Hormonal Regulation in the Pattern Triggered Immunity-mediated Resistance or Susceptibility in the Xanthomonas campestris pv. campestris-Brassica napus Pathosystem = 유채와 병원성 박테리아 Xanthomonas campestris pv. campestris (Xcc)의 병체계에서 패턴 유발 면역에 의해 매개되는 병 저항성 또는 감수성에 대한 호르몬 조절

다국어 초록 (Multilingual Abstract)

Phytohormones was found to regulate the metabolic and physiological responses to biotic stress in Xanthomonas campestris pv. campestris (Xcc)-Brassica napus pathosystem . Still, the phytohormonal regulation in pattern triggered immunity (PTI) and effector triggered immunity/susceptibility (ETI/ETS) in relation with immune related genes is unknown. The aim of the study was to characterize the phytohormonal regulation in cytoplasmic kinases?and resistance gene-signaling for activation of PTI and ETI in Brassica napusto black rot disease, caused by a destructive pathogen Xanthomonas campestris pv. campestris (Xcc), which is responsible for limiting the quality and productivity of cruciferous vegetables. In chapter 1, Xcc has found in hemibiotrophic nature as cause the asymptomatic infection in early biotrophic phase (2 DPI) and turn into necrotrophic phase with V-shaped-visual necrosis to induce the necrosis at the later necrotrophic phase (7-14 DPI). The necrotrophic phase (7-14 DPI) was initiated by the elevated H2O2 concentration, darkest spots in O2 .? localization along with Ca2+ channel-related genes (Ca2+ ATPase) along with elevated cytokinin (CK) level . The opposite results were observed at early biotrophic phase (2 DPI). In chapter 2, the aim of study was to characterize the significance of Xcc-induced phytohormones- [especially, abscisic acid; (ABA)] and exogenous ABA-induced stomatal conductance in relation with immune related genes. Xcc-infection and ABA-pretreatment were applied in Brassica napus (cv. Mosa). In this time course study, PTI-related cytoplasmic kinase BIK1 was induced in asymptomatic early phase (2 DPI) along with increased jasmonic acid (JA) level, whereas at later phase of Xcc-infection (7-15 DPI), elevated level of ABA was found along with highly expressed R-gene (TAO1) resulted in slow anion channel-1 (SLAC1)- mediated stomatal closed through calcium dependent protein kinase 5 (CDPK5) along with increment of cytosolic Ca2+. Exogenous ABA-application induced the expression of ABA- receptor (PYR1) resulted in increased endogenous ABA level leading to confirming SLAC1 mediated stomatal closer by inhibiting JA signaling with moderate cytosolic Ca2+. The aim of in ‘chapter 3’ was to characterize the hormonal regulations in the transition between biotrophic and necrotrophic phases of Xanthomonas campestris pv. campestris (Xcc) infection. The length of the V-shaped lesions increased significantly with the progression of infection along with the increasing of H2O2 accumulation and the expression of NADPHoxidase. The early biotrophic phase (2DPI) to Xcc-infection was found with reduced levels of salicylic acid (SA), ABA, whereas the opposite results were found in the necrotrophic phase transition. In chapter 4, the aim was to understand the R-genes mediated Ca2+ signaling and phytohormones in ETI and disease susceptibility (ETS), Xcc was inoculated in resistance and susceptible cultivars (cultivar Capitol and cultivar Mosa) of B. napus. The R-gene (CC-NBLRR-type, ZAR1) was found to initiate SA-mediated JA signaling through calmodulin (CaM) and calcium-sensing receptor (CAS) for ETI in cv. Capitol, whereas (TIR-NB-LRR)-type R-gene, TAO1, was involved in higher accumulation of SA and significantly lower JA level along with visual symptoms at 14 DPI in cv. Mosa. Calcium channel-related Ca2+ ATPase, CDPK5 and calcium-sensing protein 60g (CBP60g) were also found to be highly expressed in disease development (ETS). The aim of this study (in chapter 5) was to identify the hormonal interaction with proline metabolism in regulation of the transition between PTI and ETS. In early phase (3DPI), highly expressed BIK1 and moderate level of salicylic acid (SA) accumulation-initiated activation of ZAR1 paused the additional proline accumulation with moderate level of SA and JA in later phase in resistance cultivar (cv, Capitol). Whereases early elevated JA level confirmed upregulation of TAO1 was consistent with an increase in SA and abscisic acid (ABA) levels and resulted in an antagonistic depression of JA, which led to a proline accumulation along with significant disease susceptibility (ETS). Taken together, among the phytohormones, SA and JA synergism involves in plant resistance [pattern/effector triggered immunity (PTI/ETI)], whereas SA and ABA interaction was found to prohibited JA signaling to induce the disease development [effector triggered susceptibility (ETS)].

