耐重金属胁迫的能源植物筛选及其适应性研究
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摘要
采用盆栽试验,评价了8种能源植物[花生(Arachis hypogaea).大麻(Cannabis sativa).亚麻(Linum usitatissimum)、蓖麻(Ricinus communis)、大豆(Glycine max)、向日葵(Helianthus annuus)、油菜(Brassica rapa)和红花(Carthamus tinctorius)]对重金属(Zn、Cd和Cu)的耐受性和积累能力。在此基础上,以花生为研究对象,研究了叶片对重金属(Zn、Cd和Cu)的可塑性响应及其适应意义；探讨了Zn、Cd胁迫对花生光合作用的影响及其与解剖结构之间的关系；研究了花生对Zn、Cd胁迫的适应机制。同时,探讨了水杨酸(Salicylic acid, SA)对大麻,以及硅对花生Cd毒害的缓解作用及其机理。主要研究结果如下：
(1)供试的8种能源植物对Cd和Zn具有相对较强的耐受性,而对Cu的耐受性较低。其中,大麻、亚麻、蓖麻和花生对高浓度Cd耐受性较强；大麻、亚麻和油菜对高浓度Zn的耐受性较强；花生、亚麻、蓖麻、大豆则对Cu具有一定的耐性。8种能源植物的地上部分对Zn、Cd和Cu三种重金属的积累量既存在种间差异,也存在金属间差异。对于金属来说,植物的地上部分积累量以Zn为最大,Cd次之,Cu最少。对于物种而言,油菜、红花和亚麻的地上部分对Cd的积累量较大,均大于100 mgkg-1 DW;向日葵、花生、油菜、大豆和红花的地上部分对Zn的积累量较高。
(2)花生叶片对重金属(Zn、Cd和Cu)表现出一定的表型可塑性。在测定的18种性状中,叶面积(LA)、比叶重(LMA)、叶绿素a (Chl a)、叶绿素b (Chl b).总叶绿素(Chlt)、光系统Ⅱ有效量子产额(ΦPsⅡ)、上表皮气孔密度(SDU)、栅栏组织厚度(PT)和栅栏组织海绵组织厚度比(P／S)对重金属较为敏感,并表现出了较大的可塑性。其中,叶绿素含量和叶绿素荧光参数的可塑性是适应不良性可塑性,反映了重金属对叶片的毒害作用。相反,叶片的解剖可塑性则是适应性的,反映了植物对重金属胁迫的适应能力。在Zn、Cd胁迫下,花生生物量下降,光合作用受到抑制,叶片结构发生改变。Zn、Cd胁迫对花生叶片光合作用的抑制,既包括由气孔导度(Gs)下降引起的气孔限制,又包括光合色素含量降低而引起的非气孔限制。Zn、Cd胁迫均能诱导花生叶片形成了一定的旱生结构：如叶片和栅栏组织增厚,栅栏组织海绵组织厚度比增大,气孔密度增加,长度变小,这种结构使得植物既能降低水分蒸腾,又能最大限度地维持CO2的吸收,从而减轻了因气孔限制导致的光合作用下降。叶绿素荧光参数表明,Cd. Zn胁迫对叶片PSⅡ的活性中心造成损伤,但这并不是抑制光合作用的主要原因。
(3)花生幼苗对Cd、Zn都具有较强的耐受性。在器官水平,植物吸收的大部分Cd、Zn被截留在根中。在细胞水平,细胞壁是Cd、Zn在花生叶片和根细胞中贮存的主要场所,而可溶组分中的Cd、Zn大部分可能被区隔在液泡之中。低浓度Cd对花生叶片超氧化物歧化酶(SOD)、抗坏血酸过氧化物酶(APX)和谷胱甘肽还原酶(GR)活性具有抑制效应,而在高浓度Cd胁迫下,SOD、GR活性增大。同样,高浓度锌胁迫诱导SOD和APX活性增大。此外,初步发现根中可能存在诱导型Cd结合蛋白,具有结合大量Cd的能力；叶片中也可能存在与Zn结合能力较强的蛋白。
(4)大麻对Cd胁迫具有较强的耐受性。在高浓度(100 mg kg-1)下,大麻的地上、地下部分生物量分别下降46%和48%。大麻对Cd的迁移指数很小(3.5-4.0)。在Cd处理为25-100mg kg-1范围内,大麻的光合色素、叶绿素荧光参数(Fv/Fm和ΦPSⅡ)、气体交换参数(Pn, Gs、Ci、E和Rd)均没有受到明显抑制。水杨酸(SA)处理能显著改善高浓度Cd(100 mg kg-1)胁迫下大麻植株的生长状况,降低植物体内的Cd含量,但并不影响迁移指数(TF). SA能显著提高Cd胁迫下大麻植株的光合能力,其机制既包括SA诱导气孔开放而引起的气孔调节因素,同时还包括由于叶绿素和类胡萝卜素含量以及ΦPSⅡ的增加而引起的非气孔调节因素。Cd含量的下降和光合能力的增强可能是SA提高大麻耐Cd性的主要原因。
(5)在两个花生品种中,鲁资101的耐Cd性明显强于鲁花11号。在200μmol L-1Cd处理下,鲁资101的生物量下降幅度、地上部Cd含量和迁移指数均显著低于鲁花11号。细胞壁和细胞器Cd含量在品种间差异不显著,但鲁资101的可溶组分Cd含量显著高于鲁花11号。硅处理对两个花生品种Cd毒害都具有一定的缓解作用,但存在品种差异,对Cd敏感品种(鲁花11号)幼苗cd毒害的缓解作用明显强于耐Cd品种(鲁资101)。其原因可能是：①硅降低了鲁花11号植株Cd由根系向地上部迁移的迁移系数,大幅减少植株地上部分Cd含量；②降低了鲁花11号叶片细胞器中的Cd含量。
