三个水稻叶色突变体的基因克隆与功能分析
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摘要
叶片是光合作用的主要器官,是碳水化合物的主要来源。叶绿体是进行光合作用的场所,光合作用效率的高低与叶绿素的含量、叶绿体形态和结构密切相关,这些变化会影响植物的光合作用和生长发育。叶色突变体是研究叶绿素合成、调控和降解以及叶绿体的发育和叶绿体-细胞核的信号传递的重要材料。水稻是禾谷类作物中基因组最小的物种,是研究禾谷类作物遗传和发育的模式植物。随着水稻基因组测序计划的完成以及相关技术的不断发展,通过构建各种水稻突变体库,利用正反向遗传学的方法来鉴定特定生物学过程中的重要基因,进而了解基因的功能,是后基因组时代的核心任务。
本研究针对从恢复系选育和EMS诱变所获得的三份叶色突变体,即半显性黄叶自然突变体Chy(chlorophyll)、温敏型白条叶自然突变体st11(stripe11)和淡绿叶EMS诱变突变体pgl4(pale green leaf4),开展了突变体的形态学鉴定、叶绿体发育的电镜观察、遗传分析、光合生理测定、基因定位与克隆、载体构建、转基因功能验证和基因表达调控研究,其主要研究结果如下：
1、遗传分析表明突变体Chy为单基因控制的半显性遗传模式。突变体Chy缺失叶绿素a和b,叶绿体发育受阻,呈液泡状,没有完整的类囊体,突变体Chy出芽后在三叶期致死。杂合体Chy/+为黄叶色,叶绿素a和b的含量在二叶期、苗期、分蘖期和抽穗期四个不同时期均比野生型要低,但杂合体Chy/+的叶绿素a/b比值在四个时期均比野生型要高,且较为稳定一致,杂合体Chy/+的叶绿体发育也存在部分紊乱。杂合体Chy/+的农艺性状与野生型相比,主要在株高、生育期和每穗粒数上差异显著。利用混合法将突变基因CHY初定位在Chr3的RM1164和RM8208之间,位于着丝粒附近,在此区间进一步设计11对分子标记引物,将突变基因CHY定位在着丝粒两侧的2.1Mb的范围内。
2、利用网络资源和相关文献资料信息,查找发现一个位于BAC号为AC084767上的编码镁离子螯合酶Ⅰ亚基的CHLI基因(LOC_Os03g36540)可能与叶色突变体Chy的表型相关。测序结果表明CHLI基因的编码区第921个碱基由G突变成C,氨基酸由谷氨酸变成谷氨酰胺,突变位于CHLI基因的保守AAA+结构域上,突变体Chy与突变体chl9等位,基因CHLI为突变基因CHY的侯选基因。把突变基因CHY(包括启动子区、5’非翻译区和3’非翻译区在内)的6.9Kb的DNA片段连接到互补载体上,通过农杆菌介导法转入日本晴愈伤,获得5株阳性植株。与转空载体的日本晴对比,转基因植株T0代没有明显的叶色变化,T.代中分离出四分之一的(淡)黄叶植株,用转基因T1代中的(淡)黄叶色植株与突变体chl9进行杂交,F1验证T1代中分离出的(淡)黄叶植株是转基因互补植株,不是来自组培过程中叶色突变体。转基因进一步互补验证了突变基因CHY就是CHLI基因,突变基因CHY具有剂量效应。半定量RT-PCR检测发现CHY下调了叶绿素合成途径中的CHLH、PORA和CAO-1基因的表达,通过下调CHLH基因的表达间接影响了叶绿体的发育。同时CHY下调了编码叶绿体内蛋白的Cab1R、Cab2R、PsbA和RbcL基因的表达和上调了PsaA基因的表达。
3、遗传分析鉴定EMS诱变的pgl4为隐性单基因控制的突变体,三叶期叶片为淡绿色,三叶期后只有新长出来的心叶为淡绿色,随着叶片完全展开而逐渐变绿。突变体在抽穗期叶绿素含量与野生型没有明显差异,但光合速率和气孔导度明显低于野生型。在三叶期,突变体pgl4的叶绿体的类囊体发育紊乱,出现液泡状,而在抽穗期与野生型没有差异。突变基因PGL4精细定位在某号染色体的21Kb的范围内,测序分析发现一个编码CLP蛋白水解酶的基因在ATG后的第926个碱基由G突变成A,突变位点位于基因的第二个内含子与第三个外显子的剪切位点,突变导致RNA的剪切位点向后移动了9个碱基。T-DNA插入敲除了基因的功能,导致植株白化致死。RNAi干涉的转基因苗心叶为淡黄叶,叶片全展后变成绿色。T-DNA插入和RNAi干涉结果进一步验证了基因PGL4编码了一个CLP蛋白水解酶。基因PGL4在根、茎、叶、鞘和穗等五个器官中均表达,但在叶和鞘中表达最高,根中表达最低。基因PGL4被T-DNA插入敲除后,下调了核基因OsGLK的表达,从而间接影响了编码叶绿体内蛋白的基因PsaA、PsbA和RbcL的表达。本研究还对叶色突变体用作标记性状在杂交育种上的应用进行了分析。
4、突变体st1l从苗期开始叶片表现为白条状,穗颖壳成白色。在24℃处理下,突变体st1l叶片没有白条叶表型；在28℃处理下,突变体st1l叶片出现少量的白条纹；在32℃处理下,突变体st1l几乎成白化状,表明突变体st1l为高温敏感型白条叶,临界温度在28℃左右。遗传分析表明突变体st1l为单基因控制的隐性突变,但突变体的自交后代伴随出现白化致死苗,并具有细胞质效应,以突变体st1l为母本杂交,F,均出现一半的白化致死苗,其遗传模式还有待研究。利用混合法将突变基因STll初定位在Chr6短臂上的RM225和RM217之间,遗传距离为3.9cM。在此区间进一步设计5对分子标记,突变基因定位在标记RM584和WP-4之间的143Kb的范围内。在该范围内有12个具有全长cDNA支持的ORF,其中有一个编码核苷二磷酸还原酶大亚基的基因(LOC_Os06g07210),序列分析表明在该基因第15个外显子上有一个碱基发生错义突变,由G突变成了A,位于ATG起始后的第3859个碱基,氨基酸由甲硫氨酸变成异亮氨酸。突变体st1l在24℃、28℃和32℃处理下,基因ST1l表达没有明显差异。在32℃高温处理下,基因ST11下调了Cab1R和RbcL两个基因的表达。
