水稻苗期黄绿叶基因YGL2的功能研究和垩白粒率QTL qPGWC-7候选基因的功能初步分析
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摘要
本论文包括两部分研究内容,第一部分为水稻苗期黄绿叶基因YGL2(YELLOW-GREEN LEAF2)的图位克隆和功能分析,第二部分为水稻垩白粒率QTL qPGWC-7的精细定位和候选基因的功能初步分析。
第一部分：在高等植物中,血红素加氧酶(Heme Oxygenase, HO)是血红素分解代谢的限速酶,它能够催化血红素的降解,从而合成光敏色素前体。之前已经有研究报道了水稻中血红素加氧酶在控制光周期,调节水稻开花中的作用。但是,其在调节水稻叶绿素合成中的作用仍然没有研究。本文中,我们从60Co辐射诱变的冈46B突变体中发现了一个苗期表现为黄绿叶的突变体,命名为ygl2。在自然条件下,大田中生长的ygl2突变体在苗期,叶片呈现黄绿色表型,3叶期时突变体黄化表型最为明显；随着植株的生长,突变体褪绿叶片逐渐转绿,到抽穗期基本恢复到野生型的正常绿叶表型。通过测定叶绿素的含量发现,三叶期突变体中叶绿素(Chl)和类胡萝卜素的含量显著降低,而叶绿素a/叶绿素b的比例明显增加,随着植株的生长,这种差异逐渐缩小。对叶片叶绿体的扫描电镜观察发现突变体中叶绿体基粒填充不完整,每个类囊体片层的数目显著减少,导致叶片中叶绿体发育不完全,因此叶片出现黄化表型。为研究引起叶片黄化的突变基因,我们构建了ygl2和日本晴的F2群体,遗传分析表明黄叶表型是由一个单隐性基因控制,利用图位克隆的方法将该基因定位在水稻第6染色体短臂两Indel标记In44和In39之间约66.8kb的区间内。测序分析发现,在该区间内的一个编码血红素加氧酶的基因的第1外显子插入了约7kb的片段,导致突变体中编码的氨基酸的改变并且引起该基因的表达量显著下降；转基因互补实验和RNAi结果均表明该基因的突变导致了黄叶表型的产生；系统进化树分析表明该基因编码的蛋白属于血红素加氧酶1亚家族,该基因的突变使蛋白的二级和三级结构发生了轻微改变,但是水稻原生质体亚细胞定位发现ygl2中该基因的突变并没有影响其编码蛋白在细胞叶绿体中的定位；GUS染色和qRT-PCR分析表明该基因在水稻各组织中组成型表达,但是在叶片中的表达量最高,并且苗期该基因的表达量高于分蘖期；不同温度处理后,YGL2基因的表达受到影响并且与叶绿素合成和光合作用相关的基因的表达均受到影响,表明YGL2在水稻叶绿素的合成和光合作用中具有重要的作用。YGL2的克隆为进一步阐明血红素加氧酶在调节植物叶绿素合成和光合作用中的重要作用奠定了基础。
第二部分：水稻籽粒垩白的产生严重影响稻米品质,垩白是一个非常复杂的数量性状,精细定位和克隆控制垩白的QTL不仅有助于阐明水稻垩白形成的分子机制,同时还可以利用分子标记辅助选择的方法,提高育种效率。本研究中的C-51是一个以9311为轮回亲本,PA64S为供体亲本的染色体置换系材料,在不同环境下其垩白粒率均显著高于背景亲本9311,扫描电镜观察发现C-51垩白部分淀粉颗粒呈圆形或椭圆形,排列疏松,大小不一,而9311透明部分淀粉颗粒呈现多角形多面体状,棱角分明,淀粉粒相互嵌合紧密排列在一起,但是9311和C-51的灌浆速率和干物质积累无显著差异。本研究通过对前人研究结果的验证和进一步精细定位,最终将控制该垩白粒率的QTL qPGWC-7定位在第7染色体Indel18和Indel3两标记之间,区间大小约17.1kb。经过预测分析发现,该区间包含3个ORFs,其中C-51中ORF1的表达量在整个灌浆过程中均高于9311,在开花后第18天表达量达到最大,并且C-51和9311在氨基酸序列的保守结构域存在一个氨基酸的改变,因此将该ORF1作为候选基因进行功能分析。体外酶活测定证明在高垩白粒率的C-51中qPGWC-7的酶活与低垩白粒率的9311并没有明显差异,因此垩白粒率的差异可能和该基因的表达量差异有关；GUS组织化学染色检测则证明该基因主要在水稻各个组织中的维管组织中表达,在幼稳中表达量最高,并且该基因受低温诱导；拟南芥和水稻原生质体亚细胞定位将蛋白定位于细胞的高尔基体上。上述研究结果为qPGWC-7的进一步的功能研究奠定了良好的基础。
This thesis includes two parts:the first is "map-based cloning and functional analysis of YGL2gene for yellow-green leaf in rice", and the other part is "fine mapping of a QTL qPGWC-7for percentage of grains with white chalkiness and preliminary characterization of the candidate gene in rice".
