Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>

Low light intensity is common in northern China due to fog or haze, and causes stress for crop plants. To solve the problem of low light intensity stress on the growth and development of vegetable crops in China, new cropping strategies must be developed. We previously showed that an appropriate rat...

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Main Authors: Linli Hu, Yutong Li, Yue Wu, Jian Lv, Mohammed Mujitaba Dawuda, Zhongqi Tang, Weibiao Liao, Alejandro Calderón-Urrea, Jianming Xie, Jihua Yu
Format: Article
Language:English
Published: MDPI AG 2019-11-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/8/11/489
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author Linli Hu
Yutong Li
Yue Wu
Jian Lv
Mohammed Mujitaba Dawuda
Zhongqi Tang
Weibiao Liao
Alejandro Calderón-Urrea
Jianming Xie
Jihua Yu
author_facet Linli Hu
Yutong Li
Yue Wu
Jian Lv
Mohammed Mujitaba Dawuda
Zhongqi Tang
Weibiao Liao
Alejandro Calderón-Urrea
Jianming Xie
Jihua Yu
author_sort Linli Hu
collection DOAJ
description Low light intensity is common in northern China due to fog or haze, and causes stress for crop plants. To solve the problem of low light intensity stress on the growth and development of vegetable crops in China, new cropping strategies must be developed. We previously showed that an appropriate ratio of ammonium and nitrate (NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup>) can alleviate the effect of low light stress on plants, although it is not clear what mechanism is involved in this alleviation. We propose the hypothesis that an appropriate ammonium/nitrate ratio (10:90) can induce NO synthesis to regulate the AsA-GSH cycle in mini Chinese cabbage seedlings under low light intensity. To test the hypothesis, we conducted a series of hydroponic experiments. The results indicated that, under low light intensity conditions, appropriate NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> (N, NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> = 10:90) decreased the contents of malondialdehyde (MDA), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), and superoxide anion (O<sub>2</sub><sup>&#8722;</sup>) in leaves compared with nitrate treatment. Exogenous nitric oxide (SNP) had the same effects on MDA, H<sub>2</sub>O<sub>2</sub>, and O<sub>2</sub><sup>&#8722;</sup>. However, with the addition of a NO scavenger (hemoglobin, Hb) and NO inhibitors (N-nitro-l-arginine methyl ester, L-NAME), NaN<sub>3</sub> (NR inhibitor) significantly increased the contents of MDA, H<sub>2</sub>O<sub>2</sub>, and O<sub>2</sub><sup>-</sup>. The application of N solution enhanced the AsA-GSH cycle by increasing the activities of ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and ascorbate oxidase (AAO), compared with control (NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> = 0:100). Meanwhile, exogenous SNP significantly increased the above indicators. All these effects of N on AsA-GSH cycle were inhibited by the addition of Hb, L-NAME and NaN<sub>3</sub> in N solution. The results also revealed that the N and SNP treatments upregulated the relative expression level of <i>GR, MDHAR1, APXT, DHAR2</i>, and<i> AAO </i>gene in mini Chinese cabbage leaves under low light stress. These results demonstrated that the appropriate NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> (10:90) induced NO synthesis which regulates the AsA-GSH cycle in mini Chinese cabbage seedlings under low light stress.
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spelling doaj.art-e5f7d4f37af44825be016fcd55fea6fb2022-12-22T04:05:34ZengMDPI AGPlants2223-77472019-11-0181148910.3390/plants8110489plants8110489Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>Linli Hu0Yutong Li1Yue Wu2Jian Lv3Mohammed Mujitaba Dawuda4Zhongqi Tang5Weibiao Liao6Alejandro Calderón-Urrea7Jianming Xie8Jihua Yu9Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaCollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaDepartment of Biology, College of Science and Mathematics, California State University, Fresno, CA 97340, USACollege of Horticulture, Gansu Agricultural University, Lanzhou 730070, ChinaGansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou 730070, ChinaLow light intensity is common in northern China due to fog or haze, and causes stress for crop plants. To solve the problem of low light intensity stress on the growth and development of vegetable crops in China, new cropping strategies must be developed. We previously showed that an appropriate ratio of ammonium and nitrate (NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup>) can alleviate the effect of low light stress on plants, although it is not clear what mechanism is involved in this alleviation. We propose the hypothesis that an appropriate ammonium/nitrate ratio (10:90) can induce NO synthesis to regulate the AsA-GSH cycle in mini Chinese cabbage seedlings under low light intensity. To test the hypothesis, we conducted a series of hydroponic experiments. The results indicated that, under low light intensity conditions, appropriate NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> (N, NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> = 10:90) decreased the contents of malondialdehyde (MDA), hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), and superoxide anion (O<sub>2</sub><sup>&#8722;</sup>) in leaves compared with nitrate treatment. Exogenous nitric oxide (SNP) had the same effects on MDA, H<sub>2</sub>O<sub>2</sub>, and O<sub>2</sub><sup>&#8722;</sup>. However, with the addition of a NO scavenger (hemoglobin, Hb) and NO inhibitors (N-nitro-l-arginine methyl ester, L-NAME), NaN<sub>3</sub> (NR inhibitor) significantly increased the contents of MDA, H<sub>2</sub>O<sub>2</sub>, and O<sub>2</sub><sup>-</sup>. The application of N solution enhanced the AsA-GSH cycle by increasing the activities of ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and ascorbate oxidase (AAO), compared with control (NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> = 0:100). Meanwhile, exogenous SNP significantly increased the above indicators. All these effects of N on AsA-GSH cycle were inhibited by the addition of Hb, L-NAME and NaN<sub>3</sub> in N solution. The results also revealed that the N and SNP treatments upregulated the relative expression level of <i>GR, MDHAR1, APXT, DHAR2</i>, and<i> AAO </i>gene in mini Chinese cabbage leaves under low light stress. These results demonstrated that the appropriate NH<sub>4</sub><sup>+</sup>:NO<sub>3</sub><sup>&#8722;</sup> (10:90) induced NO synthesis which regulates the AsA-GSH cycle in mini Chinese cabbage seedlings under low light stress.https://www.mdpi.com/2223-7747/8/11/489low light intensitynitric oxideascorbate–glutathione cycleammonium: nitrate ratiomini chinese cabbage
spellingShingle Linli Hu
Yutong Li
Yue Wu
Jian Lv
Mohammed Mujitaba Dawuda
Zhongqi Tang
Weibiao Liao
Alejandro Calderón-Urrea
Jianming Xie
Jihua Yu
Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
Plants
low light intensity
nitric oxide
ascorbate–glutathione cycle
ammonium: nitrate ratio
mini chinese cabbage
title Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
title_full Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
title_fullStr Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
title_full_unstemmed Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
title_short Nitric Oxide Is Involved in the Regulation of the Ascorbate–Glutathione Cycle Induced by the Appropriate Ammonium: Nitrate to Mitigate Low Light Stress in <i>Brassica pekinensis</i>
title_sort nitric oxide is involved in the regulation of the ascorbate glutathione cycle induced by the appropriate ammonium nitrate to mitigate low light stress in i brassica pekinensis i
topic low light intensity
nitric oxide
ascorbate–glutathione cycle
ammonium: nitrate ratio
mini chinese cabbage
url https://www.mdpi.com/2223-7747/8/11/489
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