白菜花粉发育与授粉受精相关基因BcJMJ30和BcMF22的表达分析与功能验证
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摘要
花粉发育与授粉受精是一个多步骤、多基因调控的复杂生物学过程。近年来,通过拟南芥、水稻的花粉转录组和蛋白质组大规模分析,发现成熟花粉中储存有后续花粉萌发和花粉管生长过程所需的mRNA,也储存了该过程所需的蛋白质。在花粉发育与授粉受精这个多步骤的复杂过程中,目前的研究基本都只关注基因在某一步骤的功能。虽然早就有猜测花粉中积累和储存的多种mRNA可能是用于花粉萌发和花粉管生长。但目前尚未研究这些持续表达基因在这两个步骤中的作用,也未明确它们如何通过表达调控与不同发育过程联系起来。本实验室采用ATH1芯片分析了白菜ajhGMS 'Bajh97-01A/B花蕾差异表达基因和ajhGMS 'Bajh97-01A授粉前后雌蕊差异表达基因时,检测到一批花粉发育与授粉受精持续特异表达基因(黄鹂等,未发表；蒋晶晶等,未发表)。其中转录本标识为At3g20810的基因可编码含有JmjC域的组蛋白去甲基化酶可能作用于花粉发育与授粉受精过程。在植物中,含有JmjC域的组蛋白去甲基化酶对植物的生长发育具有重要的作用,但对于其功能的研究较少。另一个转录本标识为Atlg58120的基因编码一个甲基转移酶亦可能作用于花粉发育与授粉受精过程。为了研究这两个基因的结构和表达特征,为进一步确定其功能打下基础,本研究采用同源扩增和RACE技术克隆基因全长,分析其序列特征并预测其蛋白结构,进而采用RT-PCR或qRT-PCR方法分析其在可育株系和不育株系不同发育阶段花蕾和授粉前后雌蕊的表达情况,采用组织原位杂交技术进一步确定基因的细胞定位,分析其与花粉发育与授粉受精的关系；最后构建反义RNA表达载体,利用农杆菌介导的方法导入菜心中,对获得的HygR植株进行分子、形态和细胞学的检测,从而初步分析其功能。取得的主要结果如下：
(1)在分析白菜核隐性雄性不育两用系'Bajh97-01AB花蕾和授粉前后雌蕊的基因表达差异时,检测到一批花粉发育与授粉受精持续特异表达的基因,发现一个含JmjC域的组蛋白去甲基化酶基因,利用同源扩增、TAIL-PCR及3'RACE相结合的方法扩增获得其cDNA和DNA全长。该基因DNA全长共1956bp,其ORF全长为1245bp,包含6段内含子。该基因编码414个氨基酸,其二级结构含有46.8%的α螺旋,46.8%的β折叠和16.9%的环状结构。通过SMART数据库推测该蛋白存在含JmjC域组蛋白去甲基化酶经典的结构域JmjC,该结构域位于第257～414个氨基酸位点。该基因与拟南芥中AtJMJ30编码的氨基酸序列比较,发现具有相同的特征,同源性高,故将其命名为Brassica campestris JMJ30(BcJMJ30)。
(2)对BcJMJ30在可育株系开放花、嫩角果、花茎、叶和根中的表达情况进行RT-PCR和qRT-PCR分析,发现BcJMJ30在开放花和花茎中表达量较高；对不育株系和可育株系5级花蕾进行表达分析,结果表明该基因在可育株系的5级花蕾中均有表达,到第V级花蕾时表达水平下降,在不育株系的第Ⅰ、Ⅱ级花蕾中亦有表达,随着花蕾的继续发育,该基因在不育株系第Ⅲ～V级花蕾中不表达；对其在不育株系授粉后雌蕊的表达情况进行分析,发现在授粉后的雌蕊中,BcJMJ30仍持续表达,在授粉后2～8h表达量高,随后又下降。应用组织原位杂交方法对BcJMJ30进行细胞定位,结果表明该基因在第Ⅱ～V花蕾的花粉中特异表达。
(3)为了研究BcJMJ30在花粉发育与授粉受精过程中的功能,我们构建了BcJMJ30反义表达载体,并对获得的反义BaJMJ30菜心阳性转基因植株进行分子、形态和细胞学的检测。结果发现BcJMJ30的表达被抑制会影响花粉的发育过程,导致部分花粉发育异常,表型为花粉体积小、花粉不饱满、形状不规则、网纹模糊等,其花粉的异常率是25.21%,且降低花粉萌发率,导致花粉管异常,如花粉管呈念珠状,花粉管顶端爆裂等。花粉体内萌发实验表明,在转基因菜心植株中BcJMJ30表达的抑制会导致部分花粉停留在柱头表面不萌发。
(4)在分析白菜核隐性雄性不育两用系'Bajh97-01A/B花蕾和授粉前后雌蕊的基因表达差异,发现一个可编码甲基转移酶的基因,利用利用同源扩增及3'RACE相结合的方法扩增得到了其cDNA全长。cDNA全长为1870bp, DNA全长为1260bp, ORF为1260bp,不包含内含子。该基因编码419个氨基酸,利用ProtParam数据库分析该蛋白为脂肪族的,且不稳定的蛋白。通过数据库TMHMM分析,发现该蛋白含有一个跨膜区域,其二级结构为29.6%螺旋结构,18.6%折叠结构,51.8%呈环结构。
(5)对BcMF22在可育株系开放花、花茎、嫩角果和叶片中的表达情况进行qRT-PCR分析,发现该基因在开放花中大量表达,嫩角果和叶片中少量表达：对其在不育株系和可育株系5级花蕾进行表达分析,发现其在可育株系5级花蕾中均表达,到第V级花蕾时表达量达到最高；对其在不育株系授粉前后雌蕊的表达情况进行分析,发现其在授粉后雌蕊中的表达明显高于未授粉的雌蕊,于授粉后4h的雌蕊表达量最高,之后表达量降低；进而选取第V级花蕾的花瓣、萼片、雌蕊、雄蕊和蜜腺进行表达分析,结果表明其在雄蕊中表达量最高,其它组织几乎不表达。故将该基因命名为Brassica campestrismale fertility22(BcMF22)。应用组织原位杂交方法对BcMF22进行细胞定位,结果表明BcMF22mRNA的杂交信号在花粉母细胞到成熟花粉粒中检测到,成熟花粉粒杂交信号最强,且在授粉后4h的雌蕊中检测到,信号出现在授粉后雌蕊的柱头和花柱中。
