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研究生：	安鳳鳴 An, Feng-Ming
論文名稱：	利用高通量定序分析進行蝴蝶蘭功能性小核醣核酸在涼溫反應之研究 Study of functional small RNAs responded to low ambient temperature using high-throughput sequencing in Phalaenopsis aphrodite subsp. formosana
指導教授：	詹明才 Chan, Ming-Tsair
共同指導教授:	黃浩仁 Huang, Hao-Jen 陳榮芳 Chen, Long-Fang
學位類別：	博士 Doctor
系所名稱：	生物科學與科技學院 - 生物科技研究所 Institute of Biotechnology
論文出版年：	2012
畢業學年度：	101
語文別：	英文
論文頁數：	169
中文關鍵詞：	高通量定序、蝴蝶蘭、小核醣核酸、微小核糖核酸、涼溫、降解體
外文關鍵詞：	deep sequencing, Phalaenopsis, small RNA, microRNA, low ambient temperature, degradome
相關次數：	點閱：99 下載：2
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蝴蝶蘭為台灣高經濟花卉作物，其中白花蝴蝶蘭為台灣的原生種，常利用作為育種的親本。白花蝴蝶蘭與其他蘭科植物相比，具備有對環境溫度敏感的特性。工業上常利用高溫抑梗以及涼溫催花的方式調控白花蝴蝶蘭的開花時期。對於涼溫影響到開花時期的研究甚少，多數對於溫度影響開花時期的研究專注在低溫所誘導的春化作用，並多以模式植物作為研究對象。是故我們的研究以白花蝴蝶蘭這種非模式生物作為研究對象，針對小核醣核酸，研究在涼溫催花下受到小核醣核酸的影響。本研究利用高通量定序的方式，分別建立了轉錄體、小核醣核酸以及降解體的序列資料庫。比較生物資訊的分析以及小核醣核酸雜合實驗下歸納出4種保守的微小核醣核酸家族為受涼溫影響之因子 (miR156, miR162, miR528 and miR535)，並獲得可能之目標基因，並進而討論微小核醣核酸在涼溫催花中所扮演的角色。結合了轉錄體、小核醣核酸及降解體的分析可以提供在小核醣核酸主導的目標基因降解產物大量的實驗佐證。除了保守的微小核醣核酸外，降解體的分析也可以鑑定新發現的微小核醣核酸之目標基因。再者，其他有類似降解機制的小核醣核酸以及其目標基因也可以被鑑定出來。我們後續針對鑑定出來的新的微小核醣核酸以及小核醣核酸進行表達量的分析。其中7個新的微小核醣核酸皆為涼溫抑制。小核醣核酸則有9個受到涼溫影響。後續我們亦發現在這些表達量很高的小核醣核酸中有許多來自於自然反股轉錄子，而這些很長的自然反股轉錄子可以進一步生成有功能的小核醣核酸，進一步的影響到目標基因的表達。總結我們的研究利用了高通量定序為工具，建立序列資料庫，結合生物資訊分析以及實驗佐證，證明了在蝴蝶蘭中許多受涼溫調控的小核醣核酸。我們認為這樣的策略能廣泛的適用於非模式植物的研究之中。

Phalaenopsis aphrodite subsp. formosana is a native orchid species with high economic value and high polymorphism in floral appearance. Industries often use high temperatures (>28°C) to inhibit spike initiation and low temperatures (24°C/18°C, day/night) to synchronize the flowering date in certain Phalaenopsis species. To date, limited studies focus on the regulatory roles of miRNAs as well as functional small RNAs (sRNAs) in orchid. To identify sRNAs in Phalaenopsis responding to low temperatures, a sRNA profiling analysis using high-throughput sequencing technology was performed. Subsequent bioinformatic analysis was applied to categorize the miRNAs identified. A total of 37,533,509 sRNA reads yielded 11,129 independent orchid miRNA sequences, representing 329 known miRNA families identified in other plant species. Comparing sequencing data and sRNA northern hybridization results identified miR156, miR162, miR528 and miR535 as low temperature-induced miRNAs. In addition, tissue-specific expression of these miRNAs was investigated. It was concluded that miR156 and miR172 may be components of a regulatory pathway mediating transition from the vegetative to the reproductive phase in Phalaenopsis. We also combined the analyses of transcriptome and small RNA, and degradome library for identification of sRNA-directed transcript cleavages in Phalaenopsis orchid. Degradome analysis gave large-scaled evidences of conserved and novel miRNA-directed cleavage of target transcripts. Additionally, 46 abundant sRNA groups and their target transcripts were identified using this approach. Low temperature-responsive sRNAs were validated using normalized reads in sRNA library and quantitative stem-loop RT-PCR analysis. The target transcripts of novel miRNAs and sRNAs were functionally involved in some metabolic processes or