Study on the tolerant function of soybean GmGST7 gene to acidic aluminum stress
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摘要:目的
耐酸铝基因GsMYB7过表达转化大豆品种‘华春6号’后，从转基因株系的表达谱中获得目标基因GmGST7，该基因受酸铝胁迫诱导上调，且位于GsMYB7基因下游，进一步分析其耐酸铝功能，以期提高大豆酸铝耐受能力。
方法采用生物信息学方法分析GmGST7基因的碱基序列、蛋白结构域和构建系统进化树。通过烟草叶片瞬时转化法完成亚细胞定位。通过RT-qPCR分析该基因组织表达特异性。设计0、25、50、75 和 100 µmol/L 5个AlCl3浓度梯度，研究GmGST7对酸铝胁迫的响应。在50 µmol/L AlCl3处理下，设计0、4、8、12、16、24、36、48和72 h共9个时间梯度，对GmGST7的表达模式进行分析。过表达GmGST7基因遗传转化拟南芥，鉴定阳性植株，并对转基因株系进行耐酸铝表型验证、氧化水平测定、耐酸铝标志基因及下游基因的表达分析。
结果GmGST7基因位于大豆第7号染色体，序列全长为1 128 bp。该基因含有2个外显子和1个内含子，2个外显子分别编码GST高度保守的N端和不保守的C端；GmGST7基因编码226个氨基酸，编码的蛋白为大豆GST蛋白的tau类家族成员，定位于细胞质和细胞核中；GmGST7基因在大豆根、茎、叶、花和幼荚中均有表达，且在根中的表达量最高；GmGST7基因在50 µmol/L AlCl3处理24 h时表达最高；AlCl3处理后，野生型拟南芥相对根伸长显著低于转基因株系的，野生型拟南芥氧化水平高于转基因株系的，耐酸铝标志基因和下游基因的表达量在转基因株系中较高。
结论GmGST7基因属于大豆GST tau类家族成员，在细胞核和细胞质中行使功能，呈组成型表达模式，且在大豆根中表达最高，对酸铝胁迫响应显著；GmGST7过表达通过激活酸铝胁迫标志基因及其下游基因的表达提高拟南芥的酸铝耐受能力。
Abstract:ObjectiveThe GmGST7 gene was obtained from the gene expression profile of the GsMYB7 overexpressed lines of soybean ‘Huachun 6’ which was tolerant to acidic aluminum stress. GmGST7 lied downstream of the GsMYB7 gene, and was up-regulated by acidic aluminum stress. Its function of acidic aluminum resistance was further investigated to enhance the tolerance to aluminum stress in soybean.
MethodThe bioinformatics of the GmGST7 gene was analyzed using the base sequence, protein domain and phylogenetic tree. Subcellular localization of GmGST7 protein was accomplished by transient transformation in tobacco leaves. The tissue expression specificity of the GmGST7 gene was analyzed by RT-qPCR. Five AlCl3 concentration gradients of 0, 25, 50, 75 and 100 µmol/L were designed to study the response of GmGST7 to aluminum stress. Under the treatment of 50 µmol/L AlCl3, nine time gradients of 0, 4, 8, 12, 16, 24, 36, 48 and 72 h were designed to investigate the expression patterns of GmGST7. Arabidopsis (Col-0) was transformed by overexpression of GmGST7, positive plants were identified by molecular technology. The phenotype identification of Arabidopsis tolerant to acidic aluminum stress were performed with the oxidation level determination, the expression analysis of the genes response to aluminum stress and downstream genes of GmGST7.
ResultThe full-length sequence of GmGST7 located on chromosome 7 of soybean was 1 128 bp. The GmGST7 gene contained two exons and one intron which encodes a highly conserved N domain and a unconserved C domain of GST, respectively. GmGST7 encoded 226 amino acids. The GmGST7 protein was a tau member of the GST family in soybean, and localized in the nuclear and cytoplasm. GmGST7 was expressed in soybean root, stem, leaf, flower and young pod, and rich in root. The GmGST7 gene was up-regulated by AlCl3 with the highest relative expression under 50 µmol/L AlCl3 for 24 h. The relative root elongation of wild type was significantly lower than that of the transgenic lines, the oxidation level was higher, and the expression levels of acidic aluminum stress response genes and downstream genes were higher.
