棉花黄萎病菌诱导陆地棉和野生棉差异表达分析及抗病相关基因克隆
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摘要
黄萎病是棉花的主要病害,严重影响棉花产量和品质。抗病育种无疑是防治黄萎病最经济、最环保和最有效的手段,但由于对棉花抗病机理认识不清,加上现有栽培品种中抗源缺乏,棉花抗黄萎病育种一直难以突破。深入研究棉花抗黄萎病机理、克隆抗病基因仍是目前努力的方向。本研究从接菌诱导入手,采用SSH技术从转录组水平探讨了陆地棉基因的差异表达；采用2-DE技术从蛋白质组水平探讨了栽培棉近缘野生种瑟伯氏棉的蛋白差异表达,并以此为基础克隆了7个抗病相关基因。
(1)以中等致病性棉花黄萎病菌W菌系接种诱导我国棉花抗黄萎病标准品种豫棉21号,构建了正反两个SSH文库,富集筛选到抗病相关的早期诱导表达Unigene169个,其中上调表达68个,下调表达91个。提交到NCBI的Nr和Nt核酸数据库、Swissprot蛋白数据库比对注释,并通过GO、COG和KEGG数据库进行组份、功能和代谢路径聚类分析,共解析了152个基因；另外16个基因为未能注释,可能代表了新发现基因。结果表明：①这些基因分属18种生物学过程、8种细胞组份和5种分子功能,集中于19种生物学功能和53个代谢路径,说明陆地棉响应黄萎病菌胁迫,是多种类型不同功能基因通过多种代谢和过程,通过上调和下调表达协同作用,以达到抗耐目的；②差异表达基因主要参与代谢、细胞过程、对刺激的反应和生物过程调控,分别占基因总数的26.9%、24.7%、14%和12.9%,最少的是生长和免疫过程,均只有0.37%；从细胞组份看,涉及细胞或细胞结构最多占65.4%,其次是细胞器和细胞器结构占28.0%,然后是大分子复合体及内膜内壁,分别占3.9%和1.9%；从分子功能看,最多的是催化活性和结合活性,分别占50%、42.5%,其它如分子转导、运输和受体活性占7.5%。从生物学功能看,除了通用功能预测占13.2%外,信号转导、翻译和翻译后修饰与蛋白折叠互作最多,各占11.4%。从参与的代谢路径看,这些基因主要参与基础代谢和次生物质代谢,分别占注释基因的33.33%和27.03%；其它代谢均在10%以下。③发现有三个上调基因FH11(calmodulin-related protein), FH42(elongation factor Tu), FH67(heat shock protein90)参与植物与病原菌的互作。这一结果提示钙信号介导诱导结构抗性、乙烯信号介导抗病和未知R介导抗病是陆地棉21号抗黄萎病的三条可能的途径。
(2)接菌诱导,采用双向电泳(2-DE)和串联飞行质谱(MALDI-TOF-MS)联用技术,鉴定到瑟伯氏棉57个上调表达差异蛋白点,代表了51个已知同源蛋白,占总蛋白点的11%。这些蛋白参与抗病抗逆、转录调控、蛋白质加工与降解、光合作用、产能和基础代谢等过程,表明瑟伯氏棉抗病性是多种基因协同作用的综合效应；同时,5个TIR-NBS-LRR抗病蛋白类似物集中上调表达,提示R基因在瑟伯氏棉抗黄萎病中可能起主导作用。
(3)克隆了两个陆地棉结构抗性基因GhDIR和GhSUMO。前者cDNA全长为768bp,开放读框525bp,编码175个氨基酸的蛋白,含有典型的dirigent-like结构域；系统进化分析表明,该基因与海岛棉的同源序列表现了最高的相似性；后者编码区全长为393bp,编码130个氨基酸的小蛋白,蛋白序列分析表明,该蛋白具有保守泛素结构域和C端双Gly的断裂/连接位点,以及保守的疏水表面和Ulp1-Smt3互作位点。系统进化分析表明,该蛋白与蓖麻的同源序列表现了最高的相似性。两基因均无内含子,均受黄萎病菌诱导表达。两个基因的克隆,为进一步研究陆地棉的诱导结构抗性机理奠定了基础。
(4)克隆了瑟伯氏棉根的GPIP基因,全长1165pb,开放阅读框1095pb,编码364个氨基酸残基。分析表明,该蛋白属LRR蛋白超家族,有一个信号肽和跨膜区,应属分泌型受体蛋白。基因组PCR表明,该基因无内含子。系统分析表明,该蛋白与高丽参(Panax ginseng)进化关系近而与陆地棉和海岛棉较远。定量结果显示,该基因在瑟伯氏棉根中接菌20小时,可诱导表达。
(5)克隆了瑟伯氏棉根的四个TIR-NBS-LRR类抗病基因类似物的cDNA全长,分别命名为ThTNLR1、ThTNLR2、ThTNLR3和ThTNLR4,长度分别为3149bp、2011bp、1379bp和4683bp。序列分析表明,均含有抗病相关的TIR、P-loop、Kinase-2和LRR等结构域。与已知同类抗病基因构建系统树,发现四者与烟草抗病毒基因N关系最接近,而与拟南芥的RPP系列基因和CS1基因较远。定量分析表明,四者在瑟伯氏棉根中,均受黄萎病菌诱导表达,其中前两个基因20小时诱导上调表达,而后两个基因则刚好相反。这四个基因的克隆,为进一步研究其互作和抗病功能奠定了基础。
Verticillium wilt is one of the major cotton diseases and has significantly affected both the yield and quality of cotton. Because of the lack of understanding of the mechanism of cotton disease resistance, the lack of existing cultivars to serve as sources of resistance, the breeding of Verticillium wilt resistant cottons has been unsuccessful. To reveal the mechanism of disease resistance in uplandcotton and wild cotton and identify key genes related to resistance, SSH、2-DE and MALDI-TOF-MS were employed to identify the differential expressed ESTs/proteins related to the disease resistance in cotton inoculated with Verticillium dahliae. Seven full-length cDNAs of genes related to the disease resistance were cloned.
