detected in Seriatopora corals, I extended the determination of complete mitogenomes to three confamilial genera in order to understand whether these mt characteristics are also present in other pocilloporid corals (Chapter 4). The mitogenomes of the Madracis formosa, Pocillopora damicornis, and Stylophora pistillata were amplified and determined. The entire mitogenomes of pocilloporid corals ranged from 16,951 to 17,426 bp with the A+T contents ranging from 68.3% to 70.1%. The gene order of protein-coding genes was identical to those of other scleractinian corals. The novel atp8 gene, first described in Seriatopora corals, was also confirmed using RT-PCR, Northern blot, and sequence analyses in other genera of the Pocilloporidae. The intergenic spacer between atp6 and nad4, containing distinct repeated elements, conserved sequence blocks and domains, and functional structures, possesses typical characteristics of a putative control region for the four coral genera. A duplicated trnW, detected in the region close to the cox1 which shares the highly conserved primary and secondary structures of its original counterpart, was discovered in both Seriatopora and Stylophora. These molecular characteristics are unique and provide phylogenetic information for future evaluation of the status of the family Pocilloporidae in the evolutionary history of scleractinian corals.
The phylogenetic status of the pocilloporid corals were revised in various aspects according to the mt system (Chapter 5). Different approaches, such as differences in amino-acid usage and molecular phylogeny of 13 protein-coding genes, were utilized to clarify the unsolved discordance between traditional taxonomy and former molecular phylogeny. My results support the former phylogenetic evidence of rDNA sequence. Results of the amino-acid usage and the phylogenetic analyses indicated that the extant Scleractinia was polyphyletically distributed into 3 separate clades, including pocilloporid, complex- and robust-clade corals. The pocilloporid was jointed as a sister clade to robust-clade corals, indicating its most recent common ancestor with robust clade rather than the implicated relationship in conventional taxonomy.
Molecular-dating analysis of the phylogenetic trees was used to estimate the development of the pocilloporid lineage. The molecular-dating analysis showed a 330 million years (MY) divergence between the pocilloporid and the robust-clade corals, which is about 100 MY earlier than the oldest fossil Astrocoeniina (middle Triassic). After examining several possible key factors, I suggest that the discrepancy between the oldest fossil record and the molecular-dating estimate may be an evidence of the “naked-coral” hypothesis. The soft-bodied Pocilloporidae (Astrocoeniina) group might have diverged from the robust-clade scleractinian during in the Carboniferous (about 330 Ma), then evolved their skeleton later in the Triassic.
Comparisons of mitogenome size, nucleotide composition, and initiation/termination of protein-coding genes indicate that scleractinians could be separated into 3 groups which were concordant with previous studies (Chapter 6). Based on the results of mitogenomic analyses, the Pocilloporidae was deeply diverged from the robust clade and could be considered a distinct lineage of scleractinian corals, in addition to the 2 scleractinian clades by former molecular evidences. The taxonomic status within the Astrocoeniina was also discussed.
Committee verified document (in Chinese) …………………………………………………………ii
Abstract in Chinese …………………………………………………………………………………iii
Abstract in English …………………………………………………………………………………..v
Table of Content …………………………………………………………………………………...viii
List of Tables ………………………………………………………………………………………...x
List of Figures ……………………………………………………………………………………....xi
Chapter 1. General introduction ……………………………………………………….…………….1
1.1 General characteristics of the animal mitochondrial genomes …………………………..1
1.2 Unique features of the cnidarian mitogenomes ………………………………………….1
1.3 Mitogenome of the scleractinian coral …………………………………………………..2
1.4 Scleractinian systematics implicated by skeleton characteristics ………………………..2
1.5 Molecular phylogenetics of the extant scleractinian …………………………………….4
1.6 Pocilloporidae: their evolutionary status remain obscure ……………………………….6
1.7 Phylogenomics …………………………………………………………………………..6
1.8 Aims to my PhD studies …………………………………………………………………9
Chapter 2. General materials and methods …………………………………………………………12