ConclusionThe GmGST7 gene is a tau member of the GST family in soybean, locates in the nucleus and cytoplasm. The GmGST7 gene holds a constitutive expression pattern, and is rich in soybean root. GmGST7 is significantly up-regulated by acidic aluminum stress. Overexpression of GmGST7 enhances the tolerance to aluminum stress in Arabidopsis by activating the expression of the marker genes response to acidic aluminum stress and its downstream genes.
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Keywords:
- Soybean /
- GmGST7 /
- Acidic aluminum stress /
- Genetic transformation
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普通大蓟马Megalurothrips usitatus又名豆大蓟马、豆花蓟马，隶属于缨翅目蓟马科大蓟马属，主要分布于澳大利亚、马来西亚、斯里兰卡、菲律宾、斐济、印度、日本等[1-3]，在我国海南、台湾、广东、广西、湖北、贵州、陕西等地也均有发生为害[4-5]。据报道，该虫有28种寄主，其中16种为豆科植物，目前它已成为危害华南地区豆科作物的主要害虫[6-9]，田间调查和室内试验均表明豇豆为其嗜好寄主[10-11]。普通大蓟马主要以锉吸式口器取食豇豆幼嫩组织的汁液，可造成叶片皱缩、生长点萎缩、豆荚痂疤等，严重影响豇豆品质[12-13]。此外，该虫体积小、发生量大、隐秘性强，大部分时间都躲在花中取食，从豇豆苗期至采收期均可为害[14-15]，以上特点均增加了农户的防治难度。当其为害严重时，农户只能增加施药频率和施药量，这也导致该虫对多种常用化学农药产生了严重的抗药性[16-17]。
目前关于普通大蓟马的研究主要集中在生物学特性[18]及综合防治技术[19-20]等层面，随着抗药性的不断发展与研究的不断深入，从分子层面解析普通大蓟马的抗药性机制和寄主选择机制等以寻求新型绿色防控方法势在必行，室内种群的大规模饲养是展开这些研究的基础。化蛹基质作为影响昆虫种群规模的关键因子，韩云等[21]曾指出普通大蓟马在含水量(w)为15%的砂壤土中羽化率显著高于砂土、壤土和黏土，但不适用于室内大规模饲养，因为实际应用中，存在土壤类型无法明确区分、配制砂壤土会增加人工饲养的工作量等问题。土壤以外的其他基质对普通大蓟马化蛹的适合度鲜见研究报道。
本研究以普通大蓟马为试验对象，室内观测其在沙子、蛭石和厨房用纸3种基质及无基质条件下的羽化规律，分析该虫对不同化蛹基质的适合度，以期为普通大蓟马的室内大规模饲养提供基础资料，为该虫的综合治理提供理论依据。
1. 材料与方法
1.1 供试材料
普通大蓟马于2017年采自广东省广州市增城区朱村豇豆田，采回后在RXZ-500C型智能人工气候箱(宁波江南仪器厂)内用豇豆豆荚饲养，饲养条件为温度(26±6) ℃，光照周期12 h光∶12 h暗，相对湿度(70±5)%。室内饲养多代后，选取发育一致的老熟2龄若虫(以体色变为橙红色为标准)进行室内试验。
供试基质包括沙子、蛭石、锯末和厨房用纸，并以无基质作为空白对照。试验前将沙子、蛭石和锯末置于DHG-9140型电热恒温鼓风干燥箱(上海精宏实验设备有限公司)中105 ℃恒温烘烤6 h备用。
1.2 试验方法
首先称取过筛烘干后的沙子50 g 3组，分别加入2.5、3.5和4.5 mL蒸馏水，充分混匀，配制成含水量(w)分别为5%、7%和9%的沙子化蛹基质；称取过筛烘干后的蛭石10 g 3组，分别加入10.0、12.5和15.0 mL蒸馏水，充分混匀，配制成含水量(w)分别为20%、25%和30%的蛭石化蛹基质；称取过筛烘干后的蛭石10 g 3组，分别加入12.5、15.0和17.5 mL蒸馏水，充分混匀，配制成含水量(w)分别为25%、30%和35%的锯末化蛹基质。将以上基质分别转移至350 mL玻璃组培瓶内，基质深度均为5 cm，将厨房用纸对折成合适大小后平铺在组培瓶底部作为基质。在所有基质上放置纱网，再加入1根新鲜的豇豆豆荚(长度约4~5 cm)，分别接入50头普通大蓟马老熟2龄若虫，用250目纱布封口后置于人工气候箱中饲养，每日观察并记录成虫羽化数量。每个处理设6次重复。设置不加入任何化蛹基质的空白对照。
含水量的测定方法按以下公式[22]进行：
含水量=实际含水质量/烘干后基质质量×100%。
1.3 数据分析
运用SPSS 24.0软件进行试验数据处理分析，不同基质及含水量对普通大蓟马羽化率、蛹历期和性比(雄性∶雌性)的影响采用单因素方差分析，并运用Duncan’s法检验差异显著性。
2. 结果与分析
2.1 不同基质对普通大蓟马羽化率、蛹历期和性比的影响
普通大蓟马在不同基质中的羽化率、蛹历期和性比具有显著差异(图1)。由图1A可知，普通大蓟马在厨房用纸中的羽化率显著高于其他基质，为54.33%，其次为含水量5%(w)的沙子，羽化率为44.67%；锯末最不适宜于普通大蓟马羽化，在含水量(w)为25%、30%、35%的锯末中普通大蓟马的羽化率分别为10.33%、5.33%、16.67%，显著低于空白对照与其他基质。