(1) To analyze the differential gene expressions related to Verticillium wilt resistance, forward and reverse subtractive cDNA libraries were constructed by suppression subtractive hybridization (SSH). The Yumian21, designated as standard cultivar resistant to Verticillium wilt in China, was used as material, in which the cDNA from roots inoculated with medium pathogenicity W strain of Verticillium dahliae was used as tester and drive, and roots without inoculation as corresponding driver and tester. A total of169unigenes of early induced expression related to disease-resistance were enriched, including68up-regulated genes and91down-regulated genes. By means of Blast and cluster analysis in the six databases of Nr, Nt, Swissprot, GO,COG&KEGG,152genes were annotated successfully, and the other16unclear genes couldn't be annotated, which may represent the new genes. Results were as follows,(i) These genes which play19biological functions were divided into18biological processes and53metabolic pathways, and the coding proteins of which were the subunits of eight different cellular components. The results indicated that the response to Verticillium dahliae in upland cotton is complex.(ii) These gene expressions mainly involved in metabolic process, cellular process, response to stimulus, biological regulation and regulation of biological process. The percentages of the genes were26.9%,24.7%,14%and12.9%, respectively. The genes involved in growth and immune system process were only3.7%equally. From the perspective of cellular components, the genes involved in the cells or cell structures accounted for65.4%, and followed by organelles and organelle parts, accounting for28.0%.The percentages of the genes involved in Macrocomplexes and membrane-enclosed lumens were the least, accounting for3.9%and1.9%, respectively.For the molecular functions, the genes involved in catalytic activity and binding activity accounted for50%and42.5%, respectively. Others involved in molecular transduction, transport and receptor activity accounted for7.5%. For the biological functions, in addition to the genes involved in general function prediction accounting for13.2%, the genes involved in signal transduction and translation, post-translational modification and protein folding interactions occupied up to 11.4%equally. For the metabolic pathways, these genes mainly acted in basal metabolism and biosynthesis of secondary metabolites, accounting for33.33%and27.03%, respectively. The other genes were less than10%.(iii) Three up-regulated genes, including FH11(calmodulin-related protein), FH42(Elongation factor Tu), FH67(heat shock protein90) were involved in the plant-pathogen interaction. The result suggested that induced structural resistance manipulated by calcium signal, the disease-resistance pathway mediated by ethylene signal and the unknown R-mediated disease-resistance are likely to the three important pathways in upland cotton.
