水稻显性矮秆基因Epi-df的图位克隆、表观修饰特征分析及功能研究
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摘要
株高是与产量相关的重要农艺性状,株高超过一定范围容易引起倒伏而减产,矮秆不仅有利于抗倒伏,而且耐贫瘠,有利于提高产量。20世纪50年代末开始的矮化育种,使水稻株高降低至半矮秆,水稻单产获得了第一次飞跃,成为“绿色革命”的标志性成就之一。目前正在进行的超级稻育种主要利用理想株型和籼粳亚种间杂种优势以期水稻单产得到进一步提高。迄今水稻育种中利用的矮秆基因都是隐性基因,杂交水稻育种中隐性矮秆基因的使用往往要求双亲必须具有同一矮秆基因,这就限制了在更广泛的资源中选择有利亲本。但是如果利用显性矮秆基因,则能够使水稻种质资源得到更有效的利用和缩短育种时间。因此发掘新的水稻株高控制基因特别是显性矮秆基因,对进一步提高水稻单产具有重要意义。本研究对显性矮秆突变体Epi-df进行了系统的表型考察和降秆能力分析,并对产生矮化的分子机制进行了深入研究。
主要研究结果如下：
(1) Epi-df从苗期至成熟期表现矮化,并且与野生型杂交F1表现类似突变体的表型,因此,Epi-df属于显性矮秆突变体。Epi-df与籼稻品种培矮64正反交F1株高介于两者之间,F2代分离群体中高株和矮株数比例接近1：3,表明Epi-df表型是由单显性核基因控制。将Epi-df与3个籼稻品种和3个粳稻品种杂交,降秆率介于16.3%至50.4%之间,表明Epi-df具有较强的降秆能力,有望在水稻籼粳交杂种优势利用育种中得到应用。
(2)利用图位克隆方法将突变基因精细定位在49kb区域内,但并未发现DNA序列突变,却发现其中的ORF5在突变体中表达强烈，而在野生型中沉默。Epi-df还存在另外一个特征,即虽然表现遗传稳定但存在低水平的回复突变频率,因此ORF5的异位表达可能是由表观遗传变异引起的。DNA甲基化测序结果表明FIE15’端发生了DNA去甲基化,这与FIE1的异位表达是一致的。尽管FIEl在回复突变株中保持沉默,但DNA甲基化并未恢复到野生型水平,发生恢复的位点主要集中在转录起始点附近和第3个外显子。另外,Epi-df中FIE15’端H3K9me2水平下降,而H3K4me3水平上升,这与FIE1基因的异位表达和DNA去甲基化是一致的。因此,Epi-df是一个表观遗传突变体,这为研究表观遗传修饰对单子叶植物尤其是重要作物的生长发育的调控提供了重要材料。
(3) FIE1是胚乳特异性表达的基因,并且具有仅母本表达的印记特征。FIE1在叶片、茎和幼穗中存在高水平的DNA甲基化,而在受精后第6、9和12天的胚乳中甲基化水平严重降低,并且F1胚乳中母本FIE1的DNA甲基化水平比父本低很多,因此FIE1的表达模式和印记特征受DNA甲基化调控。与拟南芥仅有一个FIE基因不同,水稻含有两个FIE基因,另一个FIE基因FIE2是组成性表达的,因此我们推测水稻基因组复制以及随后的进化过程中,表观遗传修饰对两个FIE基因的功能分化起了重要作用。
(4)酵母双杂交结果表明FIE1与iEZ1以及CLF互作,表明FIE1参与水稻中PRC2介导的转录抑制。基因芯片分析发现Epi-df中有305个基因的表达发生了改变,其中222个基因下调,83个基因上调。利用染色质免疫共沉淀技术发现这些表达量改变的基因同时伴随着H3K27me3修饰的改变。因此,FIE1的异位表达导致靶基因H3K27me3修饰水平和表达量的改变,从而使Epi-df表现突变表型。
(5) H3K9me2和H3K27me3是与转录抑制相关非常保守的两种表观遗传修饰,H3K9me2主要集中在异染色质,起抑制转座子和逆转座子转录和转座的功能；H3K27me3基本存在于常染色质,起抑制基因转录和维持细胞记忆的功能。染色质免疫共沉淀分析表明FIE15’端存在高水平的H3K9me2,而Epi-df中H3K9me2水平降低引起FIE1异位表达和基因组水平上H3K27me3分布异常,从而导致水稻发育缺陷。因止匕,H3K9me2控制的FIE1转录抑制对水稻中H3K27me3的正常功能是必需的。
Plant height is an agronomically important trait for grain yield, the higher plant is easy to be lodging and decreasing yield, whereas dwarf plant has a great harvest index because of improved lodging resistance and increasing use of nitrogen fertilizers. Dwarfism breeding resulted in the first qualitative leap for yield increase, which was well known as "green revolution". The objective of super rice breeding is to make a breakthrough in rice yield by using ideotype and inter-subspecific heterosis. Whereas all the dwarf genes used in rice breeding is recessive by now, thus both the male and female parents must carry the same recessive dwarf gene in hybrid rice breeding process. But when one parent carries a dominant dwarf allele, the germplasm of the other parent would not be restricted. Therefore, isolation new genes that control plant height especially the dominant dwarf genes is crucial for improving rice yield. In this study, we systematacially characterized a dominant dwarf mutant Epi-df and analyzed the molecular mechanism for dwarfism.
The main results as follows:
(1) From seedling to mature stage, Epi-df showes dwarf phenotype. When crossed with WT, the F1plants show the phenotype similar to Epi-df, thus, Epi-df is a dominant dwarf mutant. When crossed with PA64, the plant height of F1is between two parents, and the ratio of normal to dwarf plants in F2population is nearly to1:3, suggesting that the mutant phenotype is controlled by one dominant nuclear gene. When Epi-df was crossed with three indica varieties and three japonica varieties respectively, the plant height reduction is from16.3to50.4%, suggesting the strong plant height reduction ability. Thus, Epi-df may be used for rice inter-subspecific heterosis breeding in the future.
(2) The mutative gene was fine mapped within a49kb region, whereas there was no nucleotide mutation. However, we found ORF5(one of the seven ORFs within the mapping region) was ectopically expressed in Epi-df, but silenced in WT. Considered the revertants emerged from Epi-df population, we speculated that Epi-df was an epigenetic mutant. By using bisulfite sequencing, we found DNA hypo-methylation was occurred at5'region of FIE1. We also analyzed the methylation patterns of six revertants and found even FIE I was silenced in them, DNA methylation was not recovered to the WT level, the recovered sits were enriched around the transcriptional starting site and within the third exon. We also found there were reduced H3K9me2and increased H3K4me3at the5'region of FIE1. Thus, Epi-df is an unexpected epigenetic mutant, which would like to provide an intriguing opportunity to unravel epigenetic modifications for development regulation in important crop plants.
(3) We discovered that FIE1was a maternal-specific expressing gene in endosperm, which was coincided with the methylation pattern of FIE1in tissues. The methylation level is higher in leaf, culm and young panicle than that in endosperm6,9and12days after pollination. We also found the methylation of maternal FIE1was much lower than that of paternal. If Epi-df was used as pollen donator, the imprinting pattern was disturbed, and the methylation levels of both parental were lower. Unlike Arbidopsis, which contains only one ubiquitously expressed FIE gene, there are two FIE gene in rice, the other gene FIE2is expressed in all the tissues. We conclude that during the genome duplication and the latter evolution, epigenetic marks may play an important role in the differentiation of the two FIE gene in rice.
(4) Yeast two-hybrid assay showed FIE1interacted with rice E(z) homologs, suggesting FIE1participates in PRC2repression which catalyzes H3K27me3at targets. Microarray analysis showed305genes were misregulated in Epi-df accompanied with changed H3K27me3levels. Thus, ectopic expression of FIE1resulted in the mutant phenotype via abnormal distribution of H3K27me3.