국문 초록 (Abstract)

식물호르몬은 유채와 병원성 박테리아 Xanthomonas campestris pv. campestris(Xcc)의 병체계에서 대사적 반응 및 생리학적 반응을 조절하는 것으로 밝혀졌다. 그러나 면역 관련 유전자와 관련된 패턴 유발 면역 (pattern triggered immunity, PTI)과 효과인자 유발 면역(effector triggered immunity/susceptibility, ETI/ETS)의 식물 호르몬 조절은 아직 잘 알려져 있지 않다. 따라서, 본 연구의 목적은 작물의 품질과 생산성을 제한하는 병원체 Xcc의 접종에 의해 유발된 검은썩음병에 대한 유채의 면역 반응 PTI와 ETI의 활성화를 위한 세포질 키나아제와 저항성 유전자 신호전달에 있어서 식물호르몬 조절을 특성화 하기 위한 것이다. 제1장에서는 Xcc가 병원균 접종 초기 (2일)에 biotrophic (생물영양) 단계에서 무증상 감염을 일으키고 접종 후기 (7-14일)에 necrotrophic (괴사영양) 단계에 V자형 괴사를 유도하는 것으로 보아 hemibiotrophic (반생물영양) 특성임을 확인하였다. Necrotrophic 단계(7-14일)는 Ca2+ 채널과 관련된 유전자 (Ca2+ ATPase) 및 사이토카인의 증가와 함께 활성산조종인 O2 -와 H2O2의 증가에 의해 시작되었다. 반대되는 결과는 초기 biotrophic 단계 (2일)에서 발견되었다. 제2장에서는 면역 유전자와 관련된 Xcc에 의해 유도된 식물호르몬 [특히, 앱시스산 (ABA)]과 외인성 ABA공급에 의해 유도된 기공 전도도의 중요성을 특성화 하기 위해서 유채 품종 Mosa에 Xcc 접종 및 ABA 전처리를 수행하였다. 이 실험 기간동안, PTI와 관련된 세포질 키나아제 BIK1은 자스몬산 (JA) 농도의 증가와 함께 무증상 초기 단계 (2일)에서 유도된 반면, Xcc 감염의 후기 단계(7-14일)에서 고도로 발현된 R-유전자 (TAO1)와 함께 발견된 ABA의 증가는 세포질의 Ca2+ 증가와 calcium-dependent protein kinase 5 (CDPK5) 발현 증가를 통해 slow anion channel-1 (SLAC1) 매개 기공 폐쇄를 초래했다. 외인성 ABA 공급은 ABA-receptor (PYR1)의 발현을 유도하여 내인성 ABA 수준을 증가시켜 세포질 Ca2+ 조절에 의한 JA 신호전달을 억제함으로써 SLAC1 매개 기공 폐쇄를 일으켰다. 제3장에서는 Xcc 접종에 의한 biotrophic과 necrotrophic 단계 사이의 전환에서 호르몬 조절을 특성화 하였다. V자형 병변 길이는 H2O2축적과 NADPH-oxidase의 발현의 증가와 함께 감염이 진행됨에 따라 현저히 증가하였다. Xcc 감염에 대한 초기 biotrophic 단계 (2일)에서는 살리실산 (SA)와 ABA의 감소가 나타난 반면 necrotrophic 단계에서 반대되는 결과가 발견되었다. 제4장에서는 ETI와 질병감수성(ETS)에서 R-유전자 매개 칼슘 신호전달 및 식물호르몬을 이해하기 위해서, 유채의 병 저항성 품종인 Capitol과 감수성 품종인 Mosa에 Xcc를 접종하였다. CC-NB-LRR-type R-유전자인 ZAR1는 저항성 품종인 Capitol에서 ETI에 대한 calmodulin (CaM)과 calcium-sensing receptor (CAS)를 통한 SA 매개 JA 신호전달 개시와 관련이 있는 반면, TIR-NB-LRR-type R-유전자 TAO1은 감수성 품종인 Mosa에서 14일째에 시각적 병증과 함께 SA의 더 높은 축적 및 현저히 낮은 JA의 수준과 관련이 있었다. 또한 Ca2+ 채널과 관련된 Ca2+ ATPase, CDPK5, calcium-sensing protein 60g (CBP60g)도 질병감수성 (ETS)에서 높게 발현되었다. 제5장에서는 PTI와 ETS 사이의 전환 조절에 있어서 프롤린 대사와 호르몬 상호작용을 밝히기 위해 수행되었다. 저항성 품종 (Capitol)의 Xcc 감염 초기단계 (3일)에서 고도로 높게 발현된 BIK1과 적당한 수준의 SA 축적에 의해 개시된 ZAR1의 활성은 후기 단계에서 적당한 수준의 SA 및 JA와 더불어 추가적인 프롤린 축적을 일시적으로 중지했다. 반면에, 감수성 품종 (Mosa)에서 Xcc 감염 초기 상승된 JA 수준은 TAO1를 상향 조절했으며 이는 SA와 ABA 수준의 증가와 일치하였고 결과적으로 JA의 길항성 억제를 초래하여 현저한 질병 감수성 (ETS)과 함께 프롤린 축적을 초래했다. 이상의 결과들을 종합해 보면, 식물호르몬 중에서 SA와 JA의 상승작용은 식물 저항성 [패턴 유발 면역 /효과인자 유발 면역 (PTI/ETI)]과 관련이 있는 반면, SA와 ABA 상호 작용은 질병 발병을 유도하는 (효과인자 유발 감수성, ETS) JA 신호전달의 억제와 관련이 있다고 생각된다.