response to stress according to the gene ontology (GO) categorization. Moreover, we also found one particular homolog gene, digalactosyldiacylglycerol synthase 2 (DGD2), was targeted by a natural antisense transcripts (NAT) that is unique in Phalaenopsis orchid. We also demonstrated a sequencing-based strategy to identify novel miRNAs, functional sRNAs, and lncRNAs when face on non-model plants. Identification and characterization of target transcripts also provide useful information for elucidating the regulatory mechanism underlying low ambient temperature regulation in Phalaenopsis orchid.

Index

中文摘要	1
Abstract	3
Acknowledgements (致謝)	5
Index	7
Table Index (表目錄)	14
Figure Index (圖目錄)	15
Chapter 1 - Introduction	18
1.1. Introduction of Phalaenopsis orchids	18
1.2. Classification of small non-coding RNAs	19
1.3. microRNA biosynthesis and interfering mechanism	20
1.4. Definition of microRNAs	21
1.5. Roles of microRNAs in flowering regulation	22
1.6. Roles of microRNAs in response of environmental stimuli	25
1.7. Introduction of high-throughput sequencing technology	26
1.7.1. The 454 pyrosequencing	27
1.7.2. Illumina sequencing	28
1.7.3. The ABI SOLiD system and other sequencing technologies	28
1.8. Application of high-throughput sequencing	29
1.8.1. Transcriptome (RNA-seq)	30
1.8.2. Small RNA (sRNA-seq)	31
1.8.3. Degradome (degradome-seq)	32
1.9. Study of functional sRNAs using sequencing-based strategy	33
Chapter 2 – Materials and Methods	35
2.1.	Plant materials and growth conditions	35
2.2.	Total RNA extraction (Trizol method)	35
2.3.	High molecular weight (HMW) RNA extraction (LiCl precipitation)	36
2.4.	Low molecular weight (LMW) RNA extraction	37
2.5.	Transcriptome library preparation	38
2.6.	Small RNA library preparation	38
2.7.	Degradome library preparation	39
2.8.	Prediction of microRNA precursors	40
2.9.	Alignment of conserved microRNA families	41
2.10.	Prediction of target transcripts for microRNAs	41
2.11.	Construction of standalone command line BLAST on Windows PC	42
2.12.	Custom formatted sequence library	43
2.13.	Bioinformatic analyses of degradome library	44
2.14.	Digital gene expression analysis of small RNA libraries	44
2.15.	Small RNA northern blot (non-radioisotope-labeled method)	45
2.16.	Modified 5’-RNA ligase-mediated rapid amplification of cDNA end (modified 5’-RLM-RACE)	47
2.17.	Quantitative reverse transcription polymerase chain reaction (RT-qPCR)	48
2.18.	Stem-loop quantitative reverse transcription polymerase chain reaction (stem-loop RT-qPCR)	48
2.19.	Strand-specific reverse transcription polymerase chain reaction	49
Chapter 3 – Results	51
3.1.	Summary of transcriptome library	51
3.2.	Summary of small RNA library	52
3.3.	Summary of degradome library	53
3.4.	Identification of microRNA biosynthesis pathway genes in Phalaenopsis orchid using the transcriptome library	54
3.5.	Conserved miRNAs are identified cross species	54
3.6.	Conserved and Novel miRNA precursors are identified in transcriptome library	55
3.7.	Target gene prediction of conserved miRNAs	55
3.8.	Target gene validation of conserved miRNA families using degradome analysis	56
3.9.	Identification of novel miRNA-mediated transcripts cleavage using degradome analysis	58