Part one:Heme Oxygenase (HO) in higher plants is a rate-limiting enzyme for catabolism of heme, it can catalyze the degradation of heme to synthesize phytochrome precursor and its roles conferring the photoperiodic control of flowering in rice have been revealed. However, its involvement in regulating rice chlorophyll (Chi) synthesis is not fully explored. In this study, we isolated a rice mutant named yellow-green leaf2(ygl2) from a Co-irradiated population. Normal grown ygl2showed yellow-green leaves in seedling stage and was most obvious in three-leaf stage, from tiller initiating to heading stage, yellowish leaves gradually turned green and approached almost as normal as wild type did. Pigments contents at different developmental stages were examined and the results showed that, at three-leaf stage, the ygl2mutant had a significant reduction of Chi and Car levels but apparent increase of Chi a/b ratio compared to the wild type but these difference were decreased along with the plant grown. We compared the ultrastructures of chloroplasts between the ygl2mutant and wild type plants at three-leaf stage using transmission electron microscopy. The number of thylakoid lamellar in chloroplasts of the ygl2was significantly less than that of wild type, whereas the structure of the thylakoid lamellar seemed normal and similar to that of wild type. For map-based cloning of ygl2gene, a mapping population of F2was constructed by a cross between the ygl2mutant and Nipponbare, genetic analysis indicated that the chlorosis phenotype in the ygl2mutant was controlled by a recessive nuclear gene. The ygl2locus was finally narrowed to a region of66.8-kb between two InDel markers, In44and In39on the long arm of chromosome6. Sequencing analysis showed that a fragment of7-kb was inserted into the first exon of one gene in this region which encode Heme Oxygenase, resulting in amino acid polymorphisms and expression level declined. Genetic complementation and RNAi all indicated that the abnormal phenotype of ygl2mutant resulted from the mutation of YGL2gene. Phylogenetic tree analysis showed that YGL2belong to the HO1family, and the mutation of YGL2made little changes to the secondary and3D structures of the protein, but had no effect on the localization of chloroplast through subcellular localization of rice protoplast. qRT-PCR and GUS histochemical staining indicated that YGL2were constitutively expressed in various tissues and particularly the highest in leaf. The expression level at seedling stage was much higher than that of tillering stage and that it was affected obviously after treatment with two different temperatures, meanwhile, the expressions of genes associated with Chl biosynthesis and photosynthesis were also changed. The results indicated YGL2played an important role in the regulation network of Chl biosynthesis and photosynthesis. The cloning of YGL2established the foundation for illuminating the important roles of HO in regulating Chl biosynthesis and photosynthesis in higher plants.
Part two:Chalkiness of rice grain has profound influence on qualities of rice, it is a complicated quantitative trait and controlled by many quantitative trait locus (QTLs). Fine mapping and cloning of QTLs for chalkiness not only helps us in illuminating the molecular mechanism of chalkiness, but also improving breeding efficiency using marker-assisted selection (MAS). In this study, C-51was a chromosome segment substitution lines (CSSL) created using9311as the recurrent and PA64s as the donor, the percentage of grains with white chalkiness (PGWC) of C-51was significantly higher than that of9311in different environment. Scanning electron microscope (SEM) analysis showed the C-51starch granules of opaque part were round or oval, loosely packed and sizes, and very different from angular, densely packed, polyhedral starch granules of9311transparent part, but there were no significant differences in fresh weight of grain and dry weight of brown rice between C-51and9311in different periods after flowering. We verified the results previously and conducted further fine mapping. The QTL qPGWC-7was finally narrowed to a region of17.1-kb between two InDel markers, InDel18and InDel3on chromosome6. This region contains three ORFs, the expression of ORF1in C-51was much higher than that of9311during grain filling period, especially the highest 18days after flowering. In addition, there was a amino acid polymorphism in the conserved domain of ORF1protein between C-51and9311, so ORF1was used as the candidate gene for further functional analysis. The enzyme activity of qPGWC-7was no difference between expressed proteins of C-51and9311in vitro, so the difference for chalkiness may caused by the difference of expression levels. GUS histochemical staining indicated that qPGWC-7was constitutively expressed in vascular tissues of various organs and particularly the highest in young panicle. On the other hand, the expression level was induced by low temperature. qPGWC-7was located on Golgi through subcellular localization of rice and Arabidopsis protoplast. These results above provided a good basis for further study of qPGWC-7function.