(6)为了研究BcMF22在花粉发育与授粉受精过程中的功能,我们构建了BcMF22的反义表达载体,并对获得的BcMF22菜心阳性转基因植株进行分子、形态和细胞学的检测。结果发现BcMF22的表达被抑制会影响花粉的发育过程,导致部分花粉发育异常,表现为花粉体积小,用苯胺蓝和DAPI染色后荧光信号弱等,其花粉的异常率为25.76%,且能降低花粉萌发率,导致花粉管一旦萌发,其顶端即爆裂,爆裂的花粉管约占73%。
Pollen development and pollination are multi-step processes that regulated by thousands of genes. Recently, the large-scale pollen transcriptomic and proteomes in Arabidopsis and Rice has also shown that mRNAs which played a crucial role in pollen germination and pollen tube growth were stored in mature pollens. During the multi-step process, current researches only focus on the function of genes in one step. Although several speculations believed that pollen grain accumulation and storage of a variety of mRNA may be used for pollen germination and pollen tube growth. But there has little researches about the function of these continuously expressed genes in this process, and there is not clear that how they established the link between expression regulation and different developmental processes.
In our previous study, we analyzed the expression pattern of pollen development and fertilization-related genes by AT HI microarray of 'Aijiaohuang' genie male sterile AB line (Bajh97-01A/B) in Chinese cabbage-pak-choi (Brassica campestris L. ssp. chinensis Makino), and found several gene which specifically up regulated in pollen and pollinated pistil. Among them, one is a JmjC domain containing histone demethylase gene (Transcript ID:At3g20810) which may involved in pollen development and pollination (unpublished data), the other is a methyltransferase gene (Transcript ID:At1g58120) which may participate in pollen development and pollination. In plants, JmjC domain-containing histone demethylase play important roles in plant growth and development. But, the function of JmjC histone demethylase is not clear in plant reproductive. Therefore, in order to get the structure and expression characteristics of the homologous gene of At3g20810and Atlg58120in Chinese cabbage-pak-choi,we cloned the new gene through homological amplification and3'RACE methods and analysis its structure and speculated its biological function, we analyze the expression pattern of this gene using qRT-PCR and in situ hybridization. Through antisense RNA directional inhibition, the function of them during pollen and fertilization was identified.
