基于潘那利番茄渐渗系发掘干旱胁迫响应基因及功能分析
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摘要
番茄(Solanum lycopersicum)为世界性重要蔬菜之一,在我国蔬菜产业中具有重要地位,同时也是生物学模式生物之一。干旱直接威胁着番茄植株的生长发育,导致产量和品质下降。如何提高番茄自身的抗旱能力,培育优良耐旱新品种,已成为迫切需要解决的问题。
对植物耐旱机理的解析,前人已从生理生化、细胞结构及分子等水平进行了大量研究,并取得重要进展。植物主要通过增厚表皮蜡质层、改变气孔开度、形成发达根系和贮水组织等结构适应干旱；渗透调节物的形成、保护酶活性的提高、膜系统稳定性的维持、内源激素的调节、次生代谢物的合成等生理生化代谢都参与植物对干旱的防御；对植物耐旱的分子机理研究,近年已克隆了一大批耐旱相关基因,在植物抵御干旱过程中起直接保护或调控作用。干旱等逆境下,植物体内受ABA调控与非依赖ABA调控基因之间互作,形成复杂网络,共同调节多条信号途径转导和转录因子活性,激发下游基因表达,对干旱做出响应。
本研究以耐旱野生番茄S. pennellii与栽培番茄种S. lycopersicum cv M82及由二者构建的一套渐渗系为研究材料,从形态结构特征,分析耐旱番茄的结构特点；通过生理生化指标与耐旱性的相关性,建立适合耐旱番茄筛选的鉴定指标；利用microarray技术,从转录、信号转导及细胞分化等生物进程,分析番茄响应干旱的调控机理,候选耐旱相关基因,进行功能验证,为番茄的耐旱性改良和耐旱机理分析提供重要理论指导和实践依据。本研究的主要结果如下：
1.耐旱番茄的形态特性分析。通过对耐旱野生番茄S. pennellii与普通栽培种番茄S. lycopersicum M82形态结构的比较,分析S. pennellii的耐旱结构特点。S.pennellii植株叶、茎及花萼等地上组织全部被浓密表皮毛和粘稠腺体分泌物覆盖,利于减少水分散失的同时可能又有助于吸收空气中的水分；叶上表皮气孔数目较多,可以为吸收粘附在表皮的“露水”进入体内提供通道；叶片表皮细胞排列致密,也有利于减少体内水分散失；栅栏组织与海绵组织之比变大,可以增强机械强度；茎中薄壁组织发达,可能储藏大量水分,供应干旱等逆境下生长所需；而欠发达的根系和叶脉等组织则在S. pennellii耐旱机理中发挥并不重要的作用。
2.建立番茄耐旱评价指标体系。通过对叶片相对含水量、细胞伤害率、丙二醛含量、超氧化物岐化酶含量、脯氨酸含量等生理生化指标与耐旱性之间的相关性分析,建立适合耐旱性番茄筛选的检测指标。结果表明,轻度、中度、重度干旱胁迫下,叶片相对含水量都可用于鉴定番茄材料的耐旱性。
3.番茄干旱响应基因分析。利用筛选的耐旱渐渗系与M82,结合microarray技术,分析番茄响应干旱的调控机理。每种参试材料都获得超过1,200个差异表达基因,其中耐旱系中有359个单独表达基因。通过生物学进程分析,表达基因在逆境响应中占主要比例。耐旱系可能通过特异表达的转录因子基因(编码Zinc-finger、NAC、bHLH、AP2/EREBP及HSF等家族蛋白)、信号转导基因(编码受体蛋白激酶、促细胞分裂活性蛋白激酶、钙调结合蛋白、磷酸酯酶及膜蛋白等)、组织生长发育相关基因和一系列单独变化的生化途径(糖异生、色氨酸降解、嘌呤核苷酸生成、过氧化物清除、淀粉降解、甲硫氨酸合成)等方式调节耐旱性。而耐旱系和M82中共同表达的基因和共同变化的生化途径,如次生代谢物、无机营养、糖和多糖、氨基酸家族、激素等的合成或分解,可能分别为番茄对干旱的基本响应基因和代谢调控方式。
4.耐旱候选基因的分析。利用芯片结果,选取耐旱系与M82中有差异表达的干旱响应基因,为候选耐旱相关基因,克隆基因开放阅读编码框,对其编码蛋白序列及结构进行预测分析。
5.候选基因的表达模式。通过半定量RT-PCR法,分析候选基因在番茄不同组织器官,以及在不同干旱胁迫程度和不同外界因子作用下的表达模式。结果表明,候选基因SIWRKY、SpWRKY、SINAC表达具有组织特异性,在成熟叶和茎中表达量都较高,而在果实和/或根中不表达。候选基因SITR、SpTR和SpNAC则在根、茎、叶、花、果中都表达,但在果实和根中表达量仍比茎和叶中低。大部分候选基因在中度、重度胁迫下比轻度胁迫下表达变化明显。在盐、高低温及ABA较长时间作用下,大部分候选基因都被诱导；而在SA作用下,除NAC基因外,其它基因都被诱导。
6.候选基因的染色体定位分析。利用番茄基因组测序结果、扩增片段多态性和酶切扩增多态性序列法,对候选基因进行染色体定位。SpTR基因定位于第11染色体11-D区；SpWRKY基因定位于第8染色体,包含于克隆代号为C08SLe0011M12的BAC库中；SpNAC基因定位于第10染色体10-D区域。