(2) Fifty-seven spotes of differentially expressed protein were identified in Gossipium thurberi. They represented51known proteins in protein database,which cover11%of the total protein spots in the2-DE gel. These proteins involved in disease and stress resistance, transcriptional regulation, protein processing and degradation, photosynthesis, energy production and basic metabolic processes. The results showed that resistance to Verticillium wilt in G. thurberi was the expression of multiple proteins combined effect of synergy. More importantly, expression of five disease resistance proteins were all up-regulated, suggesting that TIR-NBS-LRR like R-genes in Gossipium thurberi may play a leading role in resistance to Verticillium wilt.
(3) Using an EST of a dirigent-like gene from the SSH as the query probe to blast cotton EST database, a full-length768bp cDNA sequence of the dirigent-like gene, named GhDIR,was obtained and cloned by PCR. Sequence analysis indicated that it contained a complete open reading fragment (ORF), from70bp to594bp, encoding175amino acids, and had no intron. Sequence comparison and phylogenetic analysis showed the GhDIR cDNA was highly identical with its ortholog from Sea Island cotton, and the next most similar orthologs coming from other dicotyledons, but sharing low homology with monocotyledons. With the above technics, a SUMO gene, named GhSUMO,with a complete open reading fragment (ORF)396bp encoding a protein of95amino acids, was successfully cloned from Yumian21(uplandcotton). The GhSUMO was verified by PCR amplifications using the cDNA and DNA templates from the cotton root, and sequencing results showed that GhSUMO gene had not intron. Amino acid sequence analysis showed that the protein had a conserved ubiqitin domain, the C-terminal double Gly fracture/Connection site, a conservative hydrophobic surface and an Ulpl-Smt3interaction site. Sequence comparison and phylogenetic analysis showed the GhSUMO protein was highly identical with its ortholog from Castor (Ricinus communis), and the next most similar orthologs coming from other dicotyledons. Quantitative RT-PCR analysis showed that GhDIR and GhSUMO were activated in roots of Upland cotton inoculated with Verticillium dahliae. It meant that the two genes may play a role in V. wilt resistance.
(4) The PGIP gene of G.thurberi, named ThPGIP was cloned. Its full lenth was1165pb, ORF1095pb, encoding364amino acids. Sequence analysis showed that the PGIP belonged to a LRR super-family and shared a singal peptide and a transmembrane region. It should belong to the secretory protein. This gene had no intron. Sequence comparison and phylogenetic analysis showed the ThPGIP protein was highly identical with its ortholog from Panax ginseng, but sharing low homology with upland cotton and sea island cotton. Quantitative RT-PCR analysis showed that the ThPGIP was induced in roots inoculated with Verticillium dahliae post of20h in G.thurberi.
(5) The four full-length cDNA of TIR-NBS-LRR gene analogs, respectively named ThTNLRl, ThTNLR2, ThTNLR3, and ThTNLR4, were cloned from roots of G.Thurberi. The length of cDNAs were3149bp、2011bp、1379bp and4683bp respectively. The analysis of those sequences showed that they all had the conserved domains related to disease resistance, such as TIR, P-loop, Kinase-2, and LRR et al. The phylogenetic tree with others known resistance genes (R genes) suggested that there was the nearest distance with the N gene of tobacco, and there were further distance with the RPP series genes and CS1gene of Arabidopsis thaliana. The results of quantitative RT-PCR showed that their expressions were indused by V. dahliae in roots of G.Thurberi. The uprelated expressions of the two former genes were the observed at20h after inoculation with V. dahliae, however, the two latters were exactly the opposite. The cloning of the four genes established the foundation for researching the interaction of the genes and their function related to disease resistance further.
