植物学报 ›› 2024, Vol. 59 ›› Issue (3): 397-413.DOI: 10.11983/CBB23130 cstr: 32102.14.CBB23130
刘笑1,2, 杜琬莹1,2, 张云秀2, 唐成名1,2, 李华伟2, 夏海勇2, 樊守金1, 孔令安1,2,*()
收稿日期:
2023-09-16
接受日期:
2024-04-15
出版日期:
2024-05-01
发布日期:
2024-05-10
通讯作者:
孔令安
基金资助:
Xiao Liu1,2, Wanying Du1,2, Yunxiu Zhang2, Chengming Tang1,2, Huawei Li2, Haiyong Xia2, Shoujin Fan1, Ling’an Kong1,2,*()
Received:
2023-09-16
Accepted:
2024-04-15
Online:
2024-05-01
Published:
2024-05-10
Contact:
Ling’an Kong
摘要: 该研究探讨了小麦(Triticum aestivum)根系NH4+毒性以及NO3-缓解其毒性机理。与7.5 mmol·L-1 NO3-处理(CK)相比, 7.5 mmol·L-1 NH4+处理(SA)抑制小麦根系生长, 添加1 mmol·L-1 NO3- (AN)后缓解了对根系生长的抑制。转录组分析表明, 与CK相比, SA处理下, 编码糖酵解途径酶、发酵关键酶、呼吸爆发性氧化酶同源物(Rbohs)、交替氧化酶(AOX)和双加氧酶相关基因显著上调表达; 编码TCA循环酶、ATP合酶和水通道蛋白(AQPs)相关基因显著下调表达。与SA相比, AN处理下, 糖酵解、发酵途径、Rbohs、AOX和双加氧酶相关基因的表达下调, 编码TCA循环酶、ATP合酶和AQPs的基因表达上调。蛋白质组分析表明, SA处理下, 糖酵解与发酵相关酶以及AOX相关基因表达上调, 而AQPs相关基因表达下调。AN处理下, 糖酵解与发酵相关酶以及AOX相关基因表达下调, AQPs相关基因表达上调。综上所述, 单独NH4+处理促进糖酵解和发酵途径, 抑制TCA循环, 能量生成减少, 最终抑制小麦根系生长, 这可能与NH4+处理引起根系缺O2胁迫有关。添加NO3-后抑制了糖酵解和发酵途径, 促进TCA循环和能量产生, 显著缓解了根系缺O2胁迫以及NH4+对根系生长的抑制。
刘笑, 杜琬莹, 张云秀, 唐成名, 李华伟, 夏海勇, 樊守金, 孔令安. NO3-缓解小麦根部NH4+毒性机理. 植物学报, 2024, 59(3): 397-413.
Xiao Liu, Wanying Du, Yunxiu Zhang, Chengming Tang, Huawei Li, Haiyong Xia, Shoujin Fan, Ling’an Kong. Nitrate-dependent Alleviation of Root Ammonium Toxicity in Wheat (Triticum aestivum). Chinese Bulletin of Botany, 2024, 59(3): 397-413.
图1 不同态氮素处理对小麦幼苗根系生长的影响 (A) 不同态氮素处理24、48、72和96小时幼苗根系鲜重净增加量(结果为3次独立实验的平均值±标准差); (B) 不同态氮素处理48小时小麦幼苗根系表型(bar=10 cm)。CK: 7.5 mmol·L-1 NO3-处理; SA: 7.5 mmol·L-1 NH4+处理; AN: 7.5 mmol·L-1 NH4++1.0 mmol·L-1 NO3-处理。* P<0.05; ** P<0.01
Figure 1 Effects of different N treatments on the root growth of wheat seedlings (A) Net increases in root fresh weight of wheat seedlings at 24, 48, 72 and 96 h after different N treatments (data are means±SD of three independent experiments); (B) Phenotype of wheat seedling roots at 48 h after different N treatments (bar=10 cm). CK: 7.5 mmol·L-1 NO3- treatment; SA: 7.5 mmol·L-1 NH4+ treatment; AN: 7.5 mmol·L-1 NH4++1.0 mmol·L-1 NO3- treatment. * P<0.05; ** P<0.01
图2 不同态氮素处理间差异表达基因(DEGs)的成对比较 (A) 不同态氮素处理间DEGs的韦恩图; (B) 不同态氮素处理间DEGs的统计图; (C) SA与CK比较下DEGs的KEGG富集分析; (D) AN与SA比较下DEGs的KEGG富集分析。CK、SA和AN同图1。
Figure 2 Paired comparisons of differentially expressed genes (DEGs) among different N treatments (A) Venn diagram of DEGs under different N treatments; (B) Statistical map of DEGs under different N treatments; (C) KEGG enrichment analysis of DEGs from SA vs CK comparison; (D) KEGG enrichment analysis of DEGs from AN vs SA comparison. CK, SA, and AN are the same as shown in Figure 1.
