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Acta Agronomica Sinica ›› 2018, Vol. 44 ›› Issue (9): 1393-1399.doi: 10.3724/SP.J.1006.2018.01393

• RESEARCH PAPERS • Previous Articles     Next Articles

Effect of Exogenous Nitric Oxide Donor on Carbon Assimilation and Antioxidant System in Leaves of Maize Seedlings under PEG-induced Water Deficit Stress

Qing-Hua YANG(),Bo-Yuan ZHENG,Lei-Lei LI,Shuang-Jie JIA,Xin-Pei HAN,Jia-Meng GUO,Yong-Chao WANG,Rui-Xin SHAO()   

  1. College of Agronomy, Henan Agricultural University, Zhengzhou 450046, Henan, China
  • Received:2017-12-22 Accepted:2018-06-12 Online:2018-09-10 Published:2018-07-02
  • Contact: Rui-Xin SHAO E-mail:yangqh2010@163.com;shao_rui_xin@126.com
  • Supported by:
    This study was supported by the National Natural Science Foundation of China (31401304)


The objective of this study was to explore the effect of exogenous nitric oxide (NO) donor (sodium nitroprusside, SNP) on key enzymes of carbon assimilation and antioxidant system of maize leaves under water deficit and its regulation mechanism. In this experiment, 20% PEG-6000 was used to stimulate water deficit stress, exogenous SNP was added into root rhizosphere of seedlings in maize variety Zhuyu 309. After three days of stresses, the changes of Rubisco and RCA activities and their gene level, antioxidase activity and their isoenzyme spectrum level were investigated. The expression levels of rbc L, rbc S, rca β were increased significantly, especially for rbc S that was increased the most by 1.86 fold, which resulted in up-regulation of Rubisco and RCA activities by 32.7% and 14.67% under exogenous SNP plus PEG stress. In addition, SNP enhanced the activity of SOD, POD, CAT, and the width in their isoenzyme spectrum, resulting in significant reduction of ROS accumulation. These results suggested that NO could increase photosynthetic carbon assimilation capacity and antioxidase activity, alleviate the damage of ROS burst on the cell membrane, which enhances PEG-simulated water deficit resistance of maize seedlings.

Key words: exogenous nitric oxide, water deficit, maize seedlings, carbon assimilation, antioxidant system

Table 1

Primers used in this study"

Primer name
Sequence (5'-3')

Fig. 1

Effects of exogenous NO on the Rubisco activity (A) and RCA activity (B) in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

Fig. 2

Effects of exogenous NO on the expression of rbc S (A), rbc L (B), and rca β (C) in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

Fig. 3

Effects of exogenous NO on O2-(A) and H2O2(B) contents in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

Fig. 4

Effects of exogenous NO on SOD activity (A) and SOD isoenzyme (B) in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

Fig. 5

Effects of exogenous NO on POD activity (A) and POD isoenzyme (B) in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

Fig. 6

Effects of exogenous NO on CAT activity (A) and CAT isoenzyme (B) in leaves of maize seedlings under drought stressTreatments including CK, SNP, PEG, and SNP + PEG indicate 0% PEG, 100 μmol L-1 SNP, 20% PEG, and 100 μmol L-1 SNP + 20% PEG, respectively."

