紫花苜蓿根瘤菌共生对干旱及盐胁迫的响应机制研究
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摘要
干旱、盐碱等逆境是全世界农业生产所面临的重要问题，我国更为严重。紫花苜蓿是我国乃至全世界最重要的牧草，以收获营养器官为主的苜蓿生产，更适应于干旱、盐碱区域，是开发旱区及盐碱地的重要选择。其抗逆机理研究，已成为草学研究重要内容，有关苜蓿根瘤菌共生对干旱及盐胁迫的响应机制研究，鲜见文献报道。
本研究分别在干旱、盐及高温处理的条件下，应用根瘤菌接种温室培养（盆、钵）苜蓿，精确控制逆境的手段，测定了逆境存活率；采用常规方法测定了相关生理指标；非损伤微测技术测定了钙、钾、氢离子的进出根细胞情况；采用基因芯片技术筛选了差异基因；并对芯片筛选的3个基因进行半定量表达与分析。旨在研究探索苜蓿根瘤菌共生对干旱及盐胁迫下的响应机制。
试验研究结论如下：
1.通过干旱、盐、高温处理及去除根瘤后存活率研究表明，接种根瘤菌可大幅度提高紫花苜蓿的抗旱、耐盐、抗高温及根部机械损伤等非生物胁迫能力，抗逆能力表现为激活根瘤菌苜蓿＞不激活根瘤菌苜蓿＞无根瘤菌苜蓿，且激活根瘤菌苜蓿抗逆性远远高于不激活根瘤菌苜蓿。
苜蓿接种根瘤菌激活后，其抗非生物胁迫能力的提高来源于三个方面：根瘤菌的固氮作用、根瘤菌和苜蓿共生的免疫作用、根瘤菌固氮对植物自身组成变化或其生理应答机制的改变。
根瘤菌对于苜蓿的抗逆性提高，在失去根瘤菌的固氮作用后，只要曾经接种根瘤菌，无论激活与否，依旧比未曾接种过根瘤菌的苜蓿具有更强的抗性，表明根瘤菌提高苜蓿的抗逆能力，不是完全依赖于根瘤菌的固氮作用，且其对抗逆能力的提高是长期的。
2.干旱和盐处理下不同组织相关生理指标测试表明，干旱和盐胁迫下，接种根瘤菌后，苜蓿具有更强的渗透调节能力，根瘤在抵御干旱/盐胁迫上具有重要作用。具有活性的根瘤能减缓植物受到干旱/盐胁迫的时间，并能维持植物细胞稳定性，细胞内环境平衡，减少氧化胁迫。
3.在干旱胁迫后复水和NaCl胁迫下，随着干旱程度的逐步增加和盐胁迫时间的延长，紫花苜蓿通过改变根部细胞离子浓度及进出细胞膜的方向来保持细胞内环境的平衡，维持渗透压。相对于不接种根瘤菌的紫花苜蓿，接种根瘤菌激活的紫花苜蓿在干旱胁迫和盐胁迫下，具有较强的渗透调节能力，能更好的维持植株根系活力、保持细胞内环境的平衡，提高紫花苜蓿的抗逆性。
4.通过基因芯片分析发现，干旱胁迫是一个多基因参与的过程。轻度干旱与充足给水相比，差异基因数量较少，差异基因中上调基因数量多，而下调基因数量少；重度干旱阶段与充足给水相比，差异表达基因数量多，上调下调基因相数目接近。接种根瘤菌不激活和无根瘤菌处理在轻度阶段下调基因多于上调基因；在充足给水、重度干旱阶段，接种根瘤菌激活、接种根瘤菌不激活和不接种根瘤菌互相之间比较，上调基因多于下调基因。
从三个干旱处理阶段来看，有5类基因有规律性的表达，有5006个基因在接种根瘤菌激活、接种根瘤菌不激活和不接种根瘤菌中表现相同相似的变化规律；从根瘤菌处理来看，有三类基因（446个）在接种根瘤菌激活中表达量上调，接种根瘤菌不激活和不接种根瘤菌中下调。有一类基因（79个）在干旱后在接种根瘤菌激活时下调，而在干旱后期接种根瘤菌不激活和不接种根瘤菌时上调。
从苯丙素途径（合成木质素）通路分析，发现25个差异基因参与了EC4.3.1.24、EC2.3.1.91、EC2.3.1.92、EC1.14.13.11、EC6.2.1.2、EC3.2.1.21、EC1.11.1.7等代谢步骤。
5.通过半定量PCR表达，对基因芯片筛选后的TC81048、TC83565和TC87183三个基因进行进一步的验证试验表明，这三个基因均对干旱有响应，不接种根瘤菌三个基因在苜蓿干旱时的表达呈现规律性升高。在接种根瘤菌后干旱时，TC83565表达量下降，而TC87183表达量增加，TC81048无变化。三个基因在干旱敏感的品种Semip中，表达量均显著升高，进一步证实这三个基因和干旱应答有关。
综上，本文已基本明确接种根瘤菌的苜蓿，可在一定程度上抵御干旱和盐胁迫。这一过程有多个基因参与，涉及细胞稳定性、细胞内环境平衡、细胞氧化代谢、根际离子(Ca~(2+)、K~+、H~+)浓度和进出方向的渗透调节等。这为今后多视角系统研究苜蓿干旱和盐胁迫机制奠定了一定的基础。
Abiotic stress such as drought and salinity is the adverse environmentalfactors reducing agriculture production. Drought and soil salinity are moreserious in China. Since alfalfa is relatively tolerant to drought and salinity, it canbe planted on arid or saline soil for harvesting high quality of forage. Thus, moreand more plant biologists focus on the mechanism of how alfalfa plants respondto drought/salt stress. There are few publications on how symbioticnitrogen-fixation affects alfalfa’s response to drought and salinity. We conductedgreenhouse experiments to study physiological and molecular responses ofalfalfa during abiotic stress treatments, with an interest in understanding hownodulation or symbiotic nitrogen-fixation affects plant stress response. Plantswere grown in pots and cones filled with quartz sand which allows us to easilyapply and control stress treatments. Alfalfa plants were subjected to drought,high salt and other treatments. Survival rate and other physiological changes were examined, such as osmotican accumulation, root fluxes of Ca2+, K+and H+.Stress-responsive genes were identified using microarray. Threedrought-responsive genes were studied in detail for their expression patterns andregulation. The major findings are:
1. Nodulated alfalfa was more tolerant to abiotic stress such as drought, salt,high temperature, and physical wounding. The stress resistance ranked fromstrong to weak as plants with active nodules, plants with inactive nodules, andplants without nodules.
The improved stress resistance in nodulated alfalfa may be resulted from:better nitrogen supply from nitrogen fixation, immune protection fromrhizobium-alfalfa interaction, and other biochemical composition changes(determining physiological changes observed).
The greater stress tolerance acquired from nodulation could be sustainedfor a long time. This was demonstrated that plants, after removal of nodules, stillshowed better stress tolerance compared to the plants that were never nodulated.
2. Physiological analyses showed that better stress tolerance in alfalfa withactive nodules was associated with greater abilities of osmotic adjustment,anti-oxidation, and intracellular homeostasis maintenance.
3. Maintenance of intracellular homeostasis was associated with betterregulation of root ion content and fluxes, and improved osmotic adjustment.
4. The microarray study revealed that dehydration stress (mimickingdrought) is a complex process involving a large set of genes. The number ofdehydration responsive genes was less in the plants at early stage of stresstreatment (when stress was mild) and increased at late stages when stressbecame severe. During early dehydration, more genes were downregulated andfewer genes were upregulated when compared alfalfa with active nodules to theones with inactive nodules. However, more upregulated and less downregulatedgenes were found in alfalfa with active nodules compared to the ones withinactive nodules or without nodules at late stages of dehydration.
Among the dehydration responsive genes (total5006), five expressionpatterns were identified. Interestingly,446genes that were found upregulated inalfalfa with active nodules were down regulated in alfalfa with inactive nodulesor no nodules. Seventy nine genes that were down regulated in alfalfa withactive nodule were upregulated in alfalfa with inactive nodules and no nodules.
In particular,25genes in the phenylpropanoid pathway (lignin biosynthesis)were highly upregulated in nodulated alfalfa plants during dehydration stress.They encode proteins, EC4.3.1.24, EC2.3.1.91, EC2.3.1.92, EC1.14.13.11,EC6.2.1.2, EC3.2.1.21, and EC1.11.1.7in the pathway, suggesting improvedlignifications may contribute to the better drought tolerance in nodulated alfalfa.
5. Using semi-quantitative PCR, we studied expression of3dehydration responsive genes, TC81048, TC83565and TC87183, in detail. These genes wereupregulated in non-nodulated alfalfa under dehydration. While they wereconfirmed as upregulated in nodulated alfalfa also, nodulation enhanced theexpression of TC83565but decreased expression of TC87183under stress.Nodulation had little effect on TC81048expression under dehydration. Alfalfacultivar SemiP showed the greatest upregulation of these genes duringdehydration stress in a multi-cultivar comparison experiment.