图3 不同态氮素处理下小麦根系与糖酵解、磷酸戊糖途径、丙酮酸代谢、TCA循环、发酵和莽草酸途径相关DEGs转录水平变化 热图中方格从左到右依次表示CK、SA和AN处理下该基因的表达水平; 彩色标尺为基因在3个不同处理下的相对表达量, 蓝色代表表达量较低, 红色代表表达量较高。CK、SA和AN同图1。
Figure 3 Changes in transcription level of DEGs involved in glycolysis, pentose phosphate pathway, pyruvate metabolism, TCA cycle, fermentation and shikimate pathway under different N treatments in the roots of wheat seedlings Squares from left to right indicate the expression level of this gene under CK, SA and AN treatments; the color scale indicates the relative gene expression, with blue color indicating lower expression and red color indicating higher expression. CK, SA, and AN are the same as shown in Figure 1.
图4 不同态氮素处理下小麦根系编码ATP合酶的差异表达基因(DEGs)转录水平变化 彩色标尺为基因在3个不同处理下的相对表达量, 蓝色代表表达量较低, 红色代表表达量较高。CK、SA和AN同图1。
Figure 4 Changes in transcription level of differentially expressed genes (DEGs) encoding ATP synthases under different N treatments in wheat roots The color scale indicates the relative gene expression, with blue color indicating lower expression and red color indicating higher expression. CK, SA, and AN are the same as shown in Figure 1.
Gene ID | Gene relative expression level ![]() | Gene description | Species | Reference |
---|---|---|---|---|
Respiratory burst oxidase homologs | ||||
TraesCS5D01G105900 | ![]() | Respiratory burst oxidase homolog protein B-like | Zea mays | Mira et al., |
TraesCS1D01G284800 | Respiratory burst oxidase homolog protein B-like | Nicotiana tabacum | Zafari et al., | |
TraesCS5A01G093600 | Respiratory burst oxidase homolog protein B-like | |||
Alternative pathway | ||||
TraesCS2A01G439400 | ![]() | Mitochondrial alternative oxidase | N. tabacum | Zafari et al., |
TraesCS2B01G459300 | Mitochondrial alternative oxidase | |||
TraesCS2D01G212500 | Internal alternative NADPH-ubiquinone oxidoreductase A1, mitochondrial-like | Z. mays | Igamberdiev and Hill, | |
TraesCS3D01G314700 | PREDICTED: external alternative NADPH-ubiquinone oxidoreductase B3, mitochondrial-like | |||
O2-binding and Fe transport | ||||
TraesCS1D01G340600 | ![]() | Non-symbiotic hemoglobin-like isoform X1 | Oryza sativa | Narsai and Whelan, |
TraesCS1B01G350800 | Non-symbiotic hemoglobin-like isoform X1 | |||
TraesCS1A01G338400 | Non-symbiotic hemoglobin-like isoform X2 | |||
TraesCS5A01G552000 | Nicotianamine synthase | Citrus junos | Xie et al., | |
TraesCS6B01G425200 | Nicotianamine synthase | |||
TraesCS6D01G148200 | Nicotianamine synthase | |||
TraesCS2A01G049900 | Nicotianamine synthase | |||
TraesCS6D01G382900 | Nicotianamine synthase-like 5 protein | |||
Aquaporin | ||||
TraesCS6A01G222100 | ![]() | Probable aquaporin PIP2-2 | Glycine max | Matsuo et al., |
TraesCS6D01G212900 | ![]() | Probable aquaporin PIP2-2 | Sorghum bicolor | Kadam et al., |
TraesCS2A01G407700 | Aquaporin PIP1-2 | |||
TraesCS2D01G404800 | Aquaporin PIP1-2 | |||
TraesCS2B01G077700 | Probable aquaporin PIP2-6 | |||
