辣椒与黄瓜抗疫病相关基因克隆及分析
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摘要
由辣椒疫霉菌（Phytophthora capsici）侵染引起的辣椒疫病是辣椒生产中的一种毁灭性病害。辣椒疫病抗性遗传规律比较复杂，辣椒基因组比较大、重复序列多，这些因素导致了目前辣椒疫病抗性机制研究进展较慢。辣椒疫霉菌还可侵染葫芦科植物，该病原菌在一些地区也对黄瓜的生产造成严重危害，但生产上还没有高抗此病的黄瓜品种。植物-病原物互作过程中，植物的一些抗病相关基因如病原识别基因、信号转导、防卫基因的表达变化决定了植物对该病原物的抗感与否。本研究对辣椒和黄瓜的一些抗病相关基因进行了克隆及分析，这些基因可进一步用于辣椒和黄瓜抗疫病分子育种。主要结果如下：
1.根据已知抗病基因保守结构域设计简并引物，在辣椒中扩增获得了10条新的辣椒抗病基因同源序列（RGAs）。另外从Genbank获取了53条辣椒RGAs。序列分析表明这些RGAs都具有NBS结构域的保守模体，系统发育分析表明可分为non-TIR-NBS-LRR和TIR-NBS-LRR两大类、5组24个亚组。对NBS结构较完整的I2类同源基因和Bs4类同源基因进行了进化分析，Ka/Ks分析表明这两类抗病基因同源基因的NBS结构域主要受纯化选择；重组分析表明辣椒I2类同源基因间发生了交换事件，推测为进化较快的TypeⅠ类抗病基因。这些辣椒RGAs的获得将为分析辣椒NBS类基因进化、开发RGA类分子标记进行辣椒抗疫病育种奠定基础。
2.利用RACE结合TAIL-PCR技术，克隆了辣椒5个NBS-LRR类基因全长，命名为CaRGA1~CaRGA5（GQ386945、GU116570、GU295217、JQ219039、JQ219041），这5个基因都具有完整的ORF。同源性比对说明这些基因是马铃薯晚疫病抗性基因Rpi-blb1的同源基因；序列分析显示其编码蛋白均属于CC-NBS-LRR类，其中CaRGA1和CaRGA2编码蛋白比其他三个基因编码蛋白缺少1个LRR结构；半定量分析表明，这5个NBS-LRR基因的表达不受辣椒疫霉菌侵染诱导，推测为低水平组成性表达；较高的同义替代率说明这5个基因属于一个古老的基因家族，Ka/Ks＜1表明主要受纯化选择。对Rpi-blb1同源基因在茄科植物中的进化进行了分析，结果说明Rpi-blb1祖先基因出现在辣椒与马铃薯、番茄分化之前，明显的直系同源基因和旁系同源基因关系以及马铃薯基因组中多个同源基因簇的存在说明复制在该基因家族进化中起了主要作用。
3.利用cDNA-AFLP技术分离了66个辣椒疫霉菌侵染诱导的差异表达片段（DE-TDFs），可预测功能的TDFs有35个，分别与细胞代谢、防卫、信号转导、物质转运等生理生化过程有关。这些基因编码产物主要与防卫、代谢、信号转导有关，说明在疫霉菌侵染下辣椒植株细胞内基础代谢活跃，信号转导途径被激活，防卫反应启动以抵御病原物侵染。
4.克隆了辣椒几丁质酶基因CaCHI（FJ596176）、细胞凋亡抑制蛋白基因CaDAD1（JQ219041）、病程相关蛋白4基因CaPR4（JX030397）。序列分析表明CaCHI编码产物为ClassⅠ几丁质酶，预测定位于细胞外或细胞间隙；CaDAD1编码产物具跨膜结构域，预测定位于叶绿体类囊体；CaPR4编码产物具Barwin结构域。实时定量RT-PCR分析表明，不论在抗病品种还是在感病品种中，CaCHI和CaPR4都表现受疫霉菌诱导上调表达，CaDAD1则表现早期下调表达。
5.克隆了辣椒脂氧合酶基因CaLOX2（JQ219046）、CaLOX3（JQ219047）。序列分析显示CaLOX2可能定位于叶绿体。组织表达特异性分析显示，CaLOX2在辣椒各个器官都表达，在叶片中表达量最高，在花中表达量最低；CaLOX3基因在叶和花中不表达，在萌发的种子中表达量最高。这两个基因在辣椒与疫霉菌亲和与非亲和互作中均受诱导，但在非亲和组合中受诱导表达的强度更大，并且诱导表达的时间在非亲和组合中也相对较早。CaLOX2受茉莉酸甲酯、水杨酸和H2O2、机械伤害和高盐胁迫诱导上调表达，受低温诱导下调表达。和已知生物学功能的其它植物脂氧合酶基因聚类及表达模式比较揭示CaLOX2可能参与茉莉酸合成。
