小麦根系在碱胁迫下的生理代谢反应

doi:10.17521/cjpe.2016.0136

植物生态学报 ›› 2017, Vol. 41 ›› Issue (6): 683-692.DOI: 10.17521/cjpe.2016.0136

小麦根系在碱胁迫下的生理代谢反应

郭瑞^1,^2,^*(), 周际³, 杨帆⁴, 李峰¹

¹中国农业科学院农业环境与可持续发展研究所, 北京 100081
²农业部旱作节水农业重点实验室, 北京 100081
³国土资源部土地整治中心, 北京 100034
⁴吉林省农业科学院, 长春 130033

收稿日期:2017-04-05 接受日期:2016-04-14 出版日期:2017-06-10 发布日期:2017-07-19
通讯作者: 郭瑞
作者简介:* 通信作者Author for correspondence (E-mail:sunzhiqiang1956@sina.com)
基金资助:
基金项目国家自然科学基金(31200243和31570328)

Metabolic responses of wheat roots to alkaline stress

Rui GUO^1,^2,^*(), Ji ZHOU³, Fan YANG⁴, Feng LI¹

¹Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing 100081, China

²Key Laboratory of Dryland Agriculture, Ministry of Agriculture, Beijing 100081, China

³Land Consolidation and Rehabilitation Centre, the Ministry of Land and Resources, Beijing 100034, China
and
⁴Jilin Academy of Forestry Science, Changchun 130033, China

Received:2017-04-05 Accepted:2016-04-14 Online:2017-06-10 Published:2017-07-19
Contact: Rui GUO
About author:KANG Jing-yao(1991-), E-mail: kangjingyao_nj@163.com。

摘要/Abstract

摘要：

为明确碱胁迫对小麦(Triticum aestivum)根系离子组及代谢组的影响, 探讨其响应变化规律及机制, 该研究以小麦为实验材料, 采用两种碱性盐(NaHCO₃和Na₂CO₃)按摩尔比1:1混合模拟不同碱胁迫强度, 利用气相色谱-质谱联用(GC-MS)技术结合多元变量分析方法, 系统分析小麦根系在碱胁迫下的矿质元素、游离阴离子、代谢产物及代谢途径变化。结果显示: 低浓度碱胁迫下小麦根系仍能维持一定的生长, 但在高浓度碱胁迫下根系生长受到了明显抑制。当碱胁迫强度超过小麦根系调节能力时, 根系中Na含量急剧增加的同时K含量明显减少。碱胁迫刺激根中Ca积累, 而Mg、Cu和Fe含量呈现下降趋势。碱胁迫明显减少根中游离阴离子(主要是Cl^-)含量。检测代谢物组包括有机酸、氨基酸、碳水化合物、嘧啶和嘌呤等70个代谢产物, 主成分分析结果表明代谢物均分布在95%的置信区间内。碱胁明显迫促进苹果酸、琥珀酸等代谢物积累, 但造成糖类(果糖、蔗糖)及多元醇(肌醇、山梨糖醇)和氨基酸(γ-氨基丁酸、丙氨酸)含量显著下降。结果表明: 根系中Na⁺含量剧增, 加上高pH值危害, 导致根系生长率降低; 与此同时, 游离阴离子明显减少, 造成根系内负电荷亏缺和pH不稳定, 导致离子平衡遭到破坏, 进而引起一系列代谢途径的协变反应。小麦根系在碱胁迫下糖酵解、细胞膜脂代谢和氨基酸合成受到明显的抑制, 但三羧酸循环显著增强。这些结果表明碱胁迫(高pH值)对碳素合成和储存有明显的负效应, 降低代谢合成碳骨架和能量, 使得清除活性氧能力明显下降。碱胁迫下根外部质子缺乏造成NO₃^-含量降低, 影响氮素吸收利用, 导致氨基酸合成受阻。三羧酸循环增强为生成有机酸类化合物和调控pH平衡提供能量, 这可能是植物适应碱胁迫的一种特殊对应策略。

关键词: 小麦, 碱胁迫, 根系, 生长特性, 代谢调控

Abstract:

Aims The aim of this study was to investigate the effects of alkaline stress on primary, secondary metabolites and metabolic pathways in the roots of wheat (Triticum aestivum). The results were used to evaluate the physiological adaptive mechanisms by which wheat tolerated alkali stress.Methods A pot experiment was carried out in the greenhouse. For each plastic pot, five wheat seeds were planted. After germination, seedlings were allowed to grow under controlled water and nutrient conditions for two months, then seedlings were exposed to alkaline stress (NaHCO₃-Na₂CO₃) for 12 days. The relative growth rate (RGR), absolute water content (AWC), metal elements, free cations and metabolites were measured.Important findings The alkaline stress caused the reduction of RGR and AWC. Alkaline stress caused a rapid increase of Na content with the concurrent decrease in K and Cl content, resulting in inhibited metal element accumulation and an ionic imbalance. In the present study, alkaline stress strongly enhanced Ca accumulation in wheat roots, suggesting that an increased Ca concentration can immediately trigger the salt overly sensitive (SOS)-Na exclusion system and reduce Na-associated injuries. Also, 70 metabolites, including organic acids, amino acids, sugars/polyols and others, behaved differently in the alkaline stress treatments according to a GC-MS analysis. The metabolic profiles of wheat were closely associated with alkaline-stress conditions. Alkaline stress caused the accumulation of organic acids, accompanied by the depletion of sugars/polyols and amino acids. Organic acids could play a central role in the regulation of intracellular pH by accumulating vacuoles to neutralize excess cations. Glycolysis and amino acid synthesis in roots were inhibited under salt stress while prolonged alkaline stress led to a progressive tricarboxylic acid (TCA) cycle. The severe negative effects of alkaline stress on sugar synthesis and storage may reflect the toxic levels of Na⁺ accumulating in plant cells in a high-pH environment, implying that the reactive oxygen species detoxification capacity was diminished by the high pH. A lack of NO₃^- in wheat roots can decrease synthase enzyme activities, limiting the synthesis of amino acids. Under salt stress, the TCA cycle and organic acid accumulation increased, but glycolysis and amino acid synthesis were inhibited in roots. Thus, energy levels and high concentrations of organic acids may be the key adaptive mechanisms by which wheat seedlings maintain their intracellular ion balance under alkaline stress.

Key words: wheat (Triticum aestivum), alkaline stress, roots, growth characters, metabolic profiles

郭瑞, 周际, 杨帆, 李峰. 小麦根系在碱胁迫下的生理代谢反应. 植物生态学报, 2017, 41(6): 683-692. DOI: 10.17521/cjpe.2016.0136

Rui GUO, Ji ZHOU, Fan YANG, Feng LI. Metabolic responses of wheat roots to alkaline stress. Chinese Journal of Plant Ecology, 2017, 41(6): 683-692. DOI: 10.17521/cjpe.2016.0136

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2016.0136

https://www.plant-ecology.com/CN/Y2017/V41/I6/683

图/表 7

参考文献 29

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处理 Treatment	碱浓度 Alkaline concentration (mmol·L^-1)	电导率 EC (dS·m^-1)	渗透势 Osmotic potential (MPa)	pH值 pH value
对照 Control	0	2.16	-0.05	6.95
碱胁迫 Alkaline stress	50	4.98	-0.28	9.69
	100	9.21	-0.51	9.92

处理 Treatment	碱浓度 Alkaline concentration (mmol·L^-1)	电导率 EC (dS·m^-1)	渗透势 Osmotic potential (MPa)	pH值 pH value
对照 Control	0	2.16	-0.05	6.95
碱胁迫 Alkaline stress	50	4.98	-0.28	9.69
	100	9.21	-0.51	9.92

处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	矿质元素 Metal elements (mmol·g^-1dry mass)
处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	Na	K	Ca	Mg	Cu	Fe	Zn	Mn
对照 Control	0	4.25 ± 1.01^b	69.90 ± 3.03^a	17.11 ± 1.01^b	7.80 ± 0.29^a	1.25 ± 0.04^a	1.56 ± 0.08^a	0.07 ± 0.01^a	0.06 ± 0.00^a
碱胁迫 Alkaline stress	50	15.89 ± 2.06^ab	45.20 ± 1.54^b	20.53 ± 1.00^b	6.01 ± 0.16^b	1.02 ± 0.02^a	1.26 ± 0.03^a	0.05 ± 0.00^b	0.05 ± 0.00^a
碱胁迫 Alkaline stress	100	19.09 ± 2.11^a	16.83 ± 1.02^c	32.85 ± 1.30^a	4.96 ± 0.47^c	0.55 ± 0.03^b	0.84 ± 0.05^b	0.03 ± 0.00^c	0.06 ± 0.00^a

处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	矿质元素 Metal elements (mmol·g^-1dry mass)
处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	Na	K	Ca	Mg	Cu	Fe	Zn	Mn
对照 Control	0	4.25 ± 1.01^b	69.90 ± 3.03^a	17.11 ± 1.01^b	7.80 ± 0.29^a	1.25 ± 0.04^a	1.56 ± 0.08^a	0.07 ± 0.01^a	0.06 ± 0.00^a
碱胁迫 Alkaline stress	50	15.89 ± 2.06^ab	45.20 ± 1.54^b	20.53 ± 1.00^b	6.01 ± 0.16^b	1.02 ± 0.02^a	1.26 ± 0.03^a	0.05 ± 0.00^b	0.05 ± 0.00^a
碱胁迫 Alkaline stress	100	19.09 ± 2.11^a	16.83 ± 1.02^c	32.85 ± 1.30^a	4.96 ± 0.47^c	0.55 ± 0.03^b	0.84 ± 0.05^b	0.03 ± 0.00^c	0.06 ± 0.00^a

