NO3-缓解小麦根部NH4+毒性机理(长英文摘要）

doi:10.11983/CBB23130

植物学报 ›› 2024, Vol. 59 ›› Issue (3): 397-413.DOI: 10.11983/CBB23130 cstr: 32102.14.CBB23130

NO₃^-缓解小麦根部NH₄⁺毒性机理(长英文摘要）

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^,^*()

¹山东师范大学生命科学学院, 济南 250014
²山东省农业科学院作物研究所, 济南 250100

收稿日期:2023-09-16 接受日期:2024-04-15 出版日期:2024-05-10 发布日期:2024-05-10
通讯作者: 孔令安
基金资助:
山东省自然科学基金(ZR2020MC087);国家重点研发计划(2022YFD2300801);山东省现代农业技术产业体系(SDAIT-01-07)

Nitrate-dependent Alleviation of Root Ammonium Toxicity in Wheat (Triticum aestivum)

Xiao Liu¹^,², Wanying Du¹^,², Yunxiu Zhang², Chengming Tang¹^,², Huawei Li², Haiyong Xia², Shoujin Fan¹, Ling’an Kong¹^,²^,^*()

¹College of Life Sciences, Shandong Normal University, Jinan 250014, China
²Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, China

Received:2023-09-16 Accepted:2024-04-15 Online:2024-05-10 Published:2024-05-10
Contact: Ling’an Kong

摘要/Abstract

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。

关键词: 能量代谢, 发酵, 根, 三羧酸循环, 小麦

Abstract:
INTRODUCTION Nitrogen (N) is one of the most essential nutrients for the plant growth and development, and NH₄⁺-N is the main form of N source. Appropriate amount of NH₄⁺ promotes plant growth and increase crop yield. However, when used as the only N source, NH₄⁺ suppresses the growth and production of crops. Wheat (Triticum aestivum) is the third largest cereal crop in China, and its production has a profound impact on the food production. As the indispensable raw material for foods, wheat is crucial to daily life, so studying NH₄⁺ toxicity and mitigation mechanisms are of great significance for wheat production.

RATIONALE NH₄⁺toxicity is a ubiquitous issue in plants. The mechanisms of how NH₄⁺ causes phytotoxicity are not fully understood. To explore the mechanisms of NO₃^--dependent alleviation of NH₄⁺toxicity in the roots of wheat, both transcriptomic and proteomic approaches were used to investigate the differential expressions of genes and proteins under different nitrogen treatments.

RESULTS Compared with 7.5 mmol·L^-1NO₃^- (control), 7.5 mmol·L^-1NH₄⁺treatment inhibited the root growth of wheat seedlings. Transcriptome analysis showed that sole NH₄⁺ treatment upregulated the expressions of genes encoding glycolysis- and fermentation-related enzymes, including pyruvate decarboxylase, alcohol dehydrogenase and lactate dehydrogenase, while downregulated the expressions of genes encoding TCA cycle enzymes and the ATP synthases in the roots compared with control. Expressions of genes encoding the respiratory burst oxidase homologs (Rbohs), alternative oxidase (AOX) and dioxygenases were significantly upregulated, and expression of the PIP-type aquaporin genes were downregulated. The addition of 1 mmol·L^-1NO₃^- to the solution containing 7.5 mmol·L^-1NH₄⁺downregulated the expression of genes encoding glycolysis enzymes, fermentation enzymes, Rbohs, AOX and dioxygenases, and increased the expression of genes encoding the TCA cycle enzymes, the ATP synthases and PIP-type aquaporins. Proteome analysis showed that expressions of glycolysis enzymes, fermentation enzymes and AOX were upregulated, while PIP-type aquaporins were downregulated under sole NH₄⁺conditions compared with the control. The addition of NO₃^- downregulated the expressions of glycolysis enzymes, fermentation enzymes, Rbohs and AOX and upregulated expressions of PIP-type aquaporins.

CONCLUSION In conclusion, sole NH₄⁺ treatment promotes glycolytic and fermentation pathways, inhibits the TCA cycle and energy generation, and ultimately inhibits root growth of wheat seedlings. The inhibition of root growth may be due to the sole NH₄⁺-induced hypoxic stress in the roots. The addition of NO₃^- inhibits the glycolysis and fermentation pathways, promotes the TCA cycle and energy production, significantly alleviates the hypoxia stress and thereby attenuates the inhibitory effect of NH₄⁺ on root growth.