第一部分：在高等植物中,血红素加氧酶(Heme Oxygenase, HO)是血红素分解代谢的限速酶,它能够催化血红素的降解,从而合成光敏色素前体。之前已经有研究报道了水稻中血红素加氧酶在控制光周期,调节水稻开花中的作用。但是,其在调节水稻叶绿素合成中的作用仍然没有研究。本文中,我们从60Co辐射诱变的冈46B突变体中发现了一个苗期表现为黄绿叶的突变体,命名为ygl2。在自然条件下,大田中生长的ygl2突变体在苗期,叶片呈现黄绿色表型,3叶期时突变体黄化表型最为明显；随着植株的生长,突变体褪绿叶片逐渐转绿,到抽穗期基本恢复到野生型的正常绿叶表型。通过测定叶绿素的含量发现,三叶期突变体中叶绿素(Chl)和类胡萝卜素的含量显著降低,而叶绿素a/叶绿素b的比例明显增加,随着植株的生长,这种差异逐渐缩小。对叶片叶绿体的扫描电镜观察发现突变体中叶绿体基粒填充不完整,每个类囊体片层的数目显著减少,导致叶片中叶绿体发育不完全,因此叶片出现黄化表型。为研究引起叶片黄化的突变基因,我们构建了ygl2和日本晴的F2群体,遗传分析表明黄叶表型是由一个单隐性基因控制,利用图位克隆的方法将该基因定位在水稻第6染色体短臂两Indel标记In44和In39之间约66.8kb的区间内。测序分析发现,在该区间内的一个编码血红素加氧酶的基因的第1外显子插入了约7kb的片段,导致突变体中编码的氨基酸的改变并且引起该基因的表达量显著下降；转基因互补实验和RNAi结果均表明该基因的突变导致了黄叶表型的产生；系统进化树分析表明该基因编码的蛋白属于血红素加氧酶1亚家族,该基因的突变使蛋白的二级和三级结构发生了轻微改变,但是水稻原生质体亚细胞定位发现ygl2中该基因的突变并没有影响其编码蛋白在细胞叶绿体中的定位；GUS染色和qRT-PCR分析表明该基因在水稻各组织中组成型表达,但是在叶片中的表达量最高,并且苗期该基因的表达量高于分蘖期；不同温度处理后,YGL2基因的表达受到影响并且与叶绿素合成和光合作用相关的基因的表达均受到影响,表明YGL2在水稻叶绿素的合成和光合作用中具有重要的作用。YGL2的克隆为进一步阐明血红素加氧酶在调节植物叶绿素合成和光合作用中的重要作用奠定了基础。
第二部分：水稻籽粒垩白的产生严重影响稻米品质,垩白是一个非常复杂的数量性状,精细定位和克隆控制垩白的QTL不仅有助于阐明水稻垩白形成的分子机制,同时还可以利用分子标记辅助选择的方法,提高育种效率。本研究中的C-51是一个以9311为轮回亲本,PA64S为供体亲本的染色体置换系材料,在不同环境下其垩白粒率均显著高于背景亲本9311,扫描电镜观察发现C-51垩白部分淀粉颗粒呈圆形或椭圆形,排列疏松,大小不一,而9311透明部分淀粉颗粒呈现多角形多面体状,棱角分明,淀粉粒相互嵌合紧密排列在一起,但是9311和C-51的灌浆速率和干物质积累无显著差异。本研究通过对前人研究结果的验证和进一步精细定位,最终将控制该垩白粒率的QTL qPGWC-7定位在第7染色体Indel18和Indel3两标记之间,区间大小约17.1kb。经过预测分析发现,该区间包含3个ORFs,其中C-51中ORF1的表达量在整个灌浆过程中均高于9311,在开花后第18天表达量达到最大,并且C-51和9311在氨基酸序列的保守结构域存在一个氨基酸的改变,因此将该ORF1作为候选基因进行功能分析。体外酶活测定证明在高垩白粒率的C-51中qPGWC-7的酶活与低垩白粒率的9311并没有明显差异,因此垩白粒率的差异可能和该基因的表达量差异有关；GUS组织化学染色检测则证明该基因主要在水稻各个组织中的维管组织中表达,在幼稳中表达量最高,并且该基因受低温诱导；拟南芥和水稻原生质体亚细胞定位将蛋白定位于细胞的高尔基体上。上述研究结果为qPGWC-7的进一步的功能研究奠定了良好的基础。
This thesis includes two parts:the first is "map-based cloning and functional analysis of YGL2gene for yellow-green leaf in rice", and the other part is "fine mapping of a QTL qPGWC-7for percentage of grains with white chalkiness and preliminary characterization of the candidate gene in rice".