(1)A pollen and fertilization related gene was isolated from B.campeatris. We determined the full-length DNA containing1956bp and an ORF of1245bp. Comparison of the cDNA and DNA sequence by Clustal X software showed that it composed of seven extrons and six introns. The secondary structural composition predicted by the PredictProtein server shows that there are46.8%helixes,34.5%sheet, and16.9%loop in the deduced protein structure. One JmjC domain of the gene was predicted by SMART, within the414deduced amino acids, JmjC domain located between the amino acid257to414. Phylogenetic tree indicated that the gene is closely related to At3g20810(AtJMJ30) in Arabidopsis, so we named it as JMJ30(BcJM.130).
(2) Here, we used qRT-PCR and in situ hybridization to determine the expression pattern of BcJMJ30. It was highly expressed in open flowers and scapes compared with germinal siliques, leaves and roots. It was continuously expressed during flower buds in fertile plants but had its strong expression in the first two stages of the ones of sterile plants. BcJMJ30mRNA mainly expressed in the stamens and petals compared with other flower parts such as sepals, pistils and nectarys. And there was a significant increased expression level in the pollinated pistils.
(3) Functional analysis of BcJMJ30by anti-sense technique revealed that it can affect the size, shape and plumpness of pollen,25.21%of the pollen grains from anti-sense transgenitc plants exhibited abnormal, and reduce the pollen germination rate, leading to abnormal pollen tube. Statistics show that, the ratio of abnormal pollen tube of it is higher than the control. Moreover, in vivo pollen germination assay showed that in transgenic plantlets can reduced the pollen germinated on pistil, after4h pollination there still exist some observable pollen on stigma of the pistil compared with the control.
(4) A pollen and fertilization related gene was isolated from B.campeatris. The cDNA sequence of the gene was1870bp and contained an open reading frame of1260bp which encoded419amino acids. ProtParam database analysis of the protein indicated it was aliphatic and unstable. Genomic sequence of it contained no introns. The secondary structural composition predicted by the PredictProtein server shows that there are29.6%helix,18.6%sheet, and51.8%%loop in the deduced protein structure. Sequence prediction indicated that the gene might encode a methyltransferase.
(5) We used qRT-PCR and in situ hybridization to determine the expression pattern of the gene. We confirmed that it was expressed at higher levels in open flowers than in other organs (siliques, scopes and leaves). In different pollen developmental stages it was continuatively expressed in flower buds at five developmental stages in fertile plants, and expressed at higher transcript levels in the flower buds of fertile plants compared to the sterile plants except Stage Ⅰ, especially on a very high level in the Stage V. So we named it as Brassica campestris Male Fertility22(BcMF22). Further expression analysis among Petal, Sepal, stamen, pistil, and nectary showed that it just expressed in stamen. After pollination, BcMF22was expressed at higher levels in pistils at1,2and4HAP than their corresponding controls, especially on a very high level in the4HAP.
(6) Functional analysis of BcMF22by anti-sense technique revealed that it can affect the pollen development, and even reduce the viability of pollen,25.76%of the pollen grains exhibited abnormal. Histochemical staining showed that transgenic plants could reduce the fluorescence signal of pollen. Transgenic plants leaded to decrease the germination ratio of pollen, once pollen germination, then the top of pollen tube was burst, abnormal pollen tube accounted for73%.
