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研究生:何穆妃
研究生(外文):MUFIDAH AFIYANTI
論文名稱:一氧化氮調節乙烯或鹽分逆境誘導的甘薯葉片老化之角色探討
論文名稱(外文):Study the role of nitric oxide in the modulation of ethephon or NaCl-induced leaf senescence in sweet potato
指導教授:陳 顯 榮
指導教授(外文):Hsien-Jung Chen
學位類別:博士
校院名稱:國立中山大學
系所名稱:生物科學系研究所
學門:生命科學學門
學類:生物學類
論文種類:學術論文
論文出版年:2015
畢業學年度:104
語文別:英文
論文頁數:234
中文關鍵詞:一氧化氮穀胱甘肽甘藷鹽分逆境葉片老化乙烯
外文關鍵詞:Leaf senescenceEthyleneSweet potatoGlutathioneNitric oxideNaCl stress
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摘要

葉片老化是葉發育過程最後街終階段且受內生發育信息及外在環境因子影響,包括植物生長調節物乙烯及非生物性鹽分(NaCl)逆境。在甘藷方面的研究,ethephon (是釋出乙烯的化合物) 及NaCl逆境會加速葉片老化,可由一氧化氮(NO)/H2O2/丙二醛(MDA) 合量增加、電解質滲漏(electrolyte leakage)程度上升、老化相關基因表現量增加、葉綠素降解、光合作用效率Fv/Fm降低、及葉片黃化等老化相關標幟變化證實。一氧化氮是氣體自由基分子,在植物生長發育及逆境反應過程扮演信息因子或活性氮族傷害來源的角色。甘藷在ethephon及NaCl逆境誘導的葉片老化過程其外加及內生一氧化氮所扮演的角色並不清楚。
在外加一氧化氮方面的研究,外加一氧化氮供給者SNP可保護對抗ethephon誘導的葉片老化,其機制與過氧化氫酶 (catalase) 及攜鈣素 (calmodulin) 的調控有關,過氧化氫酶 SPCAT1是甘藷葉中主要的同功酵素其活性受鈣及攜鈣素SPCAM調節。外加一氧化氮後1小時於ethephon處理葉片中顯著減少過氧化氫酶SPCAT1及攜鈣素SPCAM的蛋白量及酵素活性,其機制與 (1) peroxynitrite生成 (可能經由一氧化氮與超氧化物 (superoxide) 反應而來) 及(2) S-nitrosoglutathione reductase (GSNOR) 活性上升及GSSG含量增加等有關,導致蛋白質S-nitrosylation、ubiquitination及26S proteasome之降解。當處理1小時後過氧化氫酶活性下降而超氧化物歧化酶 (superoxide dismutase) 活性上升時,會導致處理葉片內H2O2合量顯著增加,並影響ethephon信息傳遞及可誘導基因的表現,這些因子的改變最後導致外加一氧化氮可保護對抗ethephon誘導的葉片老化。
在內生的一氧化氮方面的研究,ethephon處理2小時的葉片會產生內生的一氧化氮波峰,可作為ethephon下游的信息因子導致葉片老化,在添加一氧化氮清除者PTIO下此一氧化氮波峰形成、葉片老化程度、及老化相關標幟變化皆受抑制或延緩,並與穀胱甘肽含量變化、氧化還原平衡、過氧化氫酶及攜鈣素的蛋白量及酵素活性調節、及蛋白質的S-nitrosylation及ubiquitination程度有關。NaCl逆境也會在處理24小時內造成其內生一氧化氮含量增加及累積,並且可以作為NaCl逆境下游的信息因子,顯著促進甘藷葉片老化及老化相關標幟變化,在添加一氧化氮清除者PTIO下此一氧化氮含量、葉片老化程度、及老化相關標幟變化皆受抑制或延緩,過氧化氫酶SPCAT1及攜鈣素SPCAM蛋白量之S-nitrosylation and ubiquitination 與NaCl逆境促進甘藷葉片老化過程可能有關。
根據這些結果結論,一氧化氮可以作為ethephon或NaCl逆境上游或下游之信息因子調節甘藷葉片老化。外加一氧化氮可以利用不同機制抵消ethephon作用保護對抗葉片老化,而內生的一氧化氮可以作為ethephon及NaCl逆境下游信息因子促進葉片老化。
ABSTRACT

Leaf senescence has been recognized as the final stage of leaf development and is affected by developmental cues and environmental stimuli, including plant growth regulators such as ethylene, and abiotic stress such as salt (NaCl) stress. In sweet potato, ethephon, an ethylene releasing compound, and NaCl stress could accelerate leaf senescence as demonstrated by elevation of nitric oxide (NO), H2O2, malondialdehyde (MDA), membrane electrolyte leakage, senescence-associated gene expression, reduction of chlorophyll content, decline of Fv/Fm level and leaf yellowing. NO is a gaseous free radical and plays pivotal roles as a signal molecule and source of reactive nitrogen species (RNS) damage in plant development and stress response. The roles of exogenous NO and endogenous NO in association with ethephon and NaCl-induced leaf senescence were not clear in sweet potato.
