转基因抗虫棉对土壤生态系统影响的研究
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摘要
本研究以中国农业科学研究院棉花研究所(河南,安阳)的棉花农场中同一土壤类型一直种植传统非转基因常规棉(CK)和2块连续多年种植转基因抗虫棉的棉田(T-1、T-2)为对象,于棉花生长的苗期、蕾期、花铃期和吐絮期分别采集棉田表层土壤(0—20 cm),研究和比较了3块棉田土壤中可培养微生物数量、细菌群落多样性、微生物代谢功能多样性、无脊椎动物群落以及土壤线虫群落结构的变化。以2组转基因抗虫棉和其亲本常规棉为实验材料,研究转基因抗虫棉根系分泌物的成分及其对枯萎病菌生长的影响,分析转基因抗虫棉及其亲本常规棉受病原菌侵染后的生理生化特性的变化,构建转基因抗虫棉受枯萎病菌诱导后的抑制差减cDNA文库,探讨棉花抗枯萎病所涉及的信号转导、参与抗病反应的相关基因的种类与数量。以下为主要研究结果：
(一)转基因抗虫棉对土壤微生物群落数量和多样性的影响
随着棉花生长期的不同,棉田土壤中细菌、真菌、放线菌、反硝化细菌、亚硝化细菌和固氮菌数量都呈显著性季节变化。在全年采样过程中,不同棉田土壤中细菌、真菌、好气性固氮菌、反硝化细菌及亚硝化细菌的数量变化规律基本一致,而不同的微生物种群在生长期间的变化规律则不同。但是,与常规棉田(CK)相比,连续多年种植转基因抗虫棉(T-1、T-2)对土壤微生物群落中上述各类微生物数量没有显著影响。
采样PCR-DGGE的方法,分析了3块棉田土壤中细菌群落多样性,结果表明与种植常规棉相比,不同年限种植转基因抗虫棉对土壤细菌群落构成和多样性没有产生明显影响,而不同采样时期对棉田土壤细菌群落构成和多样性具有明显影响。
采用Biolog ECO平板测定了各棉田土壤微生物群落代谢特征,结果表明长期种植转基因抗虫棉在土壤微生物活性及功能多样性方面未见显著差异,但不同采样时期对土壤微生物存在一定影响。主成分分析显示糖类和酯类物质是该试验点土壤微生物主要利用的碳源,但不同采样时期微生物所利用的糖类和酯类物质各不相同,可作为区分各棉花时期对微生物影响的依据。
(二)转基因抗虫棉对土壤动物数量和多样性的影响
采用改良的Tullgren法收集3块棉田土壤中的中小型无脊椎动物种群,2年8次采样结果表明,2种转基因抗虫棉田和常规棉田中的土壤中小型无脊椎动物的群落构成一致,没有产生明显变化。广义混合线性模型分析证明,与种植常规棉相比,长期种植转基因抗虫棉对土壤中小型无脊椎动物的数量、群落多样性指数没有显著的影响,但是,随着棉花生长期的不同,棉田土壤无脊椎动物数量和多样性都呈显著性季节变化,并且各棉田中的土壤无脊椎动物多样性指数在棉花整个生长期内变化趋势一致。弹尾目、蜱螨目和后孔寡毛目在综合主成分中得分较高,为土壤无脊椎动物群落中的主导因子,可作为本地区未来转基因抗虫棉环境影响监测的指示物种。
采用蔗糖梯度离心法研究了常规棉田和2种转基因抗虫棉田土壤中线虫群落组成,结果表明与种植常规棉相比,长期种植转基因抗虫棉对土壤各营养团体线虫的数量和线虫多样性都没有显著性影响,但是不同采样时期对其有显著影响。不同年限种植转基因抗虫棉田中的土壤线虫的群落结构组成没有发生明显变化。转基因抗虫棉田和常规棉田中土壤线虫成熟指数和植物寄生指数在各采样时期没有显著性差异,说明种植转基因抗虫棉对土壤自由生活线虫和植物寄生线虫没有显著影响。
(三)转基因抗虫棉对棉花枯萎病抗性下降及其机理研究
2种转基因抗虫棉对棉花枯萎病菌的抗性低于亲本常规棉,转基因抗虫棉的根系分泌物对枯萎病菌孢子萌发和菌丝生长均表现出显著的促进作用。棉花根系分泌物中检测出烷烃类、醇类、酸类、酯类、苯酚类、醛酮类、烯烃类、杂环类等8类物质。与亲本常规棉相比,转基因抗虫棉根系分泌物的种类及相对含量减少、出现某些烷烃类和减少某些特异物质这3种情况。
采用扫描电镜研究了棉花苗期气孔结构,与亲本常规棉相比,转基因抗虫棉叶片气孔密度发生了显著降低,而气孔大小发生显著增加。枯萎病菌侵染后,转基因抗虫棉体内中的各种生理生化指标都发生了显著性变化,其中SOD酶、MDA和可溶性蛋白的含量较亲本显著升高,而POD酶、PAL和可溶性糖的含量较亲本显著下降。
转基因抗虫棉和亲本常规棉花受病菌侵染后许多基因都发生了显著的变化,多数为上调基因。转基因棉花和常规棉花受枯萎病菌诱导的反应基因的种类和数量都有明显的差异：亲本常规棉受病菌侵染后发生上调的一些基因类型主要是涉及生物过程功能和分子功能,而受病原菌侵染后转基因抗虫棉体内中的上述基因功能的表达受到相应的抑制。枯萎病菌诱导后,转基因抗虫棉和常规棉体内中过氧化氢酶、乙醇脱氢酶、p-半乳糖苷酶和叶绿素A-B结合蛋白基因表达量都发生了显著性升高,但是病菌诱导后常规棉体内中上述各种酶基因表达量显著高于转基因抗虫棉。
(四)转基因抗虫植物对土壤生态系统影响的监测技术指南
本技术指南涵盖了转基因抗虫植物对土壤生态系统影响的布点采样、监测指标、监测技术、数理统计及结果评估等监测技术内容。可用于监测转基因抗虫植物对土壤生态系统影响。
