由致病疫霉（Phytophthora infestans）引起的马铃薯晚疫病是全球农业生产中的毁灭性病害之一，严重威胁茄科作物马铃薯和番茄的安全生产。由于致病疫霉在田间的变异速度与流行速度非常快，目前选育栽培的抗病品种往往在短期内就被致病疫霉克服，从而导致抗性丧失。因此，为农业生产开发更广谱且持久的马铃薯抗病基因（Rpi）迫在眉睫。植物抗病基因发挥功能基于其编码的受体蛋白对病原菌无毒蛋白（AVR）的特异性识别，解析抗病受体识别无毒蛋白的分子机制将有助于精准设计与改良农作物的抗性，为作物安全、高效生产提供绿色解决方案。从野生茄科植物（Solanum venturii）中克隆的马铃薯抗病基因Rpi-vnt1.1编码典型的NLR（Nucleotide-binding Leucine-rich Repeat）蛋白，它能通过识别致病疫霉保守的无毒蛋白AVRvnt1介导马铃薯广谱抗性。我国已经成功培育出携带Rpi-vnt1.1及其等位基因的抗病马铃薯品种，然而该抗病受体识别AVRvnt1的分子机制尚不清楚，制约了基于该广谱抗病基因的马铃薯品种在田间的大规模使用。

本研究聚焦抗病受体Rpi-vnt1.1和无毒蛋白AVRvnt1的互作分子机制，利用马铃薯和模式茄科植物-本氏烟等材料开展深入研究。以AVRvnt1的互作蛋白-叶绿体甘油酸盐激酶（glycerate 3-kinase, GLYK）是Rpi-vnt1.1识别AVRvnt1的关键因子这一发现为切入点，深入系统地解析了马铃薯抗病受体Rpi-vnt1.1识别致病疫霉AVRvnt1的分子机制，具体内容如下：

叶绿体蛋白GLYK参与Rpi-vnt1.1介导的免疫反应。为了解析Rpi-vnt1.1识别AVRvnt1并介导免疫反应的分子机制，本研究通过酵母双杂交筛库鉴定出AVRvnt1的结合蛋白之一为GLYK。酵母双杂交以及体内体外免疫沉淀实验证明AVRvnt1与GLYK互作，并且该互作反应依赖于GLYK的叶绿体转运肽（cTP）功能域。病毒介导的本氏烟基因瞬时沉默（VIGS）实验以及人工合成序列的回补表达实验证明GLYK特异性地参与Rpi-vnt1.1介导的免疫反应。本研究进一步在DesireeRpi-vnt1.1马铃薯材料中转基因导入特异性沉默GLYK基因的RNAi载体，实现了GLYK基因的稳定沉默。研究发现GLYK沉默的DesireeRpi-vnt1.1马铃薯虽然仍正常表达Rpi-vnt1.1，但不同程度地丧失了对携带AVRvnt1的致病疫霉非亲和菌株的抗性。以上结果均鉴定到了Rpi-vnt1.1介导免疫反应的关键因子GLYK，为进一步研究Rpi-vnt1.1识别AVRvnt1并介导免疫反应的分子机制提供了遗传学基础。

StGLYK遗传位点在不同光条件下存在可变启动子选择（APS）调控，导致Rpi-vnt1.1的免疫功能具有光依赖性。本研究发现Rpi-vnt1.1在光照条件下能够正常介导抗病功能，在黑暗条件下则丧失功能，而GLYK作为Rpi-vnt1.1介导免疫反应过程中的关键蛋白，其同源基因AtGLYK在拟南芥中的转录受光依赖的APS调控，推断Rpi-vnt1.1抗病功能的光依赖性与GLYK相关。本研究进一步利用5’RACE和qRT-PCR实验发现马铃薯GLYK遗传位点在不同光照条件下存在APS调控并产生StGLYKFL和StGLYKcyt两种主要转录本。其中StGLYKFL在光照条件下为主要的转录本，其产物定位于叶绿体内并维持叶绿体功能，而StGLYKcyt在黑暗条件下积累，其产物定位于细胞质并参与光呼吸分支通路。体内外互作验证发现StGLYKcyt由于丧失了完整的cTP功能域从而不能像StGLYKFL一样被AVRvnt1靶向并结合。NbGLYK沉默本氏烟上的回补表达实验表明人工合成StGLYKcyt不能恢复沉默本氏烟上Rpi-vnt1.1识别AVRvnt1产生的免疫反应。以上结果揭示了一种Rpi-vnt1.1介导光依赖性免疫反应的分子机制。