Leaf is an important organ for photosynthesis and the major source for carbohydrates. Photosynthetic efficiency is closely related to chlorophyll content, the shape and structure of chloroplast, the place for plant photosynthesis, which will affect the photosynthesis, growth and development of the plant. Leaf color-related mutants are important materials to study the synthesis, regulation and degradation of the chlorophyll, the growth and development of the chloroplast and the signal transmission between chloroplasts and the nucleus. Rice is the cereal crops which has smallest genome size, and as a model plant, it is used to research the genetic and development of the cereal crops. Following the completion of the rice genome sequencing project and the continuous development of correlation technology, and the constructing of all kinds of rice mutant library, it is an essential task in post-genome era to identify the important genes in specific biological process and learn to know the functions by using forward genetics and reverse genetics
In this study, there were three leaf color-related mutants which were selected from restorer lines and derived from Ethylmethyl Sulfone (EMS) mutagenesis, respectively, they were natural mutant Chy (chlorophyll) with the semi-dominant yellow-leaf trait, natural mutant stll (stripe11) with the temperature-sensitive white-stripe leaf trait and the pgl4(pale green leaf4). We studied the morphological identification of the mutants, the electron microscopy of the chloroplast development, genetic analysis, the measurement of photosynthetic and physiological traits, the mapping and cloning of genes, the constructions of each vector, the complementation test and the regulation of the genes express. And the main results were summarized as follows:
1. Genetic analysis indicated that Chy belongs to a semi-dominant genetic model which was controlled by one gene locus. Chy lacked chlorophyll a and b, and the development of chloroplast obstructed, then the shape of chloroplasts were abnormal and into vacuole shape. There were not complete thylakoids in Chy which was lethal at three-leaf stage. Heterozygote Chy/+showed yellow-leaf, and the content of chlorophyll a and b were both lower than the wild-type at two-leaf stage, seedling stage, tillering stageand heading stage, respectively, but the ratio of chlorophyll a and b of Chy/+was higher than the wild-type at the stage above and stayed consistent, the development of the chloroplast disordered partially. The plant height, growth stages and the grain number per panicle showed significant difference between Chy/+and the wild-type. The CHY was located on chromosome3between the markers RM1164and RM8208, which was near the centromere, then the candidate region was delimited to a2.1Mb physical distance on either side of centromere by using the newly developed11pairs of molecular markers.