According to the different growth stages of cottons, we collected soil samples (0-20 cm) at seedling, budding, boll forming and boll opening stage during the year 2009 and 2010, and studied the population of culturable microorganisms, the diversity of bacterial community, the functional diversity of microbial metabolism, the community structure of invertebrates as well as soil nematode in the three different cotton fields at a cotton farm in China Cotton Institution of Agricultural Scientific Academy (Anyang, Henan Province) where non-transgenic field had been planted all along and other two cotton fields where transgenic insect-resistant cotton had been planted since 1997,2002 respectively. Two kinds of transgenic insect-resistant cottons and their parental cottons as the experimental materials, the composition of root exudates from transgenic cottons and conventional cottons and the effects on the growth of Fusarium oxysporum were studied, the changes of physiological and biochemical characteristics of transgenic cottons and conventional cottons after infection by the pathogen were analyzed and the SSH cDNA libraries were also constructed to study the type and quantity of disease resistance related genes of transgenic cotton induced by Fusarium oxysporum. The results show that:
(1) Effects of transgenic insect-resistant cottons on the population and diversity of soil microbial community
There were no significant differences in the number of bacterial, actinomycetes, fungal, azotobacter, denitrobacteria, nitrosobacteria and the diversity indices of soil microbial in two transgenic insect-resistant cotton fields compared with that of the non-transgenic cotton field, but significantly seasonal variation in the number of each microbial and diversity indices of microbial in all three cotton fields. The populations and diversity indices of microbial have the similar tendency of changes during the whole growing period in three cotton fields, while change rules of different microbial population differs in the growth period.
The diversity of soil bacterial in the three cotton fields was analyzed by PCR-DGGE method. The results showed that the different planting years of transgenic insect-resistant cottons have no significant effects on the composition and diversity of soil bacterial community compared to the cultivation of conventional cotton, but different sampling time has significant effects on the composition and diversity of soil bacterial community.