Rpi-vnt1.1的免疫功能依赖AVRvnt1和GLYK之间的互作。为了深入研究Rpi-vnt1.1识别AVRvnt1的分子机制，本研究获得了AVRvnt1的三维结构。根据结构所构建的羧基端带负电氨基酸突变体AVRvnt1DE不能与GLYK互作，也不能触发本氏烟HR。本研究进一步对AVRvnt1/GLYK复合体开展免疫共沉淀结合液质联用检测，在沉淀蛋白中鉴定出Rpi-vnt1.1蛋白LRR功能域的肽段。免疫共沉淀验证得出Rpi-vnt1.1LRR与GLYK和AVRvnt1互作而不与AVRvnt1DE互作，证明AVRvnt1/GLYK复合体是Rpi-vnt1.1激活免疫功能所必需的。为了筛选逃避Rpi-vnt1.1识别的AVRvnt1天然突变体,本研究搜集比对了来自致病疫霉及其3个近缘种中的8个AVRvnt1同源序列。本氏烟HR检测发现牵牛花疫霉中PipAVRvnt1能够完全逃避Rpi-vnt1.1的识别，进一步通过酵母双杂以及体外体内互作实验发现PipAVRvnt1仍能结合GLYK，提示Rpi-vnt1.1可能识别AVRvnt1/GLYK复合体空间结构激活免疫功能。以上结果初步揭示了马铃薯抗病基因Rpi-vnt1.1的激活机制，为未来进一步深入开展相关机制研究提供了突变体材料与研究线索。

AVRvnt1促进GLYK在细胞质中被蛋白酶体降解导致寄主更加感病。本研究发现在马铃薯和本氏烟中特异性沉默GLYK基因导致植物对致病疫霉更加感病，回补StGLYKFL促进本氏烟更加抗病，证明GLYK是植物免疫正调控因子，且因为激酶失活突变体StGLYKK222R不能促进抗病，说明GLYK调控植物免疫的功能依赖其激酶活性。进一步的细胞生物学观察和western blot检测实验发现AVRvnt1在植物中表达或者接种致病疫霉均能显著减少StGLYK在叶绿体中的积累，而利用26S蛋白酶体抑制剂bortezomib预处理植物叶片能提高StGLYK蛋白在细胞质中的积累，证明AVRvnt1阻遏StGLYK进入叶绿体，并导致其在细胞质中被26S蛋白酶体降解。为了揭示GLYK正调控植物免疫的机制，本研究通过转录组测序（RNA-seq）分析发现，GLYK沉默马铃薯中致病相关基因PR1、ERF4和激素相关基因GH3、EBF1的基因表达在被侵染1天和2天时相比对照植株显著下降。以上结果揭示了致病疫霉分泌效应分子AVRvnt1干扰叶绿体蛋白GLYK参与植物免疫反应的分子机制。

本论文系统阐明了马铃薯广谱抗病受体Rpi-vnt1.1识别致病疫霉AVRvnt1的分子机制，为进一步开发和利用抗病基因Rpi-vnt1.1，促进马铃薯晚疫病的绿色高效防控提供了重要的理论依据与实践指导。

Potato late blight caused by Phytophthora infestans is one of the most devastating diseases in agricultural system, threatening the global production security of potatoes and tomatoes. Due to the rapid adaptative feature of this aggressive plant pathogen, it is difficult to effectively reduce the agricultural loss caused by P. infestans through growing the current resistant cultivars. Therefore, broad-spectrum and durable Resistance genes to P. infestans (Rpi) need to be further explored and utilized. The immune function of resistance receptors encoding by plant resistance genes rely on their specific recognition of the Phytophthora avirulence (AVR). Dissecting the mode of actions of how plant Rpi receptors recognize pathogen AVR effectors will greatly help to accurately design and improve crop resistance, providing solutions for safe and efficient crop production. The potato disease resistance gene Rpi-vnt1.1 from wild potato species (Solanum venturi) encodes a typical NLR (Nucleotide-binding Leucine-rich Repeat) receptor, and recognize AVRvnt1, a conserved AVR protein, to confer broad-spectrum resistance against most of of P. infestans filed isolates. The cultivated potato cultivars carrying Rpi-vnt1.1 are available in market. However, the molecular basis of how Rpi-vnt1.1 recognize AVRvnt1 reamins unclear, which restricts the further utilization of this broad-spectrum resistance gene.

 This study focused on the potato resistant mechanism mediated by NLR receptor Rpi-vnt1.1, and conducted research using materials such as potato and model plant Nicotiana benthamiana. Our preliminary observation that chloroplast glycerate kinase (GLYK) is the interact protein of AVRvnt1 and contributes to Rpi-vnt1.1 resistance provide key clue for this study. Our study here described a systematic and in-depth analysis of the molecular mechanism how Rpi-vnt1.1 confer potato resistance to P. infestans in a AVRvnt1 specific manner:

Plant chloroplast protein GLYK was a key game player in Rpi-vnt1.1 mediated immune response. In order to dissecting the mode of actions Rpi-vnt1.1 mediates immune response, we identified GLYK as one of AVRvnt1 binding proteins through yeast two-hybrid (Y2H) screening. Y2H, in vitro and in vivo immunoprecipitation experiments demonstrated that AVRvnt1 interacts with GLYK, and the interaction require a full sequence of the chloroplast transit peptide (cTP) of GLYK. Virus induced gene silencing (VIGS) and complementation of synthetic (Syn) GLYK sequences assays in N. benthamiana collectively confirmed that GLYK is specifically requiredfor Rpi-vnt1.1 mediated immune response. In this study, an RNAi interference vector was introduced into the DesireeRpi-vnt1.1 potato to trigger stable silencing of GLYK gene. It was found that the GLYK silenced potato lines still express Rpi-vnt1.1, but their resistance against P. infestans isolates carrying AVRvnt1 was lost to different degrees. The above results validated that GLYK is a key factor for Rpi-vnt1.1 immune function, providing a genetic frame work to further study the molecular mechanism of how Rpi-vnt1.1 - AVRvnt1 interaction.

