坛紫菜响应失水胁迫的转录组和表达谱特征分析
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摘要
坛紫菜是我国特有的海洋经济作物，主要在我国的南方海域被大面积栽培，占据我国栽培紫菜总产量的75%。坛紫菜也是研究潮间带藻类生理生态以及逆境胁迫适应机制的代表性模式物种。但是，目前对坛紫菜的研究仍然比较有限，其全基因组信息不够全面，对于其适应潮间带逆境的分子机制也缺乏系统深入的调查。
本研究利用Illumina高通量测序技术开展了坛紫菜转录组测序以及失水/复水胁迫条件的表达谱特征分析，同时也利用454测序结合Sanger测序方法获得了完整的质体基因组序列。通过全面、系统地了解坛紫菜转录组特性，并深入探索坛紫菜响应失水/复水胁迫环境的分子机制，为了解坛紫菜适应潮间带失水胁迫环境的机制提供新认识，也为未来抗逆育种工作提供新参考。
主要结果如下：
（1）利用Illumina高通量测序技术对不同发育时期和不同胁迫处理的坛紫菜混合RNA样品进行转录组测序，共获得47,764,168条干净的短读长序列，碱基总量约为4.5G，拼接后得到28,536条平均长度为584bp的Unigenes。通过与多种数据库进行比对注释，发现坛紫菜转录组中包含大量响应失水胁迫、温度胁迫、光胁迫、营养盐缺乏等逆境胁迫以及抗氧化系统等相关功能基因，也发现许多发育过程相关功能基因。并且首次在红藻中发现Group1类型的晚期胚胎发育富集蛋白（LEA）同源序列，以及红藻中未曾报道过的矾依赖的卤过氧化物酶（vHPO）基因的同源序列。通过KEGG代谢途径分析，发现了坛紫菜中包含284条代谢途径，其中包括与逆境胁迫相关的细胞凋亡途径和MAPK信号途径（包含哺乳动物JNK和p38类型MAPK途径和酵母MAPK途径相关的许多酶类基因）。与数据库比对之后，仍然有10,378条Unigenes（36.4%）没有找到同源序列，说明可能存在大量功能未知的新基因。
（2）为了研究坛紫菜响应失水胁迫环境的表达谱特征，将坛紫菜配子体在不同失水率和复水胁迫条件处理的8个样品分别建库和Illumina测序（每个处理组设置两个生物学重复），每个处理组样品获得11.83M-15.04M干净的短读长序列，且与坛紫菜转录组比对（map）上的短读长序列数占短读长序列总数的96.78%-97.74%。每个处理组内生物学重复之间表达水平相关性较高（R∧2为0.916～0.941）。通过分析中度失水胁迫条件下基因表达的总体模式（与对照组相比），发现1681个基因显著差异表达。首次发现多种新基序类型的MAPK，其中新的TQA基序类型MAPK参与响应失水胁迫的信号转导过程。10个分子伴侣/共陪伴蛋白基因（包括HSP90和HSP70家族成员、HSP70共陪伴蛋白）在中度失水胁迫下上调表达，而Hsp33和HSP60家族成员呈组成性表达。同时，抗氧化系统中的过氧化物氧化还原酶和Fe-SOD呈现组成性表达来清除活性氧；蛋白质二硫化异构酶上调表达来参与修复中度失水胁迫下的氧化性损伤。细胞凋亡诱导过程也参与到耐受中度失水胁迫，而且线粒体在坛紫菜细胞凋亡诱导过程中起中心调节作用。与中度失水相比，在重度失水胁迫条件下仅18个基因显著差异表达，表明两个处理组之间基因表达模式比较相似。与重度失水胁迫相比，在复水过程中有1199个基因显著差异表达，其中1个参与细胞凋亡诱导的Caspases激活物和HSP70的共陪伴蛋白均显著下调表达，而抗氧化系统中硫氧还蛋白通过上调表达来修复复水过程中的氧化性损伤。
（3）利用454测序结合Sanger测序技术获得坛紫菜和条斑紫菜完整的质体基因组序列。这两种紫菜的环形质体基因组大小分别为195,597bp和191,975bp，是目前已测序的红色支系中最大的质体基因组。这两个基因组的基因内容相似，包含211-213个蛋白质编码基因、37个tRNA基因和6个rRNA基因，显示了红色支系中最大的编码容量。每个基因组中有14个蛋白质基因重叠，且所有基因均没有内含子，揭示了高度紧凑的质体基因组。Pyropia属的质体基因组保留了古老的基因内容和保守的基因簇，也包含了几乎完整的一套已知光合真核生物的质体基因集。基于整个质体基因组序列的相似性分析显示坛紫菜与条斑紫菜间的遗传距离（0.146）小于Porphyra purpurea与坛紫菜的距离（0.250）以及与条斑紫菜的距离（0.251）。这个结果支持了将坛紫菜和条斑紫菜划分到新属Pyropia中，而保留P. purpure在Porphyra属中的分类修订。系统发生分析显示虽然多细胞红藻与chromists的系统发生关系没有完全解决，但是支持红毛菜纲和真红藻纲之间以及Pyropia和Porphyra之间的姐妹关系。通过结合转录组和表达谱的结果发现核编码的Sigma因子和镁螯合酶活性变化介导了响应失水胁迫下核基因和质体基因的协调表达。
Pyropia haitanensis is an economically important marine crop, which has beencultivated widely along the coasts of South China, accounting for75%of the totaloutput of cultivated Pyropia in China. P. haitanensis is also considered to be researchmodels for studying physiological ecology and the molecular mechanisms for stresstolerance of intertidal seaweed communities. However, for P. haitanensis, limitedstudies have been conducted. So far, the genomic information on Pyropiaremains incomplete, and systematic molecular investigations of the mechanisms foracclimation to intertidal stress environment are very lacking at present.
Using Illumna high-throughout sequencing technology, the transcriptome andexpression profiles of P. haitanensis were sequenced and analyzed. And using454and Sanger sequencing technology, the complete plastid genomes of P. hatanensis andP. yezoensis were fully sequenced. Comprehensive and systematic study oftranscriptomic characteristics and deep exploration of molecular mechanism forresponse to the dehydration/rehydration stress environment will not only provide newunderstanding of the mechanisms for response to intertidal desiccation stressenvironment, but also provide new reference for stress-resistance breeding in future.
The major findings are as follows:
The global transcriptome of P. haitanensis was sequenced using Illuminahigh-throughput sequencing technology. A total of47,764,168clean reads (4.5Gbclean bases) were generated from the cDNA library constructed for a RNA mixture ofP. hatanensis at different development stages and under different stress treatments.These clean reads were assembled into28,536unigenes with a mean length of584bp.Based on sequence similarity searches with known proteins, a large number of genesrelated to stress response were found, including genes related to desiccation stress,temperature stress, light stress, starvation, antioxidant system and other genes relatedto stress processes, and of which group1type LEA and vanadium-dependent haloperoxidase (vHPO) homologous sequences were firstly reported. And Manygenes related to developmental process were also found in P. hatanensis. Searchingagainst the KEGG database indicated that there existed284KEGG pathways intranscriptome of P. hatanensis, including apoptosis pathway and MAPK signalingpathways related to stress environment. The MAPK signaling pathways contain manygenes involved in mammalian JNK and p38type MAPK pathway and yeast MAPKpathway. After annotation, there are still10,378unigenes unannotated (36.4%),indicating that there may be a lot of novel genes with unknown function.
In order to study the expression profile characteristics in response to desiccationstress environment in P. hatanensis, the cDNA library was constructed for eightsamples from the different dehydration and rehydration stress treatments and thensequenced by Illumina sequencing technology (two biological replicates for eachtreatment). A total of11.83M-15.04M clean reads were abtained for each sample.Moreover, the number of reads mapped to transcriptome is96.78%-97.74%of thetotal reads number. Within each treatment, correlation of gene expression levelsbetween two biological replicates was high (R∧2=0.916-0.941). By analysis of theoverall pattern of gene expression during moderate dehydration (compared with thecontrol group), a total of1681differentially expressed genes were identified. Avariety of new motif type MAPKs were firstly found, and of which the new TQAmotif type MAPK was involved in signal transduction pathway in response to thedehydration stress. A total of10molecular chaperones genes (including the membersof HSP90superfamily, HSP70superfamily and cochaperone proteins of HSP70) weresignificantly up-regulated in response to the moderate dehydration stress，whereas themembers of HSP60superfamily and the Hsp33were expressed constitutively.Additionally, peroxiredoxin and Fe-SOD were expressed constitutively to removereactive oxygen species, the protein disulfide-isomerase genes in antioxidant systemwere up-regulated and involved in repair of oxidative damage during moderatedehydration stress. And the induction of apoptosis was involved in tolerance tomoderate dehydration stress, and in which the mitochondria played a centralregulatory role. Compared with moderate dehydration stress treatment, only18differentially expressed genes were identified during the severe dehydration stresstreatment, indicating that the gene expression patterns were quite similar between thetwo stress treatment groups. Compared with severe dehydration stress treatment,1199 differentially expressed genes were identified during the rehydration stress treatment,and of which one activator of caspases involved in induction of apoptosis andcochaperone proteins of HSP70significantly downregulated, the thioredoxin inantioxidant system upregulated and was involved in repair of oxidative damage duringrehydration stress.
