白菜型油菜同源四倍体与二倍体之间盐和镉胁迫耐性的差异及其分子机理
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摘要
白菜型油菜(Brassica campestris L.)是油菜三大类型之一。中国又称小白菜、矮油菜、甜油菜等。白菜型油菜在既是油料作物,又是一种非常重要的蔬菜。“矮脚黄”白菜是长江流域的主栽品种,在浙江也有大面积种植。
多倍体与二倍体比拥有较大的营养器官和生殖器官,在生长过程中表现出一定的抗性优势,但以往的研究多集中在异源多倍体的抗性差异上,而对同源多倍体和二倍体的抗性差异研究甚少。本文采用同源四倍体“矮脚黄”白菜和二倍体“矮脚黄”白菜为材料,其中同源四倍体“矮脚黄”白菜是由二倍体“矮脚黄”白菜直接加倍而来。文章从生理生化、表观遗传、分子表达三个角度研究了二者在盐和镉逆境条件下的逆境差异机理,得到的主要结果如下：
1)同源四倍体在高盐胁迫下具有较快的发芽速度,较多的健康植株数；低浓度盐能够有效的刺激四倍体茎和根的生长。发芽7天后,四倍体和二倍体植株体内的钾钠钙离子在不同组织中的分布存在差异明显。四倍体在高盐浓度中具有一定的抗性优势,而Na+/Ca2+可以作为筛选白菜抗性品种的一个重要指标。
2)在5-7叶期间,四倍体叶绿素含量受到盐害的影响较二倍体小,四倍体体内的抗氧化还原剂GSH较二倍体含量高,四倍体白菜和二倍体白菜在盐胁迫下用不同的活性氧清除体系,四倍体的抗氧化酶体系更加稳定。盐处理后期,钾钠钙离子在地上组织和地下组织中的分布差异明显,二倍体的地上组织能够吸收更多的钠离子,四倍体能够在一定程度上阻止钠离子向地上部分运输；四倍体的地下组织吸收更高的钠离子含量以及保持高水平的钾离子水平。四倍体在根部能通过保持较高的K+／Na+比值,使其具有一定的抗盐优势。随着处理时间的增加,二倍体和四倍体的Na+/Ca2+比值差异越大,这些实验说明四倍体可以通过保持较低的Na+/Ca2+比值来缓解盐害。
3)发芽7天后发现在高浓度的镉处理中,四倍体在发芽率、根茎长以及健康植株数目指标上比二倍体具有明显的优势。随着处理浓度的增加,二倍体各组织中镉的含量逐渐增加。四倍体在高浓度的处理下发芽期可以通过限制镉的摄入来降低根部的镉浓度。
4)随着镉处理浓度和时间的增加,四倍体叶绿素和GSH含量比二倍体高,叶片内的MDA积累量要比二倍体低。四倍体白菜和二倍体白菜在镉胁迫下,抗氧化酶变化趋势存在着差异,四倍体的抗氧化酶的活性在镉环境中的缓冲力要强于二倍体。说明了四倍体在镉胁迫下其体内的活性氧、过氧化氢可以通过高含量的GSH以及稳定的抗氧化酶体系得到及时的清除,使得四倍体在镉胁迫下有一定的生长优势。镉进入四倍体根部后,有一部分运输至地上组织(叶片),减轻了镉对四倍体根部的毒害。
5)用MSAP分析四倍体和二倍体的逆境抗性的差异,56对引物共得到14382条扩增带,总甲基化条带共2924条。二倍体和四倍体在盐胁迫中,其总体甲基化水平都呈下降趋势。在镉胁迫环境中,两者的总体甲基化有上升的趋势。二倍体的甲基化水平下降了1.5个百分点,而四倍体下降了2.5个百分点,四倍体甲基化程度下降得更快；在镉处理中,二倍体的甲基化水平上升了2.7个百分点,四倍体上升了3.5个百分点,四倍体镉甲基化水平上升的程度更高。
6)二倍体和四倍体经过逆境条件下,其MSAP的甲基化模式发生了改变,四倍体在盐胁迫下与二倍体在盐胁迫下,有35%的甲基化模式发生了去甲基化(B类型)过程,20.0%发生过甲基化(C类型)转变；四倍体在镉胁迫下与二倍体在镉胁迫下,有24.8%的甲基化模式发生了去甲基化(B类型)过程,25.8%发生过甲基化(C类型)转变。盐胁迫下,四倍体发生去甲基化的位点数比二倍体多,而发生过甲基化位点数相差不大,暗示了去甲基化位点在四倍体白菜和二倍体白菜盐胁迫差异中启着重要的作用；镉胁迫下,四倍体发生过甲基化的位点数比二倍体多,而发生去甲基化位点数相差不大,说明了过甲基化位点在四倍体白菜和二倍体白菜的镉胁迫差异中启着关键性作用。
7) cDNA-AFLP实验结果表明与二倍体和四倍体各自在对照条件下相比,二者在盐和镉胁迫条件下的差异有扩大的趋势。在盐胁迫的差异片段中,二倍体基因表达被抑制的有14条(0.52%),四倍体基因表达被抑制的7条(0.26%);四倍体基因表达被诱导的差异基因有10条(0.37%),而二倍体被诱导的差异基因有5条(0.19%)。在镉胁迫的差异片断中,二倍体基因表达被抑制的有7条(0.26%),四倍体基因表达被抑制的为16条(0.60%)；四倍体基因表达被诱导的有5条(0.19%),二倍体基因表达被诱导的有12条(0.45%)。四倍体和二倍体在不同的逆境环境中基因表达的模式有很大的差异,在盐胁迫中,差异片段在二倍体中大部分被抑制,在四倍体中大部分被诱导；镉胁迫下,二倍体中大部分的基因表达差异体现为被诱导,而在四倍体中大部分的基因表达差异体现为被抑制。
8)对盐和镉的不同胁迫下,对二倍体和四倍体中的差异片段进行测序发现,盐胁迫导致的18条TDFs中有16条(88.9%)在现有数据库已有基因的功能(或者推测功能)的描述,两条TDFs中有1条其功能未知,另外一条和现有数据库中基因无任何同源性。16个TDFs按照功能可以分为三类：细胞代谢类、胁迫响应类、转录因子类。盐胁迫中的差异片段功能大部分参与了ABA信号合成及传递、过氧化物酶合成、醛脱氢酶合成、甜菜合成键酶的过程。在镉胁迫差异片段中,20条TDFs中有15条(75%)在现有数据库已有基因的功能(或者推测功能)的描述,有5条功能不明确,其中3条与数据库中的基因具有一定程度的同源性,另外2条在数据库找不到同源基因。在镉胁迫实验中,二倍体和四倍体有差异按照功能可以分为四类：细胞代谢类、胁迫响应类、转录因子类、光合作用类。镉胁迫中的差异片段所体现的基因,其功能大部分参与了蛋白激酶、热击蛋白、光合蛋白合成途径。
