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研究生：	林忠逸 Lin, Chung-Yi
論文名稱：	全面性分析植物根部遭受金屬逆境時轉錄體表現之研究 Global transcriptome profiles of plant roots exposed to metal stress
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：	2013
畢業學年度：	101
語文別：	英文
論文頁數：	109
中文關鍵詞：	阿拉伯芥、鎘、銅、微陣列分析、水稻、根毛、訊息傳遞、轉錄體、釩、囊泡運送
外文關鍵詞：	arabidopsis, cadmium, copper, microarray, rice, root hair, signaling pathway, transcriptome, vanadium, vesicle trafficking transport
相關次數：	點閱：248 下載：3
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植物生長環境中無論是遭遇長期低濃度或是大量高濃度重金屬或類金屬汙染時，經常性的會引發植物為適應生存而導致的形態改變。即使有些汙染的金屬對植物而言是屬於必需元素，植物體仍須改變其內部基因的表現以求達到具有適應金屬逆境的生理環境。然而，對於植物早期遭受到重金屬或是類金屬環境時所表現的訊息調控及細胞內的生理機制仍尚未有明顯的瞭解。因此此論文的研究目的是利用詳細且大規模分析基因體的方式，探討水稻與阿拉伯芥根部基因表現與遭逢金屬逆境時彼此間的相互關聯與反應，以求得知植體內基因彼此之間表現出的訊息途徑與可能的機制。
當植物遭受重金屬或是類金屬逆境時常具有一些共同的逆境反應。不同金屬逆境間相似的形態改變反應出早期逆境時所發生的普遍存在的分子機制過程，如活性氧的產生或是植體內離子平衡的改變。本實驗利用微陣列(microarray)技術比較了水稻根部在遭受銅(5 µM)、鎘(25 µM)與釩(1000 µM)逆境時轉錄體基因的表現情形。結果顯示出水稻根部在遭受銅逆境時會改變細胞內囊泡運送基因的表現，並且脂肪酸代謝及細胞成份的生合成亦會受到影響。鎘處理主要是改變未折疊蛋白質的結合與硫同化作用相關基因的表現。而在釩所誘導的特殊轉錄體方面，較具顯著的則為NAC轉錄因子、類受體細胞質激酶VII (RLCK-VII)及多白胺酸性磷酸激酶VIII (LRR-VIII)等相關基因的改變。此外，基因表現情形中也顯示出銅與釩處理時會誘導茉莉酸(JA)生合成相關基因的表現，但生長素(Auxin)與離層酸(ABA)的生合成及所調控的訊息基因則以釩處理的水稻根部較為顯著。
我們也發現以低濃度釩(25 µM)浸泡阿拉伯芥根部後發現會促使根尖部位根毛顯著變多並增加根毛的長度。為瞭解此現象是否受釩誘導的活性氧所調控，我們利用阿拉伯芥NADPH氧化酶突變株(rhd2/AtrbohC)以及NADPH氧化酶抑制劑diphenyleneiodonium chloride (DPI)，證明釩誘導的活性氧參與此調控途徑。並且經由阿拉伯芥突變株的分析，我們也瞭解乙烯受器(ETR1)與轉錄因子ROOT HAIR DEFECTIVE 6 (RHD6)與釩誘導根毛形成息息相關。透過阿拉伯芥微陣列實驗分析發現微量釩會促使細胞壁形成，活性氧活性和訊息傳遞相關基因的改變。
我的結果說明了水稻與阿拉伯芥根部形態上及訊息傳遞的反應是與金屬逆境具有相關性。此外，此研究更提供了我們新的知識，對於植物早期發生金屬逆境時的生理與分子層次具有更深一步的瞭解。