The complete plastid genomes of P. hatanensis (195,597bp) and P. yezoensis(191,975bp) were fully sequenced using454high-throughout sequencing togetherwith Sanger sequencing, the largest of all the plastid genomes of the red lineagesequenced to date. Organization and gene contents of the two plastids were similar,with211-213protein-coding genes,37tRNA genes, and6ribosomal RNA genes,suggesting a largest coding capacity in the red lineage. In each genome,14proteingenes overlapped and no interrupted genes were found, indicating a high degree ofgenomic condensation. Pyropia maintains an ancient gene content and conserved geneclusters in their plastid genomes, containing nearly complete repertoires of the plastidgenes known in photosynthetic eukaryotes. Similarity analysis based on the wholeplastid genome sequences showed the distance between P. haitanensis and P.yezoensis (0.146) was much smaller than that of Porphyra purpurea and P.haitanensis (0.250), and P. yezoensis (0.251); this supports re-grouping the twospecies in a resurrected genus Pyropia while maintaining P. purpurea in genusPorphyra. Phylogenetic analysis supports a sister relationship betweenBangiophyceae and Florideophyceae, though precise phylogenetic relationshipsbetween multicellular red alage and chromists were not fully resolved. Combiningwith transcriptome and expression profiling results, coordination of plastid andnuclear gene expression was found to be mainly mediated by nuclear-encoded sigmafactors and activity of Mg-chelatase in response to dehydration stress.
本研究利用Illumina高通量测序技术开展了坛紫菜转录组测序以及失水/复水胁迫条件的表达谱特征分析，同时也利用454测序结合Sanger测序方法获得了完整的质体基因组序列。通过全面、系统地了解坛紫菜转录组特性，并深入探索坛紫菜响应失水/复水胁迫环境的分子机制，为了解坛紫菜适应潮间带失水胁迫环境的机制提供新认识，也为未来抗逆育种工作提供新参考。
主要结果如下：
（1）利用Illumina高通量测序技术对不同发育时期和不同胁迫处理的坛紫菜混合RNA样品进行转录组测序，共获得47,764,168条干净的短读长序列，碱基总量约为4.5G，拼接后得到28,536条平均长度为584bp的Unigenes。通过与多种数据库进行比对注释，发现坛紫菜转录组中包含大量响应失水胁迫、温度胁迫、光胁迫、营养盐缺乏等逆境胁迫以及抗氧化系统等相关功能基因，也发现许多发育过程相关功能基因。并且首次在红藻中发现Group1类型的晚期胚胎发育富集蛋白（LEA）同源序列，以及红藻中未曾报道过的矾依赖的卤过氧化物酶（vHPO）基因的同源序列。通过KEGG代谢途径分析，发现了坛紫菜中包含284条代谢途径，其中包括与逆境胁迫相关的细胞凋亡途径和MAPK信号途径（包含哺乳动物JNK和p38类型MAPK途径和酵母MAPK途径相关的许多酶类基因）。与数据库比对之后，仍然有10,378条Unigenes（36.4%）没有找到同源序列，说明可能存在大量功能未知的新基因。