2. We found that the CHLI gene (LOC_Os03g36540) which encoded Mg-chelatase I subunit on the BAC AC084767may be related to the mutants Chy. The result of sequence analysis showed that there was a single substitution (G to C) in coding region of CHLI, which resulted in the amino acid changed from glutamate into glutamine, the substitution was in the conserved AAA+domain, Chy and the mutant chl9were allelic, then CHLI considered as the candidate gene for CHY. We connected the6.9Kb DNA fragment from CHY including the promoter region,5'non-translated region and3' non-translated region to the complementary vector, and transferred to Nipponbare by agrobacterium-mediated approach, and we got5positive plants. Compared with the control, in To generation the transgenic plants did not show significant difference in leaf colour, while in T1generation, there were a quarter of (pale) yellow leaf individuals, then we crossed the (pale) yellow leaf individuals with chl9, and the analysis on the F1showed that the segregated (pale) yellow leaf individuals were transgenic complementary plants rather than the leaf color-related mutants which were generated from the tissue culture. The complementation test further identified that the CHY was the CHLI. CHY showed dose effect. Semi-qRT-PCR analysis indicated that CHY down-regulated the CHLH, PORA and CAO-1expression, and CHY affected indirectly the development of chloroplast by down-regulating the CHLH expression. Meanwhile, CHY also down-regulated expression of CablR, Cab2R, PsbA and RbcL encoded the proteins in chloroplast and up-regulated PsaA expression.
3. Genetic analysis indicated that pgl4was a mutant with a recessive gene controlled, the leaf showed virescent at three-leaf stage, after which only the newly growing leaf showed virescent, and the leaf color gradually become green with the leaf completely unfolded. At heading, the chlorophyll content was not significant difference between pgl4and the wild-type, while the photosynthetic rate and the stomatal conductance of pgl4were obviously lower than that of the wild-type. At three-leaf stage, the development of thylakoids of pgl4disordered and vacuole appeared, while there was not difference at heading compared with the wild-type. PGL4was mapped to a21Kb physical distance on the chromosome, the result of sequence analysis indicated that there was a single substitution (G to A) at the926th base in PGL4which encoded CLP proteolytic enzymes, and the substitution was at the splice site between the second intron and the third exon, which resulted in the splice site moved backward for nine bases. PGL4in T-DNA insertion line lost the function and the mutant showed albino and lethal. The transgenic plants which transferred with the RNAi vector showed pale yellow, and the leaf turned to green when completely unfolded. Both the insertion and the RNAi results further identified that PGL4encoded a CLP proteolytic enzymes. PGL4expressed in the root, shoot, leaf, sheath and panicle organs, but it expressed highest in the leaf and the sheath, while lowest in the root. When inserted by T-DNA, it down-regulated the nuclear genes OsGLK expression, and then affected the PsaA,,PsbA and RbcL expression, which encoded the protein in chloroplast. In addition, we also analyzed that leaf color-related mutants were put into use for hybrid breeding as marker traits.
