福建桉树焦枯病菌鉴定及其诱导下桉树转录组和蛋白组学研究
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摘要
桉树（Eucalyptus spp.）是联合国粮农组织推荐的与松、杨齐名的速生丰产多用途树种。Calonectria spp.地域分布广、种类繁多、致病性强，其侵染桉树产生的桉树焦枯病（Cylindrocladium leaf blight）是热带、亚热带地区桉树商品林种植和苗木生产极具潜在危险性病害之一。从分子抗病机制角度研究桉树如何响应焦枯病菌的侵染对桉树抗焦枯病优良种系选育具有重要的现实指导意义。目前，相关研究报道主要从生理生化和形态结构水平探讨桉树对焦枯病菌的防御作用，而基因和蛋白质水平的研究鲜有报道。本研究以前期抗性筛选的福建主栽抗病种系尾细桉M1（E. urophylla×E. tereticornis M1）为材料，应用转录组学和蛋白组学，从差异表达基因和蛋白质层面探讨了焦枯病菌胁迫下桉树的响应情况，同时采用形态学结合系统发育树构建方法对福建省收集的Calonectria spp.进行分类鉴定，以及致病性测定，旨在了解福建省焦枯病菌分类地位，科学指导桉树焦枯病防治。研究初步成果如下：
（1）通过形态特征描述结合BT、HIS3和TEF-1α等3个基因联合序列系统发育树分析，将焦枯病菌16个供试菌株鉴定为Ca. pseudoreteaudii、Ca.pseudocolhounii和Ca. kyotensis3个种。致病性测定结果表明，Ca.pseudoreteaudii、Ca. pseudocolhounii和Ca. kyotensis能够侵染不同抗性桉树叶片，其致病力依次减弱。焦枯病菌的收集与鉴定，对掌握Calonectria的分布动态，加强预测预报和植物检疫防控桉树焦枯病具有重要意义。
（2）运用RNA-seq技术，对接种焦枯病菌Ca. pseudoreteaudii后第12h（潜伏期）及第24h（显症期）尾细桉M1叶片转录组进行高通量测序，将测序结果与巨桉（Eucalyptus grandis）基因组比对，并通过qRT-PCR进行验证，基因功能注释后，分析了接种Ca. pseudoreteaudii后基因的差异表达情况，并对差异基因进行GO和Pathway富集分析。结果表明：①Ca. pseudoreteaudii接种12h和24h后的差异表达基因分别为6956和7422，其中差异倍数|log2Ratio|≥15的基因分别有54个和117个，显著性富集的pathway分别有26条和28条，其中大部分pathway与植物的抗逆响应密切相关；②呼吸代谢途径相关基因上调表达，包括糖酵解、戊糖磷酸途径及三羧酸循环，这暗示了尾细桉M1在Ca. pseudoreteaudii侵染下，可能通过加强呼吸来提高对病原菌的抵御能力；③桉树在Ca.pseudoreteaudii胁迫下启动多条抗病信号通路，包括SA途径、JA/ET途径、BRs途径、CTK及Auxin途径、MAPK信号途径，其中CTK及Auxin途径基因下调表达，研究推测，作为速生植物，在受Ca. pseudoreteaudii胁迫时，尾细桉M1可能通过减缓生长速度来提高防御水平；④多个抗氧化相关基因表达发生变化，表明在Ca. pseudoreteaudii胁迫下，尾细桉M1可能通过调整活性氧清除剂的表达水平，以维持体内活性氧的平衡状态；⑤尾细桉M1苯丙烷类代谢途径及类异戊二烯代谢途径相关基因上调表达，表明尾细桉M1可能通过加强次生代谢物质（如木质素、酚类化合物、类异戊二烯化合物等）的合成来制造物理或化学障碍，以限制Ca. pseudoreteaudii的定殖及进一步扩展；⑥在尾细桉M1与焦枯病菌Ca.pseudoreteaudii互作过程中，调控因子RIN4基因下调表达，下游因子RPM1基因上调表达，这可能是尾细桉M1抗焦枯病菌的重要原因之一。
（3）在转录组学研究的基础上，运用iTRAQ技术对经Ca. pseudoreteaudii诱导尾细桉M1叶片差异蛋白组进行研究，差异蛋白GO功能注释和Pathway富集分析后，进一步将差异蛋白与差异基因进行关联分析，最后筛选出与转录组关联性较强的抗病相关蛋白。结果表明：①Ca. pseudoreteaudii接种后12h，尾细桉M1叶片的差异基因及差异蛋白均显著富集于苯丙烷类代谢，类黄酮生物合成，亚麻酸代谢及代谢途径，而24h的差异基因和蛋白则显著富集在亚麻酸代谢，次生代谢物质合成，萜类化合物生物合成，半乳糖代谢，外芪类化合物、二芳基庚醇及姜辣素生物合成，类黄酮生物合成以及代谢途径，这些代谢途径均直接或间接地参与了植物的抗病反应；②焦枯病菌接种后12h尾细桉M1叶片转录组与蛋白组关联性较差，相关性仅为0.2935，而24h的关联性较好，相关性为0.6985；③通过筛选共获得128个与转录组关联性较强的差异蛋白，其中下调表达65个，上调表达63个。这些蛋白有的在焦枯病菌接种后持续表达，有的蛋白则在接种后12h或24h特异性表达。其中多数差异蛋白参与了植物的抗逆响应，如谷胱甘肽S-转移酶、苯丙氨酸解氨酶、丙二烯氧化物合成酶、二磷酸甲羟戊酸脱羧酶、病程相关蛋白、过氧化物酶、几丁质酶、脂氧合酶、脱水蛋白、枯草杆菌蛋白酶、筛管阻塞蛋白等。
Eucalyptus spp. being of versatile usage, is considered to be fast-growing andhigh-yielding trees resembling to pine and poplar by United Nations Food andAgriculture Organization. Calonectria spp. with numerous species, wide globaldistribution and strong pathogenicity, is the pathogen of Cylindrocladium leaf blight,which is the one of the most growing threats to Eucalyptus plantation and nursery intropic and subtropic areas. How Eucalyptus spp. responses to infection by Calonectriaplays an important role in guiding the selection for excellent Eucalyptus spp. cultivarresistant to Calonectria spp.. To date, related researches exploring defense mechanismof Eucalyptus to Calonectria spp. mainly focuses on the level of morphologicalstructure, physiology and biochemistry, rare on the protein and gene level. In thispaper, proteomics and transcriptomics were used to explore the impact of Ca.pseudoreteaudii on E. urophylla×E. tereticornis at the level of differential expressedgene and protein. At the same time, Calonectria spp. collected from Fujian Provincewere identified employing morphological characteristics and phylogenetic inference,and the pathogenicity was tested. The preliminary results showed as follows:
(1) For the purpose of understanding dynamic distribution of Calonectria spp. inFujian Province, representive Calonectria spp collected from Eucalyptus commercialplantations and nurseries were identified as Ca. pseudoreteaudii、Ca. pseudocolhouniiand Ca. kyotensis employing morphological characteristics combining with DNAsequence comparisons for the β-tubulin, histone H3and translation elongationfactor-1α gene regions. And it would pay contribution to Cylindrocladium leaf blightprevention by means of forecasting and quarantine. Pathogenicity tests showed thatCa. pseudoreteaudii、Ca. pseudocolhounii and Ca. kyotensis were able to infectEucalyptus with different pathogenicity, and their pathogenicity manifested as Ca.pseudoreteaudii＞Ca. pseudocolhounii＞Ca. kyotensis. Pathogenicity tests wouldpropose that resistant cultivar to Calonectria spp. should be chosen for plantationfrom now on.
(2) Leaves of E. urophylla×E. tereticornis M1after inoculating with Ca.pseudoreteaudii for12h and24h were used for testing materials. Both of the leaves’transcriptomics were analyzed by RNA-seq. The sequencing reads were then mappedto the reference genome sequence of Eucalyptus grandis. After the functionalannotation of the genes, the GO and KEGG Pathway enrichment analysis were carriedout, and six differentially expressed genes were confirmed by quantitative real-timePCR (qRT-PCR). The results showed as follows:①For12h and24h after inoculation,the differentially expressed genes were6956and7422respectively, among which thefold changes over15were54and117. Digital expressed genes involving inenrichment pathway were26at12h after inoculation, while24h were28, and most ofthem were closely related with the plant’s response to stress.②Genes relating with respiratory metabolism were up-regulated, including embden-meyerhof-parnas pathway,pentose phosphate pathway and tricarboxylic acid cycle, which suggested that E.urophylla×E. tereticornis M1was likely to strengthen the respiratory to defense theinfection of Ca. pseudoreteaudii.③Several signaling pathways regulateddisease-resistance were activated after the inoculation of Ca. pseudoreteaudii, they wereSApathway, JA/ET pathway, BRs pathway, CTK and Auxin pathway and MAPK signalpathway. Genes involving in CTK and Auxin pathways were down-regulated. Therefore,the paper suggested that being as fast-growing tree, E. urophylla×E. tereticornis, mayslow down the growth rate to enhance resistance against Ca. pseudoreteaudii.④Theexpression level of a variety of genes related to antioxidation altered under the stressof Ca. pseudoreteaudii. It demonstrated that E. urophylla×E. tereticornis M1maymediate the expression of antioxidant to maintain the status of the balance of reactiveoxygen species (ROS).⑤Genes involved in phenylpropanoid metabolism andisoprenoid metabolism were up-regulated, which indicated that E. urophylla×E.tereticornis M1may protect the plants from Ca. pseudoreteaudii by accelerating thesynthesis of secondary substances, such as lignin, phenolic compounds, andisoprenoid compounds.⑥RIN4, a negative regulator associated with plant-pathogeninteraction, was found down-regulated, and RPM1which was a positive regulator inthe downstream was up-regulated. So the paper inferred that this may contribute to theresistance of E. urophylla×E. tereticornis M1to Ca.pseudoreteaudii.