In summary, our results indicated that nodulation could improve alfalfaplant tolerance to drought/salt stress. The improved tolerance may be a result ofdifferential regulation of stress responsive genes, leading to cellular andphysiological changes that help plant adapt to adverse growth conditions.
本研究分别在干旱、盐及高温处理的条件下，应用根瘤菌接种温室培养（盆、钵）苜蓿，精确控制逆境的手段，测定了逆境存活率；采用常规方法测定了相关生理指标；非损伤微测技术测定了钙、钾、氢离子的进出根细胞情况；采用基因芯片技术筛选了差异基因；并对芯片筛选的3个基因进行半定量表达与分析。旨在研究探索苜蓿根瘤菌共生对干旱及盐胁迫下的响应机制。
试验研究结论如下：
1.通过干旱、盐、高温处理及去除根瘤后存活率研究表明，接种根瘤菌可大幅度提高紫花苜蓿的抗旱、耐盐、抗高温及根部机械损伤等非生物胁迫能力，抗逆能力表现为激活根瘤菌苜蓿＞不激活根瘤菌苜蓿＞无根瘤菌苜蓿，且激活根瘤菌苜蓿抗逆性远远高于不激活根瘤菌苜蓿。
苜蓿接种根瘤菌激活后，其抗非生物胁迫能力的提高来源于三个方面：根瘤菌的固氮作用、根瘤菌和苜蓿共生的免疫作用、根瘤菌固氮对植物自身组成变化或其生理应答机制的改变。
根瘤菌对于苜蓿的抗逆性提高，在失去根瘤菌的固氮作用后，只要曾经接种根瘤菌，无论激活与否，依旧比未曾接种过根瘤菌的苜蓿具有更强的抗性，表明根瘤菌提高苜蓿的抗逆能力，不是完全依赖于根瘤菌的固氮作用，且其对抗逆能力的提高是长期的。
2.干旱和盐处理下不同组织相关生理指标测试表明，干旱和盐胁迫下，接种根瘤菌后，苜蓿具有更强的渗透调节能力，根瘤在抵御干旱/盐胁迫上具有重要作用。具有活性的根瘤能减缓植物受到干旱/盐胁迫的时间，并能维持植物细胞稳定性，细胞内环境平衡，减少氧化胁迫。
3.在干旱胁迫后复水和NaCl胁迫下，随着干旱程度的逐步增加和盐胁迫时间的延长，紫花苜蓿通过改变根部细胞离子浓度及进出细胞膜的方向来保持细胞内环境的平衡，维持渗透压。相对于不接种根瘤菌的紫花苜蓿，接种根瘤菌激活的紫花苜蓿在干旱胁迫和盐胁迫下，具有较强的渗透调节能力，能更好的维持植株根系活力、保持细胞内环境的平衡，提高紫花苜蓿的抗逆性。
4.通过基因芯片分析发现，干旱胁迫是一个多基因参与的过程。轻度干旱与充足给水相比，差异基因数量较少，差异基因中上调基因数量多，而下调基因数量少；重度干旱阶段与充足给水相比，差异表达基因数量多，上调下调基因相数目接近。接种根瘤菌不激活和无根瘤菌处理在轻度阶段下调基因多于上调基因；在充足给水、重度干旱阶段，接种根瘤菌激活、接种根瘤菌不激活和不接种根瘤菌互相之间比较，上调基因多于下调基因。
从三个干旱处理阶段来看，有5类基因有规律性的表达，有5006个基因在接种根瘤菌激活、接种根瘤菌不激活和不接种根瘤菌中表现相同相似的变化规律；从根瘤菌处理来看，有三类基因（446个）在接种根瘤菌激活中表达量上调，接种根瘤菌不激活和不接种根瘤菌中下调。有一类基因（79个）在干旱后在接种根瘤菌激活时下调，而在干旱后期接种根瘤菌不激活和不接种根瘤菌时上调。
从苯丙素途径（合成木质素）通路分析，发现25个差异基因参与了EC4.3.1.24、EC2.3.1.91、EC2.3.1.92、EC1.14.13.11、EC6.2.1.2、EC3.2.1.21、EC1.11.1.7等代谢步骤。
5.通过半定量PCR表达，对基因芯片筛选后的TC81048、TC83565和TC87183三个基因进行进一步的验证试验表明，这三个基因均对干旱有响应，不接种根瘤菌三个基因在苜蓿干旱时的表达呈现规律性升高。在接种根瘤菌后干旱时，TC83565表达量下降，而TC87183表达量增加，TC81048无变化。三个基因在干旱敏感的品种Semip中，表达量均显著升高，进一步证实这三个基因和干旱应答有关。
综上，本文已基本明确接种根瘤菌的苜蓿，可在一定程度上抵御干旱和盐胁迫。这一过程有多个基因参与，涉及细胞稳定性、细胞内环境平衡、细胞氧化代谢、根际离子(Ca~(2+)、K~+、H~+)浓度和进出方向的渗透调节等。这为今后多视角系统研究苜蓿干旱和盐胁迫机制奠定了一定的基础。
Abiotic stress such as drought and salinity is the adverse environmentalfactors reducing agriculture production. Drought and soil salinity are moreserious in China. Since alfalfa is relatively tolerant to drought and salinity, it canbe planted on arid or saline soil for harvesting high quality of forage. Thus, moreand more plant biologists focus on the mechanism of how alfalfa plants respondto drought/salt stress. There are few publications on how symbioticnitrogen-fixation affects alfalfa’s response to drought and salinity. We conductedgreenhouse experiments to study physiological and molecular responses ofalfalfa during abiotic stress treatments, with an interest in understanding hownodulation or symbiotic nitrogen-fixation affects plant stress response. Plantswere grown in pots and cones filled with quartz sand which allows us to easilyapply and control stress treatments. Alfalfa plants were subjected to drought,high salt and other treatments. Survival rate and other physiological changes were examined, such as osmotican accumulation, root fluxes of Ca2+, K+and H+.Stress-responsive genes were identified using microarray. Threedrought-responsive genes were studied in detail for their expression patterns andregulation. The major findings are:
1. Nodulated alfalfa was more tolerant to abiotic stress such as drought, salt,high temperature, and physical wounding. The stress resistance ranked fromstrong to weak as plants with active nodules, plants with inactive nodules, andplants without nodules.