3.10.	Some abundant sRNAs are responsible for transcript cleavages	58
3.11.	Natural antisense transcript of Phalaenopsis digalactosyldiacyl- glycerol synthase homolog gene caused non-miRNA-directed transcript cleavages	59
3.12.	Several conserved miRNAs, novel miRNAs and sRNAs respond to low ambient temperature	60
3.12.1. Conserved miRNAs	61
3.12.2. Novel miRNAs	62
3.12.3.	Other abundant sRNAs	63
3.13.	Validation the role of miRNAs in the developmental process	64
3.13.1. miR156 and miR172 play consensus roles in flowering regulation	64
3.13.2. miR396-targeted GRF homologs are low temperature-responsive and may associate with cell proliferation in Phalaenopsis aphrodite subsp. formosana.	65
3.14.	Conclusions	68
Chapter 4 – Discussions	69
4.1.	High-throughput sequencing-based strategy combines the analyses of transcriptome, sRNA, and degradome	69
4.2.	Comparison of high-throughput sequencing with other technologies	69
4.3.	Technical concerns of expression analyses of small RNAs by hybridizing methods	70
4.4.	The problems in isolation and identification of Phalaenopsis orchid’s RNA	71
4.5.	miR156 and miR172 play conserved roles in thermosensing pathway and flowering time regulation	73
4.6.	Some low ambient temperature-responsive miRNA families may participate in flowering regulation	74
4.7.	Degradome analysis also revealed the evolutionary conservation of some miRNA families and their target transcripts	76
4.8.	Degradome analysis revealed several functional sRNAs were species-specific and low temperature-responsive	78
4.9.	Other type of sRNA (siRNAs, nat-siRNAs) can be validated using degradome analysis	79
Chapter 5 – Prospections	82
References	125
Appendix	143
Appendix 1. Statistics report of export of orchids in Taiwan	143
Appendix 2. Materials used for high-throughput sequencing	144
Appendix 3. Analysis of miRNA expression levels in Phalaenopsis aphrodite subsp. formosana using northern hybridization.	145
Appendix 4. Regulatory and miRNA-mediated networks of leaf morphology	146
Appendix 5. Secondary structure simulation of conserved miRNA precursors	147
Appendix 6. Identification of conserved miRNA precursors using MIREAP program	148
Appendix 7. Identification of cleavage sites and expression patterns of PaSPL and PaAP2 in Phalaenopsis aphrodite subsp. formosana.	151
Appendix 8. Low temperature responsive miRNA families in different plant species	152
Appendix 9. miRNA orthologs in different plant species	153
Appendix 10. Comparison of Target genes of sRNA in Phalaenopsis orchid with those of the orthologs in Arabidopsis.	156
Appendix 11. Nucleotide sequence alignment of AtDGD2 and PaDGD2 (partial)	158
Appendix 12. Amino acid sequence alignment of AtDGD2 and PaDGD2 (partial)	159
Appendix 13. Predicted NATs in Phalaenopsis transcriptomic library.	160
Appendix 14. Primer list	161
Appendix 15. PHP source code for making reverse and complement sequence in fasta format	165
Appendix 16. PHP source code for converting fasta format into tabular format	166
Appendix 17. PHP source code for converting bowtie format into mireap format	167
Appendix 18. Construction of standalone WWWBLAST webserver	168
                                    

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