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图 1 不同基质对普通大蓟马羽化率、发育历期和性比(雄性∶雌性)的影响1~3分别为含水量(w)为5%、7%和1%的沙子，4~6分别为含水量(w)为20%、25%和30%的蛭石，7~9分别为含水量(w)为25%、30%和35%锯末，10：厨房用纸，11：无基质；各图中的不同小写字母表示差异显著(P<0.05，Duncan’s法)Figure 1. Effects of different substrates on eclosion rate, pupa developmental period and male-female ratio of Megalurothrips usitatus1: Sand with 5% moisture, 2: Sand with 7% moisture, 3: Sand with 10% moisture, 4: Vermiculite with 20% moisture, 5: Vermiculite with 25% moisture, 6: Vermiculite with 30% moisture, 7: Sawdust with 25% moisture, 8: Sawdust with 30% moisture, 9: Sawdust with 35% moisture, 10: Kitchen paper, 11: No substrate; Different lowercase leters in the same figure indicated significant difference among different substrate (P<0.05, Duncan’s method)由图1B可知，普通大蓟马在含水量5%(w)的沙子中蛹的发育历期最短，为5.29 d，其次为含水量7%(w)的沙子，为6.01 d，在其他基质中的蛹期则无显著差异，在6.14~7.16 d。
由图1C可知，普通大蓟马在含水量30%(w)的蛭石中性比最高，为0.60，含水量10%(w)的沙子和30%(w)的蛭石性比相对较低，分别为0.12和0.06，在其他基质中性比无显著差异。
2.2 不同基质条件下普通大蓟马的羽化情况
由表1数据可知，沙子含水量(w)为5%时普通大蓟马羽化最早，始于第2天；其次为蛭石，羽化始于第4天，其他条件下羽化均始于第3天；以锯末为基质时羽化最晚，始于第5天。沙子含水量(w)为5%和厨房用纸条件下，羽化高峰出现在第5天，羽化率分别为21%和22.67%；次高峰在第6天，羽化率分别为14.33%和21%。沙子含水量(w)为9%、锯末以及空白对照下羽化高峰出现在第7天，其他条件下羽化高峰均出现在第6天。不同基质类型及含水量条件下，普通大蓟马的羽化均结束于第8天或第9天，与不同基质培养条件下普通大蓟马蛹期之间的差异相对应。
表 1 不同基质对普通大蓟马逐日羽化率的影响1)Table 1. Effects of differents substrates on daily eclosion rate of Megalurothrips usitatus% t/d 沙子含水量(w) Water content in sand 蛭石含水量(w) Water content in vermiculite 5% 7% 9% 20% 25% 30% 1 0 0 0 0 0 0 2 1.67±0.42c 0 0 0 0 0 3 1.00±1.68c 0 0 0 0 0 4 1.33±0.67c 5.33±0.33c 0.33±0.33b 0 0 0 5 21.00±3.82a 5.33±2.17b 2.67±1.91b 3.00±2.30bc 10.33±3.48ab 0.33±0.33b 6 14.33±4.66b 17.33±1.76a 2.67±1.91b 11.67±2.09a 14.67±3.33a 7.67±2.22a 7 2.33±0.80c 5.00±0.85b 8.67±1.84a 6.33±2.28b 7.67±1.74bc 6.67±1.52a 8 0.67±0.42c 0.67±0.67c 0.67±0.42b 4.00±1.35bc 4.00±1.37cd 1.67±0.94b 9 0 0 0.33±0.33b 0.67±0.42b 0 0.67±0.42b 10 0 0 0 0 0 0 3. 讨论与结论
化蛹基质的类型对普通大蓟马化蛹具有一定影响，本研究发现锯末和蛭石不适宜于普通大蓟马化蛹，锯末和蛭石不同含水量条件下大蓟马的羽化率都显著低于空白对照。有研究指出土壤中砂土含量低于30%时，蓟马若虫不能化蛹[23]，蓟马在砂壤土中的羽化率也显著高于砂土、黏土、壤土等单一土壤[21]。
化蛹基质的含水量对普通大蓟马化蛹具有显著影响，本研究发现当沙子含水量(w)为5%时，羽化率仅次于厨房用纸，高达44.67%，与孟国玲等[23]关于豆带蓟马Taenithripsglycines在含水量(w)为5.7%时羽化率最高(43.63%)的报道相对一致。韩云等[21]研究发现普通大蓟马在含水量(w)为15%的砂壤土中羽化率最高，为52.08%，而土壤含水量(w)5%时羽化率仅为6.67%。这与本研究结果不符，究其原因可能是不同类型的基质吸水力与保水力不同，导致在相同的绝对含水量下湿度有差异。此外，有研究曾指出高含水量不利于蓟马化蛹[24]，这与本研究结果相一致，沙子含水量(w)5%时的羽化率显著高于含水量(w)7%和10%。