Combining phytoremediation with energy crop cultivation offers attractive economic alternatives, with the view of achieving low price decontamination of soil by the production of biodiesel. In order to screen potential energy plants that can be planted in heavy metal contaminated area for biodiesel, cadmium (Cd), zinc (Zn) and copper (Cu) tolerance and accumulation capacity of eight energy plants, including peanut (Arachis hypogaea), hemp (Cannabis sativa), flax (Linum usitatissimum), caster (Ricinus communis), soybean (Glycine max), sunflower (Helianthus annuus), rapeseed (Brassica rapa) and safflower (Carthamus tinctorius) were evaluated by pot experiments. On the basis of this, peanut, a metal toleranted energy plant widely cultivated in many countries for traditional food oil production, were chosen for further studies, the following questions are posed:(a) how do peanut leaves respond to distinct heavy metal in terms of morphology, anatomy and physiology; and whether the plasticity in response to heavy metal stress was adaptive; (b) do Cd or Zn toxicity affect photosynthetic performance and anatomic structure of leaves, and what relationships between these characteristics; and (c) what kind of mechanisms do peanut plants cope with Cd or Zn toxicity. Furthermore, the roles of exogenous substances, such as salicylic acid (SA) and silicon, in alleviating Cd toxicity were also studied. The results are showed as follows:
The pot study conducted with Cd (50 to 200 mg Cd kg-1 sands), Zn(200 to 800 mg Cd kg-1 sands), and Cu (200 to 800 mg Cd kg-1 sands) indicated that all plant species tested initially have ability to withstand Cd and Zn stress, whereas the capacity of Cu tolerance are relatively low. Among these plants, hemp, flax, caster and peanut exhibited a higher level of Cd tolerance, while hemp, flax, and rapeseed had a strong tolerance to high Zn concentrations, and these plants could be cultivated in Cd or Zn-contaminated soils for biodiesel production. Metal accumulation in plants were metal specific and species specific. As for metals, Zn content in tissues was the most, followed which is Cd, and Cu the least. In respect for the plant species, hemp, flax, and peanut showed a high ability of Cd accumulation, while peanut and soybean exhibited higher Zn concentrations in shoots. These energy plants, therefore, are good candidates for the implementation of this new strategy of cultivating biodiesel crops for phytoremediation of Cd or Zn-contaminated soils.
