外源有机酸对铝胁迫下菊芋生理响应系统的调控效应

doi:10.11983/CBB23006

植物学报 ›› 2023, Vol. 58 ›› Issue (4): 573-589.DOI: 10.11983/CBB23006

外源有机酸对铝胁迫下菊芋生理响应系统的调控效应

毛轩雯¹, 王志超¹, 阮心依¹, 孙靖菲¹, 张雅婷¹, 陆锦灏¹, 邵甜甜¹, 王娴¹, 肖佳敏¹, 肖莉¹, 叶梦瑶¹, 吴玉环²^,³, 刘鹏¹()

1.浙江师范大学植物学实验室, 金华 321004
2.杭州师范大学生命与环境科学学院, 杭州 310036
3.中国科学院沈阳应用生态研究所, 沈阳 110016

收稿日期:2023-01-15 接受日期:2023-03-08 出版日期:2023-07-01 发布日期:2023-03-10
通讯作者: *E-mail: sky79@zjnu.cn
基金资助:
国家自然科学基金(32001224);国家自然科学基金(41571049);国家级大学生创新创业训练计划(202310345030)

Regulatory Effects of Exogenous Organic Acids on the Physiological Responses of Helianthus tuberosus Under Aluminium Stress

Xuanwen Mao¹, Zhichao Wang¹, Xinyi Ruan¹, Jingfei Sun¹, Yating Zhang¹, Jinhao Lu¹, Tiantian Shao¹, Xian Wang¹, Jiamin Xiao¹, Li Xiao¹, Mengyao Ye¹, Yuhuan Wu²^,³, Peng Liu¹()

1. Botany Laboratory, Zhejiang Normal University, Jinhua 321004, China
2. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, China
3. Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China

Received:2023-01-15 Accepted:2023-03-08 Online:2023-07-01 Published:2023-03-10
Contact: *E-mail: sky79@zjnu.cn

摘要/Abstract

摘要： 铝(Al)是酸性土壤常见的金属污染物之一。为探明外源有机酸对铝胁迫下菊芋(Helianthus tuberosus)生理特征及根系DNA损伤的影响, 以耐铝品种徐州菊芋和铝敏感品种资阳菊芋为材料, 设置0、350和700 µmol∙L^-1铝处理, 同时分别施加0、30、60和90 µmol∙L^-1复合有机酸, 探究外源有机酸对铝胁迫下各时期(7、14和21天)菊芋生理响应和DNA损伤的影响。结果表明, 铝胁迫抑制菊芋根伸长与根系活力, 严重损害菊芋的光合机构与抗氧化系统, 随着铝浓度的增加, DNA拖尾程度升高, DNA受损加剧。而施加复合有机酸能有效缓解铝胁迫造成的损伤。施加60 µmol∙L^-1有机酸可增强抗氧化酶活性, 提高最大光化学效率并促进根尖有机酸分泌, 其中柠檬酸分泌量分别比对照高2倍(徐州菊芋)及0.75倍(资阳菊芋), 根尖铝含量降低, 根系活力增强, 徐州菊芋和资阳菊芋DNA尾距较单独铝处理组下降51.53%和35.10%, 显著缓解DNA拖尾现象, 较大程度修复了DNA断裂。综上, 铝胁迫对菊芋造成的损害严重且较难缓解, 60 µmol∙L^-1有机酸能增强低铝胁迫下菊芋生理响应, 降低DNA受损程度, 提高菊芋的抗逆性, 且在铝敏感品种资阳菊芋中缓解效果更好。该研究揭示了外源复合有机酸对铝胁迫下菊芋生理响应系统的调控作用, 可为菊芋等经济作物在南方酸铝地区的种植与生产提供理论依据。