4. stll showed white stripe during the seedling, and the glume turned white. stll that cultivated in24℃was normal, while in28℃, it showed white stripe, and in32℃, it almost showed albino, which indicated that stll was temperature-sensitive white-stripe leaf mutant and the critical temperature was28℃. Genetic analysis indicated that stll was a recessive mutant and controlled by a single gene. But when the mutant selfing, there were albinos in the descendant, and the plant showed cytoplasmic effect..To cross stll as the maternal parent, the individuals of the F1of all cross showed half albino, and the genetic model are still being worked out. The ST11was located on the short arm of the chromosome6between the markers RM225and RM217, and the genetic distance was3.9cM. Then the candidate region was delimited to a143Kb physical distance between the RM584and WP-4by using the developed5pairs molecular markers. There were12open reading frames in the candidate region, among which there was a gene (LOC_Os06g07210) encoded the large subunit nucleoside diphosphate reducase, the sequencing analysis showed that there was a missense mutation in the fifteen exon (G-A), which was the3859th base, this missense mutation resulted in the amino acid changed from methionine into isoleucine., There was no difference in the expression of ST11when stll subject to24℃,28℃and32℃. And, ST11down-regulated the expression of Cab1R and RbcL at32℃
本研究针对从恢复系选育和EMS诱变所获得的三份叶色突变体,即半显性黄叶自然突变体Chy(chlorophyll)、温敏型白条叶自然突变体st11(stripe11)和淡绿叶EMS诱变突变体pgl4(pale green leaf4),开展了突变体的形态学鉴定、叶绿体发育的电镜观察、遗传分析、光合生理测定、基因定位与克隆、载体构建、转基因功能验证和基因表达调控研究,其主要研究结果如下：
1、遗传分析表明突变体Chy为单基因控制的半显性遗传模式。突变体Chy缺失叶绿素a和b,叶绿体发育受阻,呈液泡状,没有完整的类囊体,突变体Chy出芽后在三叶期致死。杂合体Chy/+为黄叶色,叶绿素a和b的含量在二叶期、苗期、分蘖期和抽穗期四个不同时期均比野生型要低,但杂合体Chy/+的叶绿素a/b比值在四个时期均比野生型要高,且较为稳定一致,杂合体Chy/+的叶绿体发育也存在部分紊乱。杂合体Chy/+的农艺性状与野生型相比,主要在株高、生育期和每穗粒数上差异显著。利用混合法将突变基因CHY初定位在Chr3的RM1164和RM8208之间,位于着丝粒附近,在此区间进一步设计11对分子标记引物,将突变基因CHY定位在着丝粒两侧的2.1Mb的范围内。
2、利用网络资源和相关文献资料信息,查找发现一个位于BAC号为AC084767上的编码镁离子螯合酶Ⅰ亚基的CHLI基因(LOC_Os03g36540)可能与叶色突变体Chy的表型相关。测序结果表明CHLI基因的编码区第921个碱基由G突变成C,氨基酸由谷氨酸变成谷氨酰胺,突变位于CHLI基因的保守AAA+结构域上,突变体Chy与突变体chl9等位,基因CHLI为突变基因CHY的侯选基因。把突变基因CHY(包括启动子区、5’非翻译区和3’非翻译区在内)的6.9Kb的DNA片段连接到互补载体上,通过农杆菌介导法转入日本晴愈伤,获得5株阳性植株。与转空载体的日本晴对比,转基因植株T0代没有明显的叶色变化,T.代中分离出四分之一的(淡)黄叶植株,用转基因T1代中的(淡)黄叶色植株与突变体chl9进行杂交,F1验证T1代中分离出的(淡)黄叶植株是转基因互补植株,不是来自组培过程中叶色突变体。转基因进一步互补验证了突变基因CHY就是CHLI基因,突变基因CHY具有剂量效应。半定量RT-PCR检测发现CHY下调了叶绿素合成途径中的CHLH、PORA和CAO-1基因的表达,通过下调CHLH基因的表达间接影响了叶绿体的发育。同时CHY下调了编码叶绿体内蛋白的Cab1R、Cab2R、PsbA和RbcL基因的表达和上调了PsaA基因的表达。
3、遗传分析鉴定EMS诱变的pgl4为隐性单基因控制的突变体,三叶期叶片为淡绿色,三叶期后只有新长出来的心叶为淡绿色,随着叶片完全展开而逐渐变绿。突变体在抽穗期叶绿素含量与野生型没有明显差异,但光合速率和气孔导度明显低于野生型。在三叶期,突变体pgl4的叶绿体的类囊体发育紊乱,出现液泡状,而在抽穗期与野生型没有差异。突变基因PGL4精细定位在某号染色体的21Kb的范围内,测序分析发现一个编码CLP蛋白水解酶的基因在ATG后的第926个碱基由G突变成A,突变位点位于基因的第二个内含子与第三个外显子的剪切位点,突变导致RNA的剪切位点向后移动了9个碱基。T-DNA插入敲除了基因的功能,导致植株白化致死。RNAi干涉的转基因苗心叶为淡黄叶,叶片全展后变成绿色。T-DNA插入和RNAi干涉结果进一步验证了基因PGL4编码了一个CLP蛋白水解酶。基因PGL4在根、茎、叶、鞘和穗等五个器官中均表达,但在叶和鞘中表达最高,根中表达最低。基因PGL4被T-DNA插入敲除后,下调了核基因OsGLK的表达,从而间接影响了编码叶绿体内蛋白的基因PsaA、PsbA和RbcL的表达。本研究还对叶色突变体用作标记性状在杂交育种上的应用进行了分析。