（2）为了研究坛紫菜响应失水胁迫环境的表达谱特征，将坛紫菜配子体在不同失水率和复水胁迫条件处理的8个样品分别建库和Illumina测序（每个处理组设置两个生物学重复），每个处理组样品获得11.83M-15.04M干净的短读长序列，且与坛紫菜转录组比对（map）上的短读长序列数占短读长序列总数的96.78%-97.74%。每个处理组内生物学重复之间表达水平相关性较高（R∧2为0.916～0.941）。通过分析中度失水胁迫条件下基因表达的总体模式（与对照组相比），发现1681个基因显著差异表达。首次发现多种新基序类型的MAPK，其中新的TQA基序类型MAPK参与响应失水胁迫的信号转导过程。10个分子伴侣/共陪伴蛋白基因（包括HSP90和HSP70家族成员、HSP70共陪伴蛋白）在中度失水胁迫下上调表达，而Hsp33和HSP60家族成员呈组成性表达。同时，抗氧化系统中的过氧化物氧化还原酶和Fe-SOD呈现组成性表达来清除活性氧；蛋白质二硫化异构酶上调表达来参与修复中度失水胁迫下的氧化性损伤。细胞凋亡诱导过程也参与到耐受中度失水胁迫，而且线粒体在坛紫菜细胞凋亡诱导过程中起中心调节作用。与中度失水相比，在重度失水胁迫条件下仅18个基因显著差异表达，表明两个处理组之间基因表达模式比较相似。与重度失水胁迫相比，在复水过程中有1199个基因显著差异表达，其中1个参与细胞凋亡诱导的Caspases激活物和HSP70的共陪伴蛋白均显著下调表达，而抗氧化系统中硫氧还蛋白通过上调表达来修复复水过程中的氧化性损伤。
（3）利用454测序结合Sanger测序技术获得坛紫菜和条斑紫菜完整的质体基因组序列。这两种紫菜的环形质体基因组大小分别为195,597bp和191,975bp，是目前已测序的红色支系中最大的质体基因组。这两个基因组的基因内容相似，包含211-213个蛋白质编码基因、37个tRNA基因和6个rRNA基因，显示了红色支系中最大的编码容量。每个基因组中有14个蛋白质基因重叠，且所有基因均没有内含子，揭示了高度紧凑的质体基因组。Pyropia属的质体基因组保留了古老的基因内容和保守的基因簇，也包含了几乎完整的一套已知光合真核生物的质体基因集。基于整个质体基因组序列的相似性分析显示坛紫菜与条斑紫菜间的遗传距离（0.146）小于Porphyra purpurea与坛紫菜的距离（0.250）以及与条斑紫菜的距离（0.251）。这个结果支持了将坛紫菜和条斑紫菜划分到新属Pyropia中，而保留P. purpure在Porphyra属中的分类修订。系统发生分析显示虽然多细胞红藻与chromists的系统发生关系没有完全解决，但是支持红毛菜纲和真红藻纲之间以及Pyropia和Porphyra之间的姐妹关系。通过结合转录组和表达谱的结果发现核编码的Sigma因子和镁螯合酶活性变化介导了响应失水胁迫下核基因和质体基因的协调表达。
Pyropia haitanensis is an economically important marine crop, which has beencultivated widely along the coasts of South China, accounting for75%of the totaloutput of cultivated Pyropia in China. P. haitanensis is also considered to be researchmodels for studying physiological ecology and the molecular mechanisms for stresstolerance of intertidal seaweed communities. However, for P. haitanensis, limitedstudies have been conducted. So far, the genomic information on Pyropiaremains incomplete, and systematic molecular investigations of the mechanisms foracclimation to intertidal stress environment are very lacking at present.
Using Illumna high-throughout sequencing technology, the transcriptome andexpression profiles of P. haitanensis were sequenced and analyzed. And using454and Sanger sequencing technology, the complete plastid genomes of P. hatanensis andP. yezoensis were fully sequenced. Comprehensive and systematic study oftranscriptomic characteristics and deep exploration of molecular mechanism forresponse to the dehydration/rehydration stress environment will not only provide newunderstanding of the mechanisms for response to intertidal desiccation stressenvironment, but also provide new reference for stress-resistance breeding in future.
