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研究生:涂晉維
研究生(外文):Chin-Wei Tu
論文名稱:菸草Argonaute 5介導之抗病毒防禦與植物病毒的反防禦
論文名稱(外文):Argonaute 5-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana
指導教授:胡仲祺徐堯煇
指導教授(外文):Chung-Chi HuYau-Heiu Hsu
口試委員:林納生蔡慶修葉信宏
口試委員(外文):Na-Sheng LinChing-Hsiu TsaiHsin-Hung Yeh
口試日期:2023-10-03
學位類別:博士
校院名稱:國立中興大學
系所名稱:微生物基因體學博士學位學程
學門:生命科學學門
學類:生物訊息學類
論文種類:學術論文
論文出版年:2023
畢業學年度:112
語文別:英文
論文頁數:118
中文關鍵詞:AGO5基因靜默植物抗病毒防禦病毒RNA 沉默抑制因子26S蛋白酶體自噬作用miRNA
外文關鍵詞:AGO5RNA silencingPlant antiviral defenseViral suppressors of RNA silencing (VSR)26S proteasomeAutophagymiRNA
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Argonaute (AGO)蛋白家族是植物抗病毒RNA沉默機制中的重要成員,植物會通過招募特定的AGO蛋白來維護抵禦病毒入侵,以啟動不同的抗病毒機制。我們之前的研究結果發現本氏菸草(Nicotiana benthamiana)會對竹嵌紋病毒(bamboo mosaic virus, BaMV)的感染作出反應,導致NbAGO5基因表達顯著上調。然而,NbAGO5在抗病毒機制中的作用機制仍然不清楚。因此,本論文主要探討NbAGO5如何參與以及調控植物的防禦系統,以防治病毒的入侵,以及植物病毒如何對抗NbAGO5的防禦,以利在植物中存活。
在第一章節裡,我們觀察到菸草感染BaMV、馬鈴薯X病毒(potato virus X , PVX)、菸草鑲嵌病毒(tobacco mosaic virus, TMV)或胡瓜嵌紋病毒(cucumber mosaic virus, CMV)後,NbAGO5蛋白質累積量明顯增加。為了解NbAGO5的抗病毒機制和調控功能,我們建立過度表達NbAGO5(OE-NbAGO5)和缺失NbAGO5 (nbago5)的轉基因菸草。我們的研究結果顯示,OE-NbAGO5對BaMV、PVX、TMV和缺乏2b基因的突變型CMV具有防禦作用,但對野生型CMV和蕪菁嵌紋病毒(turnip mosaic virus, TuMV)無效。結合免疫沉澱技術和小分子RNA北方墨點法,我們證明NbAGO5通過結合病毒小干擾RNA(vsiRNAs)發揮其抗病毒功能。進一步研究結果發現CMV 2b和TuMV HC-Pro會結合NbAGO5,並通過26S蛋白酶體和自噬途徑降解NbAGO5,使這些病毒能夠克服NbAGO5調控的防禦。另外,TuMV HC-Pro亦會抑制vsiRNA與NbAGO5的結合,提供了另一條反制防禦的途徑。
雖然在第一章節裡,NbAGO5 蛋白與 vsiRNA 結合以進行抗病毒防禦的能力已得到證實;然而對於NbAGO5是否也會結合植物miRNAs,以調節基因表達並參與植物與病毒的相互作用,仍然不清楚。第二章節描述了我們利用免疫沉澱技術結合小分子RNA定序,識別出miR159、miR395、miR397、miR398和miR5303會參與NbAGO5的複合體中,也進一步利用小RNA北方墨點法確認了這些miRNAs。NbAGO5 的過表達反而導致這些 miRNAs 的目標基因表達增加,說明相對於基因沉默機制,NbAGO5 反而增強了基因表現。 我們進一步發現,過表達NbAGO5 會導致miR159的目標基因 GAMYB 累積,進而上調 PR 家族基因並正調控 NbAGO5 基因的表現循環。這些研究揭示了NbAGO5在植物對病毒侵入後的反應與miRNAs互動方面的重要意義,將為抗病毒策略的開發提供新的見解。
Argonaute proteins serve as essential elements of the antiviral RNA silencing pathway in plants, offering protection from viral threats by recruiting specific AGO proteins for distinct antiviral mechanisms. Our previous study highlighted the significant upregulation of Nicotiana benthamiana AGO5 (NbAGO5) expression in response to bamboo mosaic virus (BaMV) infection. However, the precise function of NbAGO5 within the antiviral framework remains to be elucidated. In this study, we explored the role of NbAGO5 in the plant defense system and examined how plant viruses counteract the defense mechanism of NbAGO5 to ensure their survival within plants.