Phenotypic plasticity in morphological, anatomical and physiological traits of peanut leaves was tested at four different concentrations of Cd, Cu and Zn under greenhouse conditions. Among 18 characteristics tested, nine were found to be the most sensitive and demonstrate the greatest phenotypic plasticity. These were:the leaf area (LA), the leaf mass per area (LMA), chlorophyll a content (Chl a), chlorophyll b content (Chl b), total chlorophyll content (Chl t), the effective quantum yield of photosystem II (ΦPS II), stomatal density of upper epidermis (SDU), palisade thickness (PT), and palisade to spongy thickness ratio (P/S). The plasticity of chlorophyll content and fluorescence parameters may be maladaptive and reflects metal toxicity to leaves, whereas the anatomical plasticity is adaptive, indicative of a tradeoff between the physiological and anatomic plasticity. Both Cd and Zn treatments caused an inhibition in the net photosynthetic rate (Pn) of peanut (Arachis hypogaea) plants, due to the reduction of stomatal conductance (Gs) and photosynthetic pigment content, as well as the alteration in leaf structure. The decrease of the transpiration rate (E) and Gs might result from the Cd or Zn-induced xerophyte anatomic features of leaves (i.e. thick lamina, upper epidermis, palisade mesophyll, high palisade to spongy thickness ratio, as well as abundant and small stomata). The decline of Pn seems to be independent of the impairment in PSⅡ.
Peanut plants had a strong tolerance to high Cd and Zn stress, and also accumulated a certain amount of Cd and Zn in the tissues. At the level of plant tissues, most of Cd and Zn absorbed by the plants were retained in the roots. At subcellular level, most of Cd and Zn in leaf and root cells were fixed in the cell wall fractions, whereas the most of Cd and Zn in the soluble fraction were compartmented in the vacuole. In respect of physiological characters, the obtained result showed that the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and glutathione reductase (GR) were inhibited by low Cd treatment, while at high level, SOD and GR were increased. Similarly, under high Zn condition, the activities of SOD and APX were also increased. Furthermore, a Cd induced Cd binding protein and a innate Zn binding protein was found in root and leaf soluble fraction, respectively. It is concluded that the tolerance of peanut plant to Cd and Zn toxicity was resulted from the metal exclusion stratedge, in which the fixation of Cd and Zn in cell wall, compartmentation of the vacuole, sequestration by metal binding protein, as well as an efficient antioxidant systems were involved.
In order to assess cadmium tolerance of hemp, and whether salicylic acid (SA) pretreatment regulate the growth and photosynthetic capacity of hemp under Cd stress, a pot experiment was conducted under greenhouse conditions. Exposure of hemp plants to low Cd (25 mg kg-1) had stimulatory effects on plant growth, whereas it was inhibited at high Cd stress (50 and 100 mg kg-1). Cd exposure showed little inhibition in photosynthetic pigment, chlorophyll fluorescence, as well as photosynthetic performance. These results demonstrated that hemp has innate capacity to tolerant Cd stress. SA pretreatment counteracted the Cd-induced growth inhibition in hemp plants; this was more obvious under high Cd stress (100 mg kg-1). SA affect on alleviating Cd toxicity in hemp seedlings was associated with reduced Cd uptake and improved photosynthetic capacity due to stomatal limitations other than photosynthetic pigments.
Silicon (Si) is generally considered a beneficial element for the growth of higher plants, especially for those grown under stressed environments. Recently, the mitigating role of Si in cadmium (Cd) stress has received some attention. However, its mechanisms involved remain poorly understood. We studied the effects of Si on tissue and subcellular distribution of Cd with two contrasting peanut cultivars (Luhua 11 and Luzi 101) differing in their Cd tolerance. The results showed that Cd exposure alone depressed plant growth for both cultivars, and this toxicity was more obvious in Cd-sensitive cultivar (Luhua 11) than in Cd-tolerant cultivar (Luzi 101). Si supply significantly alleviated the toxicity of Cd in peanut seedlings. In contrast, the alleviation of Cd toxicity was more significantly in Cd-sensitive cultivar (Luhua 11) than in Cd-tolerant cultivar (Luzi 101). The mechanisms of Si amelioration of Cd stress were cultivar dependent. In comparison to Luzi 101, Cd content in shoots, translocation factor of Cd from root to shoot, and Cd content in cell organelle fractions of leaves in Luhua 11 were more significantly inhibited by Si, indicating Si-mediated inhibition of Cd transport from roots to shoots, and reduction of Cd content in cell organelle fractions of leaves might be responsible for the role of Si in alleviating Cd toxicity in Luhua 11 seedlings.