7.候选基因的转基因创建、表达分析及转基因番茄的耐逆性鉴定。构建候选基因超量表达载体,利用农杆菌介导的遗传转化方法,将候选基因转入番茄栽培种中蔬5号中。通过PCR法检测,获得超量表达SpTR阳性植株14棵,超量表达SpWRKY阳性植株13棵,超量表达SpNAC阳性植株19棵。利用半定量RT-PCR法,鉴定转基因植株叶片中目的基因的表达量明显高于野生型。检测超量表达目的基因番茄幼苗的耐逆性,结果表明,SpTR和SpWRKY超量表达后,可增强转基因番茄幼苗的耐旱性、耐盐性和耐低温性。
Tomato (Solarium lycopersicum) is one of the most important economical vegetable crops in the Solanaceae family and also has been used as a model system. Drought stress straightly affects the growth and development of tomato seedlings, and causes of decreased quality and yield reduction. It has become one of urgent requirements to breed excellently drought-tolerant tomato variety to reduce the water deficit damage.
The elucidation of the mechanisms of drought tolerance has been studied on the base of morphological and anatomical, physiological and biochemical, and molecular level. The plant adaptation to water deficit are caused by changed morphological and anatomical structure, such as thick waxy cuticle, altered stomata aperture, well developed root system, and strong parenchyma. The physiological and biochemical characteristics including the accumulation of osmotic adjustment materials and protective enzymes, the stability of membrane system, the presence of endogenous hormones and secondary metabolites also contribute to enhanced drought tolerance. During the process of molecular research on plant responses to drought stress, a large number of genes were cloned, classifying into two major groups according to their putative functional modes. The first group comprises the genes encoding structural proteins, which are stress tolerance downstream effectors. The second group genes encoded regulatory proteins that are early response transcriptional activators including the transcription factors and the protein kinases. The expression of drought-inducible genes can be governed by ABA-dependent or ABA-independent regulatory systems, forming the cross-talks to regulate the activity of transcription factors and signal transduction in response to drought stress.