(1)在分析白菜核隐性雄性不育两用系'Bajh97-01AB花蕾和授粉前后雌蕊的基因表达差异时,检测到一批花粉发育与授粉受精持续特异表达的基因,发现一个含JmjC域的组蛋白去甲基化酶基因,利用同源扩增、TAIL-PCR及3'RACE相结合的方法扩增获得其cDNA和DNA全长。该基因DNA全长共1956bp,其ORF全长为1245bp,包含6段内含子。该基因编码414个氨基酸,其二级结构含有46.8%的α螺旋,46.8%的β折叠和16.9%的环状结构。通过SMART数据库推测该蛋白存在含JmjC域组蛋白去甲基化酶经典的结构域JmjC,该结构域位于第257～414个氨基酸位点。该基因与拟南芥中AtJMJ30编码的氨基酸序列比较,发现具有相同的特征,同源性高,故将其命名为Brassica campestris JMJ30(BcJMJ30)。
(2)对BcJMJ30在可育株系开放花、嫩角果、花茎、叶和根中的表达情况进行RT-PCR和qRT-PCR分析,发现BcJMJ30在开放花和花茎中表达量较高；对不育株系和可育株系5级花蕾进行表达分析,结果表明该基因在可育株系的5级花蕾中均有表达,到第V级花蕾时表达水平下降,在不育株系的第Ⅰ、Ⅱ级花蕾中亦有表达,随着花蕾的继续发育,该基因在不育株系第Ⅲ～V级花蕾中不表达；对其在不育株系授粉后雌蕊的表达情况进行分析,发现在授粉后的雌蕊中,BcJMJ30仍持续表达,在授粉后2～8h表达量高,随后又下降。应用组织原位杂交方法对BcJMJ30进行细胞定位,结果表明该基因在第Ⅱ～V花蕾的花粉中特异表达。
(3)为了研究BcJMJ30在花粉发育与授粉受精过程中的功能,我们构建了BcJMJ30反义表达载体,并对获得的反义BaJMJ30菜心阳性转基因植株进行分子、形态和细胞学的检测。结果发现BcJMJ30的表达被抑制会影响花粉的发育过程,导致部分花粉发育异常,表型为花粉体积小、花粉不饱满、形状不规则、网纹模糊等,其花粉的异常率是25.21%,且降低花粉萌发率,导致花粉管异常,如花粉管呈念珠状,花粉管顶端爆裂等。花粉体内萌发实验表明,在转基因菜心植株中BcJMJ30表达的抑制会导致部分花粉停留在柱头表面不萌发。
(4)在分析白菜核隐性雄性不育两用系'Bajh97-01A/B花蕾和授粉前后雌蕊的基因表达差异,发现一个可编码甲基转移酶的基因,利用利用同源扩增及3'RACE相结合的方法扩增得到了其cDNA全长。cDNA全长为1870bp, DNA全长为1260bp, ORF为1260bp,不包含内含子。该基因编码419个氨基酸,利用ProtParam数据库分析该蛋白为脂肪族的,且不稳定的蛋白。通过数据库TMHMM分析,发现该蛋白含有一个跨膜区域,其二级结构为29.6%螺旋结构,18.6%折叠结构,51.8%呈环结构。
(5)对BcMF22在可育株系开放花、花茎、嫩角果和叶片中的表达情况进行qRT-PCR分析,发现该基因在开放花中大量表达,嫩角果和叶片中少量表达：对其在不育株系和可育株系5级花蕾进行表达分析,发现其在可育株系5级花蕾中均表达,到第V级花蕾时表达量达到最高；对其在不育株系授粉前后雌蕊的表达情况进行分析,发现其在授粉后雌蕊中的表达明显高于未授粉的雌蕊,于授粉后4h的雌蕊表达量最高,之后表达量降低；进而选取第V级花蕾的花瓣、萼片、雌蕊、雄蕊和蜜腺进行表达分析,结果表明其在雄蕊中表达量最高,其它组织几乎不表达。故将该基因命名为Brassica campestrismale fertility22(BcMF22)。应用组织原位杂交方法对BcMF22进行细胞定位,结果表明BcMF22mRNA的杂交信号在花粉母细胞到成熟花粉粒中检测到,成熟花粉粒杂交信号最强,且在授粉后4h的雌蕊中检测到,信号出现在授粉后雌蕊的柱头和花柱中。
(6)为了研究BcMF22在花粉发育与授粉受精过程中的功能,我们构建了BcMF22的反义表达载体,并对获得的BcMF22菜心阳性转基因植株进行分子、形态和细胞学的检测。结果发现BcMF22的表达被抑制会影响花粉的发育过程,导致部分花粉发育异常,表现为花粉体积小,用苯胺蓝和DAPI染色后荧光信号弱等,其花粉的异常率为25.76%,且能降低花粉萌发率,导致花粉管一旦萌发,其顶端即爆裂,爆裂的花粉管约占73%。
Pollen development and pollination are multi-step processes that regulated by thousands of genes. Recently, the large-scale pollen transcriptomic and proteomes in Arabidopsis and Rice has also shown that mRNAs which played a crucial role in pollen germination and pollen tube growth were stored in mature pollens. During the multi-step process, current researches only focus on the function of genes in one step. Although several speculations believed that pollen grain accumulation and storage of a variety of mRNA may be used for pollen germination and pollen tube growth. But there has little researches about the function of these continuously expressed genes in this process, and there is not clear that how they established the link between expression regulation and different developmental processes.