在本研究中，成虫性比普遍低于1∶1，含水量(w)30%的蛭石羽化性比最高，为0.6，含水量(w)30%锯末最低，为0.06，其他处理的性比无显著差异，为0.12~0.48。张念台[8]和谭柯[24]在田间调查的结果也显示其成虫性比低于1∶1，后代总是偏于雌性，谭柯[24]则表示后代偏雌性可能是蓟马暴发的原因之一。这与本研究结果相一致，后代偏于雌性。
本研究发现普通大蓟马在厨房用纸中的羽化率最高，蛹发育历期与其他基质相比无明显差异，且以厨房用纸为化蛹基质时，可以清楚地观察到普通大蓟马蛹期的形态特征变化，可以随时根据试验需求收集不同时期的若虫或成虫。虽然沙子含水量(w)5%时蛹发育历期最短且羽化率也较高，但蓟马一旦入土化蛹便无法继续观察形态或收集虫体。因此，本试验条件下，厨房用纸是最适合室内普通大蓟马大量饲养的化蛹基质。
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图 2 GmGST7蛋白序列对比(A)和进化树(B)分析
红色横线代表GST-N，蓝色横线代表GST-C，红色点标注为目标基因GmGST7
Figure 2. Sequence comparison (A) and evolutionary tree (B) analysis of GmGST7 protein
The red horizontal line represents GST-N, the blue horizontal line represents GST-C, and the red dot is labeled as the target gene GmGST7
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图 4 GmGST7基因的组织表达模式分析
“**”表示该组织与幼荚在P < 0.01水平差异显著(t检验)
Figure 4. Analysis of tissue expression pattern of the GmGST7 gene
“**” indicates that the tissue differed from the young pod at P < 0.01 level (t test)
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图 5 GmGST7基因酸铝胁迫响应
各图中，“**”表示处理与对照(CK)在P < 0.01水平差异显著(t检验)
Figure 5. Response of the GmGST7 gene to acidic aluminum stress
“**” indicates that the treatment differed from the control (CK) at P < 0.01 level in each figure (t test)
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图 6 GmGST7基因克隆及载体构建
A：GmGST7基因cDNA序列克隆，根据引物位置克隆大小为742 bp；B：连亚细胞定位载体后，根据载体引物位置PCR产物大小为1 416 bp；C：连接过表达载体后，根据载体引物位置PCR产物大小为870 bp
Figure 6. Cloning and vector construction of the GmGST7 gene
A: Cloning of GmGST7 gene cDNA sequence, according to the location of the primer, cloning size is 742 bp; B: After connecting the subcellular localization vector, according to the location of the carrier primer, the size of the PCR product is 1 416 bp; C: After connecting the overexpressed vector, according to the location of the vector primer, the size of the PCR product was 870 bp
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图 8 GmGST7转基因拟南芥阳性苗除草剂喷洒鉴定
阳性苗正常生长，假阳性苗则枯萎
Figure 8. Herbicide spraying identification of GmGST7 transgenic Arabidopsis positive seedlings
Positive seedlings grow normally, false positive seedlings wilt
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图 9 GmGST7转基因拟南芥阳性苗DNA鉴定
Figure 9. DNA identification of GmGST7 transgenic Arabidopsis seedlings
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图 10 转基因拟南芥T3代株系中GmGST7基因表达量