Polyploidy is pursued in plant breeding programs due mainly to its ability to yield larger vegetative or reproductive organs. It could also be used to improve plant adaptation to saline or heavy metal contaminated soils because of the redundant genes implicated in stress tolerance, the status of the genome methylation degree and the pattern of gene expression at transcriptional level. However, little information is available about the ability of an autopolyploid to survive in stressed condition in comparison with its diploid progenitor. In this study, a tetraploid turnip (cv. Ai-Jiao-Huang 4X) and its diploid progenitor (cv. Ai-Jiao-Huang 2X) were compared for their tolerance to salinity stress and cadmium toxicity by investigating a group of morphological and physiological parameters. Methylation sensitive amplification polymorphism (MSAP) and cDNA-amplified fragment length polymorphism (cDNA-AFLP) analysis were employed to compare the degree of genome methylation and identify the genes induced or repressed under salinity and cadmium stresses. The major results are listed as the following.
1. The tetraploid turnip exhibited better adaptation to a highly concentrated salt medium (200 mM), as evidenced by a less affected germination rate and a healthier morphological appearance at the seedling stage. Furthermore, an extension of salinity stress up to a certain period of time at the 5-7 leaf stage shows differences between the tetraploid turnip and its diploid progenitor. The former had a higher K+/Na+ ratio in the roots, higher glutathione concentration and antioxidant activities in the leaves, and smaller reductions in photosynthetic capacity in terms of leaf chlorophyll content. On the other hand, the tetraploid turnip had a better tolerance to the cadmium treatment, reflected by higher germination rate, root length at seedling stage. An extension of cadmium toxicity at 5-7 leaf stage resulted in a less obvious impairment of chlorophyll, less alternation of antioxidants'activity and higher concentration of K+ and Ca2+ ions in shoots, but lower ratio of Na+/K+ in tetraploid, but higher concentration of Na+ in shoots and less availability of K+ and Ca2+ in both roots of the diploid.
