臺灣博碩士論文加值系統

病原菌藉由分泌致病蛋白分子注入到植物細胞中造成植物感病，這往往造成農作物的產量下降。因此瞭解植物與病原菌相互作用機制有助於提高農作物的防禦能力。本論文主要探討十字花科黑腐病和植物菌質體病原菌的致病蛋白分子如何參與調控植物的防禦機制。
第一部分，XopDXcc8004是十字花科黑腐病的致病蛋白分子之一，且具有SUMO protease酵素活性。利用β-estrodiol誘導XVE::XopDXcc8004轉殖株表現XopDXcc8004，可以發現此株會呈現胚軸延長的白化苗和其葉面有局部壞死的外表型，利用qRT-PCR分析下，此株生物逆境基因的表現量如PR1、PR2和PR5等明顯的增加，且可以抑制Xcc8004的繁殖。此外，XopDXcc8004可以和光訊息傳導路徑的轉錄因子HFR1進行交互作用，且可以將HFR1進行desumoylation，推測HFR1也參與調控植物的防禦反應。因此利用hfr1突變株進行探討，藉由植物荷爾蒙水楊酸處理後，發現hfr1突變株的生物逆境基因表現量比野生型明顯增加，且在接種Xcc8004實驗中，在hfr1突變株所偵測到Xcc8004繁殖量比野生型植株少，此結果說明HFR1也參與調控植物的防禦系統，且扮演著負調控因子。本篇研究雖然沒有直接的證據說明XopDXcc8004可以在植物細胞中和HFR1進行交互作用，但依本研究的實驗結果可以瞭解到，HFR1除了參與植物光訊息傳遞路徑外，同時在植物的防禦反應傳導路徑中也扮演著重要的調控因子，且可以被XopDXcc8004所修飾。此外，也進一步證實植物的光訊息傳遞路徑和防禦機制之間是具有crosstalk現象。
第二部分，植物菌質體的傳播媒介主要以吸食性昆蟲如葉蟬和飛蝨等為主。其所分泌致病性蛋白SAP11可以抑制植物的茉莉酸的合成，增加吸食性昆蟲取食和產卵，提高植物菌質體的傳播。利用菸草(Nicotiana benthamiana)建立35S::SAP11CaPM轉植株，發現此轉殖株缺乏野生型菸草特有的氣味。與野生型菸草進行比對，35S::SAP11CaPM轉殖菸草中的揮發性化合物IBMP (2-isobuty-3-methoxypyrazine)明顯降低，而且葉子表面的茸毛(Trichomes)數量比野生型少許多。利用即時定量聚合酶鏈鎖反應(qRT-PCR)進行分析，發現35S::SAP11CaPM轉植菸草中的NbOMT1明顯減少。進一步分析NbOMT1蛋白酵素活性反應，發現NbOMT1可以藉由S-adenosyl-L-methionine (SAM)提供甲基團，將IBHP進行甲基化形成IBMP。由於已知IBMP可作為瓢蟲費洛蒙，能吸引瓢蟲聚集，因此利用野生型和35S::SAP11CaPM轉植菸草進行吸引瓢蟲動向實驗，結果發現野生型菸草更具吸引瓢蟲的能力。已知，植物菌質體可藉由半翅目昆蟲作為傳播和繁殖媒介，而瓢蟲為半翅目昆蟲的天敵，因此推測植物菌質體利用致病蛋白分子SAP11CaPM降低菸草中的IBMP是為了減少瓢蟲來到其感染的植物中取食其傳播媒介如葉蟬等，進而增加植物菌質體的傳播。