关键词: 铝胁迫, 复合有机酸, 菊芋, 生理响应, DNA损伤

Abstract: Aluminum (Al) is one of the common metal contaminants in acidic soils. To reveal the effects of exogenous organic acids on the physiological characteristics and root DNA damage of Helianthus tuberosus under Al stress, we used Al resistant H. tuberosus cv. ‘Xuzhou’ and Al sensitive H. tuberosus cv. ‘Ziyang’ as materials. The effects of exogenous organic acids on the physiological responses and DNA damage of H. tuberosus at various periods (7, 14, and 21 d) under Al stress were investigated by setting 0, 350 and 700 µmol∙L^-1 Al concentration treatments and applying 0, 30, 60 and 90 µmol∙L^-1 compound organic acids, respectively. The results showed that Al stress inhibits root elongation and root activity, severely inhibited the photosynthetic and antioxidant systems of H. tuberosus, and the DNA damage in the root system increased with the increase of Al concentration. In contrast, the application of compound organic acid effectively alleviated Al stress. 60 µmol∙L^-1 compound organic acid improved the activity of the antioxidant system, maximum photochemical efficiency and organic acid secretion in root tips, secretion of citric acid was 2 times (H. tuberosus cv. ‘Xuzhou’) and 0.75 times (H. tuberosus cv. ‘Ziyang’) higher than the control, reduced root tip Al content and improved root activity. Besides, H. tuberosus cv. ‘Xuzhou’ and H. tuberosus cv. ‘Ziyang’ oliver tail moment decreased by 51.53% and 35.10%, and compound organic acid reduced the DNA trailing phenomenon and repaired DNA breaks to a greater extent. In conclusion, high concentration of Al causes serious damage to H. tuberosus, which is difficult to mitigate. 60 µmol∙L^-1 compound organic acid could enhance the H. tuberosus physiological responses under low Al stress, reduce DNA damage and thus improve the stress resistance. The alleviation effect was better in H. tuberosus cv. ‘Ziyang’. This study reveals the regulatory role of exogenous organic acids on the physiological responses of H. tuberosus under Al stress, and provides a theoretical basis for planting and production of H. tuberosus and production of other cash crops in the acid-aluminium areas of southern China.

Key words: aluminum stress, compound organic acids, Helianthus tuberosus, physiological response, DNA damage

毛轩雯, 王志超, 阮心依, 孙靖菲, 张雅婷, 陆锦灏, 邵甜甜, 王娴, 肖佳敏, 肖莉, 叶梦瑶, 吴玉环, 刘鹏. 外源有机酸对铝胁迫下菊芋生理响应系统的调控效应. 植物学报, 2023, 58(4): 573-589.

Xuanwen Mao, Zhichao Wang, Xinyi Ruan, Jingfei Sun, Yating Zhang, Jinhao Lu, Tiantian Shao, Xian Wang, Jiamin Xiao, Li Xiao, Mengyao Ye, Yuhuan Wu, Peng Liu. Regulatory Effects of Exogenous Organic Acids on the Physiological Responses of Helianthus tuberosus Under Aluminium Stress. Chinese Bulletin of Botany, 2023, 58(4): 573-589.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB23006

https://www.chinbullbotany.com/CN/Y2023/V58/I4/573

图/表 11

表1 实验设计

Table 1 Experimental design in this study

Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

图1 外源复合有机酸(OA)对铝胁迫下菊芋根长与株高的影响 Al0、Al350和Al700表示铝浓度分别为0、350和700 μmol?L-1; OA0、OA30、OA60和OA90表示复合有机酸浓度分别为0、30、60和90 μmol?L-1。XZ: 徐州菊芋; ZY: 资阳菊芋。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 1 The effect of exogenous compound organic acid (OA) on the root length and plant height of Helianthus tuberosus under aluminum (Al) stress Al0, Al350, and Al700 indicating concentrations of Al are 0, 350, and 700 μmol?L-1, respectively; OA0, OA30, OA60, and OA90 indicating concentrations of OA are 0, 30, 60, and 90 μmol?L-1, respectively. XZ: H. tuberosus cv. ‘Xuzhou’; ZY: H. tuberosus cv. ‘Ziyang’. Different lowercase letters indicate significant differences among treatment groups at the same period (P<0.05).