(3)On the basis of transcriptomes, the differential proteomics of the leaves,inoculated with Ca. pseudoreteaudii, were analyzed by iTRAQ technology, and GO andpathway analysis were further performed to determine which differentially expressedproteins were remarkably enriched. Then, the correlation analysis between proteomicsand transcriptomes were conducted. Finally, disease resistant proteins, obviouslyassociated with transcriptome, were screened. The results were as followed:①Differentially expressed proteins and their genes of the leaves were all enriched onphenylalanine metabolism, flavonoid biosynthesis, Linoleic acid metabolism andmetabolic pathways after infection with Ca. pseudoreteaudii for12h, while enriched onLinoleic acid metabolism, biosynthesis of secondary metabolites, terpenoid backbonebiosynthesis, galactose metabolism, stilbenoid, diarylheptanoid and gingerolbiosynthesis, flavonoid biosynthesis and metabolic pathways after inoculated with Ca.pseudoreteaudii for24h. Those pathways were directly or indirectly related withdisease reistance.②The correlation analysises showed that after infection with Ca.pseudoreteaudii for12h, the correlation between the proteomics and transcriptomeswas low (r=0.2935), while the24h was higher (r=0.6985).③128differential proteinswith high correlation were screened, and65proteins were down-regulated and63up-regulated. For those proteins, some were continuously expressed induced by Ca.pseudoreteaudii, some were specifically expressed after induced by Ca. pseudoreteaudiiat12hor24h. Most differentialproteinswere closelyrelatedto plant’s stress resistance, such asglutathione S-transferases, phenylalnine ammonialyase, allene oxide synthase,diphosphomevalonate decarboxylase, pathogenesis-related proteins, peroxidase,chitinase, lipoxygenase, dehydrins, subtilisin and sieve element occlusion.
（1）通过形态特征描述结合BT、HIS3和TEF-1α等3个基因联合序列系统发育树分析，将焦枯病菌16个供试菌株鉴定为Ca. pseudoreteaudii、Ca.pseudocolhounii和Ca. kyotensis3个种。致病性测定结果表明，Ca.pseudoreteaudii、Ca. pseudocolhounii和Ca. kyotensis能够侵染不同抗性桉树叶片，其致病力依次减弱。焦枯病菌的收集与鉴定，对掌握Calonectria的分布动态，加强预测预报和植物检疫防控桉树焦枯病具有重要意义。
（2）运用RNA-seq技术，对接种焦枯病菌Ca. pseudoreteaudii后第12h（潜伏期）及第24h（显症期）尾细桉M1叶片转录组进行高通量测序，将测序结果与巨桉（Eucalyptus grandis）基因组比对，并通过qRT-PCR进行验证，基因功能注释后，分析了接种Ca. pseudoreteaudii后基因的差异表达情况，并对差异基因进行GO和Pathway富集分析。结果表明：①Ca. pseudoreteaudii接种12h和24h后的差异表达基因分别为6956和7422，其中差异倍数|log2Ratio|≥15的基因分别有54个和117个，显著性富集的pathway分别有26条和28条，其中大部分pathway与植物的抗逆响应密切相关；②呼吸代谢途径相关基因上调表达，包括糖酵解、戊糖磷酸途径及三羧酸循环，这暗示了尾细桉M1在Ca. pseudoreteaudii侵染下，可能通过加强呼吸来提高对病原菌的抵御能力；③桉树在Ca.pseudoreteaudii胁迫下启动多条抗病信号通路，包括SA途径、JA/ET途径、BRs途径、CTK及Auxin途径、MAPK信号途径，其中CTK及Auxin途径基因下调表达，研究推测，作为速生植物，在受Ca. pseudoreteaudii胁迫时，尾细桉M1可能通过减缓生长速度来提高防御水平；④多个抗氧化相关基因表达发生变化，表明在Ca. pseudoreteaudii胁迫下，尾细桉M1可能通过调整活性氧清除剂的表达水平，以维持体内活性氧的平衡状态；⑤尾细桉M1苯丙烷类代谢途径及类异戊二烯代谢途径相关基因上调表达，表明尾细桉M1可能通过加强次生代谢物质（如木质素、酚类化合物、类异戊二烯化合物等）的合成来制造物理或化学障碍，以限制Ca. pseudoreteaudii的定殖及进一步扩展；⑥在尾细桉M1与焦枯病菌Ca.pseudoreteaudii互作过程中，调控因子RIN4基因下调表达，下游因子RPM1基因上调表达，这可能是尾细桉M1抗焦枯病菌的重要原因之一。