For exogenous NO, application of sodium nitroprusside (SNP; an NO donor) could provide protection against ethephon-induced leaf senescence. The mechanism of NO protection involves the regulation of catalase and calmodulin. Catalase SPCAT1 is the major isoform and H2O2 scavenger in sweet potato leaves, and its enzymatic activity is modulated by calcium and calmodulin SPCAM. Exogenous NO drastically reduced calmodulin SPCAM and catalase SPCAT1 protein levels and enzymatic activity starting from 1 h in ethephon-treated leaves via mechanisms associated with (1) generation of peroxynitrite (likely from exogenous NO reacting with superoxide) and (2) elevation of GSNOR activity and GSSG amount, which in turn lead to protein S-nitrosylation, ubiquitination and 26S proteasome degradation. The decreased catalase combined with enhanced superoxide dismutase (SOD) activities resulted in H2O2 increase at 1 h in treated leaves, which in turn repressed the ethephon signal for inducible gene expression. Those alterations in signal redox components finally result in protection against ethepon-induced leaf senescence.
For endogenous NO, it was produced at 2 h in treated leaves and could act as a downstream signal component of ethephon leading to leaf senescence, which was eliminated and mitigated by PTIO (an NO scavenger). Senescence-associated markers as mentioned above were also attenuated and associated with the alteration in glutathione redox balance, modulation of catalase SPCAT1 and calmodulin SPCAM protein levels and enzymatic activity via protein S-nitrosylation and ubiquitination. Senescence in sweet potato leaves was also induced by NaCl stress. Endogenous NO gradually increased and accumulated in NaCl-treated leaves within the first 24 h, and likely acted as a downstream signal component of NaCl stress leading to leaf senescence and changes of senescence-associated markers, which were attenuated in NaCl-treated leaves by PTIO. Modulation of catalase SPCAT1 and calmodulin SPCAM protein S-nitrosylation and ubiquitinations were also involved in NaCl-induced leaf senescence.
Based on these dada, NO can function as a upstream or downstream signal in the modulation of leaf senescence induced by ethephon or NaCl. Exogenous NO can function as an upstream signal to counteract ethephon action with multiple diverse mechanisms, which leads to the protection against leaf senescence. Endogenous NO can be generated and function as a downstream signal of ethephon and NaCl stress, which execute ethephon and NaCl action leading to promotion of leaf senescence.
Table of Content

Dissertation Examination Report………………………………………………….... i
Acknowledgements…………..…………………………………………………ii
Abstract in Chinese…………….………………………………………………iii
Abstract in English………………………………………………………………v
Table of Content………………………………………………………………xvi
Table of Figures……………….………………………………………………….xviii
List of Abbreviations…………………..…………………………………………xxiv
Chapter 1. General background………………….………………………………..1
1.1 Leaf Senescence……………….………………………………………1
1.2 Glutathione-ascorbate cycle as the heart of redox center…………….………1
1.3 Nitric oxide (NO) synthesis involves enzymatic and non-enzymatic process……………………………………………………………..………..….3
1.4 NO reacts with the superoxide of ROS, cysteine thiol group of GSH and protein landing to irreversible and reversible S-nitrosylation…………………4
1.5 GSNO is a natural NO reservoir and its homeostasis is regulated by GSNOR activity………………………………………………….………..…………….6
1.6 NO can act as a ubiquitous signal molecule in cope with plant developmental cues and environmental stress responses………………………………………7
1.7 NO, phytohormone and environmental stress interplay each other to weave a complex regulatory network……………………………………………………8
1.8 NO exhibits antagonistic effects on ethylene biosynthesis action…10
1.9 The possible mechanisms in association with the NO-mediated modulation of leaf senescence caused by ethylene or abiotic stresses…………...11
1.10 Leaf senescence in sweet potato………………………………………13
1.11 Specific aims…………………………….………………….……………15
Chapter 2. Exogenous nitric oxide protects against ethephon-induced leaf senescence in sweet potato………………………………………………………………16
Abstract…………………………………………………………………………..16
2.1 Introduction………………………………………………………………17
Ethylene and leaf senescence in sweet potato……………………………17
Signal components of ethephon-induced leaf senescence in sweet potato………………………………………………………………….…18