TraesCS2D01G063900 | Probable aquaporin PIP2-6 | |||
TraesCS6A01G405600 | Aquaporin PIP1-5-like | |||
TraesCS2A01G198500 | Aquaporin PIP2-1 | |||
TraesCS5D01G347600 | Nodulin-26 like intrinsic protein | Arabidopsis thaliana | Beamer et al., | |
Ethylene signaling | ||||
TraesCS2A01G026500 | ![]() | 1-aminocyclopropane-1-carboxylate oxidase homolog 1-like | Cucumis sativus | Kęska et al., |
TraesCS5A01G234200 | 1-aminocyclopropane-1-carboxylate oxidase 1-like | N. tabacum | Zafari et al., | |
TraesCS7B01G110400 | 1-aminocyclopropane-1-carboxylate oxidase homolog 4-like | |||
TraesCS2D01G028500 | 1-aminocyclopropane-1-carboxylate oxidase homolog 1-like | |||
TraesCS4A01G221300 | 1-aminocyclopropane-1-carboxylate oxidase | |||
TraesCS7B01G162100 | Ethylene-responsive transcription factor RAP2-6-like | A. thaliana | Hess et al., | |
TraesCS6D01G281200 | Ethylene-responsive transcription factor RAP2-4-like | |||
TraesCS1B01G243200 | Ethylene-responsive transcription factor RAP2-3-like | |||
S-type anion channel | ||||
TraesCS3A01G225100 | ![]() | S-type anion channel SLAH3 | A. thaliana | Lehmann et al., |
Allene oxide synthase (alpha-linolenic acid metabolism) | ||||
TraesCS6D01G172200 | ![]() | Allene oxide synthase 4-like | A. thaliana | Xie et al., |
TraesCS5B01G408000 | Allene oxide synthase 1 |
表1 小麦根系中与缺O2胁迫相关的基因
Table 1 Genes related to hypoxic stress in the roots of wheat
Gene ID | Gene relative expression level ![]() | Gene description | Species | Reference |
---|---|---|---|---|
Respiratory burst oxidase homologs | ||||
TraesCS5D01G105900 | ![]() | Respiratory burst oxidase homolog protein B-like | Zea mays | Mira et al., |
TraesCS1D01G284800 | Respiratory burst oxidase homolog protein B-like | Nicotiana tabacum | Zafari et al., | |
TraesCS5A01G093600 | Respiratory burst oxidase homolog protein B-like | |||
Alternative pathway | ||||
TraesCS2A01G439400 | ![]() | Mitochondrial alternative oxidase | N. tabacum | Zafari et al., |
TraesCS2B01G459300 | Mitochondrial alternative oxidase | |||
TraesCS2D01G212500 | Internal alternative NADPH-ubiquinone oxidoreductase A1, mitochondrial-like | Z. mays | Igamberdiev and Hill, | |
TraesCS3D01G314700 | PREDICTED: external alternative NADPH-ubiquinone oxidoreductase B3, mitochondrial-like | |||
O2-binding and Fe transport | ||||
TraesCS1D01G340600 | ![]() | Non-symbiotic hemoglobin-like isoform X1 | Oryza sativa | Narsai and Whelan, |
TraesCS1B01G350800 | Non-symbiotic hemoglobin-like isoform X1 | |||
TraesCS1A01G338400 | Non-symbiotic hemoglobin-like isoform X2 | |||
TraesCS5A01G552000 | Nicotianamine synthase | Citrus junos | Xie et al., | |
TraesCS6B01G425200 | Nicotianamine synthase | |||
TraesCS6D01G148200 | Nicotianamine synthase | |||
TraesCS2A01G049900 | Nicotianamine synthase | |||
TraesCS6D01G382900 | Nicotianamine synthase-like 5 protein | |||
Aquaporin | ||||
TraesCS6A01G222100 | ![]() | Probable aquaporin PIP2-2 | Glycine max | Matsuo et al., |