In chapter one, we observed that upon infection with BaMV, potato virus X (PVX), tobacco mosaic virus (TMV), or cucumber mosaic virus (CMV), the accumulation levels of NbAGO5 protein were induced. To unravel the antiviral mechanism and regulatory functions of NbAGO5, we generated NbAGO5 overexpression (OE-NbAGO5) and knockout (nbago5) transgenic N. benthamiana lines. Our findings demonstrate that NbAGO5 confers defense against BaMV, PVX, TMV, and a mutant CMV lacking the 2b but not against wild-type CMV and turnip mosaic virus (TuMV). Affinity purification and small RNA northern blotting revealed that NbAGO5 exerts its antiviral function by binding to viral small interfering RNAs (vsiRNAs). Furthermore, we observed that CMV 2b and TuMV HC-Pro interact with NbAGO5, leading to its degradation via the 26S proteasome and autophagy pathways, enabling these viruses to overcome NbAGO5-mediated defense. Additionally, TuMV HC-Pro interferes with vsiRNA binding by NbAGO5, providing an additional line of counter-defense.
The binding ability of NbAGO5 protein to vsiRNAs for antiviral defense is well-established in chapter one; however, the potential interaction of NbAGO5 with plant miRNAs and its role in gene regulation and plant-virus interplay was not yet clear. In chapter two, we identified the interactions between NbAGO5 and miRNAs, including miR159, miR395, miR397, miR398, and miR5303, by using immunoprecipitation and sRNA-seq, and confirmed these interactions via sRNA northern blot analysis. Overexpression of NbAGO5 led to increased expression of target genes of these miRNAs, indicating the role of NbAGO5 in enhancing gene expression. We further demonstrated that elevated NbAGO5 levels resulted in GAMYB accumulation, which in turn upregulated PR family genes and established a positive feedback loop for NbAGO5 expression. Our research unveils insights into the intricate interplay between NbAGO5 and plant viruses, shedding light on the substantial importance of NbAGO5 in mediating plant-virus responses through interactions with miRNAs and providing valuable insights into the antiviral RNA silencing mechanism.
摘要 i
Abstract iii
Content v
Figures viii
Table ix

Chapter I
Argonaute 5 and vsiRNAs-mediated antiviral defense and viral counter-defense in Nicotiana benthamiana 1
Abstract 2
Introduction 3
RNA silencing 3
Antiviral RNA silencing 4
Viral suppressors of RNA silencing (VSRs) 5
Argonaute (AGO) 6
Argonaute 5 (AGO5) 8
Materials and methods 10
Plant materials and growth conditions 10
Construction of infectious clones for TuMV and CMV-2bm and transient overexpression clones for CMV 2b and TuMV HC-Pro 10
Agroinfiltration for virus inoculation and transient overexpression 11
Construction of clones for overexpressing or knocking out NbAGO5 and plant transformation 12
Reverse transcription and Real-Time Quantitative PCR (RT-qPCR) 13
Protein extraction and western blot analysis 14
Immunoprecipitation 14
vsiRNAs analysis by sRNA northern blot 15
small RNA-seq 16
MG132 and 3-MA inhibitor treatment 16
Results 18
Accumulation of NbAGO5 protein in response to infections of different plant viruses in N. benthamiana 18
Generation and characterization of NbAGO5-overexpressing (OE-NbAGO5) and NbAGO5-knockout (nbago5) N. benthamiana plants for studying the antiviral function of NbAGO5 19
Investigation of the antiviral role of NbAGO5 in N. benthamiana plants against BaMV, PVX, TMV, CMV, and TuMV 20
The role of NbAGO5 in antiviral silencing through binding to virus-derived small RNAs (vsiRNAs) 22
Mapping the genome, coverage, and hotspots of BaMV vsiRNAs within NbAGO5-containing complexes 23
CMV 2b protein interferes with the stability of NbAGO5 and inhibits its antiviral function in systemic leaves 24
The involvement of 2b or HC-Pro in the degradation of NbAGO5 protein via the 26S proteasome and autophagy pathways 25
Discussion 29
Functional diversification of AGO5 in regulating plant physiology across species 29
The induction of AGO5 expression as a common response to viral infections in plants 31
Diverse mechanisms and functions of antiviral AGOs in plant defense 33
The role of NbAGO5 in antiviral defense in N. benthamiana 34
Plant viruses develop VSRs and utilize the ubiquitin-proteasome system (UPS) and autophagy to counteract RNA silencing factors 35
References 38
Chapter II
Argonaute 5 and miRNA-mediated cross-talk during plant-virus interactions in Nicotiana benthamiana 54
Abstract 55
Introduction 56
Materials and methods 58
Plant materials and growth conditions 58
Immunoprecipitation 58
small RNA-seq 59
miRNAs analysis by sRNA northern blot 59
Reverse transcription and Real-Time Quantitative PCR (RT-qPCR) 60
Results 61
Identification of NbAGO5 bound miRNAs in BaMV infected OE-NbAGO5 plants 61
Exploring the regulatory pathways of NbAGO5 in modulating gene expression: insights from miRNA interaction and transcription factor involvement 62
Discussion 65
The role of NbAGO5-miRNA interaction in plant-virus interactions: insights into antiviral defense and regulatory mechanisms 65
AGOs in plant-virus interactions: sequestration of miRNAs and potential degradation via SDN1 67
Interplay of salicylic acid-mediated resistance and RNA silencing in plant defense against pathogens 68
The dual regulatory role of NbAGO5 in plant antiviral defense: vsiRNA-mediated cleavage and miRNA sequestration 70
Reference 72
Publication 104
Chapter І
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Chapter ІI
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