In our previous study, we analyzed the expression pattern of pollen development and fertilization-related genes by AT HI microarray of 'Aijiaohuang' genie male sterile AB line (Bajh97-01A/B) in Chinese cabbage-pak-choi (Brassica campestris L. ssp. chinensis Makino), and found several gene which specifically up regulated in pollen and pollinated pistil. Among them, one is a JmjC domain containing histone demethylase gene (Transcript ID:At3g20810) which may involved in pollen development and pollination (unpublished data), the other is a methyltransferase gene (Transcript ID:At1g58120) which may participate in pollen development and pollination. In plants, JmjC domain-containing histone demethylase play important roles in plant growth and development. But, the function of JmjC histone demethylase is not clear in plant reproductive. Therefore, in order to get the structure and expression characteristics of the homologous gene of At3g20810and Atlg58120in Chinese cabbage-pak-choi,we cloned the new gene through homological amplification and3'RACE methods and analysis its structure and speculated its biological function, we analyze the expression pattern of this gene using qRT-PCR and in situ hybridization. Through antisense RNA directional inhibition, the function of them during pollen and fertilization was identified.
(1)A pollen and fertilization related gene was isolated from B.campeatris. We determined the full-length DNA containing1956bp and an ORF of1245bp. Comparison of the cDNA and DNA sequence by Clustal X software showed that it composed of seven extrons and six introns. The secondary structural composition predicted by the PredictProtein server shows that there are46.8%helixes,34.5%sheet, and16.9%loop in the deduced protein structure. One JmjC domain of the gene was predicted by SMART, within the414deduced amino acids, JmjC domain located between the amino acid257to414. Phylogenetic tree indicated that the gene is closely related to At3g20810(AtJMJ30) in Arabidopsis, so we named it as JMJ30(BcJM.130).
(2) Here, we used qRT-PCR and in situ hybridization to determine the expression pattern of BcJMJ30. It was highly expressed in open flowers and scapes compared with germinal siliques, leaves and roots. It was continuously expressed during flower buds in fertile plants but had its strong expression in the first two stages of the ones of sterile plants. BcJMJ30mRNA mainly expressed in the stamens and petals compared with other flower parts such as sepals, pistils and nectarys. And there was a significant increased expression level in the pollinated pistils.
(3) Functional analysis of BcJMJ30by anti-sense technique revealed that it can affect the size, shape and plumpness of pollen,25.21%of the pollen grains from anti-sense transgenitc plants exhibited abnormal, and reduce the pollen germination rate, leading to abnormal pollen tube. Statistics show that, the ratio of abnormal pollen tube of it is higher than the control. Moreover, in vivo pollen germination assay showed that in transgenic plantlets can reduced the pollen germinated on pistil, after4h pollination there still exist some observable pollen on stigma of the pistil compared with the control.
(4) A pollen and fertilization related gene was isolated from B.campeatris. The cDNA sequence of the gene was1870bp and contained an open reading frame of1260bp which encoded419amino acids. ProtParam database analysis of the protein indicated it was aliphatic and unstable. Genomic sequence of it contained no introns. The secondary structural composition predicted by the PredictProtein server shows that there are29.6%helix,18.6%sheet, and51.8%%loop in the deduced protein structure. Sequence prediction indicated that the gene might encode a methyltransferase.
(5) We used qRT-PCR and in situ hybridization to determine the expression pattern of the gene. We confirmed that it was expressed at higher levels in open flowers than in other organs (siliques, scopes and leaves). In different pollen developmental stages it was continuatively expressed in flower buds at five developmental stages in fertile plants, and expressed at higher transcript levels in the flower buds of fertile plants compared to the sterile plants except Stage Ⅰ, especially on a very high level in the Stage V. So we named it as Brassica campestris Male Fertility22(BcMF22). Further expression analysis among Petal, Sepal, stamen, pistil, and nectary showed that it just expressed in stamen. After pollination, BcMF22was expressed at higher levels in pistils at1,2and4HAP than their corresponding controls, especially on a very high level in the4HAP.
(6) Functional analysis of BcMF22by anti-sense technique revealed that it can affect the pollen development, and even reduce the viability of pollen,25.76%of the pollen grains exhibited abnormal. Histochemical staining showed that transgenic plants could reduce the fluorescence signal of pollen. Transgenic plants leaded to decrease the germination ratio of pollen, once pollen germination, then the top of pollen tube was burst, abnormal pollen tube accounted for73%.
引文
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