NO counteracts ethylene biosynthesis and action………………………….18
The possible mechanisms of NO-mediated protection………….………19
Specific aims……………………………………………………………..20
2.2 Materials and Methods…………………………………………………….21
Plant materials and chemicals……………………………………………21
Natural mature and senescent leaves………………………………………22
Ethephon and dark treatment……………………………………………….22
Effectors/ inhibitor treatments……………………………………………...22
Leaf morphology…………………………………………………………23
Measurement of chlorophyll content……………………………………….23
Measurement of Fv/Fm…………………………………………………..23
Determination of NO amount………………………………………………23
DAB staining……………………………………………………………….24
Determination of H2O2 amount…………………………………………..24
Measurement of MDA content……………………………………………..24
Determination of membrane electrolyte leakage level……………………25
Determination of glutathione content and GSH:GSSG ratio………….25
Total GSNOR activity assay………………………………………………26
In-gel catalase activity assay………………………………………………26
In-gel superoxide dismutase activity assay………………………………27
RT-PCR……………………………………………………………………..27
Immunodetection of S-nitrosylated protein with biotin switch assay……28
Immunodetection of ubiquitinated proteins with Ubiquitinated Protein Enrichment Kit……………………………………………………………28
Western blot hybridization…………………………………………….29
Statistical analysis…………………………………………………………29
2.3 Results…………………………………………………………………….30
Ethephon enhances leaf senescence in sweet potato………………………30
Exogenous NO mitigates ethephon-induced leaf senescence in sweet potato...............................................................................30
Exogenous NO modulates calmodulin, catalase and superoxide dismutase levels in ethephon-treated leaves…………………………………………31
Exogenous NO alters protein S-nitrosylation and ubiquitination levels of calmodulin SPCAM and catalase SPCAT1 in ethephon-treated leaves….32
Exogenous NO alters glutathione content and GSH:GSSG ratio in ethephon-treated leaves……………………………………………………32
Exogenous NO enhances total GSNOR activity in ethephon-treated leaves…………………………………………………………………33
Exogenous NO represses ethephon-inducible gene expression in treated leaves……………………………………………………………………..33
2.4 Discussion…………………..……………………………………………34
A protective role of exogenous NO against ethephon-induced leaf senescence in sweet potato………………………………………………34
Exogenous NO modulates calmodulin, catalase and superoxide dismutase levels in ethephon-treated leaves…………………………………………35
Exogenous NO alters glutathione content and GSH:GSSG ration in ethephon-treated leaf………………………………………………………37
Exogenous NO retained higher GSNOR activity in ethephon-treated leaf……………………………………………………………………….38
Exogenous NO represses ethephon-inducible gene induction….39
Conclusion…………………………………………………………………40
Chapter 3. Catalase activity is modulated by Ca2+ ion and calmodulin in sweet potato leaves…………………………………………………………………………………55
Abstract…………………………………………………………………………….55
3.1 Introduction……………………………………………………………….57
Plant catalase………………………………………………………………57
Catalases play important roles in the modulation of H2O2 homeostasis in cope with developmental cues and environmental stimuli………………58
Catalase activity is modulated with Ca2+ ion and calmodulin..…………….59
Catalases in sweet potato………………………………………………...…60
Specific aims…………………………………………………………..60
3.2 Materials and Methods…………………………………………………….61
Plant materials……………………………………………………………61
Protein structure analysis of plant catalases……………………………..61
Induction, expression, and purification of catalase SPCAT1 and calmodulin SPCAM fusion proteins from E. coli…………………………………...62
Temporal expression of catalase SPCAT1 and calmodulin SPCAM in leaves………………………………………………………………………63
EGTA and CaCl2 treatments………………………………………………64
Boiled and non-boiled treatments………………………………………….64
Treatment of catalase SPCAT1 fusion protein…………………………65
Catalase activity assay……………………………………………………….65
Assay methods…………………………………………………………….66
Statistical analysis………………………………..…………………………67
3.3 Results………………………………………………………………………….67
Sweet potato catalase SPCAT1 contains a putative conserved calmodulin binding domain and peroxisomal targeting signal around C-terminus…………………67
Sweet potato catalase activity is regulated by Ca2+ ions……………………67
Sweet potato catalase SPCAT1 activity is also modulated by calmodulin SPCAM…………………………………………………………………68
Exogenous catalase SPCAT1 fusion protein alleviates ethephon-induced leaf senescence……………………………………………………………………..69