Phytopathogens cause a variety of diseases in economically important crops and lead to major losses of yields. The virulence of phytopathogens mainly depend on their effector proteins which are translocated or secreted into host cells in order to suppress plant immune responses. Therefore, understanding the mechanism of plant-pathogen interactions will be helpful to develop better strategies to against plant diseases. In this dissertation, the virulence functions of Xanthomonas XopD (part I) and phytoplasma SAP11 (part II) effectors will be characterized, and their roles in plant-pathogen interaction will be discussed.
Part I: XopDXcc8004 is a type III effector of Xanthomonas campestris pv. campestris (Xcc) 8004, which has been shown to possess a SUMO protease activity. Here, transgenic approach combined with inducible promoter was carried out to analyze the effects of XopDXcc8004 in plant immunity. The long hypocotyl and lesion-mimic phenotypes were observed in XVE::XopDXcc8004 transgenic Arabidopsis after treating with β-estradiol. XopDXcc8004 elicited the accumulation of host defense-response genes such as PR1, PR2 and PR5, that suppressed the growth of Xcc8004. Moreover, XopDXcc8004 was able to interact with HFR1, a basic helix-loop-helix transcription factor involved in photomorphogenesis, and desumoylated the sumoylated HFR1 through SUMO protease activity. Interestingly, the increased expression of host defense-response genes and displayed a resistance phenotype to Xcc8004 were observed in hfr1-201 mutant. These results suggest that HFR1 is potentially regulated by XopDXcc8004, and acts as a negative regulator in plant immunity. These findings not only indicate that HFR1 is required for the fine-tuning of plant immune responses, but also contribute to our knowledge of the crosstalk between light signaling pathway and immune response.
Part II: SAP11 is a secreted effector of phytoplasma, which has been shown to suppress JA synthesis and increase the proliferation of their insect vectors. In this study, Nicotiana benthamiana expressing SAP11 from Candidatus Phytoplasma mali (CaPM) was carried out. Interestingly, a dramatic reduction of tobacco odors was observed in 35S::SAP11CaPM transgenic tobacco. This altered aroma phenotype was correlated with the modification of glandular trichomes and the suppression of biosynthesis of a volatile organic compound 3-isobutyl-2-methoxypyrazine (IBMP). Furthermore, the absence of expression of NbOMT1 was found to be responsible for the loss of accumulation of IBMP in SAP11CaPM-transgenic plants. Enzyme activity characterizations demonstrated that NbOMT1 possesses an O-methyltransferase activity and is able to methylate IBHP and leads to the production of IBMP in the presence of SAM. Given the importance of IBMP as an aggregation pheromone between ladybird beetles, we showed that SAP11-transgenic plants loss the ability to attract ladybird beetles, Oenopia sauzeti and Lemnia biplagiata. Because ladybird beetles are one of the natural enemies of psyllids, we propose that psyllids, the insect vectors of phytoplasmas, may take advantage of a reduction in predators’ attacks and increase their fitness on phytoplasma-infected plants. Here, our study provides valuable insights into the molecular communication between plants and the associated community members in an ecological relevant context.

誌謝................................................... i
摘要................................................... ii
Abstract............................................... iv
Content................................................ vi

Chapter Ⅰ............................................. 1
Introduction........................................... 2
Plant Immune System.................................... 2
Hormones in the Plant Immune System.................... 3
Pathogenicity of Xanthomonas........................... 4
Pathogenicity of Phytoplasma........................... 5
References............................................. 8

Chapter Ⅱ............................................. 14
Arabidopsis HFR1 Is a Potential Nuclear Substrate Regulated by the Xanthomonas Type III Effector XopDXcc8004.......... 14
Abstract............................................... 15
Introduction........................................... 16
Materials and Methods.................................. 18
Plant materials and growth conditions.................. 18
Plasmid constructions.................................. 18
Arabidopsis transformations............................ 19
Trypan blue staining................................... 19
Quantitative reverse transcription-polymerase chain reaction (qRT-PCR).............................................. 19
Recombinant protein purifications and antibody production ........................................................19
Bacterial strains and inoculations..................... 20
Yeast two-hybrid assays................................ 20
Subcellular localization assays........................ 21
In vitro pull-down assays.............................. 21
In vitro sumoylation assays............................ 21
Primers................................................ 22
Results................................................ 23
Expression of XopDXcc8004 elicits a SA-mediated defense response in Arabidopsis................................ 23
Suppression of Xcc8004 growth by XopDXcc8004........... 24
XopDXcc8004-eliciting defense responses are mainly dependent on the SUMO protease activity............................. 24
XopDXcc8004 interacts with Arabidopsis HFR1............ 25
K72 in HFR1 is desumoylated by XopDXcc8004 in vitro.... 26
hfr1-201 increases resistance to Xcc8004............... 26
Discussion............................................. 28
References............................................. 30
Figure Legends......................................... 35
Figure 1 Salicylic acid-dependent defense responses were elicited by the expression of XopDXcc8004 in Arabidopsis.. ........................................................35
Figure 2 XopDXcc8004 suppresses the virulence of the Xcc8004 ........................................................36
Figure 3 XopDXcc8004(C355A) loses the activity for activating plant immunity......................................... 37
Figure 4 Expression of XopDXcc8004 induces a long hypocotyl phenotype in Arabidopsis............................... 38
Figure 5 hfr1-201 increases plant immunity against Xcc8004 spp.................................................... 39
Table 1 Primer sequences for plasmid constructions and qRT-PCR.................................................... 40
Appendixes............................................. 41
Figure A1 XopDXcc8004 interacts with HFR1............ 41
Figure A2 K72 in HFR1 is desumoylated by XopDXcc8004 in vitro ........................................................42
Table A1 Annotation of the differentially expressed genes (p < 0.001) involved in plant defense responses...........43