TraesCS6D01G212900 | ![]() | Probable aquaporin PIP2-2 | Sorghum bicolor | Kadam et al., |
TraesCS2A01G407700 | Aquaporin PIP1-2 | |||
TraesCS2D01G404800 | Aquaporin PIP1-2 | |||
TraesCS2B01G077700 | Probable aquaporin PIP2-6 | |||
TraesCS2D01G063900 | Probable aquaporin PIP2-6 | |||
TraesCS6A01G405600 | Aquaporin PIP1-5-like | |||
TraesCS2A01G198500 | Aquaporin PIP2-1 | |||
TraesCS5D01G347600 | Nodulin-26 like intrinsic protein | Arabidopsis thaliana | Beamer et al., | |
Ethylene signaling | ||||
TraesCS2A01G026500 | ![]() | 1-aminocyclopropane-1-carboxylate oxidase homolog 1-like | Cucumis sativus | Kęska et al., |
TraesCS5A01G234200 | 1-aminocyclopropane-1-carboxylate oxidase 1-like | N. tabacum | Zafari et al., | |
TraesCS7B01G110400 | 1-aminocyclopropane-1-carboxylate oxidase homolog 4-like | |||
TraesCS2D01G028500 | 1-aminocyclopropane-1-carboxylate oxidase homolog 1-like | |||
TraesCS4A01G221300 | 1-aminocyclopropane-1-carboxylate oxidase | |||
TraesCS7B01G162100 | Ethylene-responsive transcription factor RAP2-6-like | A. thaliana | Hess et al., | |
TraesCS6D01G281200 | Ethylene-responsive transcription factor RAP2-4-like | |||
TraesCS1B01G243200 | Ethylene-responsive transcription factor RAP2-3-like | |||
S-type anion channel | ||||
TraesCS3A01G225100 | ![]() | S-type anion channel SLAH3 | A. thaliana | Lehmann et al., |
Allene oxide synthase (alpha-linolenic acid metabolism) | ||||
TraesCS6D01G172200 | ![]() | Allene oxide synthase 4-like | A. thaliana | Xie et al., |
TraesCS5B01G408000 | Allene oxide synthase 1 |
图5 不同态氮素处理下小麦根系编码双加氧酶的差异表达基因(DEGs)转录水平变化 彩色标尺为基因在3个不同处理下的相对表达量, 蓝色代表表达量较低, 红色代表表达量较高。CK、SA和AN同图1。
Figure 5 Changes in transcription levels of differentially expressed genes (DEGs) encoding kinds of dioxygenases under different N treatments in roots of wheat seedlings The color scale indicates the relative gene expression, with blue color indicating lower expression and red color indicating higher expression. CK, SA, and AN are the same as shown in Figure 1.
图6 RNA-seq数据的准确性验证 横坐标轴和纵坐标轴分别表示SA与CK和AN与SA比较下qRT- PCR的2-ΔΔCT值和RNA-seq的log2(FC)值。CK、SA和AN同图1。
Figure 6 RNA-seq data accuracy verification The X-axis and Y-axis represent the 2-ΔΔCT values for qRT- PCR analysis and the log2(FC) values for RNA-seq for comparisons of SA vs CK and AN vs SA, respectively. CK, SA, and AN are the same as shown in Figure 1.
图7 不同态氮素处理下小麦根系差异表达蛋白(DEPs)火山图 (A) SA与CK比较; (B) AN与SA比较; (C) AN与CK比较。绿色表示蛋白表达下调, 红色表示蛋白表达上调, 黑色表示蛋白表达无显著变化。FC: 差异倍数。CK、SA和AN同图1。
Figure 7 Volcano plots of differentially expressed proteins (DEPs) under different N treatments in the roots of wheat seedlings (A) SA vs CK; (B) AN vs SA; (C) AN vs CK. Green dots indicate downregulated proteins, red dots indicate upregulated proteins and black dots indicate not significantly changed proteins. FC: Fold change. CK, SA, and AN are the same as shown in Figure 1.