(1)供试的8种能源植物对Cd和Zn具有相对较强的耐受性,而对Cu的耐受性较低。其中,大麻、亚麻、蓖麻和花生对高浓度Cd耐受性较强；大麻、亚麻和油菜对高浓度Zn的耐受性较强；花生、亚麻、蓖麻、大豆则对Cu具有一定的耐性。8种能源植物的地上部分对Zn、Cd和Cu三种重金属的积累量既存在种间差异,也存在金属间差异。对于金属来说,植物的地上部分积累量以Zn为最大,Cd次之,Cu最少。对于物种而言,油菜、红花和亚麻的地上部分对Cd的积累量较大,均大于100 mgkg-1 DW;向日葵、花生、油菜、大豆和红花的地上部分对Zn的积累量较高。
(2)花生叶片对重金属(Zn、Cd和Cu)表现出一定的表型可塑性。在测定的18种性状中,叶面积(LA)、比叶重(LMA)、叶绿素a (Chl a)、叶绿素b (Chl b).总叶绿素(Chlt)、光系统Ⅱ有效量子产额(ΦPsⅡ)、上表皮气孔密度(SDU)、栅栏组织厚度(PT)和栅栏组织海绵组织厚度比(P／S)对重金属较为敏感,并表现出了较大的可塑性。其中,叶绿素含量和叶绿素荧光参数的可塑性是适应不良性可塑性,反映了重金属对叶片的毒害作用。相反,叶片的解剖可塑性则是适应性的,反映了植物对重金属胁迫的适应能力。在Zn、Cd胁迫下,花生生物量下降,光合作用受到抑制,叶片结构发生改变。Zn、Cd胁迫对花生叶片光合作用的抑制,既包括由气孔导度(Gs)下降引起的气孔限制,又包括光合色素含量降低而引起的非气孔限制。Zn、Cd胁迫均能诱导花生叶片形成了一定的旱生结构：如叶片和栅栏组织增厚,栅栏组织海绵组织厚度比增大,气孔密度增加,长度变小,这种结构使得植物既能降低水分蒸腾,又能最大限度地维持CO2的吸收,从而减轻了因气孔限制导致的光合作用下降。叶绿素荧光参数表明,Cd. Zn胁迫对叶片PSⅡ的活性中心造成损伤,但这并不是抑制光合作用的主要原因。
(3)花生幼苗对Cd、Zn都具有较强的耐受性。在器官水平,植物吸收的大部分Cd、Zn被截留在根中。在细胞水平,细胞壁是Cd、Zn在花生叶片和根细胞中贮存的主要场所,而可溶组分中的Cd、Zn大部分可能被区隔在液泡之中。低浓度Cd对花生叶片超氧化物歧化酶(SOD)、抗坏血酸过氧化物酶(APX)和谷胱甘肽还原酶(GR)活性具有抑制效应,而在高浓度Cd胁迫下,SOD、GR活性增大。同样,高浓度锌胁迫诱导SOD和APX活性增大。此外,初步发现根中可能存在诱导型Cd结合蛋白,具有结合大量Cd的能力；叶片中也可能存在与Zn结合能力较强的蛋白。
(4)大麻对Cd胁迫具有较强的耐受性。在高浓度(100 mg kg-1)下,大麻的地上、地下部分生物量分别下降46%和48%。大麻对Cd的迁移指数很小(3.5-4.0)。在Cd处理为25-100mg kg-1范围内,大麻的光合色素、叶绿素荧光参数(Fv/Fm和ΦPSⅡ)、气体交换参数(Pn, Gs、Ci、E和Rd)均没有受到明显抑制。水杨酸(SA)处理能显著改善高浓度Cd(100 mg kg-1)胁迫下大麻植株的生长状况,降低植物体内的Cd含量,但并不影响迁移指数(TF). SA能显著提高Cd胁迫下大麻植株的光合能力,其机制既包括SA诱导气孔开放而引起的气孔调节因素,同时还包括由于叶绿素和类胡萝卜素含量以及ΦPSⅡ的增加而引起的非气孔调节因素。Cd含量的下降和光合能力的增强可能是SA提高大麻耐Cd性的主要原因。
(5)在两个花生品种中,鲁资101的耐Cd性明显强于鲁花11号。在200μmol L-1Cd处理下,鲁资101的生物量下降幅度、地上部Cd含量和迁移指数均显著低于鲁花11号。细胞壁和细胞器Cd含量在品种间差异不显著,但鲁资101的可溶组分Cd含量显著高于鲁花11号。硅处理对两个花生品种Cd毒害都具有一定的缓解作用,但存在品种差异,对Cd敏感品种(鲁花11号)幼苗cd毒害的缓解作用明显强于耐Cd品种(鲁资101)。其原因可能是：①硅降低了鲁花11号植株Cd由根系向地上部迁移的迁移系数,大幅减少植株地上部分Cd含量；②降低了鲁花11号叶片细胞器中的Cd含量。
Combining phytoremediation with energy crop cultivation offers attractive economic alternatives, with the view of achieving low price decontamination of soil by the production of biodiesel. In order to screen potential energy plants that can be planted in heavy metal contaminated area for biodiesel, cadmium (Cd), zinc (Zn) and copper (Cu) tolerance and accumulation capacity of eight energy plants, including