Part one:Heme Oxygenase (HO) in higher plants is a rate-limiting enzyme for catabolism of heme, it can catalyze the degradation of heme to synthesize phytochrome precursor and its roles conferring the photoperiodic control of flowering in rice have been revealed. However, its involvement in regulating rice chlorophyll (Chi) synthesis is not fully explored. In this study, we isolated a rice mutant named yellow-green leaf2(ygl2) from a Co-irradiated population. Normal grown ygl2showed yellow-green leaves in seedling stage and was most obvious in three-leaf stage, from tiller initiating to heading stage, yellowish leaves gradually turned green and approached almost as normal as wild type did. Pigments contents at different developmental stages were examined and the results showed that, at three-leaf stage, the ygl2mutant had a significant reduction of Chi and Car levels but apparent increase of Chi a/b ratio compared to the wild type but these difference were decreased along with the plant grown. We compared the ultrastructures of chloroplasts between the ygl2mutant and wild type plants at three-leaf stage using transmission electron microscopy. The number of thylakoid lamellar in chloroplasts of the ygl2was significantly less than that of wild type, whereas the structure of the thylakoid lamellar seemed normal and similar to that of wild type. For map-based cloning of ygl2gene, a mapping population of F2was constructed by a cross between the ygl2mutant and Nipponbare, genetic analysis indicated that the chlorosis phenotype in the ygl2mutant was controlled by a recessive nuclear gene. The ygl2locus was finally narrowed to a region of66.8-kb between two InDel markers, In44and In39on the long arm of chromosome6. Sequencing analysis showed that a fragment of7-kb was inserted into the first exon of one gene in this region which encode Heme Oxygenase, resulting in amino acid polymorphisms and expression level declined. Genetic complementation and RNAi all indicated that the abnormal phenotype of ygl2mutant resulted from the mutation of YGL2gene. Phylogenetic tree analysis showed that YGL2belong to the HO1family, and the mutation of YGL2made little changes to the secondary and3D structures of the protein, but had no effect on the localization of chloroplast through subcellular localization of rice protoplast. qRT-PCR and GUS histochemical staining indicated that YGL2were constitutively expressed in various tissues and particularly the highest in leaf. The expression level at seedling stage was much higher than that of tillering stage and that it was affected obviously after treatment with two different temperatures, meanwhile, the expressions of genes associated with Chl biosynthesis and photosynthesis were also changed. The results indicated YGL2played an important role in the regulation network of Chl biosynthesis and photosynthesis. The cloning of YGL2established the foundation for illuminating the important roles of HO in regulating Chl biosynthesis and photosynthesis in higher plants.
Part two:Chalkiness of rice grain has profound influence on qualities of rice, it is a complicated quantitative trait and controlled by many quantitative trait locus (QTLs). Fine mapping and cloning of QTLs for chalkiness not only helps us in illuminating the molecular mechanism of chalkiness, but also improving breeding efficiency using marker-assisted selection (MAS). In this study, C-51was a chromosome segment substitution lines (CSSL) created using9311as the recurrent and PA64s as the donor, the percentage of grains with white chalkiness (PGWC) of C-51was significantly higher than that of9311in different environment. Scanning electron microscope (SEM) analysis showed the C-51starch granules of opaque part were round or oval, loosely packed and sizes, and very different from angular, densely packed, polyhedral starch granules of9311transparent part, but there were no significant differences in fresh weight of grain and dry weight of brown rice between C-51and9311in different periods after flowering. We verified the results previously and conducted further fine mapping. The QTL qPGWC-7was finally narrowed to a region of17.1-kb between two InDel markers, InDel18and InDel3on chromosome6. This region contains three ORFs, the expression of ORF1in C-51was much higher than that of9311during grain filling period, especially the highest 18days after flowering. In addition, there was a amino acid polymorphism in the conserved domain of ORF1protein between C-51and9311, so ORF1was used as the candidate gene for further functional analysis. The enzyme activity of qPGWC-7was no difference between expressed proteins of C-51and9311in vitro, so the difference for chalkiness may caused by the difference of expression levels. GUS histochemical staining indicated that qPGWC-7was constitutively expressed in vascular tissues of various organs and particularly the highest in young panicle. On the other hand, the expression level was induced by low temperature. qPGWC-7was located on Golgi through subcellular localization of rice and Arabidopsis protoplast. These results above provided a good basis for further study of qPGWC-7function.
引文
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