Plants exposed to low, chronic or high, acute concentrations of heavy metal or metalloid can cause a broad range of morphogenic responses. Gene expression networks regulate suitable plasticity to adapt to metal stress even though some of them are considered essential metal for higher plants. However, signaling pathways and cellular mechanisms in the early stage response of the plant seedlings to heavy metal or metalloid are poorly understood. The aim of this study set out to investigate the possible signal networks and possible mechanisms using genome-wide assays at high spatiotemporal resolution to understand the processes that link gene expression and stress in the rice and Arabidopsis root.
Common stress responses appear to exist between metal and metalloid. It is hypothesized that the similarities in the morphogenic responses induced by distinct metal stresses, reflect common molecular processes such as increased ROS production and altered ion homeostasis at the early stage. Comparison of the rice transcriptome expression between Cu (5 µM)-, Cd- (25 µM) and V (1000 µM)-array revealed that Cu specifically altered levels of genes involved in vesicle trafficking transport, fatty acid metabolism and cellular component biogenesis. Cd-regulated genes related to unfolded protein binding and sulfate assimilation. Among the V-specific responsive transcriptomes, the most predominant expressions were NAC (NAM, ATAF, CUC) transcription factor, receptor-like cytoplasmic kinase VII (RLCK-VII) and leucine-rich repeat kinase VIII (LRR-VIII). Furthermore, gene expression profiling revealed that jasmonic acid (JA) biosynthesis related genes were enriched by Cu and V treatment, but signaling and biosynthesis of auxin and abscisicacid (ABA) were significant in V-treated rice roots.
In addition, during mild V treatment (25 µM), the Arabidopsis roots showed significantly increased Arabidopsis root hair density and length. A possible role of NADPH oxidase in V-induced alteration of root system architecture was examined by using NADPH oxidase mutant (rhd2/AtrbohC) and diphenyleneiodonium chloride (DPI), an inhibitor of NADPH oxidase. Ethylene receptor (ETR1) and RHD6 were also found to participate in inducing root hair formation. Exposure to V triggered changes in transcript levels of genes related to cell-wall formation, ROS activity, and signalling.
These results reveal linkages between metal stress and morphogenic responses in rice and Arabidopsis root, and provide new insights into understanding the molecular basis of the early metal stress response in plants.

中文摘要 I

Abstract III

Acknowledgements V

Abbreviations VI

CHAPTER 1: General Introduction 1
1.1 General responses to metal stress 2
1.2 Signals that mediate metal-induced morphogenic response4
1.3 Aims of this study 5

CHAPTER 2: Materials and Methods 7
2.1 Plant materials and heavy metal treatments 8
2.2 Root length determination 9
2.3 Detection of Reactive oxygen species in roots 9
2.4 Histochemical staining for lipid peroxidation 10
2.5 cyc1At::GUS staining 11
2.6 2, 3, 5-triphenyl-2H-tetrazolium chloride (TTC) assay 11
2.7 Inhibitor treatments 11
2.8 Purification of total RNA 12
2.9 Microarray preparation and data analysis 13
2.10 MapMan display 15
2.11 Semi-quantitative RT-PCR 15
2.12 Statistical analyses 16


CHAPTER 3: Comparison of Early Transcriptome Responses to Copper and Cadmium in Rice Roots 17
3.1 Abstract 18
3.2 Introduction 19
3.3 Results
3.3.1 Effect of metal stress on root growth of rice seedling 23
3.3.2 Genes that were commonly regulated by exposure to Cu and Cd in rice roots 23
3.3.3 Gene expression specifically in response to Cu and Cd 24
3.3.4 Comparison of Cu and Cd responses using MapMan 24
3.4 Discussion 26

List of tables and figures
Table 3.1 Gene ontology analysis of 568 genes commonly regulated by Cu and Cd in rice 32
Table 3.2 Gene ontology/pathway terms for selected genes regulated ≥ 2-fold with 5 μM Cu and 25 μM Cd in rice roots 33
Table 3.3 Expression profiles of glutathione S-transferase-related genes with Cu and Cd treatment in rice roots 34
Table 3.4 Expression ratios for selected heat-shock protein and heat-shock factors significantly regulated with Cu and Cd stress in rice roots 35
Table 3.5 Vesicle-trafficking-related genes with changed expression with Cu and Cd treatment in rice roots 36
Table 3.6 Putative transporters involved in homeostasis of Cu and Cd stress in rice root 37
Table 3.7 Expression profiles of jasmonic-acid-related genes with Cu and Cd treatment in rice roots 38
Fig. 3.1 Root growth of rice seedlings with (a) Cu and (b) Cd treatment 39
Fig. 3.2 Transcription profiles of rice roots with 5 μM Cu and 25 μM Cd treatment by Venn diagram 40
Fig. 3.3 MapMan analysis of genes involved in (a) flavonoid metabolism and (b) transport, (c) large enzymes, and genes involved in (d) sulfate assimilation 41
Fig. 3.4 ROS production and lipid peroxidation detected in rice roots during Cu and Cd treatment 42
Fig. 3.5 Schematic representations of 2 different regulation pathways with Cu and Cd stress in rice roots 43

