2种美人蕉属植物对镉的积累及其耐受生理机制的研究
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摘要
土壤重金属镉（Cd）污染已成为世界广泛关注的环境问题之一，利用环境友好型技术—植物修复技术清除环境Cd污染已取得了重大进展，寻找有经济价值的Cd污染修复新植物仍是科学家孜孜追求的目标。美人蕉属植物对Cd耐受性强，生物量大，生长速度快，可用于土壤Cd污染的原位修复。同属植物芭蕉芋是一种新型能源观赏植物，其根茎可用于工业酒精的生产。但芭蕉芋对重金属Cd的吸收积累特性未见报道，对Cd污染的修复能力缺少评价。本研究选用我国主栽的3个芭蕉芋品种（PLRF、Xingyu-1和Xingyu-2）为试材，以大花美人蕉品种Australia为对照，利用盆栽实验研究了芭蕉芋和大花美人蕉Cd积累特征及Cd对芭蕉芋及大花美人蕉生长的影响；并从光合生理、逆境氧化胁迫、根际土壤微环境变化及矿质元素吸收与分配4大部分探讨了美人蕉属植物对Cd的忍耐和解毒机制。主要获得的结果如下：
1.美人蕉属植物生物量大，生长速度快，对Cd具有一定的富集作用，可作为Cd污染土壤修复的候选植物，但美人蕉属植物不符合Cd超富集植物的标准，不属于Cd超富集植物。美人蕉属植物种间对Cd的富集能力存在差异，芭蕉芋对Cd的富集效率高于大花美人蕉，且生物量大于大花美人蕉，因此，芭蕉芋的Cd修复效果优于大花美人蕉。芭蕉芋种内不同品种间对Cd的富集也存在差异，‘Xingyu-1’的富集作用最大，‘Xingyu-2’的富集作用最小，‘PLRF’介于二者之间，用于土壤Cd修复选择‘Xingyu-1’或‘PLRF’效果较好。3个芭蕉芋品种间，‘Xingyu-2’为Cd低富集品种，作为粮食作物种植安全性较高。
2. Cd在美人蕉属植物体内分配不均匀，70%~80%的Cd存在于地下器官（根和根茎）中，美人蕉属植物根系对Cd的固定和截留是降低Cd毒害的一种适应机制。
3.低浓度Cd促进了苗期美人蕉属植物生长，高浓度Cd对苗期美人蕉属植物生长具有抑制作用；成龄期美人蕉属植物生长受Cd胁迫影响小于苗期。Cd对美人蕉属植物生长的影响存在种间差异，对大花美人蕉的影响大于对芭蕉芋的影响。
4. Cd胁迫降低了美人蕉属植物叶片光合色素含量和净光合速率（Pn）。Cd降低芭蕉芋Pn的同时，伴随着对气孔导度（Gs）和胞间二氧化碳浓度（Ci）的抑制作用；Cd胁迫导致了大花美人蕉Pn的下降，对Gs和Ci无显著影响。因此，芭蕉芋Pn的下降既存在气孔限制因素，又存在非气孔限制因素，而Cd对大花美人蕉Pn的降低作用主要由非气孔限制因素导致的。Cd胁迫显著降低了美人蕉属植物叶片蒸腾速率，减小植物的蒸腾拉力，从而限制了Cd从地下器官向地上器官的转移，这是美人蕉属植物降低Cd毒害的另一种保护机制。
5.低浓度的Cd处理未导致美人蕉属植物叶片光系统Ⅱ（PSⅡ）的损伤，但高浓度Cd显著降低了美人蕉属植物最大量子产量（Fv/Fm）和实际量子产量（Yield），损伤光合器官PSⅡ，减少光能捕获，阻断光合电子传递速度，降低了参与光化学反应的能量，导致光合速率降低。大花美人蕉通过提高热耗散（qN）的方式降低高浓度Cd对其产生的伤害，而在芭蕉芋中不存在这种保护机制。
6.外施Cd处理对美人蕉属植物叶片和根系产生了不同程度的氧化胁迫，Cd对过氧化氢（H2O2）含量的影响强于（或早于）对相对电导率（REC）和丙二醛（MDA）含量的影响，对根系的氧化胁迫程度强于对叶片的，大花美人蕉的胁迫程度强于芭蕉芋的。美人蕉属植物同时启动了抗氧化酶保护系统和非酶抗氧化系统应对Cd胁迫，耐Cd毒害强的种（芭蕉芋）或品种‘Xingyu-1’的保护系统活性或含量较高，耐性差的种（大花美人蕉）和品种‘Australia’的保护系统活性或含量较低，过氧化物酶（POD）负责大花美人蕉根系内过氧化物的解毒作用，过氧化氢酶（CAT）则负责芭蕉芋根系过氧化物的清除。
7. Cd处理改变了根际土壤微环境，提高了微生物的数量，降低了根际土壤酶活性，影响了根际土壤矿质元素的活化和利用。低浓度Cd对根际土壤微生物影响较小，高浓度Cd胁迫增加了根际土壤真菌和放线菌数量，但对细菌数量影响较小。Cd胁迫降低了美人蕉属植物根际土壤脲酶、蛋白酶和蔗糖酶活性，蛋白酶的下降幅度最大，其次是脲酶，蔗糖酶的降幅最小；且苗期的抑制作用小于成龄期。Cd胁迫提高了土壤过氧化氢酶的活性。
8.低浓度Cd处理促进了芭蕉芋对矿质营养元素和氮素的吸收，改变了地上部和地下部矿质的分配比例，而高浓度的Cd处理则抑制了芭蕉芋对矿质元素的吸收和运转。但不同的元素在不同品种之间存在差异，Cd对芭蕉芋大量元素的影响小于对微量元素的影响；Cd胁迫明显抑制大花美人蕉对矿质元素的积累。Cd对芭蕉芋矿质元素吸收的促进作用与对根际土壤微环境的改变有关，而对矿质元素吸收和运转的抑制作用则主要是由于高浓度Cd胁迫抑制了矿质元素的主动吸收（降低光合能量的产生或降低了代谢过程中的酶活性）和被动吸收（破坏离子通道和转运蛋白），降低了蒸腾拉力，减少了矿质从地下部向地上部的转运。从矿质元素含量变化来看，美人蕉属植物叶绿素降低和叶片黄化不是由于Fe、Mg、Cu、Mn、Ca和K等矿质元素的亏缺造成的。