The improved stress resistance in nodulated alfalfa may be resulted from:better nitrogen supply from nitrogen fixation, immune protection fromrhizobium-alfalfa interaction, and other biochemical composition changes(determining physiological changes observed).
The greater stress tolerance acquired from nodulation could be sustainedfor a long time. This was demonstrated that plants, after removal of nodules, stillshowed better stress tolerance compared to the plants that were never nodulated.
2. Physiological analyses showed that better stress tolerance in alfalfa withactive nodules was associated with greater abilities of osmotic adjustment,anti-oxidation, and intracellular homeostasis maintenance.
3. Maintenance of intracellular homeostasis was associated with betterregulation of root ion content and fluxes, and improved osmotic adjustment.
4. The microarray study revealed that dehydration stress (mimickingdrought) is a complex process involving a large set of genes. The number ofdehydration responsive genes was less in the plants at early stage of stresstreatment (when stress was mild) and increased at late stages when stressbecame severe. During early dehydration, more genes were downregulated andfewer genes were upregulated when compared alfalfa with active nodules to theones with inactive nodules. However, more upregulated and less downregulatedgenes were found in alfalfa with active nodules compared to the ones withinactive nodules or without nodules at late stages of dehydration.
Among the dehydration responsive genes (total5006), five expressionpatterns were identified. Interestingly,446genes that were found upregulated inalfalfa with active nodules were down regulated in alfalfa with inactive nodulesor no nodules. Seventy nine genes that were down regulated in alfalfa withactive nodule were upregulated in alfalfa with inactive nodules and no nodules.
In particular,25genes in the phenylpropanoid pathway (lignin biosynthesis)were highly upregulated in nodulated alfalfa plants during dehydration stress.They encode proteins, EC4.3.1.24, EC2.3.1.91, EC2.3.1.92, EC1.14.13.11,EC6.2.1.2, EC3.2.1.21, and EC1.11.1.7in the pathway, suggesting improvedlignifications may contribute to the better drought tolerance in nodulated alfalfa.
5. Using semi-quantitative PCR, we studied expression of3dehydration responsive genes, TC81048, TC83565and TC87183, in detail. These genes wereupregulated in non-nodulated alfalfa under dehydration. While they wereconfirmed as upregulated in nodulated alfalfa also, nodulation enhanced theexpression of TC83565but decreased expression of TC87183under stress.Nodulation had little effect on TC81048expression under dehydration. Alfalfacultivar SemiP showed the greatest upregulation of these genes duringdehydration stress in a multi-cultivar comparison experiment.
In summary, our results indicated that nodulation could improve alfalfaplant tolerance to drought/salt stress. The improved tolerance may be a result ofdifferential regulation of stress responsive genes, leading to cellular andphysiological changes that help plant adapt to adverse growth conditions.
引文
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