The metabolic characteristics of soil microbial communities in the cotton fields were determined using Biolog-ECO plate. The results showed that long-term cultivation of transgenic insect-resistant cottons has no significant effects on the functional diversity of microbial activity, but different sampling time has some effects. Principal component analysis showed that the sugars and esters were the main carbon sources of soil microbial in these fields, but the use of sugars and esters by soil microbial were different at different sampling time, which can be used as basis to distinguish the effects of different cotton growth stages.
(2) Effects of transgenic insect-resistant cottons on the population and diversity of soil fauna community
Soil meso-and microarthropodas were collected from the soil samples with the modified Tullgren method to monitor environmental impact of long-term cultivation of transgenic insect-resistant cotton in field conditions. The data from 8 sampling times during the 2 years showed that it was similar for community composition of soil meso-and microarthropodas in two transgenic cotton fields and one conventional cotton field, and there were no significant variations. The generalized linear mixed model (GLMM) analysis of the 2-year data on soil arthropods showed that no significant difference was found between cotton fields in individual number and the community diversity indices of the soil meso-and microarthropodas of the main soil arthropod groups, but significant seasonal variation was observed in the individual numbers and the diversity indices of the main soil meso-and microarthropodas. The principal component analysis suggested that Collembola, Acarina and Opisthopora were relatively higher in value and could be cited as important indicator organisms to monitor environmental impacts of transgenic plants in the future in this region.
The soil nematodes were collected from soil using sugar flotation and centrifugation method. The ecological index such as species richness, abundance, diversity index and trophic group index were analyzed. Results showed that there were no significant difference in the individual density and diversity indices of soil nematode in two transgenic cotton fields compared with that of the non-transgenic cottons, but had significant seasonal variation in the individual density of main trophie groups and diversity indices of nematode in all three cotton fields. There were no significant changes for community composition of soil nematodes in two transgenic cotton fields and one conventional cotton field. In addition, no significant difference was found between cotton fields in the indices of the functional structure of the nematode communities (Maturity Index, Plant Parasite Index and EMI index), which indicated no significant effect of continuously planting transgenic insect-resistant cottons on free-living marine nematodes and plant parasite nematodes.
(3) The mechanism for attenuation of disease resistance in transgenic insect-resistant cotton to Fusarium wilt
The resistance of the two insect-resistant cotton lines to F. oxysporum was inferior to the parental lines, and that their root exudates promoted fungal spore germination and mycelial growth. Alkanes, alcohols, acids, esters, phenols, aldehydes, ketones, olefins and heterocyclic were detected in root exudates of cottons. Compared with the parent conventional cottons, the kinds and relative contents of root exudates decreased, some hydrocarbons appeared and some specific substances reduced in transgenic insect-resistant cottons.
The structure of leaf pore in cotton seedling stage was studied by scanning electron microscopy. Compared with the parent conventional cottons, the stomatal density significantly reduced, and the pore size significantly increased in transgenic insect-resistant cottons. There were significant changes of physiological and biochemical indicators in transgenic insect-resistant cottons inoculated with cotton F.oxysporum, in which SOD activity, MDA and soluble protein content were significantly higher, and POD enzymes, PAL enzymes and soluble sugar content decreased significantly compared with the parents.
Many genes of transgenic insect-resistant cottons and parental cottons have significantly changed when inoculated with cotton F.oxysporum and mostly were up-regulated genes. There were significant differences in the types and numbers of response genes of transgenic insect-resistant cottons inoculated with cotton F.oxysporum compared to conventional cottons. Some types of up-regulated genes in parental cottons infected by pathogen mainly referred to the function of biological processes and molecular, and they were inhibited in the expression of transgenic insect-resistant cottons after infected by pathogen. The expressions of catalase, alcohol dehydrogenase,β-galactosidase and chlorophyll AB binding protein gene were significantly increased in transgenic insect-resistant cottons and conventional cottons infected by pathogen. The expression of the above genes in conventional cotton infected by pathogens was significantly higher than that of transgenic insect-resistant cottons.