处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	阴离子 Anions (mmol·g^-1dry mass)
处理 Treatment	碱胁迫浓度 Alkaline concentration (mmol)	Cl^-	NO₃^-	H₂PO₄^-	SO₄^2-
对照 Control	0	0.12 ± 0.01^a	0.41 ± 0.02^a	0.05 ± 0.00^a	0.03 ± 0.00^a
碱胁迫 Alkaline stress	50	0.09 ± 0.00^b	0.34 ± 0.01^b	0.03 ± 0.01^b	0.02 ± 0.00^a
碱胁迫 Alkaline stress	100	0.04 ± 0.01^c	0.07 ± 0.00^c	0.02 ± 0.00^b	0.03 ± 0.00^a

小麦根系在碱胁迫下的生理代谢反应

Metabolic responses of wheat roots to alkaline stress

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代谢路径和代谢物名称 Metabolic pathways and metabolites		相对含量 Relative concentration			倍性变量Fold changes
代谢路径和代谢物名称 Metabolic pathways and metabolites		CK	AS-50 mmol	AS-100 mmol	log₂(50/CK)	log₂(100/CK)
三羧酸循环 Tricarboxylic acid cycle	柠檬酸 Citric acid	75.73	150.14	231.23	0.99^*	1.61^**
	乌头酸 Aconitic acid	1.34	1.70	5.13	0.34	1.93^**
	α-酮戊二酸 α-ketoglutaric acid	0.18	0.33	0.85	0.89	2.23^**
	琥珀酸 Succinic acid	19.05	61.45	120.69	1.69^**	2.66^**
	延胡索酸 Fumaric acid	1.34	1.56	9.63	0.23	2.85^**
	苹果酸 Malic acid	10.47	23.10	30.35	1.14^*	1.54^**
糖酵解过程 Glycolysis	葡萄糖 Glucose	26.37	13.67	7.91	-0.95^*	-1.74^**
	葡萄糖-6-磷酸 Fructose-6-phosphate	0.57	0.25	0.08	-1.16^*	-2.75^**
	果糖-6-磷酸 Glucose-6-phosphate	0.22	0.13	0.04	-0.80	-2.58^**
	3-磷酸甘油酸 3-phosphoglyceric acid	0.50	0.34	0.11	-0.57	-2.19^**
	丙酮酸 Pyruvate	0.54	0.50	0.31	-0.10	-0.81
	磷酸烯醇式丙酮酸 Enolphosphopyruvate	0.73	0.61	0.22	-0.26	-1.74^**
莽草酸途径 Shikimic path way	莽草酸 Shikimic acid	1.84	1.22	3.84	-0.60	1.06^*
	奎尼酸 Quinic acid	4.17	6.17	23.11	0.58	2.47^**
	苯丙氨酸 Phenylalanine	0.65	0.17	0.11	-1.91^*	-2.60^**
	色氨酸 Tryptophan	0.05	0.03	0.02	-0.71	-1.45^*
	酪氨酸 Tyrosine	1.59	0.03	0.02	-4.18^**	-6.57^**
	肉桂酸 Cinnamic acid	0.25	0.15	0.12	-0.77	-1.12^*
细胞膜脂代谢 Metabolism of plasma membrane	肌醇 Myo-inositol	19.17	9.63	3.07	-0.99^*	-2.64^**
	甘氨酸 Glycine	0.74	0.34	0.12	-1.56^**	-2.69^**
	丝氨酸 Serine	17.83	9.56	1.64	-0.90^*	-3.44^**
	乙醇胺 Ethanolamine	20.23	11.31	3.26	-0.84^*	-2.63^**
氨基酸 Amino acid	γ-氨基丁酸 γ-aminobutyric acid	137.19	41.77	23.92	-1.72^**	-2.52^**
	丙氨酸 Alanine	106.58	56.88	10.64	-0.91^*	-3.32^**
	谷氨酸 Glutamate	24.93	13.73	8.40	-0.86^*	-1.57^**
	天冬酰胺 Asparagine	12.65	4.38	0.91	-1.53^**	-3.79^**
	天冬氨酸 Aspartic acid	7.60	4.06	3.34	-0.90^*	-1.19^*
	脯氨酸 Proline	10.04	15.47	11.57	0.62	0.20
	赖氨酸 Lysine	17.32	0.33	0.11	-5.72^**	-7.26^**
糖类及多元醇 Sugars and polyols	果糖 Fructose	814.31	574.62	173.68	-0.78^*	-2.23^**
	蔗糖 Sucrose	136.11	92.04	65.17	-0.56	-1.06^*
	塔罗糖 Talose	114.17	75.07	23.13	-0.60	-2.30^**
	蔗果三糖 Kestose	57.63	42.47	19.69	-0.44	-1.55^**
	核糖 Ribose	8.24	4.25	1.38	-0.96^*	-2.58^**

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