“**”表示株系与WT在0.01水平差异显著(t检验)
Figure 10. Expression of GmGST7 gene in T3 transgenic Arabidopsis thaliana
“**” indicates that the line differed from the WT at 0.01 level (t test)
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图 11 过表达GmGST7拟南芥耐酸铝表型
Figure 11. Overexpressed GmGST7 Arabidopsis aluminium-resistant phenotype
表 1 引物序列
Table 1 Primer sequence
引物名称
Primer name引物序列(5′→3′)
Primer sequencepTF101-GmGST7-F gagaacacgggggactctagaATGGCTGCTAATCAGGAAGATGTG pTF101-GmGST7-R cgatcggggaaattcgagctcTTTTGAAGCAGAAAGACTTTCATGG Super1300-GmGST7-F acgggggactcttgaccatggCTATGGCTGCTAATCAGGAAGATGTG Super1300-GmGST7-R aagttcttctcctttactagtTTTTGAAGCAGAAAGACTTTCATGG GmGST7-F GTCCTGATTCCCGGCTCAAT GmGST7-R AACTCACAAATGAGAGACCAGT RT-GmGST7-F TCAACCACCCTGTTGTCAAAC RT-GmGST7-R AAGACTTTCATGGCAGGCTTTGT 
下载: 导出CSV
表 2 荧光定量引物序列
Table 2 qPCR primer sequence
基因
Gene引物序列(5′→3′)
Primer sequenceAtALMT F: TCCCATGGGTAAAGACAAAG
R: ATAGTCTGCTTTCTGCCAAAAtMATE F: CATTCGAATCCATCGAGATT
R: CGAATGTTGCACTCTGTTTTAtALS3 F: AGCTTCGAGATGACATCAAA
R: ACGGTTTTGCAGCTATCTAAAtWAK1 F: TGGCCGCTGATATTACAAAT
R: CAGATTGGCTACTGGTTAGTAt1G78660 F: CAGGTTTGAGTGTATCGGTG
R: CATCTGATTCTTCTGCCCAAAt1G78670 F: TCCTCTGAGATGTGGAGATT
R: TAGTTGAGGTTTGGATCAGCAt1G78680 F: AAAATGGTGGATTTTGCAGG
R: ATAGGCTGACGTTCAAAGTTAt4G33090 F: TGGATCAGTTCAAAGGTGAG
R: GACTATGTCGAGATCGATGG
下载: 导出CSV
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[1] VON UEXKÜLL H R, MUTERT E. Global extent, development and economic impact of acid soils[J]. Plant and Soil, 1995, 171(1): 1-15. doi: 10.1007/BF00009558
[2] KINRAIDE T B, PARKER D R. Cation amelioration of aluminum toxicity in wheat[J]. Plant Physiology, 1987, 83(3): 546-551. doi: 10.1104/pp.83.3.546
[3] KINRAIDE T B. Assessing the rhizotoxicity of the aluminate ion, Al(OH)4−[J]. Plant Physiology, 1990, 93(4): 1620-1625. doi: 10.1104/pp.93.4.1620
[4] DELHAIZE E, RYAN P R, RANDALL P J. Aluminum tolerance in wheat (Triticum aestivum L.) II: Aluminum-stimulated excretion of malic acid from root apices)[J]. Plant Physiology, 1993, 103(3): 695-702. doi: 10.1104/pp.103.3.695
[5] SIVAGURU M, BALUSKA F, VOLKMANN D, et al. Impacts of aluminum on the cytoskeleton of the maize root apex. short-term effects on the distal part of the transition zone[J]. Plant Physiology, 1999, 119(3): 1073-1082. doi: 10.1104/pp.119.3.1073