CHAPTER 4: Transcriptome analysis of phytohormone, transporters and signaling pathways in response to vanadium stress in rice roots 44
4.1 Abstract 45
4.2 Introduction 46
4.3 Results
4.3.1 Rice response to V 48
4.3.2 Global expression profiles of rice root in response to V 48
4.3.3 ROS-related genes induced by V 48
4.3.4 Hormone-signaling genes regulated by V 48
4.3.5 Transporter genes regulated by V 49
4.3.6 Transcription regulation and signal transduction under vanadium stress 49
4.3.7 Semi-quantitative RT-PCR analysis of selected genes 49
4.4 Discussion 51

List of tables and figures
Table 4.1 Gene ontology analysis of biological processes and molecular functions of genes among 1,087 with expression upgregulated in response to vanadium 55
Table 4.2 Vanadium-responsive transcripts related to oxidative stress response and hormones 56
Table 4.3 Expression of oxidative stress- and hormone-related genes in response to vanadium stress in rice root 57
Table 4.4 Vanadium-responsive transcripts related to transporters. aFC (log2): log2-fold change 58
Fig. 4.1 The effect of vanadium (V) on rice root growth. (A) 6-day-old rice seedlings were treated with different concentrations of V for 3 days, and root length was measured 60
Fig. 4.2 MapMan analysis of genes involved in transport 61
Fig. 4.3 (A) Transcription factor and (B) IRAK families responding to V stress 62
Fig. 4.4 Semi-quantitative RT-PCR analysis of the mRNA levels of candidate transcripts induced by metal stress 63
Fig. 4.5 (A) Upregulated- and (B) downregulated- transporter families responding to V stress 65
Fig. 4.6 Comparison of (A) transporter, (B) transcription factor and (C) interleukin-1 receptor-associated kinase (IRAK) kinase families among genes upregulated specifically with vanadium and heavy metals 66

CHAPTER 5: Pathways involved in vanadium-induced root hair formation in Arabidopsis 68
5.1 Abstract 69
5.2 Introduction 70
5.3 Results
5.3.1 Specificity of root hair formation response to V exposure 73
5.3.2 Reactive oxygen species (ROS) production increased in V-treated roots 73
5.3.3 Role of NADPH oxidase in V-induced root hair elongation 73
5.3.4 V-induced root hair formation in mutant backgrounds 74
5.3.5 The mechanism of V-induced root hair formation 74
5.3.6 Identification of genes with changed expression on exposure to V 75
5.4 Discussion 76

List of tables and figures
Table 5.1 Regulated transcripts in Arabidopsis roots treated with 25 µM V 80
Table 5.2 Groups of functionally root hair related genes that are differentially regulated in response to V exposure 81
Fig. 5.1 Promotion of Arabidopsis root hair formation by vanadium 82
Fig. 5.2 Changes in root length and root hair number of Arabidopsis rice after vanadium supply 83
Fig. 5.3 Cell viability and cell division in Arabidopsis root tips 84
Fig. 5.4 Effect of V on ROS accumulation in the roots of Arabidopsis 85
Fig. 5.5 Effect of NADPH oxidase on vanadium-induced root hair formation in Arabidopsis seedlings 86
Fig. 5.6 Effect of vanadium on root hair development of hormone mutant seedlings 87
Fig. 5.7 Effects of various signal transduction-inhibitors on V-induced root hair formation in Arabidopsis 88
Fig. 5.8 Expression analysis of the root hair cell specification genes, GLABRA2 (GL2) and WEREWOLF (WER), in roots from V-treated plants by RT-PCR 89

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