6.分析了三个辣椒疫病不同抗性材料AA5（高抗）、AA3（小种专化型抗性）、EC（高感）VIGS后表现，EC最适宜做VIGS试材，AA5不适宜，AA3虽然植株矮化，但不影响抗病表型观察。考虑到试验要沉默的基因都与抗病性相关，因此以AA3为试验材料，利用VIGS技术分析了CaDAD1、CaPR4、CaLOX2三个辣椒抗病相关基因的功能。离体叶片接种疫霉菌，CaDAD1沉默的辣椒叶片接种疫霉菌后症状与对照无明显区别；而CaPR4沉默的叶片病斑比对照变小，推测可能是一种敏感因子；CaLOX2沉默的叶片病斑比对照变大，可能起正调控作用。
7.克隆了黄瓜多聚半乳糖醛酸酶抑制蛋白基因CsPGIP1（JQ219048）和CsPGIP2（JQ219049）。对其基因编码序列分析表明，这两个基因属于Pgip基因家族，其编码蛋白均具有xxLxLxxNxLt/sGxIPxxLxxLxxL结构域。组织表达特异性分析表明，CsPGIP1和CsPGIP2在黄瓜各个器官都表达，CsPGIP1在嫩叶中表达量最高，在茎中表达量最低；CsPGIP2在根中表达量最高，功能叶中最低。在水杨酸和辣椒疫霉菌诱导下CsPGIP1上调表达，CsPGIP2表达无变化。把这两个基因进行原核表达，比色法和琼脂糖扩散法分析表明CsPGIP1编码蛋白对疫霉菌PG有抑制活性。这一结论为超量表达CsPGIP1进行黄瓜抗辣椒疫霉分子育种提供了理论支持。
Pepper phytophthora blight caused by Phytophthora capsici, is a serious disease inpepper production. Unfortunately, the resistance gene against P. capsici of pepper has notbeen cloned. Because of the complexity of the genetics of resistance to P. capsici and the largegenome, it is difficult to isolate the resistance gene using map-based method. Fruit rot causedby P. capsici is an increasingly serious desease in some area. But there are no cultivarresistant to P. capsici. The expression change of some resistance-related genes (pathogenrecognize gene, defense-related genes, signal transduction, etc.) can dominant the plantsresistance or susceptible to pathogens. In this study, some disease resistance-related genes ofpepper cultivar “AA5” and cucumber cultivar “NW99” were isolated, and these genes can beused for molecular breeding of phytophthora blight resistance cultivars of pepper andcucumber.
1. Ten new pepper NBS-RGAs were cloned using degenerate primer by PCR-basedapproach, and other53RGAs were retrived from Genbank. These RGAs can be divided intotwo classes: CNL and TNL. According70%similarity and the Polygenetic tree, the RGAs canbe divided into5groups and24subgroups. Recombination signal was found in the pepperI2-like genes. NBS domain of pepper I2-like and Bs4-like genes are under purifyingselection. We can development RGA-markers according to these RGA sequences forresistance gene mapping.