Cadmium (Cd) pollution in soil has been one of the most important environmentalconcerns in the world. Phytoremediation, used to clear Cd pollution, has gained significantprogress in recent decades as cost-effective, eco-friendly technologies. Scientists arededicated to find new plants with ecomomic value or landscape value used in Cd pollutionarea. Some canna species might be an interesting alternative for use in phytoremediationtechnology with their high tolerance to Cd, high biomass production and fast-growingadvantage. Canna edulis is a new energy plants with ornamental value, its rhizome can beused to produce industrial alcohol due to high starch content. But the absorptioncharacteristics and remediation ability of C. edulis to Cd have not repored until now. In thispaper, three edible canna cultivars (PLRF, Xingyu-1and Xingyu-2) which are the mostcommon cultivars in China, and a C. generalis cultivar (Australia) were used as materials.This study mainly focused on the Cd accumulation characteristics in two Canna species andthe effect on their growth under Cd stress, discussed the tolerance mechamisns of Canna fromphotosynthetic physiology, antioxidative stress, micro-environment change in the rhizospheresoil and absorption and distribution of mineral elements under Cd stress by pot experientment.The main results are described as follows:
1. Canna plants could be used for the remediation in situ decontamination of soilspolluted with Cd because of their high biomass, high tolerance and accumulation of Cd andfast-growing advantage, but they were not hyperacculmulators because they didn’t meet thestandard of Cd huperaccumulators. There were differences between C. edulis and C. generalis,the biomatter, tolerance and accumulation of C. edulis were higher than those of C. generalis,so the remediation effect of C. edulis was better than C. generalis. There were differencesamong the cultivars of C. edulis as well. The accumulation ability of the Xingyu-1was thehighest among three cultivars, followed by PLRF and the Xingyu-2. The remedationefficiency of Xingyu-1or PLRF was better than Xingyu-2in Cd polluted soil. However theXingyu-2had higher security as food crops for cultibation because it belonged to a relativelylower accumulator in three cultivars.