4、突变体st1l从苗期开始叶片表现为白条状,穗颖壳成白色。在24℃处理下,突变体st1l叶片没有白条叶表型；在28℃处理下,突变体st1l叶片出现少量的白条纹；在32℃处理下,突变体st1l几乎成白化状,表明突变体st1l为高温敏感型白条叶,临界温度在28℃左右。遗传分析表明突变体st1l为单基因控制的隐性突变,但突变体的自交后代伴随出现白化致死苗,并具有细胞质效应,以突变体st1l为母本杂交,F,均出现一半的白化致死苗,其遗传模式还有待研究。利用混合法将突变基因STll初定位在Chr6短臂上的RM225和RM217之间,遗传距离为3.9cM。在此区间进一步设计5对分子标记,突变基因定位在标记RM584和WP-4之间的143Kb的范围内。在该范围内有12个具有全长cDNA支持的ORF,其中有一个编码核苷二磷酸还原酶大亚基的基因(LOC_Os06g07210),序列分析表明在该基因第15个外显子上有一个碱基发生错义突变,由G突变成了A,位于ATG起始后的第3859个碱基,氨基酸由甲硫氨酸变成异亮氨酸。突变体st1l在24℃、28℃和32℃处理下,基因ST1l表达没有明显差异。在32℃高温处理下,基因ST11下调了Cab1R和RbcL两个基因的表达。
Leaf is an important organ for photosynthesis and the major source for carbohydrates. Photosynthetic efficiency is closely related to chlorophyll content, the shape and structure of chloroplast, the place for plant photosynthesis, which will affect the photosynthesis, growth and development of the plant. Leaf color-related mutants are important materials to study the synthesis, regulation and degradation of the chlorophyll, the growth and development of the chloroplast and the signal transmission between chloroplasts and the nucleus. Rice is the cereal crops which has smallest genome size, and as a model plant, it is used to research the genetic and development of the cereal crops. Following the completion of the rice genome sequencing project and the continuous development of correlation technology, and the constructing of all kinds of rice mutant library, it is an essential task in post-genome era to identify the important genes in specific biological process and learn to know the functions by using forward genetics and reverse genetics
In this study, there were three leaf color-related mutants which were selected from restorer lines and derived from Ethylmethyl Sulfone (EMS) mutagenesis, respectively, they were natural mutant Chy (chlorophyll) with the semi-dominant yellow-leaf trait, natural mutant stll (stripe11) with the temperature-sensitive white-stripe leaf trait and the pgl4(pale green leaf4). We studied the morphological identification of the mutants, the electron microscopy of the chloroplast development, genetic analysis, the measurement of photosynthetic and physiological traits, the mapping and cloning of genes, the constructions of each vector, the complementation test and the regulation of the genes express. And the main results were summarized as follows:
1. Genetic analysis indicated that Chy belongs to a semi-dominant genetic model which was controlled by one gene locus. Chy lacked chlorophyll a and b, and the development of chloroplast obstructed, then the shape of chloroplasts were abnormal and into vacuole shape. There were not complete thylakoids in Chy which was lethal at three-leaf stage. Heterozygote Chy/+showed yellow-leaf, and the content of chlorophyll a and b were both lower than the wild-type at two-leaf stage, seedling stage, tillering stageand heading stage, respectively, but the ratio of chlorophyll a and b of Chy/+was higher than the wild-type at the stage above and stayed consistent, the development of the chloroplast disordered partially. The plant height, growth stages and the grain number per panicle showed significant difference between Chy/+and the wild-type. The CHY was located on chromosome3between the markers RM1164and RM8208, which was near the centromere, then the candidate region was delimited to a2.1Mb physical distance on either side of centromere by using the newly developed11pairs of molecular markers.