(4) Technical guide for monitoring effect of transgenic insect-resistant plants on soil ecosystem
This technical guide covers the distribution of sampling, monitoring indicators, monitoring techniques, mathematical statistics and assessment of results in monitoring effect of transgenic insect-resistant plants on soil ecosystems. It can be used for monitoring the effect of transgenic insect-resistant plants on soil ecosystems.
(一)转基因抗虫棉对土壤微生物群落数量和多样性的影响
随着棉花生长期的不同,棉田土壤中细菌、真菌、放线菌、反硝化细菌、亚硝化细菌和固氮菌数量都呈显著性季节变化。在全年采样过程中,不同棉田土壤中细菌、真菌、好气性固氮菌、反硝化细菌及亚硝化细菌的数量变化规律基本一致,而不同的微生物种群在生长期间的变化规律则不同。但是,与常规棉田(CK)相比,连续多年种植转基因抗虫棉(T-1、T-2)对土壤微生物群落中上述各类微生物数量没有显著影响。
采样PCR-DGGE的方法,分析了3块棉田土壤中细菌群落多样性,结果表明与种植常规棉相比,不同年限种植转基因抗虫棉对土壤细菌群落构成和多样性没有产生明显影响,而不同采样时期对棉田土壤细菌群落构成和多样性具有明显影响。
采用Biolog ECO平板测定了各棉田土壤微生物群落代谢特征,结果表明长期种植转基因抗虫棉在土壤微生物活性及功能多样性方面未见显著差异,但不同采样时期对土壤微生物存在一定影响。主成分分析显示糖类和酯类物质是该试验点土壤微生物主要利用的碳源,但不同采样时期微生物所利用的糖类和酯类物质各不相同,可作为区分各棉花时期对微生物影响的依据。
(二)转基因抗虫棉对土壤动物数量和多样性的影响
采用改良的Tullgren法收集3块棉田土壤中的中小型无脊椎动物种群,2年8次采样结果表明,2种转基因抗虫棉田和常规棉田中的土壤中小型无脊椎动物的群落构成一致,没有产生明显变化。广义混合线性模型分析证明,与种植常规棉相比,长期种植转基因抗虫棉对土壤中小型无脊椎动物的数量、群落多样性指数没有显著的影响,但是,随着棉花生长期的不同,棉田土壤无脊椎动物数量和多样性都呈显著性季节变化,并且各棉田中的土壤无脊椎动物多样性指数在棉花整个生长期内变化趋势一致。弹尾目、蜱螨目和后孔寡毛目在综合主成分中得分较高,为土壤无脊椎动物群落中的主导因子,可作为本地区未来转基因抗虫棉环境影响监测的指示物种。
采用蔗糖梯度离心法研究了常规棉田和2种转基因抗虫棉田土壤中线虫群落组成,结果表明与种植常规棉相比,长期种植转基因抗虫棉对土壤各营养团体线虫的数量和线虫多样性都没有显著性影响,但是不同采样时期对其有显著影响。不同年限种植转基因抗虫棉田中的土壤线虫的群落结构组成没有发生明显变化。转基因抗虫棉田和常规棉田中土壤线虫成熟指数和植物寄生指数在各采样时期没有显著性差异,说明种植转基因抗虫棉对土壤自由生活线虫和植物寄生线虫没有显著影响。
(三)转基因抗虫棉对棉花枯萎病抗性下降及其机理研究
2种转基因抗虫棉对棉花枯萎病菌的抗性低于亲本常规棉,转基因抗虫棉的根系分泌物对枯萎病菌孢子萌发和菌丝生长均表现出显著的促进作用。棉花根系分泌物中检测出烷烃类、醇类、酸类、酯类、苯酚类、醛酮类、烯烃类、杂环类等8类物质。与亲本常规棉相比,转基因抗虫棉根系分泌物的种类及相对含量减少、出现某些烷烃类和减少某些特异物质这3种情况。
采用扫描电镜研究了棉花苗期气孔结构,与亲本常规棉相比,转基因抗虫棉叶片气孔密度发生了显著降低,而气孔大小发生显著增加。枯萎病菌侵染后,转基因抗虫棉体内中的各种生理生化指标都发生了显著性变化,其中SOD酶、MDA和可溶性蛋白的含量较亲本显著升高,而POD酶、PAL和可溶性糖的含量较亲本显著下降。
转基因抗虫棉和亲本常规棉花受病菌侵染后许多基因都发生了显著的变化,多数为上调基因。转基因棉花和常规棉花受枯萎病菌诱导的反应基因的种类和数量都有明显的差异：亲本常规棉受病菌侵染后发生上调的一些基因类型主要是涉及生物过程功能和分子功能,而受病原菌侵染后转基因抗虫棉体内中的上述基因功能的表达受到相应的抑制。枯萎病菌诱导后,转基因抗虫棉和常规棉体内中过氧化氢酶、乙醇脱氢酶、p-半乳糖苷酶和叶绿素A-B结合蛋白基因表达量都发生了显著性升高,但是病菌诱导后常规棉体内中上述各种酶基因表达量显著高于转基因抗虫棉。
(四)转基因抗虫植物对土壤生态系统影响的监测技术指南
本技术指南涵盖了转基因抗虫植物对土壤生态系统影响的布点采样、监测指标、监测技术、数理统计及结果评估等监测技术内容。可用于监测转基因抗虫植物对土壤生态系统影响。
According to the different growth stages of cottons, we collected soil samples (0-20 cm) at seedling, budding, boll forming and boll opening stage during the year 2009 and 2010, and studied the population of culturable microorganisms, the diversity of bacterial community, the functional diversity of microbial metabolism, the community structure of invertebrates as well as soil nematode in the three different cotton fields at a cotton farm in China Cotton Institution of Agricultural