Chapter Ⅲ............................................. 44
Suppression of Biosynthesis of IBMP, a Volatile Compound Required for Aggregation of Ladybird Beetles, by Phytoplasma Effector SAP11CaPM..................................... 44
Abstract............................................... 45
Introduction........................................... 46
Materials and Methods.................................. 49
Plant materials and growth conditions.................. 49
Plasmid constructions.................................. 49
Generation of transgenic plants........................ 49
qRT-PCR................................................ 49
ddPCR.................................................. 50
Co-expression assays................................... 50
HS-SPME/GC-MS analyses................................. 50
In vitro O-methylation assays.......................... 51
Cryo-SEM............................................... 51
Phylogenetic analysis.................................. 52
VIGS (Virus-induced gene silencing) assays............. 52
Y-tube olfactometer assays............................. 52
Results................................................ 53
Expression of the phytoplasma SAP11CaPM causes morphological changes and attenuates the JA response pathway in N. benthamiana............................................ 53
Expression of the phytoplasma SAP11CaPM suppresses the accumulation of IBMP in N. benthamiana................. 53
Expression of the phytoplasma SAP11CaPM alters the phenotypes of glandular trichomes and blocks the expression of NbOMT1 in N. benthamiana......................................... 54
Down-regulation of NbOMT1 represses the biosynthesis of IBMP in N. benthamiana......................................... 56
NbOMT1 catalyzes the formation of IBMP in vivo and in vitro. ........................................................56
Functional similarities between SAP11CaPM and SAP11AYWB. ........................................................57
Behavioral responses of ladybird beetles to the SAP11CaPM-overexpressing N. benthamiana.......................... 58
Discussion............................................. 59
References............................................. 63
Figure Legends......................................... 72
Figure 1 Investigation of growth phenotypes altered by SAP11CaPM in N. benthamiana............................ 72
Figure 2 SAP11CaPM destabilizes class II TCPs and alters the transcript levels of the genes involved in the JA response pathway in N. benthamiana.............................. 73
Figure 3 Investigation of growth phenotypes and JA responses altered by SAP11CaPM in Arabidopsis.................... 74
Figure 4 GC-MS analysis of VOCs altered by SAP11CaPM in N. benthamiana............................................ 75
Figure 5 Investigation of IBMP production in WT and SAP11CaPM-transgenic Arabidopsis....................... 76
Figure 6 Comparison of transcript levels of potential genes required for the storage or biosynthesis of IBMP in leaves of WT and SAP11CaPM-transgenic N. benthamiana............. 77
Figure 7 Precise measurements of the transcript levels of genes in N. benthamiana by ddPCR....................... 78
Figure 8 Silencing of NbOMT1 by VIGS represses the production of IBMP in N. benthamiana.............................. 79
Figure 9 Examination of the activity of recombinant NbOMT1 in IBMP production ........................................ 80
Figure 10 NbOMT1 possesses the ability to catalyze the O-methylation of IBHP in E. coli and in vitro............ 81
Figure 11 SAP11AYWB alters leaf morphology and suppresses IBMP accumulation in N. benthamiana.................... 82
Figure 12 Investigation of behavioral responses of ladybird beetles altered by SAP11CaPM in N. benthamiana......... 83
Table1 Primer sequences for plasmid constructions, qRT-PCR, and ddPCR.............................................. 84
Appendixes............................................. 85
Figure A1 Comparison of trichome morphology in leaves of WT and SAP11CaPM-transgenic N. benthamiana................ 85
Figure A2 Sequence alignment of the deduced proteins of N. benthamiana OMTs (NbOMTs) with Vitis vinifera OMT3 (VvOMT3) ....................................................... 86
Figure A3 Phylogenetic analysis of N. benthamiana OMTs with other previously characterized plant OMTs (class II), COMTs (class I), and CCoAOMTs (class I)...................... 87
Figure A4 A working model to explain the role of phytoplasma SAP11 in plant-mediated interactions between pathogen and natural enemy of insect vector......................... 88

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