peanut (Arachis hypogaea), hemp (Cannabis sativa), flax (Linum usitatissimum), caster (Ricinus communis), soybean (Glycine max), sunflower (Helianthus annuus), rapeseed (Brassica rapa) and safflower (Carthamus tinctorius) were evaluated by pot experiments. On the basis of this, peanut, a metal toleranted energy plant widely cultivated in many countries for traditional food oil production, were chosen for further studies, the following questions are posed:(a) how do peanut leaves respond to distinct heavy metal in terms of morphology, anatomy and physiology; and whether the plasticity in response to heavy metal stress was adaptive; (b) do Cd or Zn toxicity affect photosynthetic performance and anatomic structure of leaves, and what relationships between these characteristics; and (c) what kind of mechanisms do peanut plants cope with Cd or Zn toxicity. Furthermore, the roles of exogenous substances, such as salicylic acid (SA) and silicon, in alleviating Cd toxicity were also studied. The results are showed as follows:
The pot study conducted with Cd (50 to 200 mg Cd kg-1 sands), Zn(200 to 800 mg Cd kg-1 sands), and Cu (200 to 800 mg Cd kg-1 sands) indicated that all plant species tested initially have ability to withstand Cd and Zn stress, whereas the capacity of Cu tolerance are relatively low. Among these plants, hemp, flax, caster and peanut exhibited a higher level of Cd tolerance, while hemp, flax, and rapeseed had a strong tolerance to high Zn concentrations, and these plants could be cultivated in Cd or Zn-contaminated soils for biodiesel production. Metal accumulation in plants were metal specific and species specific. As for metals, Zn content in tissues was the most, followed which is Cd, and Cu the least. In respect for the plant species, hemp, flax, and peanut showed a high ability of Cd accumulation, while peanut and soybean exhibited higher Zn concentrations in shoots. These energy plants, therefore, are good candidates for the implementation of this new strategy of cultivating biodiesel crops for phytoremediation of Cd or Zn-contaminated soils.