Scientific Academy (Anyang, Henan Province) where non-transgenic field had been planted all along and other two cotton fields where transgenic insect-resistant cotton had been planted since 1997,2002 respectively. Two kinds of transgenic insect-resistant cottons and their parental cottons as the experimental materials, the composition of root exudates from transgenic cottons and conventional cottons and the effects on the growth of Fusarium oxysporum were studied, the changes of physiological and biochemical characteristics of transgenic cottons and conventional cottons after infection by the pathogen were analyzed and the SSH cDNA libraries were also constructed to study the type and quantity of disease resistance related genes of transgenic cotton induced by Fusarium oxysporum. The results show that:
(1) Effects of transgenic insect-resistant cottons on the population and diversity of soil microbial community
There were no significant differences in the number of bacterial, actinomycetes, fungal, azotobacter, denitrobacteria, nitrosobacteria and the diversity indices of soil microbial in two transgenic insect-resistant cotton fields compared with that of the non-transgenic cotton field, but significantly seasonal variation in the number of each microbial and diversity indices of microbial in all three cotton fields. The populations and diversity indices of microbial have the similar tendency of changes during the whole growing period in three cotton fields, while change rules of different microbial population differs in the growth period.
The diversity of soil bacterial in the three cotton fields was analyzed by PCR-DGGE method. The results showed that the different planting years of transgenic insect-resistant cottons have no significant effects on the composition and diversity of soil bacterial community compared to the cultivation of conventional cotton, but different sampling time has significant effects on the composition and diversity of soil bacterial community.
The metabolic characteristics of soil microbial communities in the cotton fields were determined using Biolog-ECO plate. The results showed that long-term cultivation of transgenic insect-resistant cottons has no significant effects on the functional diversity of microbial activity, but different sampling time has some effects. Principal component analysis showed that the sugars and esters were the main carbon sources of soil microbial in these fields, but the use of sugars and esters by soil microbial were different at different sampling time, which can be used as basis to distinguish the effects of different cotton growth stages.
