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研究生： 阮氏翠瓊
Nguyen, Thi Thuy-Quynh
論文名稱： 利用轉錄體探討植物對砷逆境的反應及耐受性以及其中的機制
Transcriptome analyses provide insights into Arsenic-stress responses and tolerance mechanisms in plants
指導教授： 黃浩仁
Huang, Hao-Jen
學位類別： 博士
Doctor
系所名稱： 生物科學與科技學院 - 生命科學系
Department of Life Sciences
論文出版年： 2014
畢業學年度： 103
語文別： 英文
論文頁數： 194
外文關鍵詞： Arsenic, Oryza sativa, Arabiopsis, Glutathione, Oxalate oxidase, WRKY76, LRR-RLK VIII
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    • 砷為一具有毒性的類金屬，且廣泛的存在於環境中，並對植物具備很強的毒性。然而，目前為止植物對砷逆境的反應還未被徹底的瞭解。在砷的逆境中，三價砷造成的毒性反應遠比五價砷來的強。此篇研究試圖找出植物中造成此不同毒性反應的基因。我們利用生物晶片分析水稻對三價砷與五價砷的反應，生物資訊分析顯示有一群基因對兩者皆具有反應。這群因大多與解毒機制相關，列如熱休克蛋白、細胞色素P450、UDP糖基轉移酶以及谷胱甘肽s-轉移酶 (GST)。有趣的是大部分被三價砷誘導表現量上升的基因，其表現量遠高於對五價砷的反應。脫落酸反應片段結合因子(ABA response element binding factor) (Os01g0859300) 以及 WRKY76 (Os09g0417600)在三價砷的逆境下有較高的表現量(大於八倍)。除此之外，三價砷處理下我們也發現草酸氧化酶(OXO)表現量以及活性的增強。另外，麩胱甘肽(glutathione)的表現量在兩種砷處理下都先下降(12小時處理)，而在處理24小時候上升。過氧化氫酶以及過氧化酶活性在12小時及24小時處理下皆上升。
    除了水稻之外，我們發現了兩種生態型的阿拉伯芥對砷俱備不同程度的耐受性。耐受性較強的為Col-0，較弱的為Ws-2. 我們利用生物晶片比較兩種生態型在遇到五價砷時的轉錄體變化。被Col0獨特調控的基因中，大多數為熱休克蛋白，熱休克因子、泛素以及水通道蛋白。除此之外，我們發現了與Col-0 耐受性相關的基因。我們研究了其中一個耐受性相關的蛋白質激酶(Leucine-Rich Repeat receptor-like kinase VIII)的突變株，發現在此Col-0 的突變株中，五價砷的耐受性與累積量皆會受到影響。
    針對植物對不同價數砷的耐受性，本研究提供了更深入的探討，有助於未來更進一步研究與砷耐受性相關的基因以及植物中砷的去毒性機制 

    Arsenic (As) is metalloid found ubiquitously in natural environment and is generally highly toxic to plants. However, the molecular mechanisms of plants in response to As have not been extensively characterized. Thus, we aimed to identify genes that discriminate the effect of Asenite (AsIII) and Asenate (AsV) during early response to rice roots (Oryza sativa L. cv. TN67). To gain more insights into cellular responses to arsenic, we have undertaken a large-scale analysis of the rice transcriptome challenged with AsIII and AsV stresses. Bioinformatic analysis indicated that a series of transcripts differently appeared in general responses to both of arsenic. Most of these common response genes related to detoxification such as heat shock proteins, Cytochrome P450, UDP-glycosyltransferase and Glutathione S-transferase. Interestingly, expression levels of most of AsIII-induced genes were strongly increased than that found in the AsV-induced. Expression level of genes encoding to bZIP10 (Os01g0859300) and WRKY76 (Os09g0417600) under AsIII treatment was higher (> 8-folds) than that in AsV treatment. The enhanced expression and activity of oxalate oxidase (OXO) were observed in AsIII-subjected rice roots. Additionally, the glutathione contents from both treatments at 12 h decreased, whereas increasing during 24 h treatment with As. Catalase (CAT) and peroxidase (POD) activities in rice roots were induced after 12 h and 24 h in both of arsenic treatments.