2. The full length of five pepper NBS-LRR genes are isolated by TAIL-PCR and RACEapproach. These five genes designated CaRGA1~5are Rpi-blb1homologs, and share above80%similarity with the Rpi-blb1cluster members of potato. There is a LRR lack of CaRGA1and CaRGA2in contrast to the other three. There are several Rpi-blb1homolog clusters of thepotato genome. The microsynteny of this R gene cluster was interrupted in the tomato and S.phureja genome. There maybe unequal recombination occurred in this locus. The existance ofparalogs and othologs and the homologous clusters implied that replication played main rolein the evolution of this R gene family.
3. Sixty-six DE-TDFs were isolated from pepper challenged by P. capsici usingcDNA-AFLP approach. Function of Thirty-five TDFs can be predicted. They involve theprocess of signal transduction, metabolism, defense, transcription, etc. Expression change ofthese TDFs indicated the plangt strengthen its metabolism and inactive signal transduction inthe incompatible interaction between P. capsici and C. annuum.
4. Three disease resistance related genes, CaCHI，CaDAD1，CaPR4，of pepper wereobtained by in silo PCR and RT-PCR. Protein encoded by CaCHI is a chitinase of ClassⅠ,which has a CBD and N-terminal signal peptide. The deduced amino acid sequence ofCaDAD1has a DAD1domain, which is conserved between animals and plants. PR4proteinencoded by CaPR4has a Barwin domain, which has the weak activity of chitinase. Theexpression changes postinoculated by P. capsici of the three genes were detected by qRT-PCR.CaCHI and CaPR4were both up-regulated by the P. capsici, however CaDAD1weredown-regulated in the early stage of P. capsici infecton.
5. Two novel LOX genes designated as CaLOX2and CaLOX3were isolated andcharacterized in Capsicum annuum L. using in silico cloning and RT-PCR techniques. Thededuced amino acid sequence of the two genes contained the typical domain of lipoxygenase,and CaLOX3has putative transit peptides for chloroplast import. Phylogenetic analysisrevealed that CaLOX2clustered together with well-characterized plastidic typeⅡ13-LOXs,while CaLOX3clustered together with the typeⅠLOXs groups. Real-time quantitative PCRanalysis showed that CaLOX2transcripts were expressed in all tissues of pepper, hand thetranscripts were most abundantly expressed in the leaf but much less in flower. CaLOX3wereabundantly expressed in the germinated seeds. The expression level of the CaLOX2andCaLOX3mRNA could be up-regulated significantly after inoculation with zoospores ofPhytophthora capsici in both incompatible and compatible interaction. The comparison ofCaLOX2with the well-studied LOXs from other plant species in phylogenetic analysis andexpression patterns indicated that the most likely biochemical function of CaLOX2is in thebiosynthesis of JA through allene oxide synthase（AOS）pathway but not in the hydroperoxidelyase mediated （HPL-mediated） production of C6-aldehydes. These results indicated thatCaLOX2was probably involved in the disease resistance and defense response toPhytophthara capsici and other environment stress，such as low temperature and high salt,through SA and JA pathways.
6. The comparison of the efficiency of VIGS revealed that AA5is not suit for VIGS. SoAA3was chosen for characterize the functions of CaDAD1, CaPR4and CaLOX2. Thedepletion of CaDAD1didn’t cause distinctive change in the infection of P. capsici. But thedepletion of CaLOX2caused pepper leave more susceptible to the pathgon. And knocking out of CaPR4delayed the cell death.
7. Polygalacturonase-inhibiting protein (PGIP) can inhibit the activity of pathogen PGand improve the plant resistance level. Two novel PGIP genes designated as CsPGIP1andCsPGIP2were isolated and characterized in Cucumis sativus L. The deduced amino acidsequence of the two genes contained a the typical domain ofxxLxLxxNxLt/sGxIPxxLxxLxxL domain and belonged to Pgip gene family. Phylogeneticanalysis revealed the significant evolutionary homologous in the sequences of melon PGIPgene and PGIP genes in Cruciferae. Real-time quantitative PCR analysis showed thatCsPGIP1transcripts were expressed in all tissues, but the transcripts were most abundantlyexpressed in the young leaf but much less in stem. While CsPGIP2transcripts were abundantin root. The expression level of the CsPGIP1mRNA could be up-regulated significantly aftertreated with pathogen and salicylic acid (SA) compared to the normal growth environment.While CsPGIP2was not inducible by SA. UV spectrophotometry and agar diffusion analysisshowed that the protein CsPGIP1can inhibit the PG activity of P. capsici.