(2) Effects of transgenic insect-resistant cottons on the population and diversity of soil fauna community
Soil meso-and microarthropodas were collected from the soil samples with the modified Tullgren method to monitor environmental impact of long-term cultivation of transgenic insect-resistant cotton in field conditions. The data from 8 sampling times during the 2 years showed that it was similar for community composition of soil meso-and microarthropodas in two transgenic cotton fields and one conventional cotton field, and there were no significant variations. The generalized linear mixed model (GLMM) analysis of the 2-year data on soil arthropods showed that no significant difference was found between cotton fields in individual number and the community diversity indices of the soil meso-and microarthropodas of the main soil arthropod groups, but significant seasonal variation was observed in the individual numbers and the diversity indices of the main soil meso-and microarthropodas. The principal component analysis suggested that Collembola, Acarina and Opisthopora were relatively higher in value and could be cited as important indicator organisms to monitor environmental impacts of transgenic plants in the future in this region.
The soil nematodes were collected from soil using sugar flotation and centrifugation method. The ecological index such as species richness, abundance, diversity index and trophic group index were analyzed. Results showed that there were no significant difference in the individual density and diversity indices of soil nematode in two transgenic cotton fields compared with that of the non-transgenic cottons, but had significant seasonal variation in the individual density of main trophie groups and diversity indices of nematode in all three cotton fields. There were no significant changes for community composition of soil nematodes in two transgenic cotton fields and one conventional cotton field. In addition, no significant difference was found between cotton fields in the indices of the functional structure of the nematode communities (Maturity Index, Plant Parasite Index and EMI index), which indicated no significant effect of continuously planting transgenic insect-resistant cottons on free-living marine nematodes and plant parasite nematodes.
(3) The mechanism for attenuation of disease resistance in transgenic insect-resistant cotton to Fusarium wilt
The resistance of the two insect-resistant cotton lines to F. oxysporum was inferior to the parental lines, and that their root exudates promoted fungal spore germination and mycelial growth. Alkanes, alcohols, acids, esters, phenols, aldehydes, ketones, olefins and heterocyclic were detected in root exudates of cottons. Compared with the parent conventional cottons, the kinds and relative contents of root exudates decreased, some hydrocarbons appeared and some specific substances reduced in transgenic insect-resistant cottons.
The structure of leaf pore in cotton seedling stage was studied by scanning electron microscopy. Compared with the parent conventional cottons, the stomatal density significantly reduced, and the pore size significantly increased in transgenic insect-resistant cottons. There were significant changes of physiological and biochemical indicators in transgenic insect-resistant cottons inoculated with cotton F.oxysporum, in which SOD activity, MDA and soluble protein content were significantly higher, and POD enzymes, PAL enzymes and soluble sugar content decreased significantly compared with the parents.
Many genes of transgenic insect-resistant cottons and parental cottons have significantly changed when inoculated with cotton F.oxysporum and mostly were up-regulated genes. There were significant differences in the types and numbers of response genes of transgenic insect-resistant cottons inoculated with cotton F.oxysporum compared to conventional cottons. Some types of up-regulated genes in parental cottons infected by pathogen mainly referred to the function of biological processes and molecular, and they were inhibited in the expression of transgenic insect-resistant cottons after infected by pathogen. The expressions of catalase, alcohol dehydrogenase,β-galactosidase and chlorophyll AB binding protein gene were significantly increased in transgenic insect-resistant cottons and conventional cottons infected by pathogen. The expression of the above genes in conventional cotton infected by pathogens was significantly higher than that of transgenic insect-resistant cottons.
(4) Technical guide for monitoring effect of transgenic insect-resistant plants on soil ecosystem
This technical guide covers the distribution of sampling, monitoring indicators, monitoring techniques, mathematical statistics and assessment of results in monitoring effect of transgenic insect-resistant plants on soil ecosystems. It can be used for monitoring the effect of transgenic insect-resistant plants on soil ecosystems.
引文
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