목차 (Table of Contents)

• LIST OF TABLE AND FIGURES IV
• ABBREVIATIONS IX
• ABSTRACT 1
• 1. GENERAL INTRODUCTION 3
• 1.1 Pattern triggered immunity 4
• 1.2 Effector triggered immunity 4
• 1.3 Significance of phytohormones in plant defense 5
• 1.3.1 Salicylic acid signaling 5
• 1.3.2 Abscisic acid signaling 6
• 1.3.3 Jasmonic acid signaling 6
• 1.3.4 Hormonal crosstalk in plant immunity 6
• 1.4 Proline metabolism in innate immunity 7
• 1.5 Ca2+ signaling in plant immunity 7
• OBJECTIVES 8
• 2. MATERIALS AND METHODS 9
• 2.1 Plant culture 9
• 2.2 The parameters analysis 9
• 2.2.1 Bacterial inoculation and sampling 9
• 2.2.2 Determination of H2O2 and lipid peroxidation 10
• 2.2.3 ROS localization in situ 10
• 2.2.4 Determination of cytosolic Ca2+ concentration 11
• 2.2.5 Determination of proline and pyrroline-5-carboxylate 11
• 2.2.6 Phytohormonal analysis 11
• 2.2.7 Chlorophyll content analysis 12
• 2.2.8 Isolation of total RNA and quantitative real-time PCR 12
• 2.2.9 Glutathione redox assays 12
• 2.2.10 Stomatal view 13
• 2.2.11 Statistical analysis 13
• Chapter 1 15
• Xcc-induced disease symptom development in relation with reactive oxidative
• stress signaling 15
• Abstract 15
• 1.1 Introduction 16
• 1.2 Experimental design 17
• 1.3 Results 17
• 1.4 Discussion 22
• Chapter 2 25
• Phytohormonal-involvement in ROS and Ca2+ signaling in stomatal movement in
• Xcc-Brassica napus pathosystem 25
• Abstract 25
• 2.1 Introduction 26
• 2.2 Experimental Design 27
• 2.3 Results 28
• 2.4 Discussion 34
• Chapter 3 38
• Phytohormonal regulation in transition between biotrophic-necrotrophic phase in relation with hormonal signaling 38
• Abstract 38
• 3.1 Introduction 39
• 3.2 Experimental design 40
• 3.3 Results 41
• 3.4 Discussion 46
• Chapter 4 50
• Resistance gene-mediated hormonal regulation in calcium signaling in effector triggered immunity or susceptibility 50
• Abstract 50
• 4.1 Introduction 51
• 4.2 Experimental design 52
• 4.3 Results 53
• 4.4 Discussion 58
• Chapter 5 62
• Resistance gene-mediated hormonal regulation in proline metabolism in pattern triggered immunity and effector triggered immunity or susceptibility 62
• Abstract 62
• 5.1 Introduction 63
• 5.2 Experimental design 65
• 5.3 Results 65
• 5.4 Discussion 73
• GENERAL CONCLUSION 78
• REFERENCES 82
• LIST OF PUBLICATIONS 90
• ABSTRACT IN KOREAN 91

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