2. The distribution of Cd in canna plants was non-uniform.70%to80%of Cd presentedin the underground organs (roots and rhizomes). The retention of Cd in the roots played animportant role in detoxifying Cd.
3. Low concentration of Cd treated in seedling stage promoted the growth of Canna, buthigh concentration of Cd inhibited the growth of Canna. The inhibited effects showeddifference between two treatment stages and two species, the mature stage was lower thanseedling stage, C. edulis was lower than the C. generalis.
4. Cd stress decreased the photosynthetic pigment contents of canna plants, resulting tothe declines of net photosysthesis rate (Pn). At the same time, the stomatal conductance (Gs)and intercellular CO2concentration (Ci) of edible canna were also inhibited under Cd stress,but Cd stress had no significant effect on the Gs and Ci of C. generalis. So the Pn declines ofedible canna were due to both stomatal and non-stomatal inhibiting factors, while that of C.generalis was only dedicated to the non-stomatal inhibiting factors. Cd stress significantlydecreased the transpiration rate (Tr) of canna plants, led to the reduction of transpiration pulland limitment of the Cd uptake and transfication from the underround organ to aerial organ,which was another protection mechanism to reduce Cd toxicity.
5. Low concentrations of Cd did not damage PSII of canna plant, but high concentrationsof Cd significantly reduced the maximum quantum yield (Fv/Fm), the actual quantum yield,energy capturing and the energy involved in the photochemical reaction, damagedphotosystem II (PSII), blocked photosynthetic electron transfer rate (ETR), resulted in Pndeclines. C. generalis reduced toxicity of high concentrations Cd by improvingnon-photochemical quenching (qN). However, there were no such protection mechanisms inC edulis.
6. Oxidative stress was induced by Cd treatment in both leaves and roots. The changes ofH2O2contents were stronger and earlier than the relative electric conductivity (REC) and thecontents of malondialdehyde (MDA). The degree of oxidative stress in the roots was strongerthan in the leaves, in C. generalis than in C edulis. At the same time, canna plants started theantioxidant enzymes protection system and non-enzymes antioxidant system in response toCd stress. High Cd-tolerant species or cultivar, such as C edulis or Xingyu-1, had higherantioxidant enzymes activity and antioxidant contents than the low Cd-tolerance ones, such asC. generalis cultivar Australia. Peroxidase (POD) was responsible for the peroxidedetoxification in roots of C. generalis, while catalase (CAT) was responsible for the peroxidedetoxification in roots of C edulis.
7. Cd treatment changed the soil microenvironment of canna plants rhizosphere,improved the quantity of microbial community, reduced the soil enzyme activities, and affected the activation and utilization of the soil mineral elements in the rhizosphere. Lowconcentration Cd had little effect on the soil microenvironment of canna plants rhizosphere,but high oncentrations of Cd stress increased numbers of fungi and actinomycetes in soilrhizosphere and had little effect on the numbers of bacteria. Cd stress decreased urease,protease and invertase activity in rhizosphere soil of canna plants. The decline of protease wasthe largest, followed by urease, sucrase was the smallest. The inhibition effect in seedlingstage was less than in mature stage. Cd stress also increased soil catalase activity.
8. Low concentration of Cd promoted abosorption of the mineral and nitrogen nutrientelements of edible canna, and changed the distribution ratio of mineral elements inabove-ground organ and underground organ. However, high contentration Cd inhibited theuptake and the translation of mineral elements in organ of edible canna. The variation ofdifferent mineral elements showed the significant difference among the different cultivars.The effects of Cd stress on macroelements were less than that of microelements in C edulis.Cd stress significantly inhibited abosorption and accumulation of the mineral and nitrogennutrient elements in C. generalis Australia. The promoted effect of Cd on the mineralelements in edible canna was related to the changes of soil microenvironment in rhizosphere,whereas the inhibition effect of high concentration Cd strss on the mineral elements in cannaplants was mainly due to the reduction of active absorption of mineral elements by reducingphotosynthetic energy and enzyme activity in metabolism, of passive absorption bydestruction ion channael and transporter protein. Cd stress reduced the transpiration pull andblocked the translocation of the mineral elements from the underground organ to arieal organtoo. According to the results of mineral elements, declines of chlorophyll content andchlorosis of the cannal plants induced by Cd were not caused by Fe, Mg, Cu, Mn, Ca and Kdeficit.