1.根据已知抗病基因保守结构域设计简并引物，在辣椒中扩增获得了10条新的辣椒抗病基因同源序列（RGAs）。另外从Genbank获取了53条辣椒RGAs。序列分析表明这些RGAs都具有NBS结构域的保守模体，系统发育分析表明可分为non-TIR-NBS-LRR和TIR-NBS-LRR两大类、5组24个亚组。对NBS结构较完整的I2类同源基因和Bs4类同源基因进行了进化分析，Ka/Ks分析表明这两类抗病基因同源基因的NBS结构域主要受纯化选择；重组分析表明辣椒I2类同源基因间发生了交换事件，推测为进化较快的TypeⅠ类抗病基因。这些辣椒RGAs的获得将为分析辣椒NBS类基因进化、开发RGA类分子标记进行辣椒抗疫病育种奠定基础。
2.利用RACE结合TAIL-PCR技术，克隆了辣椒5个NBS-LRR类基因全长，命名为CaRGA1~CaRGA5（GQ386945、GU116570、GU295217、JQ219039、JQ219041），这5个基因都具有完整的ORF。同源性比对说明这些基因是马铃薯晚疫病抗性基因Rpi-blb1的同源基因；序列分析显示其编码蛋白均属于CC-NBS-LRR类，其中CaRGA1和CaRGA2编码蛋白比其他三个基因编码蛋白缺少1个LRR结构；半定量分析表明，这5个NBS-LRR基因的表达不受辣椒疫霉菌侵染诱导，推测为低水平组成性表达；较高的同义替代率说明这5个基因属于一个古老的基因家族，Ka/Ks＜1表明主要受纯化选择。对Rpi-blb1同源基因在茄科植物中的进化进行了分析，结果说明Rpi-blb1祖先基因出现在辣椒与马铃薯、番茄分化之前，明显的直系同源基因和旁系同源基因关系以及马铃薯基因组中多个同源基因簇的存在说明复制在该基因家族进化中起了主要作用。
3.利用cDNA-AFLP技术分离了66个辣椒疫霉菌侵染诱导的差异表达片段（DE-TDFs），可预测功能的TDFs有35个，分别与细胞代谢、防卫、信号转导、物质转运等生理生化过程有关。这些基因编码产物主要与防卫、代谢、信号转导有关，说明在疫霉菌侵染下辣椒植株细胞内基础代谢活跃，信号转导途径被激活，防卫反应启动以抵御病原物侵染。
4.克隆了辣椒几丁质酶基因CaCHI（FJ596176）、细胞凋亡抑制蛋白基因CaDAD1（JQ219041）、病程相关蛋白4基因CaPR4（JX030397）。序列分析表明CaCHI编码产物为ClassⅠ几丁质酶，预测定位于细胞外或细胞间隙；CaDAD1编码产物具跨膜结构域，预测定位于叶绿体类囊体；CaPR4编码产物具Barwin结构域。实时定量RT-PCR分析表明，不论在抗病品种还是在感病品种中，CaCHI和CaPR4都表现受疫霉菌诱导上调表达，CaDAD1则表现早期下调表达。
5.克隆了辣椒脂氧合酶基因CaLOX2（JQ219046）、CaLOX3（JQ219047）。序列分析显示CaLOX2可能定位于叶绿体。组织表达特异性分析显示，CaLOX2在辣椒各个器官都表达，在叶片中表达量最高，在花中表达量最低；CaLOX3基因在叶和花中不表达，在萌发的种子中表达量最高。这两个基因在辣椒与疫霉菌亲和与非亲和互作中均受诱导，但在非亲和组合中受诱导表达的强度更大，并且诱导表达的时间在非亲和组合中也相对较早。CaLOX2受茉莉酸甲酯、水杨酸和H2O2、机械伤害和高盐胁迫诱导上调表达，受低温诱导下调表达。和已知生物学功能的其它植物脂氧合酶基因聚类及表达模式比较揭示CaLOX2可能参与茉莉酸合成。
6.分析了三个辣椒疫病不同抗性材料AA5（高抗）、AA3（小种专化型抗性）、EC（高感）VIGS后表现，EC最适宜做VIGS试材，AA5不适宜，AA3虽然植株矮化，但不影响抗病表型观察。考虑到试验要沉默的基因都与抗病性相关，因此以AA3为试验材料，利用VIGS技术分析了CaDAD1、CaPR4、CaLOX2三个辣椒抗病相关基因的功能。离体叶片接种疫霉菌，CaDAD1沉默的辣椒叶片接种疫霉菌后症状与对照无明显区别；而CaPR4沉默的叶片病斑比对照变小，推测可能是一种敏感因子；CaLOX2沉默的叶片病斑比对照变大，可能起正调控作用。
7.克隆了黄瓜多聚半乳糖醛酸酶抑制蛋白基因CsPGIP1（JQ219048）和CsPGIP2（JQ219049）。对其基因编码序列分析表明，这两个基因属于Pgip基因家族，其编码蛋白均具有xxLxLxxNxLt/sGxIPxxLxxLxxL结构域。组织表达特异性分析表明，CsPGIP1和CsPGIP2在黄瓜各个器官都表达，CsPGIP1在嫩叶中表达量最高，在茎中表达量最低；CsPGIP2在根中表达量最高，功能叶中最低。在水杨酸和辣椒疫霉菌诱导下CsPGIP1上调表达，CsPGIP2表达无变化。把这两个基因进行原核表达，比色法和琼脂糖扩散法分析表明CsPGIP1编码蛋白对疫霉菌PG有抑制活性。这一结论为超量表达CsPGIP1进行黄瓜抗辣椒疫霉分子育种提供了理论支持。