The major findings are as follows:
The global transcriptome of P. haitanensis was sequenced using Illuminahigh-throughput sequencing technology. A total of47,764,168clean reads (4.5Gbclean bases) were generated from the cDNA library constructed for a RNA mixture ofP. hatanensis at different development stages and under different stress treatments.These clean reads were assembled into28,536unigenes with a mean length of584bp.Based on sequence similarity searches with known proteins, a large number of genesrelated to stress response were found, including genes related to desiccation stress,temperature stress, light stress, starvation, antioxidant system and other genes relatedto stress processes, and of which group1type LEA and vanadium-dependent haloperoxidase (vHPO) homologous sequences were firstly reported. And Manygenes related to developmental process were also found in P. hatanensis. Searchingagainst the KEGG database indicated that there existed284KEGG pathways intranscriptome of P. hatanensis, including apoptosis pathway and MAPK signalingpathways related to stress environment. The MAPK signaling pathways contain manygenes involved in mammalian JNK and p38type MAPK pathway and yeast MAPKpathway. After annotation, there are still10,378unigenes unannotated (36.4%),indicating that there may be a lot of novel genes with unknown function.
In order to study the expression profile characteristics in response to desiccationstress environment in P. hatanensis, the cDNA library was constructed for eightsamples from the different dehydration and rehydration stress treatments and thensequenced by Illumina sequencing technology (two biological replicates for eachtreatment). A total of11.83M-15.04M clean reads were abtained for each sample.Moreover, the number of reads mapped to transcriptome is96.78%-97.74%of thetotal reads number. Within each treatment, correlation of gene expression levelsbetween two biological replicates was high (R∧2=0.916-0.941). By analysis of theoverall pattern of gene expression during moderate dehydration (compared with thecontrol group), a total of1681differentially expressed genes were identified. Avariety of new motif type MAPKs were firstly found, and of which the new TQAmotif type MAPK was involved in signal transduction pathway in response to thedehydration stress. A total of10molecular chaperones genes (including the membersof HSP90superfamily, HSP70superfamily and cochaperone proteins of HSP70) weresignificantly up-regulated in response to the moderate dehydration stress，whereas themembers of HSP60superfamily and the Hsp33were expressed constitutively.Additionally, peroxiredoxin and Fe-SOD were expressed constitutively to removereactive oxygen species, the protein disulfide-isomerase genes in antioxidant systemwere up-regulated and involved in repair of oxidative damage during moderatedehydration stress. And the induction of apoptosis was involved in tolerance tomoderate dehydration stress, and in which the mitochondria played a centralregulatory role. Compared with moderate dehydration stress treatment, only18differentially expressed genes were identified during the severe dehydration stresstreatment, indicating that the gene expression patterns were quite similar between thetwo stress treatment groups. Compared with severe dehydration stress treatment,1199 differentially expressed genes were identified during the rehydration stress treatment,and of which one activator of caspases involved in induction of apoptosis andcochaperone proteins of HSP70significantly downregulated, the thioredoxin inantioxidant system upregulated and was involved in repair of oxidative damage duringrehydration stress.
The complete plastid genomes of P. hatanensis (195,597bp) and P. yezoensis(191,975bp) were fully sequenced using454high-throughout sequencing togetherwith Sanger sequencing, the largest of all the plastid genomes of the red lineagesequenced to date. Organization and gene contents of the two plastids were similar,with211-213protein-coding genes,37tRNA genes, and6ribosomal RNA genes,suggesting a largest coding capacity in the red lineage. In each genome,14proteingenes overlapped and no interrupted genes were found, indicating a high degree ofgenomic condensation. Pyropia maintains an ancient gene content and conserved geneclusters in their plastid genomes, containing nearly complete repertoires of the plastidgenes known in photosynthetic eukaryotes. Similarity analysis based on the wholeplastid genome sequences showed the distance between P. haitanensis and P.yezoensis (0.146) was much smaller than that of Porphyra purpurea and P.haitanensis (0.250), and P. yezoensis (0.251); this supports re-grouping the twospecies in a resurrected genus Pyropia while maintaining P. purpurea in genusPorphyra. Phylogenetic analysis supports a sister relationship betweenBangiophyceae and Florideophyceae, though precise phylogenetic relationshipsbetween multicellular red alage and chromists were not fully resolved. Combiningwith transcriptome and expression profiling results, coordination of plastid andnuclear gene expression was found to be mainly mediated by nuclear-encoded sigmafactors and activity of Mg-chelatase in response to dehydration stress.
引文
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