Phenotypic plasticity in morphological, anatomical and physiological traits of peanut leaves was tested at four different concentrations of Cd, Cu and Zn under greenhouse conditions. Among 18 characteristics tested, nine were found to be the most sensitive and demonstrate the greatest phenotypic plasticity. These were:the leaf area (LA), the leaf mass per area (LMA), chlorophyll a content (Chl a), chlorophyll b content (Chl b), total chlorophyll content (Chl t), the effective quantum yield of photosystem II (ΦPS II), stomatal density of upper epidermis (SDU), palisade thickness (PT), and palisade to spongy thickness ratio (P/S). The plasticity of chlorophyll content and fluorescence parameters may be maladaptive and reflects metal toxicity to leaves, whereas the anatomical plasticity is adaptive, indicative of a tradeoff between the physiological and anatomic plasticity. Both Cd and Zn treatments caused an inhibition in the net photosynthetic rate (Pn) of peanut (Arachis hypogaea) plants, due to the reduction of stomatal conductance (Gs) and photosynthetic pigment content, as well as the alteration in leaf structure. The decrease of the transpiration rate (E) and Gs might result from the Cd or Zn-induced xerophyte anatomic features of leaves (i.e. thick lamina, upper epidermis, palisade mesophyll, high palisade to spongy thickness ratio, as well as abundant and small stomata). The decline of Pn seems to be independent of the impairment in PSⅡ.
Peanut plants had a strong tolerance to high Cd and Zn stress, and also accumulated a certain amount of Cd and Zn in the tissues. At the level of plant tissues, most of Cd and Zn absorbed by the plants were retained in the roots. At subcellular level, most of Cd and Zn in leaf and root cells were fixed in the cell wall fractions, whereas the most of Cd and Zn in the soluble fraction were compartmented in the vacuole. In respect of physiological characters, the obtained result showed that the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and glutathione reductase (GR) were inhibited by low Cd treatment, while at high level, SOD and GR were increased. Similarly, under high Zn condition, the activities of SOD and APX were also increased. Furthermore, a Cd induced Cd binding protein and a innate Zn binding protein was found in root and leaf soluble fraction, respectively. It is concluded that the tolerance of peanut plant to Cd and Zn toxicity was resulted from the metal exclusion stratedge, in which the fixation of Cd and Zn in cell wall, compartmentation of the vacuole, sequestration by metal binding protein, as well as an efficient antioxidant systems were involved.
In order to assess cadmium tolerance of hemp, and whether salicylic acid (SA) pretreatment regulate the growth and photosynthetic capacity of hemp under Cd stress, a pot experiment was conducted under greenhouse conditions. Exposure of hemp plants to low Cd (25 mg kg-1) had stimulatory effects on plant growth, whereas it was inhibited at high Cd stress (50 and 100 mg kg-1). Cd exposure showed little inhibition in photosynthetic pigment, chlorophyll fluorescence, as well as photosynthetic performance. These results demonstrated that hemp has innate capacity to tolerant Cd stress. SA pretreatment counteracted the Cd-induced growth inhibition in hemp plants; this was more obvious under high Cd stress (100 mg kg-1). SA affect on alleviating Cd toxicity in hemp seedlings was associated with reduced Cd uptake and improved photosynthetic capacity due to stomatal limitations other than photosynthetic pigments.
Silicon (Si) is generally considered a beneficial element for the growth of higher plants, especially for those grown under stressed environments. Recently, the mitigating role of Si in cadmium (Cd) stress has received some attention. However, its mechanisms involved remain poorly understood. We studied the effects of Si on tissue and subcellular distribution of Cd with two contrasting peanut cultivars (Luhua 11 and Luzi 101) differing in their Cd tolerance. The results showed that Cd exposure alone depressed plant growth for both cultivars, and this toxicity was more obvious in Cd-sensitive cultivar (Luhua 11) than in Cd-tolerant cultivar (Luzi 101). Si supply significantly alleviated the toxicity of Cd in peanut seedlings. In contrast, the alleviation of Cd toxicity was more significantly in Cd-sensitive cultivar (Luhua 11) than in Cd-tolerant cultivar (Luzi 101). The mechanisms of Si amelioration of Cd stress were cultivar dependent. In comparison to Luzi 101, Cd content in shoots, translocation factor of Cd from root to shoot, and Cd content in cell organelle fractions of leaves in Luhua 11 were more significantly inhibited by Si, indicating Si-mediated inhibition of Cd transport from roots to shoots, and reduction of Cd content in cell organelle fractions of leaves might be responsible for the role of Si in alleviating Cd toxicity in Luhua 11 seedlings.
引文
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