1.美人蕉属植物生物量大，生长速度快，对Cd具有一定的富集作用，可作为Cd污染土壤修复的候选植物，但美人蕉属植物不符合Cd超富集植物的标准，不属于Cd超富集植物。美人蕉属植物种间对Cd的富集能力存在差异，芭蕉芋对Cd的富集效率高于大花美人蕉，且生物量大于大花美人蕉，因此，芭蕉芋的Cd修复效果优于大花美人蕉。芭蕉芋种内不同品种间对Cd的富集也存在差异，‘Xingyu-1’的富集作用最大，‘Xingyu-2’的富集作用最小，‘PLRF’介于二者之间，用于土壤Cd修复选择‘Xingyu-1’或‘PLRF’效果较好。3个芭蕉芋品种间，‘Xingyu-2’为Cd低富集品种，作为粮食作物种植安全性较高。
2. Cd在美人蕉属植物体内分配不均匀，70%~80%的Cd存在于地下器官（根和根茎）中，美人蕉属植物根系对Cd的固定和截留是降低Cd毒害的一种适应机制。
3.低浓度Cd促进了苗期美人蕉属植物生长，高浓度Cd对苗期美人蕉属植物生长具有抑制作用；成龄期美人蕉属植物生长受Cd胁迫影响小于苗期。Cd对美人蕉属植物生长的影响存在种间差异，对大花美人蕉的影响大于对芭蕉芋的影响。
4. Cd胁迫降低了美人蕉属植物叶片光合色素含量和净光合速率（Pn）。Cd降低芭蕉芋Pn的同时，伴随着对气孔导度（Gs）和胞间二氧化碳浓度（Ci）的抑制作用；Cd胁迫导致了大花美人蕉Pn的下降，对Gs和Ci无显著影响。因此，芭蕉芋Pn的下降既存在气孔限制因素，又存在非气孔限制因素，而Cd对大花美人蕉Pn的降低作用主要由非气孔限制因素导致的。Cd胁迫显著降低了美人蕉属植物叶片蒸腾速率，减小植物的蒸腾拉力，从而限制了Cd从地下器官向地上器官的转移，这是美人蕉属植物降低Cd毒害的另一种保护机制。
5.低浓度的Cd处理未导致美人蕉属植物叶片光系统Ⅱ（PSⅡ）的损伤，但高浓度Cd显著降低了美人蕉属植物最大量子产量（Fv/Fm）和实际量子产量（Yield），损伤光合器官PSⅡ，减少光能捕获，阻断光合电子传递速度，降低了参与光化学反应的能量，导致光合速率降低。大花美人蕉通过提高热耗散（qN）的方式降低高浓度Cd对其产生的伤害，而在芭蕉芋中不存在这种保护机制。
6.外施Cd处理对美人蕉属植物叶片和根系产生了不同程度的氧化胁迫，Cd对过氧化氢（H2O2）含量的影响强于（或早于）对相对电导率（REC）和丙二醛（MDA）含量的影响，对根系的氧化胁迫程度强于对叶片的，大花美人蕉的胁迫程度强于芭蕉芋的。美人蕉属植物同时启动了抗氧化酶保护系统和非酶抗氧化系统应对Cd胁迫，耐Cd毒害强的种（芭蕉芋）或品种‘Xingyu-1’的保护系统活性或含量较高，耐性差的种（大花美人蕉）和品种‘Australia’的保护系统活性或含量较低，过氧化物酶（POD）负责大花美人蕉根系内过氧化物的解毒作用，过氧化氢酶（CAT）则负责芭蕉芋根系过氧化物的清除。
7. Cd处理改变了根际土壤微环境，提高了微生物的数量，降低了根际土壤酶活性，影响了根际土壤矿质元素的活化和利用。低浓度Cd对根际土壤微生物影响较小，高浓度Cd胁迫增加了根际土壤真菌和放线菌数量，但对细菌数量影响较小。Cd胁迫降低了美人蕉属植物根际土壤脲酶、蛋白酶和蔗糖酶活性，蛋白酶的下降幅度最大，其次是脲酶，蔗糖酶的降幅最小；且苗期的抑制作用小于成龄期。Cd胁迫提高了土壤过氧化氢酶的活性。
8.低浓度Cd处理促进了芭蕉芋对矿质营养元素和氮素的吸收，改变了地上部和地下部矿质的分配比例，而高浓度的Cd处理则抑制了芭蕉芋对矿质元素的吸收和运转。但不同的元素在不同品种之间存在差异，Cd对芭蕉芋大量元素的影响小于对微量元素的影响；Cd胁迫明显抑制大花美人蕉对矿质元素的积累。Cd对芭蕉芋矿质元素吸收的促进作用与对根际土壤微环境的改变有关，而对矿质元素吸收和运转的抑制作用则主要是由于高浓度Cd胁迫抑制了矿质元素的主动吸收（降低光合能量的产生或降低了代谢过程中的酶活性）和被动吸收（破坏离子通道和转运蛋白），降低了蒸腾拉力，减少了矿质从地下部向地上部的转运。从矿质元素含量变化来看，美人蕉属植物叶绿素降低和叶片黄化不是由于Fe、Mg、Cu、Mn、Ca和K等矿质元素的亏缺造成的。
Cadmium (Cd) pollution in soil has been one of the most important environmentalconcerns in the world. Phytoremediation, used to clear Cd pollution, has gained significantprogress in recent decades as cost-effective, eco-friendly technologies. Scientists arededicated to find new plants with ecomomic value or landscape value used in Cd pollutionarea. Some canna species might