The alternative promoter selection (APS) regulated by light conditions occurs in potato GLYK gene locus was, leding to a light-dependent resistance conferred by Rpi-vnt1.1. In this study, we found that Rpi-vnt1.1 conferred resistance to late blight depends on light and was significantly impaired in dark. The transcription of AtGLYK, potato GLYK orthologous gene, is regulated by light-dependent APS in Arabidopsis. We therefore speculated that Rpi-vnt1.1 mediated light-dependent resistance links to APS in GLYK locus. In this study, 5’RACE and qRT-PCR assays were used to validate that APS exists in potato GLYK gene locus under different light conditions, yielding two major transcript isoforms namely StGLYKFL and StGLYKcyt. StGLYKFL is the dominant transcript under light condition, and its translation product StGLYKFL are located and functions in chloroplast, while the isoform StGLYKcyt accumulates in dark condition with its product locates in cytoplasm and participates in the photorespiratory bypass. In vivo and in vitro assays found that StGLYKcyt are not able to be targeted by AVRvnt1 due to the loss of cTP domain. The genetic complementation assays on NbGLYK silenced plants validated that StGLYKcyt does not restore the Rpi-vnt1.1 immune function in GLYK silenced plants. In summary, these results revealed that the APS regulation of GLYK is one of the major mechanisms of light-dependent immune response conferred by Rpi-vnt1.1.

The immune function of Rpi-vnt1.1 depends on the physical interaction between AVRvnt1 and GLYK. In order to further explore the molecular mechanism how Rpi-vnt1.1 recognize AVRvnt1, we examined the three-dimensional crystal structure of AVRvnt1 harvested from our collaborator. AVRvnt1DE, a C-terminal negatively charged amino acid mutant, does not interact with GLYK and fails to trigger HR on N. benthamiana. The in vivo AVRvnt1/GLYK complex was further co-immunoprecipitated and submitted for Liquid chromatography-tandem mass spectrometry (LC-MS/MS) detection. The peptides from the LRR domain of the Rpi-vnt1.1 were consistently identified. Further Co-immunoprecipitation assay verified that LRR domain of the Rpi-vnt1.1(Rpi-vnt1.1LRR) interacts with GLYK and AVRvnt1, but it fails to interact with AVRvnt1DE, suggesting that AVRvnt1/GLYK complex is necessary for Rpi-vnt1.1 activated immune function. In order to screen natural AVRvnt1 allele that evade Rpi-vnt1.1 recognition, we harvested 8 AVRvnt1 allelic sequences from P. infestans and its sister species. The HR assays found that PipAVRvnt1 from Phytophthora ipomoeae completely escapes Rpi-vnt1.1 recognition. The interaction experiments such as Y2H, in vitro pull-down and in vivo Co-IP, it was found that PipAVRvnt1 still binds GLYK, suggesting that in additional to AVRvnt1/GLYK interaction, the biochemical features or and conformation of AVRvnt1/GLYK complex is required for Rpi-vnt1.1 immune function. These results not only provide insight into the activation mechanism of Rpi-vnt1.1, but also spark research clues for the future research on the mode of actions of.

 AVRvnt1 promotes GLYK degradation leading to increased host susceptibility. In this study, we found that silencing of the GLYK in potato and N. benthamiana promote plant susceptibility to P. infestans. Complementation of synthetic functional StGLYK instead of the kinase dead mutant StGLYKK222R rescured the basal immunity in N. benthamiana, indicating that GLYK is a positive immune regulator in a kinase activity dependent manner. Cell biology observations and western blot detections revealed that AVRvnt1 expression in planta or inoculation with P. infestans significantly abolished StGLYK accumulation in chloroplast. Whereas pretreatment with 26S proteasome inhibitor Bortezomib in N. benthamiana leaves increased StGLYK accumulation in the cytoplasm, indicating that AVRvnt1 blocked StGLYK uptake into chloroplast and promote its cytosolic degradation by 26S proteasome. We used transcriptome sequencing (RNA-seq) analysis revealed that the expression of PR genes PR1, ERF4 and hormone-related genes GH3, EBF1 in GLYK silenced potato at 1 dpi and 2 dpi were significantly down-regulated. These result reveals a novel mechanism that P. infestans effector protein interferes with chloroplast function and consequently impairs plant immune responses.

In summary, this thesis systematically clarified the mode of actions of how potato disease resistance receptor Rpi-vnt1.1 recognition P. infestans AVRvnt1 to activate plant immunity in a light dependent manner, providing both theoretical frame concept and practical guidance for developing and utilizing potato Rpi-vnt1.1 gene, and as such to contribute the sustainable and efficient disease management for potato late blight.

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