Changes in transcription level of DEGs involved in fermentation pathway and TCA cycle under different N treatments in the roots of wheat seedlings. Sole NH₄⁺treatment may induce the fermentation pathway, inhibit the capacity of TCA cycle, and ultimately inhibit the root growth in wheat. The addition of NO₃^- remarkably alleviates the sole NH₄⁺-induced inhibitory effects on the root growth.

Key words: energy metabolism, fermentation, root, TCA cycle, wheat

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(长英文摘要）. 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.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB23130

https://www.chinbullbotany.com/CN/Y2024/V59/I3/397

图/表 10

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.

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 description	Species	Reference
Respiratory burst oxidase homologs
TraesCS5D01G105900	Respiratory burst oxidase homolog protein B-like	Zea mays	Mira et al., 2016
TraesCS1D01G284800	Respiratory burst oxidase homolog protein B-like	Nicotiana tabacum	Zafari et al., 2022
TraesCS5A01G093600	Respiratory burst oxidase homolog protein B-like
Alternative pathway
TraesCS2A01G439400	Mitochondrial alternative oxidase	N. tabacum	Zafari et al., 2022
TraesCS2B01G459300	Mitochondrial alternative oxidase
TraesCS2D01G212500	Internal alternative NADPH-ubiquinone oxidoreductase A1, mitochondrial-like	Z. mays	Igamberdiev and Hill, 2018
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, 2013
TraesCS1B01G350800	Non-symbiotic hemoglobin-like isoform X1
TraesCS1A01G338400	Non-symbiotic hemoglobin-like isoform X2
TraesCS5A01G552000	Nicotianamine synthase	Citrus junos	Xie et al., 2021b
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., 2012
TraesCS6D01G212900	Probable aquaporin PIP2-2	Sorghum bicolor	Kadam et al., 2017
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., 2021
Ethylene signaling
TraesCS2A01G026500	1-aminocyclopropane-1-carboxylate oxidase homolog 1-like	Cucumis sativus	Kęska et al., 2021
TraesCS5A01G234200	1-aminocyclopropane-1-carboxylate oxidase 1-like	N. tabacum	Zafari et al., 2022
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., 2011
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., 2021
Allene oxide synthase (alpha-linolenic acid metabolism)
TraesCS6D01G172200	Allene oxide synthase 4-like	A. thaliana	Xie et al., 2021a
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 description	Species	Reference
Respiratory burst oxidase homologs
TraesCS5D01G105900	Respiratory burst oxidase homolog protein B-like	Zea mays	Mira et al., 2016
TraesCS1D01G284800	Respiratory burst oxidase homolog protein B-like	Nicotiana tabacum	Zafari et al., 2022
TraesCS5A01G093600	Respiratory burst oxidase homolog protein B-like
Alternative pathway
TraesCS2A01G439400	Mitochondrial alternative oxidase	N. tabacum	Zafari et al., 2022
TraesCS2B01G459300	Mitochondrial alternative oxidase
TraesCS2D01G212500	Internal alternative NADPH-ubiquinone oxidoreductase A1, mitochondrial-like	Z. mays	Igamberdiev and Hill, 2018
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, 2013
TraesCS1B01G350800	Non-symbiotic hemoglobin-like isoform X1
TraesCS1A01G338400	Non-symbiotic hemoglobin-like isoform X2
TraesCS5A01G552000	Nicotianamine synthase	Citrus junos	Xie et al., 2021b
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., 2012
TraesCS6D01G212900	Probable aquaporin PIP2-2	Sorghum bicolor	Kadam et al., 2017
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., 2021
Ethylene signaling
TraesCS2A01G026500	1-aminocyclopropane-1-carboxylate oxidase homolog 1-like	Cucumis sativus	Kęska et al., 2021
TraesCS5A01G234200	1-aminocyclopropane-1-carboxylate oxidase 1-like	N. tabacum	Zafari et al., 2022
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., 2011
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., 2021
Allene oxide synthase (alpha-linolenic acid metabolism)
TraesCS6D01G172200	Allene oxide synthase 4-like	A. thaliana	Xie et al., 2021a
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.

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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NO₃^-缓解小麦根部NH₄⁺毒性机理(长英文摘要）

Nitrate-dependent Alleviation of Root Ammonium Toxicity in Wheat (Triticum aestivum)

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