be an interesting alternative for use in phytoremediationtechnology with their high tolerance to Cd, high biomass production and fast-growingadvantage. Canna edulis is a new energy plants with ornamental value, its rhizome can beused to produce industrial alcohol due to high starch content. But the absorptioncharacteristics and remediation ability of C. edulis to Cd have not repored until now. In thispaper, three edible canna cultivars (PLRF, Xingyu-1and Xingyu-2) which are the mostcommon cultivars in China, and a C. generalis cultivar (Australia) were used as materials.This study mainly focused on the Cd accumulation characteristics in two Canna species andthe effect on their growth under Cd stress, discussed the tolerance mechamisns of Canna fromphotosynthetic physiology, antioxidative stress, micro-environment change in the rhizospheresoil and absorption and distribution of mineral elements under Cd stress by pot experientment.The main results are described as follows:
1. Canna plants could be used for the remediation in situ decontamination of soilspolluted with Cd because of their high biomass, high tolerance and accumulation of Cd andfast-growing advantage, but they were not hyperacculmulators because they didn’t meet thestandard of Cd huperaccumulators. There were differences between C. edulis and C. generalis,the biomatter, tolerance and accumulation of C. edulis were higher than those of C. generalis,so the remediation effect of C. edulis was better than C. generalis. There were differencesamong the cultivars of C. edulis as well. The accumulation ability of the Xingyu-1was thehighest among three cultivars, followed by PLRF and the Xingyu-2. The remedationefficiency of Xingyu-1or PLRF was better than Xingyu-2in Cd polluted soil. However theXingyu-2had higher security as food crops for cultibation because it belonged to a relativelylower accumulator in three cultivars.
2. The distribution of Cd in canna plants was non-uniform.70%to80%of Cd presentedin the underground organs (roots and rhizomes). The retention of Cd in the roots played animportant role in detoxifying Cd.