3.4 Discussion…………………………………………………………………69
Sweet potato leaves contain a major catalase isoform………………………...69
Sweet potato major catalase SPCAT1 activity is modulated by its dimer (active) or monomer (inactive) status in cells………………………………………….70
Sweet potato catalase SPCAT1 activity play an important role in the modulation of H2O2 homeostasis and attenuation of ethephon-induced leaf senescence in sweet potato……………………………………………………………………..71
Sweet potato catalase activity is regulated by Ca2+ ions………………..72
Sweet potato catalase SPCAT1 activity is also modulated by calmodulin SPCAM…………………………………………………………………72
Modulation of catalase activity requires intimate association among catalase SPCAT1, calmodulin SPCAM and Ca2+ ion in sweet potato…………………..73
Conclusion…………………………………………………………………75
Chapter 4. catalase SPCAT1, calmodulin SPCAM, GSSG and peroxynitrite participate in exogenous NO protection against ethephon-induced leaf senescence in sweet potato……………………………………………………………………………….82
Abstract……………………………………………………………………………..82
4.1 Introduction………………………………………………………………..84
Ethephon alters morphological, biochemical, and physiological characteristics to promote leaf senescence in sweet potato……………………………………..84
NO modulates diverse molecular, biochemical, and physiological characteristics in plants……………………………………………………………………..86
Specific aims………………………………………………………………..88
4.2 Materials and Methods………………………………………………….89
Plant materials and chemicals…………………………………………………89
Ethephon, NO donor SNP and dark treatments…………………………….90
Effector/inhibitor treatment………………………………………………...90
GSSG treatment……………………………………………………………….92
Assay methods………………………………………………………………..92
Statistical analysis…………………………………………………………….93
4.3 Results………………………………………………………………………93
Exogenous NO rapidly produces an NO peak earlier than the NO peaks generated by ethephon in treated leaves……………………………………93
Exogenous NO represses ethephon-enhanced calmodulin SPCAM and catalase SPCAT1 protein and activity levels starting from 1 h after treatment ………94
26S proteasome and peroxynitrite are likely associated with exogenous NO-mediated repression of calmodulin SPCAM and catalase SPCAT1 protein and activity levels………………………………………………………….95
Peroxynitrite is likely associated with exogenous NO-mediated repression of ethephon-inducible gene expression on day 1 after treatment …….....96
Exogenous NO alters protein S-nitrosylation and ubiquitination levels of calmodulin SPCAM and catalase SPCAT1 at 1 h after treatment in ethephon-treated leaves…………………………………………………….96
Exogenous NO enhances superoxide dismutase activity and H2O2 levels at 1 h after treatment in ethephon-treated leaves ……………………..............97
Exogenous NO enhances GSSG amount and GSNOR activity at 1 h after treatment in ethephon-treated leaves………………………………………....98
Exogenous GSSG provides protection against ethephon-induced leaf senescence………............................................................................................98
4.4 Discussion…………………………………………………………………101
Exogenous NO rapidly produces an NO peak at 30 min, which may function as a signal to protect against ethephon-induced leaf senescence…………101
Exogenous NO-mediated reduction of catalase activity and calmodulin SPCAM/catalase SPCAT1 proteins possibly by modulation of gene expression, 26S proteasome degradation, peroxynitrite, protein ubiquitination and S-nitrosylation level……………………………………………………102
Peroxynitrite may also function as a downstream component of exogenous NO to modulate ethephon-inducible gene expression ………………………...105
Exogenous NO produces elevated H2O2 amount at 1 h after treatment possibly by modulation of catalase and superoxide dismutase activities, and is likely associated with protection against ethephon-mediated leaf senescence…….106
Exogenous GSSG provides protection against ethephon-induced leaf senescence possibly by reduction of calmodulin SPCAM and catalase SPCAT1 protein levels, elevation of intracellular GSSG content and reduction of GSH:GSSG ratio similar to exogenous NO effects…………………….108
A proposed model for exogenous NO protection against ethephon-induced leaf senescence in sweet potato ………………..………………………………….111
Conclusion……………………………………………………………………111
Chapter 5 Nitric oxide acts as a downstream signal component of ethephon to promote leaf senescence in sweet potato…………………………………………134
Abstract…………………………………………………………………………..134
5.1 Introduction……………………………………………………………..136