[1] 山仑 . 科学应对农业干旱. 干旱地区农业研究, 2011,29(2):1-5
Shan L. To cope rationally with agricultural drought.. Agric Res Arid Areas, 2011 29(2):1-5 (in Chinese with English abstract)
[2] 付凤玲, 阎雨, 刘卫国, 李晚忱 . 玉米海藻糖含量测定及其合成酶(TPS)基因序列分析. 核农学报, 2011,25:1107-1116
Fu F L, Yan Y, Liu W G, Li W Z . Test of trehalose content and sequence analysis of trehalosephosphate synthase gene (TPS) in maize. Acta Agric Nucl Sin, 2011,25:1107-1116 (in Chinese with English abstract)
[3] Pinheiro C, Chaves M M . Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot, 2011,62:869-882
doi: 10.1093/jxb/erq340 pmid: 21172816
[4] 张兴华, 高杰, 杜伟莉, 张仁和, 薛吉全 . 干旱胁迫对玉米品种苗期叶片光合特性的影响. 作物学报, 2015,41:154-159
Zhang X H, Gao J, Du W L, Zhang R H, Xue J Q . Effects of drought stress on photosynthetic characteristics of maize hybrids at seedling stage. Acta Agron Sin, 2015,41:154-159 (in Chinese with English abstract)
[5] Kaiser E, Morales A, Harbinson J, Kromdijk J, Heuvelink E, Marcelis L F . Dynamic photosynthesis in different environmental conditions. J Exp Bot, 2014,66:2415-2426
doi: 10.1093/jxb/eru406 pmid: 25324402
[6] Chew J . I am kneeling on the outside, but I am standing on the inside: another look at the story of naaman through the lenses of Kraft. Asbury J, 2015,70:5
[7] Zhang J, Du H, Chao M, Yin Z, Yang H, Li Y, Huang F, Yu D . Identification of two bZIP transcription factors interacting with the promoter of soybean rubisco activase gene (GmRCAα). Front Plant Sci, 2016,7:628
[8] Cao B, Ma Q, Zhao Q, Wang L, Xu K . Effects of silicon on absorbed light allocation, antioxidant enzymes and ultrastructure of chloroplasts in tomato leaves under simulated drought stress. Sci Hortic, 2015,194:53-62
[9] Gonorazky G, Distéfano A M, García-Mata C, Lamattina L, Laxalt A M. Phospholipases in nitric oxide-mediated plant signaling. In: Phospholipases in Plant Signaling. Signaling and Communication in Plants. Berlin: Springer, 2014. pp 135-158
[10] Khan M N, Mobin M, Mohammad F , Corpas F J, eds. Nitric Oxide Action in Abiotic Stress Responses in Plants.Springer International Publishing, 2015. pp 21-41
[11] 邵瑞鑫, 上官周平 . 外源一氧化氮供体SNP对受旱小麦光合色素含量和PSII光能利用能力的影响. 作物学报, 2008,34:818-822
Shao R X , Shang-Guan Z P. Effects of exogenous nitric oxide donor sodium nitroprusside on photosynthetic pigment content and light use capability of PSII in wheat under water stress. Acta Agron Sin, 2008,34:818-822 (in Chinese with English abstract)
[12] 李利红 . 水杨酸、Ca 2+和 NO 对高温强光胁迫下小麦叶绿体 D1蛋白和PSII功能的调节作用. 河南农业大学博士学位论文, 河南郑州, 2010
Li L H . Regulation of Exogenous Salicylic Acid, Calcium and Nitric Oxide to D1 Protein and Function of Photosystem II in Wheat (Triticum asetinum L.) Leaves under Heat and High Irradiance Stress. PhD Dissertation of Henan Agricultural University, Zhengzhou, Henan, China, 2010 ( in Chinese with English abstract)
[13] Tan J, Zhao H, Hong J, Han Y, Li H, Zhao W . Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline accumulation in wheat seedlings subjected to osmotic stress. World J Agric Sci, 2008,4:307-313
[14] Farooq M Basra S M A, Wahid A, Rehman H. , Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agric Crop Sci, 2009,195:254-261
[15] 施溯筠, 陈翠云 . 外源一氧化氮供体SNP对UV-B辐射下红芸豆叶片中SOD、CAT和POD同工酶的影响. 兰州大学学报(自科科学版), 2009,45(4):78-82
Shi S Y, Chen C Y . Effect of SNP: a NO donor on antioxidative enzymes of bean by UV-B irradiation. J Lanzhou Univ (Nat Sci), 2009,45(4):78-82 (in Chinese with English abstract)