Protein ID | Protein expression![]() | Protein description | ||
---|---|---|---|---|
Glycolysis | ||||
CDM81680.1 | 6-phosphofructokinase 1 | |||
SPT18714.1 | 6-phosphofructokinase 1 | |||
AAO32641.1 | Phosphoglycerate kinase | |||
CAA33303.1 | Phosphoglycerate kinase | |||
CBN64599.1 | Phosphoglycerate kinase | |||
CBG02671.1 | Pyruvate kinase | |||
CBG02673.1 | Pyruvate kinase | |||
CDM82952.1 | Pyruvate kinase | |||
Pyruvate metabolism | ||||
AIV42031.1 | Pyruvate dehydrogenase E2 component | |||
CCA64976.1 | Pyruvate dehydrogenase E1 component beta subunit | |||
SPT15511.1 | Pyruvate dehydrogenase E1 component alpha subunit | |||
CAW61069.1 | Phosphoenolpyruvate carboxylase | |||
CDM84220.1 | Phosphoenolpyruvate carboxylase | |||
ABW77317.1 | Malic enzyme | |||
SPT17588.1 | Malic enzyme | |||
CDM81737.1 | Malic enzyme | |||
Fermentation | ||||
CBM36708.1 | Pyruvate decarboxylase | |||
CBM36829.1 | Pyruvate decarboxylase | |||
ABL74255.1 | Alcohol dehydrogenase class-P | |||
ABL74259.1 | Alcohol dehydrogenase class-P | |||
ABL74258.1 | Alcohol dehydrogenase class-P | |||
SPT16036.1 | L-lactate dehydrogenase | |||
Alternative pathway | ||||
SPT19754.1 | Alternative oxidase | |||
Aquaporin | ||||
ABI96816.1 | Aquaporin TIP | |||
BAP33940.1 | Aquaporin TIP | |||
SPT19521.1 | Aquaporin TIP | |||
AAD10494.1 | Aquaporin TIP | |||
ACZ51371.1 | Aquaporin PIP | |||
AEO13898.1 | Aquaporin PIP | |||
Fe transport | ||||
AND77086.1 | Nicotianamine synthase | |||
AHG95976.1 | Nicotianamine synthase | |||
AND77090.1 | Nicotianamine synthase | |||
AND77092.1 | Nicotianamine synthase |
表2 不同态氮素处理下小麦根系能量代谢与低O2胁迫相关差异表达蛋白(DEPs)
Table 2 Differentially expressed proteins (DEPs) related to hypoxia and energy metabolism under different N treatments in wheat roots
Protein ID | Protein expression![]() | Protein description | ||
---|---|---|---|---|
Glycolysis | ||||
CDM81680.1 | 6-phosphofructokinase 1 | |||
SPT18714.1 | 6-phosphofructokinase 1 | |||
AAO32641.1 | Phosphoglycerate kinase | |||
CAA33303.1 | Phosphoglycerate kinase | |||
CBN64599.1 | Phosphoglycerate kinase | |||
CBG02671.1 | Pyruvate kinase | |||
CBG02673.1 | Pyruvate kinase | |||
CDM82952.1 | Pyruvate kinase | |||
Pyruvate metabolism | ||||
AIV42031.1 | Pyruvate dehydrogenase E2 component | |||
CCA64976.1 | Pyruvate dehydrogenase E1 component beta subunit | |||
SPT15511.1 | Pyruvate dehydrogenase E1 component alpha subunit | |||
CAW61069.1 | Phosphoenolpyruvate carboxylase | |||
CDM84220.1 | Phosphoenolpyruvate carboxylase | |||
ABW77317.1 | Malic enzyme | |||
SPT17588.1 | Malic enzyme | |||
CDM81737.1 | Malic enzyme | |||
Fermentation | ||||
CBM36708.1 | Pyruvate decarboxylase | |||
CBM36829.1 | Pyruvate decarboxylase | |||
ABL74255.1 | Alcohol dehydrogenase class-P | |||
ABL74259.1 | Alcohol dehydrogenase class-P | |||
ABL74258.1 | Alcohol dehydrogenase class-P | |||
SPT16036.1 | L-lactate dehydrogenase | |||
Alternative pathway | ||||
SPT19754.1 | Alternative oxidase | |||
Aquaporin | ||||
ABI96816.1 | Aquaporin TIP | |||
BAP33940.1 | Aquaporin TIP | |||
SPT19521.1 | Aquaporin TIP | |||
AAD10494.1 | Aquaporin TIP | |||
ACZ51371.1 | Aquaporin PIP | |||
AEO13898.1 | Aquaporin PIP | |||
Fe transport | ||||
AND77086.1 | Nicotianamine synthase | |||
AHG95976.1 | Nicotianamine synthase | |||
AND77090.1 | Nicotianamine synthase | |||
AND77092.1 | Nicotianamine synthase |
图8 蛋白质组和转录组测序数据相关性分析 横坐标轴和纵坐标轴分别表示SA与CK和AN与SA比较下基因和蛋白表达差异log2(FC)值。FC同图7。CK、SA和AN同图1。
Figure 8 Correlation analysis of proteomic and transcriptomic sequencing data The X-axis and Y-axis represent the log2(FC) values from paired comparison of SA vs CK and AN vs SA for gene and protein expressions, respectively. FC is the same as shown in Figure 7. CK, SA, and AN are the same as shown in Figure 1.
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