Nitric oxide as signal in plant response……………………………………136
GSNOR activity modulate NO availability, glutathione content and protein S-nitrosylation and ubiquitination levels……………………………………137
NO and Leaf senescence in sweet potato………………………………139
Specific Aim.…………………………………………………………..140
5.2 Materials and Methods………………………………………………..141
Plant materials and chemicals…………………………………………..141
Ethephon, PTIO and dark treatments …………………………………..142
Effector/inhibitor treatment ………………………………………142
5.3 Results…………………………………………………………………………143
An endogenous NO peak rapidly produced by ethephon at 2 h in treated leaves may come from NOS and NR activities in sweet potato……………………..143
Endogenous NO peak generation positively correlates with ethephon-induced leaf …………………………………………………………………………...144
PTIO attenuates ethephon-mediated reduction of GSH content, GSH:GSSG ratio, and GSNOR activity on day 3 in treated leaves…………………….144
PTIO represses ethephon-inducible gene induction on day 1 in treated leaves………………………………………………………………………145
PTIO alters glutathione content, GSH:GSSG ratio, and GSNOR activity level at 24 h in ethephon-treated leaves…………………………………..145
PTIO attenuates ethephon-mediated reduction of calmodulin SPCAM and catalase SPCAT1 protein levels on day 3 in treated leaves…………….146
PTIO alters S-nitrosylation and ubiquitination levels on catalase SPCAT1 and calmodulin SPCAM ……………………………………………………….146
5.4 Discussion……………………………………………………………….147
Endogenous NO functions as a downstream component of ethephon in induced leaf senescence ……………………………………………………………..147
PTIO attenuates ethephon-mediated reduction of antioxidant activities and delay of leaf senescence ………………………………………………..148
PTIO attenuates ethephon-mediated reduction of GSH content/GSH:GSSG ratio/GSNOR activity and promotion of leaf senescence…………………..150
NO scavenger PTIO mitigates ethephon-inducible gene induction in sweet potato leaves……………………………………………………………..151
NO scavenger PTIO attenuates ethephon-mediated reduction of calmodulin SPCAM and catalase SPCAT1 protein amount possibly by alternation of protein S-nitrosylation and ubiquitination levels ………………………152
A model is proposed for the endogenous NO generation by ethephon in the promotion of leaf senescence in sweet potato ………………………….154
Conclusion…………………………………………………………………154
Chapter 6 NO scavenger PTIO attenuates NaCl-induced leaf senescence in sweet potato……………………………………………………………………….168
Abstract…………………………………………………………………………168
6.1 Introduction……………………………………………………………………170
Leaf senescence………………………………………………………...170
NO and leaf senescence………………………………………………...170
The role of Catalase and calmodulin in stress-induced Leaf senescenc……172
NO and Leaf senescence in sweet potato………………………………172
Specific Aim……………………………………………………………173
6.2 Materials and Methods……………….………………………………………..174
Plant materials and chemicals……………………………………………..174
NaCl and dark treatment………….…………………………………………174
Effector/inhibitor treatment ……………………………………………174
6.3 Results……………………………………………………………………175
NaCl stress promotes leaf senescence in sweet potato ……………………….175
NO scavenger PTIO attenuates NaCl-induced leaf senescence in sweet potato………………………………………………………………………176
NaCl-mediated elevation of endogenous NO may come from nitric oxide synthase and nitrite reductase activities in sweet potato………………..177
PTIO attenuates the reduction of catalase activity, catalase SPCAT1/calmodulin SPCAM protein amounts and S-nitrosylation/ubiquitination levels in NaCl-treated leaves……………………………………………………..……177
6.4 Discussion……………………………………………………………….…….179
NaCl stress promotes leaf senescence in sweet potato……………………179
The endogenous NO generated by NaCl likely functions as a downstream signal component in the promotion of leaf senescence in sweet potato…….180
NaCl alters catalase activity and calmodulin SPCAM/catalase SPCAT1 protein levels during treatment in sweet potato……………………………………181
NaCl-enhanced catalase activity and calmodulin SPCAM/catalase SPCAT1 protein levels on day 3 are temporarily attenuated by NO scavenger PTIO in sweet potato…………………………………………………………………182
NaCl-mediated reduction of catalase activity and catalase SPCAT1/calmodulin SPCAM protein levels on day 9 are attenuated by NO scavenger PTIO in sweet potato…………………………………………………………………184
Conclusion...……………………………….…………………...……………185
References………………………………………………………..………………198
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