Pepper phytophthora blight caused by Phytophthora capsici, is a serious disease inpepper production. Unfortunately, the resistance gene against P. capsici of pepper has notbeen cloned. Because of the complexity of the genetics of resistance to P. capsici and the largegenome, it is difficult to isolate the resistance gene using map-based method. Fruit rot causedby P. capsici is an increasingly serious desease in some area. But there are no cultivarresistant to P. capsici. The expression change of some resistance-related genes (pathogenrecognize gene, defense-related genes, signal transduction, etc.) can dominant the plantsresistance or susceptible to pathogens. In this study, some disease resistance-related genes ofpepper cultivar “AA5” and cucumber cultivar “NW99” were isolated, and these genes can beused for molecular breeding of phytophthora blight resistance cultivars of pepper andcucumber.
1. Ten new pepper NBS-RGAs were cloned using degenerate primer by PCR-basedapproach, and other53RGAs were retrived from Genbank. These RGAs can be divided intotwo classes: CNL and TNL. According70%similarity and the Polygenetic tree, the RGAs canbe divided into5groups and24subgroups. Recombination signal was found in the pepperI2-like genes. NBS domain of pepper I2-like and Bs4-like genes are under purifyingselection. We can development RGA-markers according to these RGA sequences forresistance gene mapping.
2. The full length of five pepper NBS-LRR genes are isolated by TAIL-PCR and RACEapproach. These five genes designated CaRGA1~5are Rpi-blb1homologs, and share above80%similarity with the Rpi-blb1cluster members of potato. There is a LRR lack of CaRGA1and CaRGA2in contrast to the other three. There are several Rpi-blb1homolog clusters of thepotato genome. The microsynteny of this R gene cluster was interrupted in the tomato and S.phureja genome. There maybe unequal recombination occurred in this locus. The existance ofparalogs and othologs and the homologous clusters implied that replication played main rolein the evolution of this R gene family.