(1)以中等致病性棉花黄萎病菌W菌系接种诱导我国棉花抗黄萎病标准品种豫棉21号,构建了正反两个SSH文库,富集筛选到抗病相关的早期诱导表达Unigene169个,其中上调表达68个,下调表达91个。提交到NCBI的Nr和Nt核酸数据库、Swissprot蛋白数据库比对注释,并通过GO、COG和KEGG数据库进行组份、功能和代谢路径聚类分析,共解析了152个基因；另外16个基因为未能注释,可能代表了新发现基因。结果表明：①这些基因分属18种生物学过程、8种细胞组份和5种分子功能,集中于19种生物学功能和53个代谢路径,说明陆地棉响应黄萎病菌胁迫,是多种类型不同功能基因通过多种代谢和过程,通过上调和下调表达协同作用,以达到抗耐目的；②差异表达基因主要参与代谢、细胞过程、对刺激的反应和生物过程调控,分别占基因总数的26.9%、24.7%、14%和12.9%,最少的是生长和免疫过程,均只有0.37%；从细胞组份看,涉及细胞或细胞结构最多占65.4%,其次是细胞器和细胞器结构占28.0%,然后是大分子复合体及内膜内壁,分别占3.9%和1.9%；从分子功能看,最多的是催化活性和结合活性,分别占50%、42.5%,其它如分子转导、运输和受体活性占7.5%。从生物学功能看,除了通用功能预测占13.2%外,信号转导、翻译和翻译后修饰与蛋白折叠互作最多,各占11.4%。从参与的代谢路径看,这些基因主要参与基础代谢和次生物质代谢,分别占注释基因的33.33%和27.03%；其它代谢均在10%以下。③发现有三个上调基因FH11(calmodulin-related protein), FH42(elongation factor Tu), FH67(heat shock protein90)参与植物与病原菌的互作。这一结果提示钙信号介导诱导结构抗性、乙烯信号介导抗病和未知R介导抗病是陆地棉21号抗黄萎病的三条可能的途径。
(2)接菌诱导,采用双向电泳(2-DE)和串联飞行质谱(MALDI-TOF-MS)联用技术,鉴定到瑟伯氏棉57个上调表达差异蛋白点,代表了51个已知同源蛋白,占总蛋白点的11%。这些蛋白参与抗病抗逆、转录调控、蛋白质加工与降解、光合作用、产能和基础代谢等过程,表明瑟伯氏棉抗病性是多种基因协同作用的综合效应；同时,5个TIR-NBS-LRR抗病蛋白类似物集中上调表达,提示R基因在瑟伯氏棉抗黄萎病中可能起主导作用。
(3)克隆了两个陆地棉结构抗性基因GhDIR和GhSUMO。前者cDNA全长为768bp,开放读框525bp,编码175个氨基酸的蛋白,含有典型的dirigent-like结构域；系统进化分析表明,该基因与海岛棉的同源序列表现了最高的相似性；后者编码区全长为393bp,编码130个氨基酸的小蛋白,蛋白序列分析表明,该蛋白具有保守泛素结构域和C端双Gly的断裂/连接位点,以及保守的疏水表面和Ulp1-Smt3互作位点。系统进化分析表明,该蛋白与蓖麻的同源序列表现了最高的相似性。两基因均无内含子,均受黄萎病菌诱导表达。两个基因的克隆,为进一步研究陆地棉的诱导结构抗性机理奠定了基础。
(4)克隆了瑟伯氏棉根的GPIP基因,全长1165pb,开放阅读框1095pb,编码364个氨基酸残基。分析表明,该蛋白属LRR蛋白超家族,有一个信号肽和跨膜区,应属分泌型受体蛋白。基因组PCR表明,该基因无内含子。系统分析表明,该蛋白与高丽参(Panax ginseng)进化关系近而与陆地棉和海岛棉较远。定量结果显示,该基因在瑟伯氏棉根中接菌20小时,可诱导表达。
(5)克隆了瑟伯氏棉根的四个TIR-NBS-LRR类抗病基因类似物的cDNA全长,分别命名为ThTNLR1、ThTNLR2、ThTNLR3和ThTNLR4,长度分别为3149bp、2011bp、1379bp和4683bp。序列分析表明,均含有抗病相关的TIR、P-loop、Kinase-2和LRR等结构域。与已知同类抗病基因构建系统树,发现四者与烟草抗病毒基因N关系最接近,而与拟南芥的RPP系列基因和CS1基因较远。定量分析表明,四者在瑟伯氏棉根中,均受黄萎病菌诱导表达,其中前两个基因20小时诱导上调表达,而后两个基因则刚好相反。这四个基因的克隆,为进一步研究其互作和抗病功能奠定了基础。
Verticillium wilt is one of the major cotton diseases and has significantly affected both the yield and quality of cotton. Because of the lack of understanding of the mechanism of cotton disease resistance, the lack of existing cultivars to serve as sources of resistance, the breeding of Verticillium wilt resistant cottons has been unsuccessful. To reveal the mechanism of disease resistance in uplandcotton and wild cotton and identify key genes related to resistance, SSH、2-DE and MALDI-TOF-MS were employed to identify the differential expressed ESTs/proteins related to the disease resistance in cotton inoculated with Verticillium dahliae. Seven full-length cDNAs of genes related to the disease resistance were cloned.