（3）在转录组学研究的基础上，运用iTRAQ技术对经Ca. pseudoreteaudii诱导尾细桉M1叶片差异蛋白组进行研究，差异蛋白GO功能注释和Pathway富集分析后，进一步将差异蛋白与差异基因进行关联分析，最后筛选出与转录组关联性较强的抗病相关蛋白。结果表明：①Ca. pseudoreteaudii接种后12h，尾细桉M1叶片的差异基因及差异蛋白均显著富集于苯丙烷类代谢，类黄酮生物合成，亚麻酸代谢及代谢途径，而24h的差异基因和蛋白则显著富集在亚麻酸代谢，次生代谢物质合成，萜类化合物生物合成，半乳糖代谢，外芪类化合物、二芳基庚醇及姜辣素生物合成，类黄酮生物合成以及代谢途径，这些代谢途径均直接或间接地参与了植物的抗病反应；②焦枯病菌接种后12h尾细桉M1叶片转录组与蛋白组关联性较差，相关性仅为0.2935，而24h的关联性较好，相关性为0.6985；③通过筛选共获得128个与转录组关联性较强的差异蛋白，其中下调表达65个，上调表达63个。这些蛋白有的在焦枯病菌接种后持续表达，有的蛋白则在接种后12h或24h特异性表达。其中多数差异蛋白参与了植物的抗逆响应，如谷胱甘肽S-转移酶、苯丙氨酸解氨酶、丙二烯氧化物合成酶、二磷酸甲羟戊酸脱羧酶、病程相关蛋白、过氧化物酶、几丁质酶、脂氧合酶、脱水蛋白、枯草杆菌蛋白酶、筛管阻塞蛋白等。
Eucalyptus spp. being of versatile usage, is considered to be fast-growing andhigh-yielding trees resembling to pine and poplar by United Nations Food andAgriculture Organization. Calonectria spp. with numerous species, wide globaldistribution and strong pathogenicity, is the pathogen of Cylindrocladium leaf blight,which is the one of the most growing threats to Eucalyptus plantation and nursery intropic and subtropic areas. How Eucalyptus spp. responses to infection by Calonectriaplays an important role in guiding the selection for excellent Eucalyptus spp. cultivarresistant to Calonectria spp.. To date, related researches exploring defense mechanismof Eucalyptus to Calonectria spp. mainly focuses on the level of morphologicalstructure, physiology and biochemistry, rare on the protein and gene level. In thispaper, proteomics and transcriptomics were used to explore the impact of Ca.pseudoreteaudii on E. urophylla×E. tereticornis at the level of differential expressedgene and protein. At the same time, Calonectria spp. collected from Fujian Provincewere identified employing morphological characteristics and phylogenetic inference,and the pathogenicity was tested. The preliminary results showed as follows:
(1) For the purpose of understanding dynamic distribution of Calonectria spp. inFujian Province, representive Calonectria spp collected from Eucalyptus commercialplantations and nurseries were identified as Ca. pseudoreteaudii、Ca. pseudocolhouniiand Ca. kyotensis employing morphological characteristics combining with DNAsequence comparisons for the β-tubulin, histone H3and translation elongationfactor-1α gene regions. And it would pay contribution to Cylindrocladium leaf blightprevention by means of forecasting and quarantine. Pathogenicity tests showed thatCa. pseudoreteaudii、Ca. pseudocolhounii and Ca. kyotensis were able to infectEucalyptus with different pathogenicity, and their pathogenicity manifested as Ca.pseudoreteaudii＞Ca. pseudocolhounii＞Ca. kyotensis. Pathogenicity tests wouldpropose that resistant cultivar to Calonectria spp. should be chosen for plantationfrom now on.