[6] KOLLMEIER M, FELLE H H, HORST W J. Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?[J]. Plant Physiology, 2000, 122(3): 945-956. doi: 10.1104/pp.122.3.945
[7] VAZQUEZ M D, POSCHENRIEDER C, et al. Change in apoplastic aluminum during the initial growth response to aluminum by roots of a tolerant maize variety[J]. Plant Physiology, 1999, 119(2): 435-444. doi: 10.1104/pp.119.2.435
[8] SILVA I R, SMYTH T J, MOXLEY D F, et al. Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy[J]. Plant Physiology, 2000, 123(2): 543-552. doi: 10.1104/pp.123.2.543
[9] TAYLOR G J, MCDONALD-STEPHENS J L, HUNTER D B, et al. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina[J]. Plant Physiology, 2000, 123(3): 987-996. doi: 10.1104/pp.123.3.987
[10] FRANTZIOS G, GALATIS B, APOSTOLAKOS P. Aluminium causes variable responses in actin filament cytoskeleton of the root tip cells of Triticum turgidum[J]. Protoplasma, 2005, 225(3/4): 129-140.
[11] ČIAMPOROVÁ M. Morphological and structural responses of plant roots to aluminium at organ, tissue, and cellular levels[J]. Biologia Plantarum, 2002, 45(2): 161-171. doi: 10.1023/A:1015159601881
[12] JONES D L, KOCHIAN L V. Aluminum inhibition of the inositol 1, 4, 5-trisphosphate signal transduction pathway in wheat roots: A role in aluminum toxicity?[J]. The Plant Cell, 1995: 1913-1922.
[13] BARCELÓ J, POSCHENRIEDER C. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: A review[J]. Environmental and Experimental Botany, 2002, 48(1): 75-92. doi: 10.1016/S0098-8472(02)00013-8
[14] KOCHIAN L V, PIÑEROS M A, HOEKENGA O A. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity[J]. Plant and Soil, 2005, 274(1/2): 175-195. doi: 10.1007/s11104-004-1158-7
[15] WANG H J. GsMYB7 encoding a R2R3-type MYB transcription factor enhances the tolerance to aluminum stress in soybean (Glycine max L.) [J]. BMC Genomics, 2022. 23(1): 529. doi: 10.1186/s12864-022-08744-w.
[16] SHEEHAN D, MEADE G, FOLEY V M, et al. Structure, function and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily[J]. The Biochemical Journal, 2001, 360(Pt1): 1-16.
[17] SAADAT M, MOHABATKAR H. Polymorphisms of glutathione S-transferases M1 and T1 do not account for inter individual differences for smoking behavior[J]. Pharmacology Biochemistry and Behavior, 2004, 77(4): 793-795. doi: 10.1016/j.pbb.2004.02.003
[18] SASAN M, BABAK S, HASSAN M. A new member of tau-class glutathione S-transferase from barley leaves[J]. Excli Journal, 2009, 8: 190-194.