2.1 Coral species used in this study ………………………………………………………...12
2.2 Genomic DNA extraction …………………………………………...………………….13
2.3 Molecular protocol and analyses of mitogenomes ……………………………………..14
2.3.1 Amplification, cloning and sequencing ………………………………………14
2.3.2 Genome annotation and sequence analysis …………………………………..16
2.4 Identifying the ATP8 gene ……………………………………………………………..17
2.4.1 Hydropathy profile …………………………………………………………...18
2.4.2 Reverse-transcription PCR (RT-PCR) ………………………………………..18
2.4.3 Northern blot analysis ………………………………………………………...19
2.5 Evaluating the mtDNA for phylogenetic utility below the species level ………………20
2.5.1 Sample collection and DNA extraction ………………………………………20
2.5.2 PCR amplification ……………………………………………………………21
2.5.3 Genetic distances and phylogenetic analyses ………………………………...22
2.6 Phylogenetic revision of the Pocilloporidae ……………………………………………23
2.6.1 Taxa sampling ………………………………………………………………...23
2.6.2 Amno acid usage ……………………………………………………………...24
2.6.3 Molecular phylogeny …………………………………………………………24
2.6.4 Molecular dating ……………………………………………………………...26
Chapter 3. The complete mitogenomes of Seriatopora corals and hypervariable regions used to determine species phylogenies and recently diverged populations …………………….36
3.1 Introduction …………………………………………………………………………….36
3.2 Results ………………………………………………………………………………….38
3.2.1 Characterization of the Seriatopora mitogenomes ………………………………..38
3.2.2 Evaluating the utilities of mtDNA for species-level phylogeny …………………..40
3.2.3 Phylogenetic implications …………………………………………………………41
3.3 Discussion ………………………………………………………………………………43
3.3.1 Molecular phylogeny of Seriatopora over the Indo-West Pacific …………………43
3.3.2 Applications of the hypervariable regions to the phylogeny of coral species and population …………………………………………………………………………44
Chapter 4. Novel atp8, putative control region between atp6 and nad4, and duplicated trnW are unique features in scleractinian family Pocilloporidae as indicated by mitogenomic analyses………………………………………………………………………………….57
4.1 Introduction …………………………………………………………………………….57
4.2 Results ………………………………………………………………………………….58
4.2.1 Composition and organization of mitogenome in the Pocilloporidae ……………..58
4.2.2 Protein-coding genes ………………………………………………………………58
4.2.3 Idiosyncratic ATP8 gene …………………………………………………………...59
4.2.4 Codon usage ……………………………………………………………………….60
4.2.5 Transfer RNA genes ……………………………………………………………….61
4.2.6 Intergenic spacers ………………………………………………………………….62
4.2.7 The intergenic spacer between atp6 and nad4 containing features of the mitochondrial control region ………………………………………………………62
4.3 Discussion ………………………………………………………………………………66
4.3.1 Novel ATP8 genes …………………………………………………………………66
4.3.2 Duplicated trnW for Se. hystrix and St. pistillata ………………………………….67
4.3.3 A putative control region locates between atp6 and nad4 …………………………68
4.4 Conclusions …………………………………………………………………………….70
Chapter 5. Evolution and phylogenetic status of the Pocilloporidae corals, based on mitogenomic analyses …………………………………………………………………………………91
5.1 Introduction …………………………………………………………………………….91
5.2 Results ………………………………………………………………………………….93
5.2.1 Amino acid usage …………………………………………………………………93
5.2.2 Molecular phylogeny ……………………………………………………………...94
5.2.3 Molecular dating …………………………………………………………………...95
5.3 Discussion ………………………………………………………………………………97
5.3.1 Divergence between Pocilloporidae and Acroporidae …………………………….97
5.3.2 The phylogenetic status of the Pocilloporidae ……………………………………..99
5.3.3 Phylogeny and systematics of the Pocilloporidae and Astrocoeniina ……………101
Chapter 6. Summary and general discussion ……………………………………………………...115
References ………………………………………………………………………………………...124
Appendix A. Percentage of pairwise nucleotide sequences similarity among corresponding mt IGSs (intergenic spacer) of pocilloporid corals …………………………………………...133
Appendix B. Species abbreviations ……………………………………………………………….134
Appendix C. The complete mitochondrial genomes of needle corals, Seriatopora spp. (Scleractinia: Pocilloporidae): an indiosyncratic atp8, duplicated trnW gene, and hypervariable regions used to determine species phylogenies and recently diverged populations ..135
Appendix D. Mitogenomic analyses indicate that the novel atp8, putative control region spanning atp6 to nad4 and duplicated trnW are phylogenetically unique features in the scleractinian family Pocilloporidae (Scleractinia: Astrocoeniina) ………………….150
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