[16] 邵瑞鑫, 李蕾蕾, 郑会芳, 张寄阳, 杨慎娇, 马野, 信龙飞, 苏小雨, 冉午玲, 毛俊, 郑博元, 杨青华 . 外源一氧化氮对干旱胁迫下玉米幼苗光合作用的影响. 中国农业科学, 2016,49:251-259
Shao R X, Li L L, Zheng H F, Zhang J Y, Yang S J, Ma Y, Xin L F, Su X Y, Ran W L, Mao J, Zheng B Y, Yang Q H . Effects of exogenous nitric oxide on photosynthesis of maize seedlings under drought stress. Sci Agric Sin, 2016,49:251-259 (in Chinese with English abstract)
[17] 李忠光, 龚明 . 植物中超氧阴离子自由基测定方法的改进. 云南植物研究, 2005,27:211-216
Li Z G, Gong M . Improvement of measurement method for superoxide anion radical in plant. Acta Bot Yunnan, 2005,27:211-216 (in Chinese with English abstract)
[18] Zhao L, Shi L, Zhao L C, Shi LG . Metabolism of hydrogen peroxide between univoltine and polyvoltine strains of silkworm (Bombyx mori). Comp Biochem Physiol B: Biochem Mol Biol, 2009,152:339-345
[19] 邹琦 . 植物生理学实验指导. 北京: 中国农业出版社, 2001. pp 166-170
Zou Q. Experimental Guide for Plant Physiology. Beijing: China Agriculture Press, 2001.pp 166-170(in Chinese)
[20] 李文鹤 . 干旱胁迫对野菊生理特性的影响. 东北林业大学硕士学位论文, 黑龙江哈尔滨, 2011
Li W H . Effect of Drought Stress on Physiological Characteristics of Dendrathema indicum L. MS Thesis of Northeast Forestry University, Harbin, Heilongjiang,China, 2011 ( in Chinese with English abstract)
[21] 李翔, 桑勤勤, 束胜, 孙锦, 郭世荣 . 外源油菜素内酯对弱光下番茄幼苗光合碳同化关键酶及其基因的影响. 园艺学报, 2016,43:2012-2020
Li X, Sang Q Q, Su S, Sun J, Guo S R . Effects of epibrassinolide on the activities and gene expression of photosynthetic enzymes in tomato seedlings under low light . Acta Hortic Sin, 2016,43:2012-2020 (in Chinese with English abstract)
[22] 徐思 . 利用Rubisco编码基因探究BBCC基因组四倍体的核质互作. 曲阜师范大学硕士学位论文, 山东曲阜, 2015
Xu S . Exploring Nuclear and Cytoplasmic Interaction of BBCC Genome Tetraploid Using Rubisco Coding Gene. MS Thesis of Qufu Normal University Qufu, Shandong, China, 2011 ( in Chinese with English abstract)
[23] Yin Z, Zhang Z, Deng D, Chao M, Gao Q, Wang Y, Yang Z, Bian Y, Hao D, Xu C . Characterization of rubisco activase genes in maize: an α-isoform gene functions alongside a β-isoform gene. Plant Physiol, 2014,4:2096-2106
[24] 王松 . 外源NO对盐胁迫下番茄光合碳同化的影响. 石河子大学硕士学位论文, 新疆石河子, 2016
Wang S . Effect of Exogenous NO on Photosynthetic Carbon Assimilation in Tomato Seedlings under NaCl Stress. MS Thesis of Shihezi University. Shihezi, Xinjiang, China, 2016 ( in Chinese with English abstract)
[25] 闻志彬, 张明理 . 干旱胁迫对2种光合类型C4荒漠植物叶片光合特征酶和抗氧化酶活性的影响. 西北植物学报, 2015,35:1815-1822
Wen Z B, Zhang M L . C4 photosynthetic enzymes and antioxidant enzymes activities in two photosynthetic subtypes of C4 desert plants under soil drought stress. Acta Bot Boreali-Occident Sin, 2015,35:1815-1822 (in Chinese with English abstract)
[26] Fazeli F, Ghorbanli M, Niknam V . Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two sesame cultivars. Biol Plant, 2007,51:98-103
[27] 赵丽英, 邓西平, 山仑 . 活性氧清除系统对干旱胁迫的响应机制. 西北植物学报, 2005,25:413-418
Zhao L Y, Deng X P, Shan L . The response mechanism of active oxygen species removing system to drought stress . Acta Bot Boreali-Occident Sin, 2005,25:413-418 (in Chinese with English abstract)
[28] Choudhury F K, Rivero R M, Blumwald E, Mittler R . Reactive oxygen species, abiotic stress and stress combination. Plant J, 2017,90:856-867
doi: 10.1111/tpj.13299 pmid: 27801967
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