(5) H3K9me2and H3K27me3are two conserved repressive epigenetic marks in both animal and higher plants. H3K9me2is mainly enriched in heterochromatin and functions in suppressing transposons, while H3K27me3is mainly localized in euchromatin and provides a cellular memory to maintain the repressive state of target genes. We found there was high level of H3K9me2at5'region of FIE1, whereas in Epi-df, H3K9me2was reduced and resulted in ectopic expression of FIE1and abnormal distribution of H3K27me3. We conclude that silencing of FIE1via H3K9me2is essential for normal function of H3K27me3in rice.
主要研究结果如下：
(1) Epi-df从苗期至成熟期表现矮化,并且与野生型杂交F1表现类似突变体的表型,因此,Epi-df属于显性矮秆突变体。Epi-df与籼稻品种培矮64正反交F1株高介于两者之间,F2代分离群体中高株和矮株数比例接近1：3,表明Epi-df表型是由单显性核基因控制。将Epi-df与3个籼稻品种和3个粳稻品种杂交,降秆率介于16.3%至50.4%之间,表明Epi-df具有较强的降秆能力,有望在水稻籼粳交杂种优势利用育种中得到应用。
(2)利用图位克隆方法将突变基因精细定位在49kb区域内,但并未发现DNA序列突变,却发现其中的ORF5在突变体中表达强烈，而在野生型中沉默。Epi-df还存在另外一个特征,即虽然表现遗传稳定但存在低水平的回复突变频率,因此ORF5的异位表达可能是由表观遗传变异引起的。DNA甲基化测序结果表明FIE15’端发生了DNA去甲基化,这与FIE1的异位表达是一致的。尽管FIEl在回复突变株中保持沉默,但DNA甲基化并未恢复到野生型水平,发生恢复的位点主要集中在转录起始点附近和第3个外显子。另外,Epi-df中FIE15’端H3K9me2水平下降,而H3K4me3水平上升,这与FIE1基因的异位表达和DNA去甲基化是一致的。因此,Epi-df是一个表观遗传突变体,这为研究表观遗传修饰对单子叶植物尤其是重要作物的生长发育的调控提供了重要材料。
(3) FIE1是胚乳特异性表达的基因,并且具有仅母本表达的印记特征。FIE1在叶片、茎和幼穗中存在高水平的DNA甲基化,而在受精后第6、9和12天的胚乳中甲基化水平严重降低,并且F1胚乳中母本FIE1的DNA甲基化水平比父本低很多,因此FIE1的表达模式和印记特征受DNA甲基化调控。与拟南芥仅有一个FIE基因不同,水稻含有两个FIE基因,另一个FIE基因FIE2是组成性表达的,因此我们推测水稻基因组复制以及随后的进化过程中,表观遗传修饰对两个FIE基因的功能分化起了重要作用。
(4)酵母双杂交结果表明FIE1与iEZ1以及CLF互作,表明FIE1参与水稻中PRC2介导的转录抑制。基因芯片分析发现Epi-df中有305个基因的表达发生了改变,其中222个基因下调,83个基因上调。利用染色质免疫共沉淀技术发现这些表达量改变的基因同时伴随着H3K27me3修饰的改变。因此,FIE1的异位表达导致靶基因H3K27me3修饰水平和表达量的改变,从而使Epi-df表现突变表型。
(5) H3K9me2和H3K27me3是与转录抑制相关非常保守的两种表观遗传修饰,H3K9me2主要集中在异染色质,起抑制转座子和逆转座子转录和转座的功能；H3K27me3基本存在于常染色质,起抑制基因转录和维持细胞记忆的功能。染色质免疫共沉淀分析表明FIE15’端存在高水平的H3K9me2,而Epi-df中H3K9me2水平降低引起FIE1异位表达和基因组水平上H3K27me3分布异常,从而导致水稻发育缺陷。因止匕,H3K9me2控制的FIE1转录抑制对水稻中H3K27me3的正常功能是必需的。
Plant height is an agronomically important trait for grain yield, the higher plant is easy to be lodging and decreasing yield, whereas dwarf plant has a great harvest index because of improved lodging resistance and increasing use of nitrogen fertilizers. Dwarfism breeding resulted in the first qualitative leap for yield increase, which was well known as "green revolution". The objective of super rice breeding is to make a breakthrough in rice yield by using ideotype and inter-subspecific heterosis. Whereas all the dwarf genes used in rice breeding is recessive by now, thus both the male and female parents must carry the same recessive dwarf gene in hybrid rice breeding process. But when one parent carries a dominant dwarf allele, the germplasm of the other parent would not be restricted. Therefore, isolation new genes that control plant height especially the dominant dwarf genes is crucial for improving rice yield. In this study, we systematacially characterized a dominant dwarf mutant Epi-df and analyzed the molecular mechanism for dwarfism.