2. Salinity stress and cadmium toxicity gave rise the significant changes of genome DNA methylation degree, as reflected by the MSAP analysis, which identified a total of 14382 bands generated by 56 primer pairs. A among a total of 2924 methylaiton bands,1731 were full the methylaiton type and 1193 were the half methylation type. The total methylaton ratio of the diploid in the control, salinity, and cadmium stressed conditions were 20.3,18.8,22.7; whereas the total methylaton ratio of the tetraploid in the control, salinity and cadmium stressed conditions were 20.3,18.8,22.7. The total methylaton level declined in both the diploid and tetraploid after salt treatment, but increased after cadmium treatment. In diploid the methylaton level decreased by 1.5 point, whereas in the tetraploid it decreased by 2.5 point after salt treatment. The full methylation ratio in diploid was 2.2 points higher than in tetraploid, while half methylation ratio in tetraploid was 1.6 points higher than in the diploid.
3. By using 96 primer pair combinations, about 2648,2650,2703,2730,2551 and 2580 cDNA fragments were generated respectively under the following treatments (1) tetraploid without stress; (2) diploid without stress; (3) tetraploid under salinity stress; (4) diploid under salinity stress; (5) tetraploid with cadmium toxicity; (6) diploid with cadmium toxicity. Salinity stress and cadmium toxicity led to 36 and 40 TDFs, respectively, which represented the functional genes that can be classified in to 3 or 4 categories, namely, transcriptional factors, stress responsive genes, genes relating to signal transduction and so on. Among the TDFs caused by salinity stress,14 and 7 were repressed in the diploid and tetraploid, respectively; 5 and 10 were induced in the diploid and tetraploid, respectively. On the other hand, among the TDFs resulted from cadmium toxicity, 7 and 16 were repressed in the diploid and tetraploid, respectively; and 12 and 5 were induced in the diploid and tetraploid, respectively.
Taken together, the tetraploid turnip had a better adaptation in the salinity and cadmium stressed environments. The MSAP and cDNA-AFLP analysis revealed the underlying genetic mechanisms that cause the morphological and physiological differences. Our work is a contribution to the advancement of our understanding on the mechanism that an autopolyploid turnip deals with adverse environment.
多倍体与二倍体比拥有较大的营养器官和生殖器官,在生长过程中表现出一定的抗性优势,但以往的研究多集中在异源多倍体的抗性差异上,而对同源多倍体和二倍体的抗性差异研究甚少。本文采用同源四倍体“矮脚黄”白菜和二倍体“矮脚黄”白菜为材料,其中同源四倍体“矮脚黄”白菜是由二倍体“矮脚黄”白菜直接加倍而来。文章从生理生化、表观遗传、分子表达三个角度研究了二者在盐和镉逆境条件下的逆境差异机理,得到的主要结果如下：
1)同源四倍体在高盐胁迫下具有较快的发芽速度,较多的健康植株数；低浓度盐能够有效的刺激四倍体茎和根的生长。发芽7天后,四倍体和二倍体植株体内的钾钠钙离子在不同组织中的分布存在差异明显。四倍体在高盐浓度中具有一定的抗性优势,而Na+/Ca2+可以作为筛选白菜抗性品种的一个重要指标。