(1) To analyze the differential gene expressions related to Verticillium wilt resistance, forward and reverse subtractive cDNA libraries were constructed by suppression subtractive hybridization (SSH). The Yumian21, designated as standard cultivar resistant to Verticillium wilt in China, was used as material, in which the cDNA from roots inoculated with medium pathogenicity W strain of Verticillium dahliae was used as tester and drive, and roots without inoculation as corresponding driver and tester. A total of169unigenes of early induced expression related to disease-resistance were enriched, including68up-regulated genes and91down-regulated genes. By means of Blast and cluster analysis in the six databases of Nr, Nt, Swissprot, GO,COG&KEGG,152genes were annotated successfully, and the other16unclear genes couldn't be annotated, which may represent the new genes. Results were as follows,(i) These genes which play19biological functions were divided into18biological processes and53metabolic pathways, and the coding proteins of which were the subunits of eight different cellular components. The results indicated that the response to Verticillium dahliae in upland cotton is complex.(ii) These gene expressions mainly involved in metabolic process, cellular process, response to stimulus, biological regulation and regulation of biological process. The percentages of the genes were26.9%,24.7%,14%and12.9%, respectively. The genes involved in growth and immune system process were only3.7%equally. From the perspective of cellular components, the genes involved in the cells or cell structures accounted for65.4%, and followed by organelles and organelle parts, accounting for28.0%.The percentages of the genes involved in Macrocomplexes and membrane-enclosed lumens were the least, accounting for3.9%and1.9%, respectively.For the molecular functions, the genes involved in catalytic activity and binding activity accounted for50%and42.5%, respectively. Others involved in molecular transduction, transport and receptor activity accounted for7.5%. For the biological functions, in addition to the genes involved in general function prediction accounting for13.2%, the genes involved in signal transduction and translation, post-translational modification and protein folding interactions occupied up to 11.4%equally. For the metabolic pathways, these genes mainly acted in basal metabolism and biosynthesis of secondary metabolites, accounting for33.33%and27.03%, respectively. The other genes were less than10%.(iii) Three up-regulated genes, including FH11(calmodulin-related protein), FH42(Elongation factor Tu), FH67(heat shock protein90) were involved in the plant-pathogen interaction. The result suggested that induced structural resistance manipulated by calcium signal, the disease-resistance pathway mediated by ethylene signal and the unknown R-mediated disease-resistance are likely to the three important pathways in upland cotton.