2. We found that the CHLI gene (LOC_Os03g36540) which encoded Mg-chelatase I subunit on the BAC AC084767may be related to the mutants Chy. The result of sequence analysis showed that there was a single substitution (G to C) in coding region of CHLI, which resulted in the amino acid changed from glutamate into glutamine, the substitution was in the conserved AAA+domain, Chy and the mutant chl9were allelic, then CHLI considered as the candidate gene for CHY. We connected the6.9Kb DNA fragment from CHY including the promoter region,5'non-translated region and3' non-translated region to the complementary vector, and transferred to Nipponbare by agrobacterium-mediated approach, and we got5positive plants. Compared with the control, in To generation the transgenic plants did not show significant difference in leaf colour, while in T1generation, there were a quarter of (pale) yellow leaf individuals, then we crossed the (pale) yellow leaf individuals with chl9, and the analysis on the F1showed that the segregated (pale) yellow leaf individuals were transgenic complementary plants rather than the leaf color-related mutants which were generated from the tissue culture. The complementation test further identified that the CHY was the CHLI. CHY showed dose effect. Semi-qRT-PCR analysis indicated that CHY down-regulated the CHLH, PORA and CAO-1expression, and CHY affected indirectly the development of chloroplast by down-regulating the CHLH expression. Meanwhile, CHY also down-regulated expression of CablR, Cab2R, PsbA and RbcL encoded the proteins in chloroplast and up-regulated PsaA expression.
3. Genetic analysis indicated that pgl4was a mutant with a recessive gene controlled, the leaf showed virescent at three-leaf stage, after which only the newly growing leaf showed virescent, and the leaf color gradually become green with the leaf completely unfolded. At heading, the chlorophyll content was not significant difference between pgl4and the wild-type, while the photosynthetic rate and the stomatal conductance of pgl4were obviously lower than that of the wild-type. At three-leaf stage, the development of thylakoids of pgl4disordered and vacuole appeared, while there was not difference at heading compared with the wild-type. PGL4was mapped to a21Kb physical distance on the chromosome, the result of sequence analysis indicated that there was a single substitution (G to A) at the926th base in PGL4which encoded CLP proteolytic enzymes, and the substitution was at the splice site between the second intron and the third exon, which resulted in the splice site moved backward for nine bases. PGL4in T-DNA insertion line lost the function and the mutant showed albino and lethal. The transgenic plants which transferred with the RNAi vector showed pale yellow, and the leaf turned to green when completely unfolded. Both the insertion and the RNAi results further identified that PGL4encoded a CLP proteolytic enzymes. PGL4expressed in the root, shoot, leaf, sheath and panicle organs, but it expressed highest in the leaf and the sheath, while lowest in the root. When inserted by T-DNA, it down-regulated the nuclear genes OsGLK expression, and then affected the PsaA,,PsbA and RbcL expression, which encoded the protein in chloroplast. In addition, we also analyzed that leaf color-related mutants were put into use for hybrid breeding as marker traits.
4. stll showed white stripe during the seedling, and the glume turned white. stll that cultivated in24℃was normal, while in28℃, it showed white stripe, and in32℃, it almost showed albino, which indicated that stll was temperature-sensitive white-stripe leaf mutant and the critical temperature was28℃. Genetic analysis indicated that stll was a recessive mutant and controlled by a single gene. But when the mutant selfing, there were albinos in the descendant, and the plant showed cytoplasmic effect..To cross stll as the maternal parent, the individuals of the F1of all cross showed half albino, and the genetic model are still being worked out. The ST11was located on the short arm of the chromosome6between the markers RM225and RM217, and the genetic distance was3.9cM. Then the candidate region was delimited to a143Kb physical distance between the RM584and WP-4by using the developed5pairs molecular markers. There were12open reading frames in the candidate region, among which there was a gene (LOC_Os06g07210) encoded the large subunit nucleoside diphosphate reducase, the sequencing analysis showed that there was a missense mutation in the fifteen exon (G-A), which was the3859th base, this missense mutation resulted in the amino acid changed from methionine into isoleucine., There was no difference in the expression of ST11when stll subject to24℃,28℃and32℃. And, ST11down-regulated the expression of Cab1R and RbcL at32℃
引文
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