S. pennellii (LA0716), one of the wild crossable relatives of cultivated species, has a distinct ability to withstand desiccation in extreme arid condition. A collection of 50 introgression lines that covers the entire genome of their donor parent, S. pennellii, in the background of the cultivated species, S. lycopersicum M82, a drought-sensitive cultivar, were generated. In this study, we firstly use the drought-tolernat lines together with the currently expanding tomato research platforms such as genome sequencing and microarray applications to study the chacteraization of drought responsive genes and investigate the drought tolerance mechanism in tomato. The main results were as following:
1. The structure characteristics analysis of S. pennellii. A comparative observation of morphological and anatomical structure between S. pennellii and M82 were performed to study the drought-tolerant structure characteristics. The aerial tissues including leaf, stem, calyx and fruit of S. pennellii plant are covered with dense trichomes and glandular secretion, which may be benefit in reducing of water loss and absorbing moisture in the air. The increased number of stomata on the upper epidermis of S. pennellii leaf might support the channel for adsorbed dew. The thickness ratio of stockade tissue to sponge tissue in S. pennellii leaf is higher than that in M82, which could reinfoce the mechanical strength under drought stress. The parenchyma cells are widely distributed throughout stem of S. pennellii, suggesting they are benefit for water store and stronger water retention capacity, while the root and leaf vein are weak, indicating these tissues play unimportant roles in drought tolerance.
2. An analysis on index system of tomato drought tolerance evaluation. The correlation of index/index and index/drought tolerance under different drought stresses were studied. The relative water content can be used for selecting the drought-tolerant tomato genotype under mild, moderate and serve drought stress. The malondialdehyde content is also effective index for detecting the tomato drought tolerance under moderate drought stress.
3. The expression characteristics of drought responsive genes in tomato. Gene expression profiles between two drought-tolerant lines identified from introgression line population of S. pennellii and M82 were investigated under drought stress using tomato Oligo chips TOM2. More than 1,200 drought-responsive genes were identified in each of tested genotypes. The "response to stress" and "response to abiotic stimulus" were among the largest groups in all three genotypes. Based on biological function of drought-responsive genes, the enhanced drought tolerance of tomato may be closely related to upstream regulation of transcription factors and signal regulators specifically identified in the drought tolerant lines. However, those genes expressed in both tolerant and sensitive genotypes may act as basal drought-responsive factors in tomato under drought stress. The specifically expressed gene involved in cell differentiation, growth and anatomical structure morphogenesis in the tolerant genotypes might also be beneficial to enhanced drought tolerance. The biochemical adaptation to water deficit in the tolerant genotypes may be performed by specifically expressed genes that were involved in biochemical pathways of gluconeogenesis, purine and pyrimidine nucleotides biosynthesis, tryptophan degradation, starch degradation, methionine biosynthesis, and removal of superoxide radicals. In addition,19 pathways belonging to the metabolism of secondary metabolites, hormones, nutrients, amino acids, sugars and polysaccharides, fatty acids and lipids, and C1 compounds were significantly affected in all three genotypes, which might be the primary biochemical processes in tomato under drought stress.
4. The cloning, sequencing and protein structure analysis of candidate genes related to drought-tolerance. The differently expressed genes between tolerant and sensitive genotypes were selected to be subject for further analysis. Based on bioinformatics and biological technologies, the open reading frames of these genes were cloned and sequenced, whose amino acids and protein structure were deduced and predicted.
5. The expression pattern of candidate genes in different tissues of tomato and in leaf treataed with different external factors. Semi-quantitative RT-PCR analysis of different tissues of tomato showed that SIWRKY, SpWRKY and SINAC had tissue-specific expression, while SITR, SpTR and SpNAC were constitutively expressed in all the tested tissues. All aimed genes were detected abundantly in leaves and stems, and weakly in fruits and/or roots of tomato. Most of them had higher expression under moderate and serve drought stress than mild treatment. Almost these genes were induced by salt, high and low temperature, longer exogenous ABA treatment and salicylic acid.
6. The chromosome location of candidate genes. This study was conducted by PCR and digestion polymorphism based on tomato genome sequencing results. SpTR, SpWRKY and SpNAC were located on tomato chromosome 11,8 and 10, respectively.
7. Function characterization of candidate genes. Overexpression vectors were transformed into one tomato cultivar by Agrobacterium-mediated transformation. The PCR analysis of putative transgenic plants showed that a total of 14,13 and 19 transgenic plants of SpTR, SpWRKY and SpNAC were obtained, respectively, indicating that T-DNA had integrated into the tomato genome. Semi-quantitative RT-PCR analysis of aimed genes expression showed that the higher expression abundance in the transgenic plants than wild type. Evaluation for abiotic stress tolerance of transgenic plants was measured. These results indicated that overexpression of SpTR and SpWRKY could improve the tolerance of drought, salt and low temperature.
