Chinese Bulletin of Botany ›› 2024, Vol. 59 ›› Issue (3): 397-413.DOI: 10.11983/CBB23130 cstr: 32102.14.CBB23130
• RESEARCH PAPERS • Previous Articles Next Articles
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
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)[J]. Chinese Bulletin of Botany, 2024, 59(3): 397-413.
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
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.
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.
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 |
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 |
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.
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.
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 |
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 |
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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