图2 外源复合有机酸(OA)对铝胁迫下菊芋叶片气孔导度(Gs) (A, E)、蒸腾速率(Tr) (B, F)、净光合速率(Pn) (C, G)和细胞间CO2浓度(Ci) (D, H)的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 2 The effect of exogenous compound organic acid (OA) on the stomatal conductance (Gs) (A, E), transpiration rate (Tr) (B, F), net photosynthetic rate (Pn) (C, G), and intercellular CO2 concentration (Ci) (D, H) of Helianthus tuberosus leaves under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图3 外源复合有机酸(OA)对铝胁迫下菊芋叶片初始荧光(F0) (A, D)、非光化学猝灭系数(qN) (B, E)和最大荧光(Fm) (C, F)的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 3 The effect of exogenous compound organic acid (OA) on the initial fluorescence (F0) (A, D), non-photochemical quenching (qN) (B, E) and maximal fluorescence (Fm) (C, F) of Helianthus tuberosus leaves under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图4 外源复合有机酸(OA)对铝胁迫下菊芋叶片电子传递效率(ETR) (A, C)和PSII最大光化学量子产量(Fv/Fm) (B, D)的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 4 The effect of exogenous compound organic acid (OA) on the electron transport rate (ETR) (A, C) and maximum photochemical quantum yield of PSII (Fv/Fm) (B, D) of Helianthus tuberosus leaves under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图5 外源复合有机酸(OA)对铝胁迫下菊芋叶片超氧化物歧化酶(SOD) (A, D)、过氧化物酶(POD) (B, E)和过氧化氢酶(CAT) (C, F)活性的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 5 The effect of exogenous compound organic acid (OA) on the superoxide dismutase (SOD) (A, D), peroxidase (POD) (B, E) and catalase (CAT) (C, F) activities of Helianthus tuberosus leaves under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图6 外源复合有机酸(OA)对铝胁迫下菊芋叶片抗坏血酸(AsA) (A, C)和谷胱甘肽(GSH) (B, D)含量的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 6 The effect of exogenous compound organic acid (OA) on the ascorbic acid (AsA) (A, C) and glutathione (GSH) (B, D) contents of Helianthus tuberosus leaves under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图7 外源复合有机酸(OA)对铝胁迫下菊芋根尖铝含量与根系活力的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母和*表示同一时期不同处理组间差异显著(P<0.05)。

Figure 7 Effect of exogenous compound organic acid (OA) on the aluminum (Al) content of root tip and root activity of Helianthus tuberosus under aluminum stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters and * indicate significant differences among different treatment groups at the same period (P<0.05).

图8 外源复合有机酸(OA)对铝胁迫下菊芋根系分泌物柠檬酸(CA) (A)、苹果酸(MA) (B)和草酸(EA) (C)含量的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。不同小写字母表示同一时期不同处理组间差异显著(P<0.05)。

Figure 8 The effect of exogenous compound organic acid (OA) on the content of citric acid (CA) (A), malic acid (MA) (B) and ethanedioic acid (EA) (C) in root exudates of Helianthus tuberosus under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. Different lowercase letters indicate significant differences among different treatment groups at the same period (P<0.05).

图9 外源复合有机酸(OA)对铝胁迫下菊芋根细胞Olive尾矩(OTM)的影响 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。XZ和ZY同图1。*表示同一时期不同处理组间差异显著(P<0.05)。

Figure 9 The effect of exogenous compound organic acid (OA) on oliver tail moment (OTM) of root cells of Helianthus tuberosus under aluminum (Al) stress Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. XZ and ZY are the same as shown in Figure 1. * indicate significant differences among different treatment groups at the same period (P<0.05).

图10 不同浓度复合有机酸(OA)及铝处理下菊芋根系DNA损伤 Al0、Al350、Al700、OA0、OA30、OA60和OA90同图1。Bars=20 μm

Figure 10 DNA damage of Helianthus tuberosus root under different concentration of compound organic acid (OA) and aluminum (Al) treatments Al0, Al350, Al700, OA0, OA30, OA60, and OA90 are the same as shown in Figure 1. Bars=20 μm

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外源有机酸对铝胁迫下菊芋生理响应系统的调控效应

Regulatory Effects of Exogenous Organic Acids on the Physiological Responses of Helianthus tuberosus Under Aluminium Stress

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Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

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Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90

Group	Aluminium concentration (μmol?L^-1)	Compound organic acid (OA) concentration (μmol?L^-1)
1	0	0
2	0	30
3	0	60
4	0	90
5	350	0
6	350	30
7	350	60
8	350	90
9	700	0
10	700	30
11	700	60
12	700	90