对植物耐旱机理的解析,前人已从生理生化、细胞结构及分子等水平进行了大量研究,并取得重要进展。植物主要通过增厚表皮蜡质层、改变气孔开度、形成发达根系和贮水组织等结构适应干旱；渗透调节物的形成、保护酶活性的提高、膜系统稳定性的维持、内源激素的调节、次生代谢物的合成等生理生化代谢都参与植物对干旱的防御；对植物耐旱的分子机理研究,近年已克隆了一大批耐旱相关基因,在植物抵御干旱过程中起直接保护或调控作用。干旱等逆境下,植物体内受ABA调控与非依赖ABA调控基因之间互作,形成复杂网络,共同调节多条信号途径转导和转录因子活性,激发下游基因表达,对干旱做出响应。
本研究以耐旱野生番茄S. pennellii与栽培番茄种S. lycopersicum cv M82及由二者构建的一套渐渗系为研究材料,从形态结构特征,分析耐旱番茄的结构特点；通过生理生化指标与耐旱性的相关性,建立适合耐旱番茄筛选的鉴定指标；利用microarray技术,从转录、信号转导及细胞分化等生物进程,分析番茄响应干旱的调控机理,候选耐旱相关基因,进行功能验证,为番茄的耐旱性改良和耐旱机理分析提供重要理论指导和实践依据。本研究的主要结果如下：
1.耐旱番茄的形态特性分析。通过对耐旱野生番茄S. pennellii与普通栽培种番茄S. lycopersicum M82形态结构的比较,分析S. pennellii的耐旱结构特点。S.pennellii植株叶、茎及花萼等地上组织全部被浓密表皮毛和粘稠腺体分泌物覆盖,利于减少水分散失的同时可能又有助于吸收空气中的水分；叶上表皮气孔数目较多,可以为吸收粘附在表皮的“露水”进入体内提供通道；叶片表皮细胞排列致密,也有利于减少体内水分散失；栅栏组织与海绵组织之比变大,可以增强机械强度；茎中薄壁组织发达,可能储藏大量水分,供应干旱等逆境下生长所需；而欠发达的根系和叶脉等组织则在S. pennellii耐旱机理中发挥并不重要的作用。
2.建立番茄耐旱评价指标体系。通过对叶片相对含水量、细胞伤害率、丙二醛含量、超氧化物岐化酶含量、脯氨酸含量等生理生化指标与耐旱性之间的相关性分析,建立适合耐旱性番茄筛选的检测指标。结果表明,轻度、中度、重度干旱胁迫下,叶片相对含水量都可用于鉴定番茄材料的耐旱性。
3.番茄干旱响应基因分析。利用筛选的耐旱渐渗系与M82,结合microarray技术,分析番茄响应干旱的调控机理。每种参试材料都获得超过1,200个差异表达基因,其中耐旱系中有359个单独表达基因。通过生物学进程分析,表达基因在逆境响应中占主要比例。耐旱系可能通过特异表达的转录因子基因(编码Zinc-finger、NAC、bHLH、AP2/EREBP及HSF等家族蛋白)、信号转导基因(编码受体蛋白激酶、促细胞分裂活性蛋白激酶、钙调结合蛋白、磷酸酯酶及膜蛋白等)、组织生长发育相关基因和一系列单独变化的生化途径(糖异生、色氨酸降解、嘌呤核苷酸生成、过氧化物清除、淀粉降解、甲硫氨酸合成)等方式调节耐旱性。而耐旱系和M82中共同表达的基因和共同变化的生化途径,如次生代谢物、无机营养、糖和多糖、氨基酸家族、激素等的合成或分解,可能分别为番茄对干旱的基本响应基因和代谢调控方式。
4.耐旱候选基因的分析。利用芯片结果,选取耐旱系与M82中有差异表达的干旱响应基因,为候选耐旱相关基因,克隆基因开放阅读编码框,对其编码蛋白序列及结构进行预测分析。
5.候选基因的表达模式。通过半定量RT-PCR法,分析候选基因在番茄不同组织器官,以及在不同干旱胁迫程度和不同外界因子作用下的表达模式。结果表明,候选基因SIWRKY、SpWRKY、SINAC表达具有组织特异性,在成熟叶和茎中表达量都较高,而在果实和/或根中不表达。候选基因SITR、SpTR和SpNAC则在根、茎、叶、花、果中都表达,但在果实和根中表达量仍比茎和叶中低。大部分候选基因在中度、重度胁迫下比轻度胁迫下表达变化明显。在盐、高低温及ABA较长时间作用下,大部分候选基因都被诱导；而在SA作用下,除NAC基因外,其它基因都被诱导。
6.候选基因的染色体定位分析。利用番茄基因组测序结果、扩增片段多态性和酶切扩增多态性序列法,对候选基因进行染色体定位。SpTR基因定位于第11染色体11-D区；SpWRKY基因定位于第8染色体,包含于克隆代号为C08SLe0011M12的BAC库中；SpNAC基因定位于第10染色体10-D区域。
7.候选基因的转基因创建、表达分析及转基因番茄的耐逆性鉴定。构建候选基因超量表达载体,利用农杆菌介导的遗传转化方法,将候选基因转入番茄栽培种中蔬5号中。通过PCR法检测,获得超量表达SpTR阳性植株14棵,超量表达SpWRKY阳性植株13棵,超量表达SpNAC阳性植株19棵。利用半定量RT-PCR法,鉴定转基因植株叶片中目的基因的表达量明显高于野生型。检测超量表达目的基因番茄幼苗的耐逆性,结果表明,SpTR和SpWRKY超量表达后,可增强转基因番茄幼苗的耐旱性、耐盐性和耐低温性。
Tomato (Solarium lycopersicum) is one of the most important economical vegetable crops in the Solanaceae family and also has been used as a model system. Drought stress straightly affects the growth and development of tomato seedlings, and causes of decreased quality and yield reduction. It has become one of urgent requirements to breed excellently drought-tolerant tomato variety to reduce the water deficit damage.