    Concurrently, we compared transcriptional changes on genome-wide gene expression with AsV treatment in two AsV-tolerant (Col-0) and sensitive (Ws-2) Arabidopsis ecotypes. Most of the specific response genes encoded heat shock proteins, heat shock factors, ubiquitin and aquaporin transporters. In addition, we provided a comprehensive survey of global transcriptional regulation for AsV and identified stress- and tolerance-associated genes responding to AsV. Genetic loss-of-function analysis of a tolerance-associated gene candidate encoding Leucine-Rich Repeat receptor-like kinase VIII (LRR-RLK VIII) revealed altered AsV sensitivity and the metal accumulation in roots.
    Taken together, these data provide an overview of molecular changes elicited for further investigation and may help better understand to As tolerance-associated genes and the mechanism of arsenic detoxification in plants.

    CONTENTS 論文摘要 I ABSTRACT II ACKNOWLEDGMENTS IV ABBREVIATIONS V CONTENTS VII Chapter 1 General Introduction 1 1.1 Effects of arsenic stress in plants 2 1.2. The role of antioxidants in Arsenic toxicity 3 1.3. The role of ROS and H2O2 -generating enzymes during As-stress in rice root 4 1.4. The roles of Leucine-rich repeat receptor-like protein kinases (LRR-RLKs) 5 1.5 Aims of this study 6 Chapter 2 Materials and Methods 8 2.1 Plant materials, growth and stress conditions 9 2.2 Determination of As content in Arabidopsis 9 2.3 Purification of total RNA 10 2.4 Microarray experiment 10 2.5 Microarray data analyses and organization 11 2.6. Semi-quantitative RT-PCR 12 2.7. Quantitative Real-Time PCR (qRT-PCR) 13 2.8 Measurement of glutathione content 14 2.9 Detection of Hydrogen peroxide by DAB staining 14 2.10 Native gel assay for peroxidase and catalase 14 2.11 Assay of oxalate oxidase 15 2.12 Assay of NADPH oxidase 15 2.13 Assay of α-amylase activity 16 2.14. Histochemical evaluation of Oxalate oxidase activity at the rice root surface 16 2.15 Characterization of Arabidopsis LRR-RLK VIII T-DNA insertion mutants 16 2.16 Gene construction and plant transformation 17 2.17 Histochemical GUS staining 17 Chapter 3 Comparative transcriptome profiling of the early response to arsenite and arsenate stresses reveal differences in the regulation of four Oxalate oxidase genes in rice roots 18 3.1 Abstract 19 3.2 Introduction 20 3.3 Results 24 3.3.1 Effect of arsenic stress on root growth 24 3.3.2 Identification of genes expressed under Arsenic stress in rice roots 24 3.3.3 Confirmation of the microarray by semi quantitative RT-PCR 27 3.3.4 Detection of Hydrogen peroxide in rice roots 27 3.3.5 Isoenzyme profile of peroxidase and catalase 28 3.3.6 Determination of glutathione content 28 3.3.7 Determination of Oxalate oxidase activity 28 3.3.8 Determination of α-amylase activity 29 3.4. Discussion 29 Table 3.1 Gene ontology analysis of up- and down-regulated by AsIII and AsV stresses 38 Table 3.2 The regulation of specific genes to 5μM AsIII and 10 μM AsV in rice roots 39 Table 3.3 The ratio of expression levels of up-regulated genes under AsIII and AsV treatments in rice roots 40 Table 3.4 The ratio of expression levels of up-regulated genes under AsV and AsIII treatments in rice roots 42 Fig. 3.1 Dose-dependent changes in the root length of rice seedlings exposed to AsIII and AsV stresses. 43 Fig. 3.2 Venn diagram illustrates genes with significant change expression in arsenic treated roots. 44 Fig. 3.3 As-induced transcripts encoding proteins involved in transporters (A), transcription factors (B) and kinases (C). 45 Fig. 3.4 The RT-PCR analysis of the transcripts treated with arsenic different concentrations during 24 hours. 46 Fig. 3.5 Determination of ROS of rice roots exposed to As for 24h by DAB staining. 47 Fig 3.6 Activity of catalase (a) and peroxidase (b) in-gel assay of proteins from rice roots under 12 and 24h treatment with 5µM As(III) and 10 µM As(V). 48 Fig 3.7 GSH content of in rice root in control condition or after 12h and 24h exposure to arsenic (5µM AsIII and 10µM AsV). 