2)在5-7叶期间,四倍体叶绿素含量受到盐害的影响较二倍体小,四倍体体内的抗氧化还原剂GSH较二倍体含量高,四倍体白菜和二倍体白菜在盐胁迫下用不同的活性氧清除体系,四倍体的抗氧化酶体系更加稳定。盐处理后期,钾钠钙离子在地上组织和地下组织中的分布差异明显,二倍体的地上组织能够吸收更多的钠离子,四倍体能够在一定程度上阻止钠离子向地上部分运输；四倍体的地下组织吸收更高的钠离子含量以及保持高水平的钾离子水平。四倍体在根部能通过保持较高的K+／Na+比值,使其具有一定的抗盐优势。随着处理时间的增加,二倍体和四倍体的Na+/Ca2+比值差异越大,这些实验说明四倍体可以通过保持较低的Na+/Ca2+比值来缓解盐害。
3)发芽7天后发现在高浓度的镉处理中,四倍体在发芽率、根茎长以及健康植株数目指标上比二倍体具有明显的优势。随着处理浓度的增加,二倍体各组织中镉的含量逐渐增加。四倍体在高浓度的处理下发芽期可以通过限制镉的摄入来降低根部的镉浓度。
4)随着镉处理浓度和时间的增加,四倍体叶绿素和GSH含量比二倍体高,叶片内的MDA积累量要比二倍体低。四倍体白菜和二倍体白菜在镉胁迫下,抗氧化酶变化趋势存在着差异,四倍体的抗氧化酶的活性在镉环境中的缓冲力要强于二倍体。说明了四倍体在镉胁迫下其体内的活性氧、过氧化氢可以通过高含量的GSH以及稳定的抗氧化酶体系得到及时的清除,使得四倍体在镉胁迫下有一定的生长优势。镉进入四倍体根部后,有一部分运输至地上组织(叶片),减轻了镉对四倍体根部的毒害。
5)用MSAP分析四倍体和二倍体的逆境抗性的差异,56对引物共得到14382条扩增带,总甲基化条带共2924条。二倍体和四倍体在盐胁迫中,其总体甲基化水平都呈下降趋势。在镉胁迫环境中,两者的总体甲基化有上升的趋势。二倍体的甲基化水平下降了1.5个百分点,而四倍体下降了2.5个百分点,四倍体甲基化程度下降得更快；在镉处理中,二倍体的甲基化水平上升了2.7个百分点,四倍体上升了3.5个百分点,四倍体镉甲基化水平上升的程度更高。
6)二倍体和四倍体经过逆境条件下,其MSAP的甲基化模式发生了改变,四倍体在盐胁迫下与二倍体在盐胁迫下,有35%的甲基化模式发生了去甲基化(B类型)过程,20.0%发生过甲基化(C类型)转变；四倍体在镉胁迫下与二倍体在镉胁迫下,有24.8%的甲基化模式发生了去甲基化(B类型)过程,25.8%发生过甲基化(C类型)转变。盐胁迫下,四倍体发生去甲基化的位点数比二倍体多,而发生过甲基化位点数相差不大,暗示了去甲基化位点在四倍体白菜和二倍体白菜盐胁迫差异中启着重要的作用；镉胁迫下,四倍体发生过甲基化的位点数比二倍体多,而发生去甲基化位点数相差不大,说明了过甲基化位点在四倍体白菜和二倍体白菜的镉胁迫差异中启着关键性作用。
7) cDNA-AFLP实验结果表明与二倍体和四倍体各自在对照条件下相比,二者在盐和镉胁迫条件下的差异有扩大的趋势。在盐胁迫的差异片段中,二倍体基因表达被抑制的有14条(0.52%),四倍体基因表达被抑制的7条(0.26%);四倍体基因表达被诱导的差异基因有10条(0.37%),而二倍体被诱导的差异基因有5条(0.19%)。在镉胁迫的差异片断中,二倍体基因表达被抑制的有7条(0.26%),四倍体基因表达被抑制的为16条(0.60%)；四倍体基因表达被诱导的有5条(0.19%),二倍体基因表达被诱导的有12条(0.45%)。四倍体和二倍体在不同的逆境环境中基因表达的模式有很大的差异,在盐胁迫中,差异片段在二倍体中大部分被抑制,在四倍体中大部分被诱导；镉胁迫下,二倍体中大部分的基因表达差异体现为被诱导,而在四倍体中大部分的基因表达差异体现为被抑制。
8)对盐和镉的不同胁迫下,对二倍体和四倍体中的差异片段进行测序发现,盐胁迫导致的18条TDFs中有16条(88.9%)在现有数据库已有基因的功能(或者推测功能)的描述,两条TDFs中有1条其功能未知,另外一条和现有数据库中基因无任何同源性。16个TDFs按照功能可以分为三类：细胞代谢类、胁迫响应类、转录因子类。盐胁迫中的差异片段功能大部分参与了ABA信号合成及传递、过氧化物酶合成、醛脱氢酶合成、甜菜合成键酶的过程。在镉胁迫差异片段中,20条TDFs中有15条(75%)在现有数据库已有基因的功能(或者推测功能)的描述,有5条功能不明确,其中3条与数据库中的基因具有一定程度的同源性,另外2条在数据库找不到同源基因。在镉胁迫实验中,二倍体和四倍体有差异按照功能可以分为四类：细胞代谢类、胁迫响应类、转录因子类、光合作用类。镉胁迫中的差异片段所体现的基因,其功能大部分参与了蛋白激酶、热击蛋白、光合蛋白合成途径。
Polyploidy is pursued in plant breeding programs due mainly to its ability to yield larger vegetative or reproductive organs. It could also be used to improve plant adaptation to saline or heavy metal contaminated soils because of the redundant genes implicated in stress tolerance, the status of the genome methylation degree and the pattern of gene expression at transcriptional level. However, little information is available about the ability of an autopolyploid to survive in stressed condition in comparison with its diploid progenitor. In this study, a tetraploid turnip (cv. Ai-Jiao-Huang 4X) and its diploid progenitor (cv. Ai-Jiao-Huang 2X) were compared for their tolerance to salinity stress and cadmium toxicity by investigating a group of morphological and physiological parameters. Methylation sensitive amplification polymorphism (MSAP) and cDNA-amplified fragment length polymorphism (cDNA-AFLP) analysis were employed to compare the degree of genome methylation and identify the genes induced or repressed under salinity and cadmium stresses. The major results are listed as the following.