[19] DROOG F, HOOYKAAS P, VAN DER ZAAL B J. 2, 4-dichlorophenoxyacetic acid and related chlorinated compounds inhibit two auxin-regulated type-III tobacco glutathione S-transferases[J]. Plant Physiology, 1995, 107(4): 1139-1146. doi: 10.1104/pp.107.4.1139
[20] ÖZTETIK E. A tale of plant glutathione S-transferases: Since 1970[J]. The Botanical Review, 2008, 74(3): 419-437. doi: 10.1007/s12229-008-9013-9
[21] LIGHT G G, MAHAN J R, ROXAS V P, et al. Transgenic cotton (Gossypium hirsutum L.) seedlings expressing a tobacco glutathione S-transferase fail to provide improved stress tolerance[J]. Planta, 2005, 222(2): 346-354. doi: 10.1007/s00425-005-1531-7
[22] DIXON D P, CUMMINS I, COLE D J, et al. Glutathione-mediated detoxification systems in plants[J]. Current Opinion in Plant Biology, 1998, 1(3): 258-266. doi: 10.1016/S1369-5266(98)80114-3
[23] NUTRICATI E, MICELI A, BLANDO F, et al. Characterization of two Arabidopsis thaliana glutathione S-transferases[J]. Plant Cell Reports, 2006, 25(9): 997-1005. doi: 10.1007/s00299-006-0146-1
[24] PANTELIDES I S, TJAMOS S E, PAPLOMATAS E J. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae[J]. Molecular Plant Pathology, 2010, 11(2): 191-202. doi: 10.1111/j.1364-3703.2009.00592.x
[25] BELA K, HORVÁTH E, GALLÉ Á, et al. Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses[J]. Journal of Plant Physiology, 2015, 176: 192-201. doi: 10.1016/j.jplph.2014.12.014
[26] BIELACH A, HRTYAN M, TOGNETTI V. Plants under stress: Involvement of auxin and cytokinin[J]. International Journal of Molecular Sciences, 2017, 18(7): 1427. doi: 10.3390/ijms18071427.
[27] LIU J P, LUO X Y, SHAFF J, et al. A promoter-swap strategy between the AtALMT and AtMATE genes increased Arabidopsis aluminum resistance and improved carbon-use efficiency for aluminum resistance[J]. The Plant Journal, 2012, 71(2): 327-337. doi: 10.1111/j.1365-313X.2012.04994.x
[28] MANGEON A, PARDAL R, MENEZES-SALGUEIRO A D, et al. AtGRP3 is implicated in root size and aluminum response pathways in Arabidopsis[J]. PLoS One, 2016, 11(3): e0150583. doi: 10.1371/journal.pone.0150583.
[29] MINERVA B. Five decades with glutathione and the GSTome[J]. Journal of Biological Chemistry, 2012, 287(9): 6072-6083. doi: 10.1074/jbc.X112.342675
[30] LABROU N E, PAPAGEORGIOU A C, PAVLI O, et al. Plant GSTome: Structure and functional role in xenome network and plant stress response[J]. Current Opinion in Biotechnology, 2015, 32: 186-194. doi: 10.1016/j.copbio.2014.12.024
[31] JHA B, SHARMA A, MISHRA A. Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance[J]. Molecular Biology Reports, 2011, 38(7): 4823-4832. doi: 10.1007/s11033-010-0625-x
[32] TIWARI V, PATEL M K, CHATURVEDI A K, et al. Functional characterization of the tau class glutathione-S-transferases gene (SbGSTU) promoter of Salicornia brachiata under salinity and osmotic stress[J]. PLoS One, 2016, 11(2): e0148494. doi: 10.1371/journal.pone.0148494.
[33] XU J, ZHENG A Q, XING X J, et al. Transgenic Arabidopsis plants expressing grape glutathione S-transferase gene (VvGSTF13) show enhanced tolerance to abiotic stress[J]. Biochemistry (Moscow), 2018, 83(6): 755-765. doi: 10.1134/S0006297918060135
[34] SRIVASTAVA D, VERMA G, CHAUHAN A S, et al. Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metal and drought stress tolerance[J]. Metallomics, 2019, 11(2): 375-389. doi: 10.1039/C8MT00204E
[35] KAMPRANIS S C, DAMIANOVA R, ATALLAH M, et al. A novel plant glutathione S-transferase/peroxidase suppresses bax lethality in yeast[J]. Journal of Biological Chemistry, 2000, 275(38): 29207-29216. doi: 10.1074/jbc.M002359200
[36] LOYALL L, UCHIDA K, BRAUN S, et al. Glutathione and a UV light-induced glutathione S-transferase are involved in signaling to chalcone synthase in cell cultures[J]. The Plant Cell, 2000, 12(10): 1939-1950.