The elucidation of the mechanisms of drought tolerance has been studied on the base of morphological and anatomical, physiological and biochemical, and molecular level. The plant adaptation to water deficit are caused by changed morphological and anatomical structure, such as thick waxy cuticle, altered stomata aperture, well developed root system, and strong parenchyma. The physiological and biochemical characteristics including the accumulation of osmotic adjustment materials and protective enzymes, the stability of membrane system, the presence of endogenous hormones and secondary metabolites also contribute to enhanced drought tolerance. During the process of molecular research on plant responses to drought stress, a large number of genes were cloned, classifying into two major groups according to their putative functional modes. The first group comprises the genes encoding structural proteins, which are stress tolerance downstream effectors. The second group genes encoded regulatory proteins that are early response transcriptional activators including the transcription factors and the protein kinases. The expression of drought-inducible genes can be governed by ABA-dependent or ABA-independent regulatory systems, forming the cross-talks to regulate the activity of transcription factors and signal transduction in response to drought stress.
S. pennellii (LA0716), one of the wild crossable relatives of cultivated species, has a distinct ability to withstand desiccation in extreme arid condition. A collection of 50 introgression lines that covers the entire genome of their donor parent, S. pennellii, in the background of the cultivated species, S. lycopersicum M82, a drought-sensitive cultivar, were generated. In this study, we firstly use the drought-tolernat lines together with the currently expanding tomato research platforms such as genome sequencing and microarray applications to study the chacteraization of drought responsive genes and investigate the drought tolerance mechanism in tomato. The main results were as following:
1. The structure characteristics analysis of S. pennellii. A comparative observation of morphological and anatomical structure between S. pennellii and M82 were performed to study the drought-tolerant structure characteristics. The aerial tissues including leaf, stem, calyx and fruit of S. pennellii plant are covered with dense trichomes and glandular secretion, which may be benefit in reducing of water loss and absorbing moisture in the air. The increased number of stomata on the upper epidermis of S. pennellii leaf might support the channel for adsorbed dew. The thickness ratio of stockade tissue to sponge tissue in S. pennellii leaf is higher than that in M82, which could reinfoce the mechanical strength under drought stress. The parenchyma cells are widely distributed throughout stem of S. pennellii, suggesting they are benefit for water store and stronger water retention capacity, while the root and leaf vein are weak, indicating these tissues play unimportant roles in drought tolerance.