1. The tetraploid turnip exhibited better adaptation to a highly concentrated salt medium (200 mM), as evidenced by a less affected germination rate and a healthier morphological appearance at the seedling stage. Furthermore, an extension of salinity stress up to a certain period of time at the 5-7 leaf stage shows differences between the tetraploid turnip and its diploid progenitor. The former had a higher K+/Na+ ratio in the roots, higher glutathione concentration and antioxidant activities in the leaves, and smaller reductions in photosynthetic capacity in terms of leaf chlorophyll content. On the other hand, the tetraploid turnip had a better tolerance to the cadmium treatment, reflected by higher germination rate, root length at seedling stage. An extension of cadmium toxicity at 5-7 leaf stage resulted in a less obvious impairment of chlorophyll, less alternation of antioxidants'activity and higher concentration of K+ and Ca2+ ions in shoots, but lower ratio of Na+/K+ in tetraploid, but higher concentration of Na+ in shoots and less availability of K+ and Ca2+ in both roots of the diploid.
2. Salinity stress and cadmium toxicity gave rise the significant changes of genome DNA methylation degree, as reflected by the MSAP analysis, which identified a total of 14382 bands generated by 56 primer pairs. A among a total of 2924 methylaiton bands,1731 were full the methylaiton type and 1193 were the half methylation type. The total methylaton ratio of the diploid in the control, salinity, and cadmium stressed conditions were 20.3,18.8,22.7; whereas the total methylaton ratio of the tetraploid in the control, salinity and cadmium stressed conditions were 20.3,18.8,22.7. The total methylaton level declined in both the diploid and tetraploid after salt treatment, but increased after cadmium treatment. In diploid the methylaton level decreased by 1.5 point, whereas in the tetraploid it decreased by 2.5 point after salt treatment. The full methylation ratio in diploid was 2.2 points higher than in tetraploid, while half methylation ratio in tetraploid was 1.6 points higher than in the diploid.
3. By using 96 primer pair combinations, about 2648,2650,2703,2730,2551 and 2580 cDNA fragments were generated respectively under the following treatments (1) tetraploid without stress; (2) diploid without stress; (3) tetraploid under salinity stress; (4) diploid under salinity stress; (5) tetraploid with cadmium toxicity; (6) diploid with cadmium toxicity. Salinity stress and cadmium toxicity led to 36 and 40 TDFs, respectively, which represented the functional genes that can be classified in to 3 or 4 categories, namely, transcriptional factors, stress responsive genes, genes relating to signal transduction and so on. Among the TDFs caused by salinity stress,14 and 7 were repressed in the diploid and tetraploid, respectively; 5 and 10 were induced in the diploid and tetraploid, respectively. On the other hand, among the TDFs resulted from cadmium toxicity, 7 and 16 were repressed in the diploid and tetraploid, respectively; and 12 and 5 were induced in the diploid and tetraploid, respectively.
Taken together, the tetraploid turnip had a better adaptation in the salinity and cadmium stressed environments. The MSAP and cDNA-AFLP analysis revealed the underlying genetic mechanisms that cause the morphological and physiological differences. Our work is a contribution to the advancement of our understanding on the mechanism that an autopolyploid turnip deals with adverse environment.
引文
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