(2) Fifty-seven spotes of differentially expressed protein were identified in Gossipium thurberi. They represented51known proteins in protein database,which cover11%of the total protein spots in the2-DE gel. These proteins involved in disease and stress resistance, transcriptional regulation, protein processing and degradation, photosynthesis, energy production and basic metabolic processes. The results showed that resistance to Verticillium wilt in G. thurberi was the expression of multiple proteins combined effect of synergy. More importantly, expression of five disease resistance proteins were all up-regulated, suggesting that TIR-NBS-LRR like R-genes in Gossipium thurberi may play a leading role in resistance to Verticillium wilt.
(3) Using an EST of a dirigent-like gene from the SSH as the query probe to blast cotton EST database, a full-length768bp cDNA sequence of the dirigent-like gene, named GhDIR,was obtained and cloned by PCR. Sequence analysis indicated that it contained a complete open reading fragment (ORF), from70bp to594bp, encoding175amino acids, and had no intron. Sequence comparison and phylogenetic analysis showed the GhDIR cDNA was highly identical with its ortholog from Sea Island cotton, and the next most similar orthologs coming from other dicotyledons, but sharing low homology with monocotyledons. With the above technics, a SUMO gene, named GhSUMO,with a complete open reading fragment (ORF)396bp encoding a protein of95amino acids, was successfully cloned from Yumian21(uplandcotton). The GhSUMO was verified by PCR amplifications using the cDNA and DNA templates from the cotton root, and sequencing results showed that GhSUMO gene had not intron. Amino acid sequence analysis showed that the protein had a conserved ubiqitin domain, the C-terminal double Gly fracture/Connection site, a conservative hydrophobic surface and an Ulpl-Smt3interaction site. Sequence comparison and phylogenetic analysis showed the GhSUMO protein was highly identical with its ortholog from Castor (Ricinus communis), and the next most similar orthologs coming from other dicotyledons. Quantitative RT-PCR analysis showed that GhDIR and GhSUMO were activated in roots of Upland cotton inoculated with Verticillium dahliae. It meant that the two genes may play a role in V. wilt resistance.
(4) The PGIP gene of G.thurberi, named ThPGIP was cloned. Its full lenth was1165pb, ORF1095pb, encoding364amino acids. Sequence analysis showed that the PGIP belonged to a LRR super-family and shared a singal peptide and a transmembrane region. It should belong to the secretory protein. This gene had no intron. Sequence comparison and phylogenetic analysis showed the ThPGIP protein was highly identical with its ortholog from Panax ginseng, but sharing low homology with upland cotton and sea island cotton. Quantitative RT-PCR analysis showed that the ThPGIP was induced in roots inoculated with Verticillium dahliae post of20h in G.thurberi.
(5) The four full-length cDNA of TIR-NBS-LRR gene analogs, respectively named ThTNLRl, ThTNLR2, ThTNLR3, and ThTNLR4, were cloned from roots of G.Thurberi. The length of cDNAs were3149bp、2011bp、1379bp and4683bp respectively. The analysis of those sequences showed that they all had the conserved domains related to disease resistance, such as TIR, P-loop, Kinase-2, and LRR et al. The phylogenetic tree with others known resistance genes (R genes) suggested that there was the nearest distance with the N gene of tobacco, and there were further distance with the RPP series genes and CS1gene of Arabidopsis thaliana. The results of quantitative RT-PCR showed that their expressions were indused by V. dahliae in roots of G.Thurberi. The uprelated expressions of the two former genes were the observed at20h after inoculation with V. dahliae, however, the two latters were exactly the opposite. The cloning of the four genes established the foundation for researching the interaction of the genes and their function related to disease resistance further.
引文
程红梅,简桂良,倪万潮等.转几丁质酶和p-1,3-葡聚糖酶基因提高棉花对枯萎病和黄萎病的抗性.中国农业科学,2005,38(6)：1160-1166
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