[37] MUELLER L A, GOODMAN C D, SILADY R A, et al. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein[J]. Plant Physiology, 2000, 123(4): 1561-1570. doi: 10.1104/pp.123.4.1561
[38] WEISERBS K F, JACOBSON J S, BEGG M D, et al. A cross-sectional study of polycyclic aromatic hydrocarbon-DNA adducts and polymorphism of glutathione S-transferases among heavy smokers by race/ethnicity[J]. Biomarkers, 2003, 8(2): 142-155. doi: 10.1080/1354750031000086269
[39] GARCERÁ A, BARRETO L, PIEDRAFITA L, et al. Saccharomyces cerevisiae cells have three Omega class glutathione S-transferases acting as 1-cys thiol transferases[J]. The Biochemical Journal, 2006, 398(2): 187-196. doi: 10.1042/BJ20060034
[40] FEDERICI L, MASULLI M, GIANNI S, et al. A conserved hydrogen-bond network stabilizes the structure of Beta class glutathione S-transferases[J]. Biochemical and Biophysical Research Communications, 2009, 382(3): 525-529. doi: 10.1016/j.bbrc.2009.03.052
[41] LALLEMENT P A, RORET T, TSAN P, et al. Insights into ascorbate regeneration in plants: Investigating the redox and structural properties of dehydroascorbate reductases from Populus trichocarpa[J]. Biochemical Journal, 2016, 473(6): 717-731. doi: 10.1042/BJ20151147
[42] GONZALEZ D, FRAICHARD S, GRASSEIN P, et al. Characterization of a Drosophila glutathione transferase involved in isothiocyanate detoxification[J]. Insect Biochemistry and Molecular Biology, 2018, 95: 33-43. doi: 10.1016/j.ibmb.2018.03.004
[43] TAJC S G, TOLBERT B S, BASAVAPPA R, et al. Direct determination of thiol pKa by isothermal titration microcalorimetry[J]. Journal of the American Chemical Society, 2004, 126(34): 10508-10509. doi: 10.1021/ja047929u
[44] ATKINSON H J, BABBITT P C. Glutathione transferases are structural and functional outliers in the thioredoxin fold[J]. Biochemistry, 2009, 48(46): 11108-11116. doi: 10.1021/bi901180v
[45] OHNO S. Patterns in genome evolution[J]. Current Opinion in Genetics & Development, 1993, 3(6): 911-914.
[46] FORCE A, LYNCH M, PICKETT F B, et al. Preservation of duplicate genes by complementary, degenerative mutations[J]. Genetics, 1999, 151(4): 1531-1545. doi: 10.1093/genetics/151.4.1531
[47] TANAKA K M, TAKAHASI K R, TAKANO-SHIMIZU T. Enhanced fixation and preservation of a newly arisen duplicate gene by masking deleterious loss-of-function mutations[J]. Genetics Research, 2009, 91(4): 267-280. doi: 10.1017/S0016672309000196
[48] 马立功, 孟庆林, 张匀华, 等. 向日葵谷胱甘肽-S-转移酶基因的克隆及抗病功能研究[J]. 中国油料作物学报, 2015, 37(5): 635-643. doi: 10.7505/j.issn.1007-9084.2015.05.007 [49] 韩少怀, 李佳佳, 张璟曜, 等. 大豆GmGST12基因的克隆及表达分析[J]. 大豆科学, 2015, 34(5): 782-788. doi: 10.11861/j.issn.1000-9841.2015.05.0782 [50] 李永生, 方永丰, 李玥, 等. 玉米逆境响应基因ZmGST23克隆和表达分析[J]. 农业生物技术学报, 2016, 24(5): 667-677. [51] 孙兰兰, 麻荣慧, 薛飞, 等. 玉米GST31基因的克隆与表达分析[J]. 作物学报, 2023, 49(10): 2717-2726. -
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