3. Low concentration of Cd treated in seedling stage promoted the growth of Canna, buthigh concentration of Cd inhibited the growth of Canna. The inhibited effects showeddifference between two treatment stages and two species, the mature stage was lower thanseedling stage, C. edulis was lower than the C. generalis.
4. Cd stress decreased the photosynthetic pigment contents of canna plants, resulting tothe declines of net photosysthesis rate (Pn). At the same time, the stomatal conductance (Gs)and intercellular CO2concentration (Ci) of edible canna were also inhibited under Cd stress,but Cd stress had no significant effect on the Gs and Ci of C. generalis. So the Pn declines ofedible canna were due to both stomatal and non-stomatal inhibiting factors, while that of C.generalis was only dedicated to the non-stomatal inhibiting factors. Cd stress significantlydecreased the transpiration rate (Tr) of canna plants, led to the reduction of transpiration pulland limitment of the Cd uptake and transfication from the underround organ to aerial organ,which was another protection mechanism to reduce Cd toxicity.
5. Low concentrations of Cd did not damage PSII of canna plant, but high concentrationsof Cd significantly reduced the maximum quantum yield (Fv/Fm), the actual quantum yield,energy capturing and the energy involved in the photochemical reaction, damagedphotosystem II (PSII), blocked photosynthetic electron transfer rate (ETR), resulted in Pndeclines. C. generalis reduced toxicity of high concentrations Cd by improvingnon-photochemical quenching (qN). However, there were no such protection mechanisms inC edulis.
6. Oxidative stress was induced by Cd treatment in both leaves and roots. The changes ofH2O2contents were stronger and earlier than the relative electric conductivity (REC) and thecontents of malondialdehyde (MDA). The degree of oxidative stress in the roots was strongerthan in the leaves, in C. generalis than in C edulis. At the same time, canna plants started theantioxidant enzymes protection system and non-enzymes antioxidant system in response toCd stress. High Cd-tolerant species or cultivar, such as C edulis or Xingyu-1, had higherantioxidant enzymes activity and antioxidant contents than the low Cd-tolerance ones, such asC. generalis cultivar Australia. Peroxidase (POD) was responsible for the peroxidedetoxification in roots of C. generalis, while catalase (CAT) was responsible for the peroxidedetoxification in roots of C edulis.
7. Cd treatment changed the soil microenvironment of canna plants rhizosphere,improved the quantity of microbial community, reduced the soil enzyme activities, and affected the activation and utilization of the soil mineral elements in the rhizosphere. Lowconcentration Cd had little effect on the soil microenvironment of canna plants rhizosphere,but high oncentrations of Cd stress increased numbers of fungi and actinomycetes in soilrhizosphere and had little effect on the numbers of bacteria. Cd stress decreased urease,protease and invertase activity in rhizosphere soil of canna plants. The decline of protease wasthe largest, followed by urease, sucrase was the smallest. The inhibition effect in seedlingstage was less than in mature stage. Cd stress also increased soil catalase activity.
8. Low concentration of Cd promoted abosorption of the mineral and nitrogen nutrientelements of edible canna, and changed the distribution ratio of mineral elements inabove-ground organ and underground organ. However, high contentration Cd inhibited theuptake and the translation of mineral elements in organ of edible canna. The variation ofdifferent mineral elements showed the significant difference among the different cultivars.The effects of Cd stress on macroelements were less than that of microelements in C edulis.Cd stress significantly inhibited abosorption and accumulation of the mineral and nitrogennutrient elements in C. generalis Australia. The promoted effect of Cd on the mineralelements in edible canna was related to the changes of soil microenvironment in rhizosphere,whereas the inhibition effect of high concentration Cd strss on the mineral elements in cannaplants was mainly due to the reduction of active absorption of mineral elements by reducingphotosynthetic energy and enzyme activity in metabolism, of passive absorption bydestruction ion channael and transporter protein. Cd stress reduced the transpiration pull andblocked the translocation of the mineral elements from the underground organ to arieal organtoo. According to the results of mineral elements, declines of chlorophyll content andchlorosis of the cannal plants induced by Cd were not caused by Fe, Mg, Cu, Mn, Ca and Kdeficit.
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