49 Fig 3.8 Activity of Oxalate oxidase (OXO) in rice root during 12h and 24h exposure to AsIII and AsV. 50 Fig 3.9 Activity of α-amylase in rice root during 12h and 24h exposure to AsIII and AsV. 51 Fig 3.10 Activity of NADPH oxidase in rice root during 12h and 24h exposure to AsIII and AsV. 52 Fig 3.11 Oxalate oxidase activity determined with the histological assay. 53 Chapter 4 Microarray analysis of genes and pathways related to arsenate toxicity and tolerance in Arabidopsis 54 4.1 Abstract 55 4.2 Introduction 56 4.3 Results 57 4.3.1 Effects of AsV stress on root growth in Arabidopsis ecotype Col-0 and Ws-2 57 4.3.2 Accumulation of As contents in roots of Arabidopsis ecotypes upon exposure to AsV 57 4.3.3 Comparison of global expression profiles between Col-0 and Ws-2 roots subjected to AsV 58 4.3.4. Validation of the expression of genes by RT-PCR 61 4.3.5 Functional analysis of putative candidate genes for AsV tolerance in Arabidopsis 61 4.3.6 Analysis structure features and function of pLRR-RLK VIII promoter in Arabiodopsis 63 4.4 Discussions 64 4.5 Conclusion 67 Table 4.1 Comparative expression of genes regulated in 2 Arabidopsis ecotypes with AsV stress 69 Table 4.2 Selection of putative AsV tolerance-associated genes by comparing the expression ratio between the two ecotypes 71 Table 4.3 Protein kinase-related genes in response to AsV stress 73 Table 4.4 Indication of sequence and position of potential cis-elements in the RLK8 promoter 74 Fig. 4.1 Effects of AsV on the root elongation of Arabidopsis ecotypes Col-0 and Ws-2. 75 Fig. 4.2 Accumulation of AsV in Arabidopsis thaliana ecotypes Col-0 and Ws-2. 76 Fig. 4.3 Venn diagram of regulated AsV-responsive genes extracted by comparing microarray probe sets of Arabidopsis thaliana ecotypes Col-0 and Ws-2. 77 Fig 4.4 Microarray expression of genes in Arabidopsis Col-0 and Ws-2 plants exposed to AsV stress. 78 Fig. 4.5 Validate of expression of AsV-induced genes using semi-quantitative RT-PCR. 79 Fig. 4.6 Expression analysis of LRR-RLK VIII genes in Arabidopsis roots in response to heavy metals stress 80 Fig. 4.7 Characterization and functional analysis of Arabidopsis LRR-RLK VIII T-DNA mutants encoding LRR-RLK VIII in response to AsV stress. 81 Fig 4.8 Histochemical analysis of GUS activity in transgenic Arabidopsis seedlings carrying the pPLRR-RLKVIII::GUS fusion after 24 h treatment. 83 References 84 APPENDIXES 104 Supplemental Table S3.1 List of Arsenic-responsive genes 105 Supplemental Table S3.2 The up or down regulated reactive oxidative stress (ROS) genes from rice root treated As(III) and As(V). 127 Supplemental Table S3.3 The up or down regulated Cytochrome P450 (CYP)-related genes from rice root treated As(III) and As(V). 128 Supplemental Table S3.4 The up or down regulated heat shock protein-related genes from rice root treated As(III) and As(V) 129 Supplemental Table S3.5 The up or down regulated UDP-glucuronosyl/UDP - glucosyltransferase-related genes treated As(III) and As(V). 130 Supplemental table S3.6 The up or down regulated transporters -related genes from rice root treated to As(III) and As(V) 131 Supplemental Table S3.7 The up or down regulated transcription factor-related genes from rice root treated to As(III) and As(V) 133 Supplemental Table S3.8 The up or down regulated protein kinases-related genes from rice root treated As(III) and As(V). 134 Supplemental Table S3.9 List of primers for RT-PCR 135 Supplemental Table S3.10 List of primers for qPCR 136 Supplemental Table S3.11 List defense response-related genes from rice root treated As(III) and As(V) 137 Supplemental Figure S3.1 Mapman was used to visual secondary metabolism (A) and sulfate assimilation pathway (B) for up-/down-regulated genes with AsIII and AsV treatments. 138 Supplemental Figure S3.2 Comparison rice root length under AsIII (A) and AsV (B) treatments, and expression level of some As-tolerance related genes (C) between two rice cultivars (IR64 and TN67) 139 CURRICULUM VITAE 140

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