3. Sixty-six DE-TDFs were isolated from pepper challenged by P. capsici usingcDNA-AFLP approach. Function of Thirty-five TDFs can be predicted. They involve theprocess of signal transduction, metabolism, defense, transcription, etc. Expression change ofthese TDFs indicated the plangt strengthen its metabolism and inactive signal transduction inthe incompatible interaction between P. capsici and C. annuum.
4. Three disease resistance related genes, CaCHI，CaDAD1，CaPR4，of pepper wereobtained by in silo PCR and RT-PCR. Protein encoded by CaCHI is a chitinase of ClassⅠ,which has a CBD and N-terminal signal peptide. The deduced amino acid sequence ofCaDAD1has a DAD1domain, which is conserved between animals and plants. PR4proteinencoded by CaPR4has a Barwin domain, which has the weak activity of chitinase. Theexpression changes postinoculated by P. capsici of the three genes were detected by qRT-PCR.CaCHI and CaPR4were both up-regulated by the P. capsici, however CaDAD1weredown-regulated in the early stage of P. capsici infecton.
5. Two novel LOX genes designated as CaLOX2and CaLOX3were isolated andcharacterized in Capsicum annuum L. using in silico cloning and RT-PCR techniques. Thededuced amino acid sequence of the two genes contained the typical domain of lipoxygenase,and CaLOX3has putative transit peptides for chloroplast import. Phylogenetic analysisrevealed that CaLOX2clustered together with well-characterized plastidic typeⅡ13-LOXs,while CaLOX3clustered together with the typeⅠLOXs groups. Real-time quantitative PCRanalysis showed that CaLOX2transcripts were expressed in all tissues of pepper, hand thetranscripts were most abundantly expressed in the leaf but much less in flower. CaLOX3wereabundantly expressed in the germinated seeds. The expression level of the CaLOX2andCaLOX3mRNA could be up-regulated significantly after inoculation with zoospores ofPhytophthora capsici in both incompatible and compatible interaction. The comparison ofCaLOX2with the well-studied LOXs from other plant species in phylogenetic analysis andexpression patterns indicated that the most likely biochemical function of CaLOX2is in thebiosynthesis of JA through allene oxide synthase（AOS）pathway but not in the hydroperoxidelyase mediated （HPL-mediated） production of C6-aldehydes. These results indicated thatCaLOX2was probably involved in the disease resistance and defense response toPhytophthara capsici and other environment stress，such as low temperature and high salt,through SA and JA pathways.
6. The comparison of the efficiency of VIGS revealed that AA5is not suit for VIGS. SoAA3was chosen for characterize the functions of CaDAD1, CaPR4and CaLOX2. Thedepletion of CaDAD1didn’t cause distinctive change in the infection of P. capsici. But thedepletion of CaLOX2caused pepper leave more susceptible to the pathgon. And knocking out of CaPR4delayed the cell death.
7. Polygalacturonase-inhibiting protein (PGIP) can inhibit the activity of pathogen PGand improve the plant resistance level. Two novel PGIP genes designated as CsPGIP1andCsPGIP2were isolated and characterized in Cucumis sativus L. The deduced amino acidsequence of the two genes contained a the typical domain ofxxLxLxxNxLt/sGxIPxxLxxLxxL domain and belonged to Pgip gene family. Phylogeneticanalysis revealed the significant evolutionary homologous in the sequences of melon PGIPgene and PGIP genes in Cruciferae. Real-time quantitative PCR analysis showed thatCsPGIP1transcripts were expressed in all tissues, but the transcripts were most abundantlyexpressed in the young leaf but much less in stem. While CsPGIP2transcripts were abundantin root. The expression level of the CsPGIP1mRNA could be up-regulated significantly aftertreated with pathogen and salicylic acid (SA) compared to the normal growth environment.While CsPGIP2was not inducible by SA. UV spectrophotometry and agar diffusion analysisshowed that the protein CsPGIP1can inhibit the PG activity of P. capsici.
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