The main results as follows:
(1) From seedling to mature stage, Epi-df showes dwarf phenotype. When crossed with WT, the F1plants show the phenotype similar to Epi-df, thus, Epi-df is a dominant dwarf mutant. When crossed with PA64, the plant height of F1is between two parents, and the ratio of normal to dwarf plants in F2population is nearly to1:3, suggesting that the mutant phenotype is controlled by one dominant nuclear gene. When Epi-df was crossed with three indica varieties and three japonica varieties respectively, the plant height reduction is from16.3to50.4%, suggesting the strong plant height reduction ability. Thus, Epi-df may be used for rice inter-subspecific heterosis breeding in the future.
(2) The mutative gene was fine mapped within a49kb region, whereas there was no nucleotide mutation. However, we found ORF5(one of the seven ORFs within the mapping region) was ectopically expressed in Epi-df, but silenced in WT. Considered the revertants emerged from Epi-df population, we speculated that Epi-df was an epigenetic mutant. By using bisulfite sequencing, we found DNA hypo-methylation was occurred at5'region of FIE1. We also analyzed the methylation patterns of six revertants and found even FIE I was silenced in them, DNA methylation was not recovered to the WT level, the recovered sits were enriched around the transcriptional starting site and within the third exon. We also found there were reduced H3K9me2and increased H3K4me3at the5'region of FIE1. Thus, Epi-df is an unexpected epigenetic mutant, which would like to provide an intriguing opportunity to unravel epigenetic modifications for development regulation in important crop plants.
(3) We discovered that FIE1was a maternal-specific expressing gene in endosperm, which was coincided with the methylation pattern of FIE1in tissues. The methylation level is higher in leaf, culm and young panicle than that in endosperm6,9and12days after pollination. We also found the methylation of maternal FIE1was much lower than that of paternal. If Epi-df was used as pollen donator, the imprinting pattern was disturbed, and the methylation levels of both parental were lower. Unlike Arbidopsis, which contains only one ubiquitously expressed FIE gene, there are two FIE gene in rice, the other gene FIE2is expressed in all the tissues. We conclude that during the genome duplication and the latter evolution, epigenetic marks may play an important role in the differentiation of the two FIE gene in rice.
(4) Yeast two-hybrid assay showed FIE1interacted with rice E(z) homologs, suggesting FIE1participates in PRC2repression which catalyzes H3K27me3at targets. Microarray analysis showed305genes were misregulated in Epi-df accompanied with changed H3K27me3levels. Thus, ectopic expression of FIE1resulted in the mutant phenotype via abnormal distribution of H3K27me3.
(5) H3K9me2and H3K27me3are two conserved repressive epigenetic marks in both animal and higher plants. H3K9me2is mainly enriched in heterochromatin and functions in suppressing transposons, while H3K27me3is mainly localized in euchromatin and provides a cellular memory to maintain the repressive state of target genes. We found there was high level of H3K9me2at5'region of FIE1, whereas in Epi-df, H3K9me2was reduced and resulted in ectopic expression of FIE1and abnormal distribution of H3K27me3. We conclude that silencing of FIE1via H3K9me2is essential for normal function of H3K27me3in rice.
引文
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