2. An analysis on index system of tomato drought tolerance evaluation. The correlation of index/index and index/drought tolerance under different drought stresses were studied. The relative water content can be used for selecting the drought-tolerant tomato genotype under mild, moderate and serve drought stress. The malondialdehyde content is also effective index for detecting the tomato drought tolerance under moderate drought stress.
3. The expression characteristics of drought responsive genes in tomato. Gene expression profiles between two drought-tolerant lines identified from introgression line population of S. pennellii and M82 were investigated under drought stress using tomato Oligo chips TOM2. More than 1,200 drought-responsive genes were identified in each of tested genotypes. The "response to stress" and "response to abiotic stimulus" were among the largest groups in all three genotypes. Based on biological function of drought-responsive genes, the enhanced drought tolerance of tomato may be closely related to upstream regulation of transcription factors and signal regulators specifically identified in the drought tolerant lines. However, those genes expressed in both tolerant and sensitive genotypes may act as basal drought-responsive factors in tomato under drought stress. The specifically expressed gene involved in cell differentiation, growth and anatomical structure morphogenesis in the tolerant genotypes might also be beneficial to enhanced drought tolerance. The biochemical adaptation to water deficit in the tolerant genotypes may be performed by specifically expressed genes that were involved in biochemical pathways of gluconeogenesis, purine and pyrimidine nucleotides biosynthesis, tryptophan degradation, starch degradation, methionine biosynthesis, and removal of superoxide radicals. In addition,19 pathways belonging to the metabolism of secondary metabolites, hormones, nutrients, amino acids, sugars and polysaccharides, fatty acids and lipids, and C1 compounds were significantly affected in all three genotypes, which might be the primary biochemical processes in tomato under drought stress.
4. The cloning, sequencing and protein structure analysis of candidate genes related to drought-tolerance. The differently expressed genes between tolerant and sensitive genotypes were selected to be subject for further analysis. Based on bioinformatics and biological technologies, the open reading frames of these genes were cloned and sequenced, whose amino acids and protein structure were deduced and predicted.
5. The expression pattern of candidate genes in different tissues of tomato and in leaf treataed with different external factors. Semi-quantitative RT-PCR analysis of different tissues of tomato showed that SIWRKY, SpWRKY and SINAC had tissue-specific expression, while SITR, SpTR and SpNAC were constitutively expressed in all the tested tissues. All aimed genes were detected abundantly in leaves and stems, and weakly in fruits and/or roots of tomato. Most of them had higher expression under moderate and serve drought stress than mild treatment. Almost these genes were induced by salt, high and low temperature, longer exogenous ABA treatment and salicylic acid.
6. The chromosome location of candidate genes. This study was conducted by PCR and digestion polymorphism based on tomato genome sequencing results. SpTR, SpWRKY and SpNAC were located on tomato chromosome 11,8 and 10, respectively.
7. Function characterization of candidate genes. Overexpression vectors were transformed into one tomato cultivar by Agrobacterium-mediated transformation. The PCR analysis of putative transgenic plants showed that a total of 14,13 and 19 transgenic plants of SpTR, SpWRKY and SpNAC were obtained, respectively, indicating that T-DNA had integrated into the tomato genome. Semi-quantitative RT-PCR analysis of aimed genes expression showed that the higher expression abundance in the transgenic plants than wild type. Evaluation for abiotic stress tolerance of transgenic plants was measured. These results indicated that overexpression of SpTR and SpWRKY could improve the tolerance of drought, salt and low temperature.
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