(2) Leaves of E. urophylla×E. tereticornis M1after inoculating with Ca.pseudoreteaudii for12h and24h were used for testing materials. Both of the leaves’transcriptomics were analyzed by RNA-seq. The sequencing reads were then mappedto the reference genome sequence of Eucalyptus grandis. After the functionalannotation of the genes, the GO and KEGG Pathway enrichment analysis were carriedout, and six differentially expressed genes were confirmed by quantitative real-timePCR (qRT-PCR). The results showed as follows:①For12h and24h after inoculation,the differentially expressed genes were6956and7422respectively, among which thefold changes over15were54and117. Digital expressed genes involving inenrichment pathway were26at12h after inoculation, while24h were28, and most ofthem were closely related with the plant’s response to stress.②Genes relating with respiratory metabolism were up-regulated, including embden-meyerhof-parnas pathway,pentose phosphate pathway and tricarboxylic acid cycle, which suggested that E.urophylla×E. tereticornis M1was likely to strengthen the respiratory to defense theinfection of Ca. pseudoreteaudii.③Several signaling pathways regulateddisease-resistance were activated after the inoculation of Ca. pseudoreteaudii, they wereSApathway, JA/ET pathway, BRs pathway, CTK and Auxin pathway and MAPK signalpathway. Genes involving in CTK and Auxin pathways were down-regulated. Therefore,the paper suggested that being as fast-growing tree, E. urophylla×E. tereticornis, mayslow down the growth rate to enhance resistance against Ca. pseudoreteaudii.④Theexpression level of a variety of genes related to antioxidation altered under the stressof Ca. pseudoreteaudii. It demonstrated that E. urophylla×E. tereticornis M1maymediate the expression of antioxidant to maintain the status of the balance of reactiveoxygen species (ROS).⑤Genes involved in phenylpropanoid metabolism andisoprenoid metabolism were up-regulated, which indicated that E. urophylla×E.tereticornis M1may protect the plants from Ca. pseudoreteaudii by accelerating thesynthesis of secondary substances, such as lignin, phenolic compounds, andisoprenoid compounds.⑥RIN4, a negative regulator associated with plant-pathogeninteraction, was found down-regulated, and RPM1which was a positive regulator inthe downstream was up-regulated. So the paper inferred that this may contribute to theresistance of E. urophylla×E. tereticornis M1to Ca.pseudoreteaudii.
(3)On the basis of transcriptomes, the differential proteomics of the leaves,inoculated with Ca. pseudoreteaudii, were analyzed by iTRAQ technology, and GO andpathway analysis were further performed to determine which differentially expressedproteins were remarkably enriched. Then, the correlation analysis between proteomicsand transcriptomes were conducted. Finally, disease resistant proteins, obviouslyassociated with transcriptome, were screened. The results were as followed:①Differentially expressed proteins and their genes of the leaves were all enriched onphenylalanine metabolism, flavonoid biosynthesis, Linoleic acid metabolism andmetabolic pathways after infection with Ca. pseudoreteaudii for12h, while enriched onLinoleic acid metabolism, biosynthesis of secondary metabolites, terpenoid backbonebiosynthesis, galactose metabolism, stilbenoid, diarylheptanoid and gingerolbiosynthesis, flavonoid biosynthesis and metabolic pathways after inoculated with Ca.pseudoreteaudii for24h. Those pathways were directly or indirectly related withdisease reistance.②The correlation analysises showed that after infection with Ca.pseudoreteaudii for12h, the correlation between the proteomics and transcriptomeswas low (r=0.2935), while the24h was higher (r=0.6985).③128differential proteinswith high correlation were screened, and65proteins were down-regulated and63up-regulated. For those proteins, some were continuously expressed induced by Ca.pseudoreteaudii, some were specifically expressed after induced by Ca. pseudoreteaudiiat12hor24h. Most differentialproteinswere closelyrelatedto plant’s stress resistance, such asglutathione S-transferases, phenylalnine ammonialyase, allene oxide synthase,diphosphomevalonate decarboxylase, pathogenesis-related proteins, peroxidase,chitinase, lipoxygenase, dehydrins, subtilisin and sieve element occlusion.
引文
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