Effects of nitric oxide and hydrogen peroxide on induction of a defense response in the root tips and root border cells of soybean plants to Al toxicity

doi:10.3724/SP.J.1258.2011.00981

Abstract

Abstract:

Aims Nitric oxide (NO) and hydrogen peroxide (H₂O₂) function as signaling molecules in plants. A role for NO and H₂O₂in the regulation of many abiotic stress responses, including drought, salt, heat, heavy metal and Al stresses, has been proposed. Our objective was to investigate (a) the Al-dependent accumulation of endogenous NO and H₂O₂ in root tips and (b) the role of exogenous NO and H₂O₂ in alleviating Al toxicity in root tips and root border cells (RBCs).
Methods Seedlings of soybean (Glycine max) ‘Zhechun No. 3’ were divided into two groups for hydroponic and aeroponic cultured experiments. In order to investigate the response of endogenous NO and H₂O₂ in root tips to 50 μmol·L^-1Al, we determined root elongation, Al content in root apexes, endogenous NO and H₂O₂ content and their location in hydroponic cultured experiments. In the aeroponic culture experiments, seedlings were pretreated with exogenous NO and H₂O₂, then RBCs viability as well as the indicators in hydroponic cultured experiments were tested to clarify the role of exogenous NO and H₂O₂ on alleviating Al toxicity in root tips and RBCs.
Important findings Al inhibited root elongation, increased Al content in root apexes and induced endogenous NO and H₂O₂ accumulation with the hydroponic culture. Results of the aeroponic experiments demonstrated that both 0.25 mmol·L^-1NO donor sodium nitroprusside (SNP) and 0.1 mmol·L^-1 H₂O₂ alleviated the inhibitory effect of Al, decreased Al accumulation in root tips and enhanced RBCs viability. The 0.05 mmol·L^-1 NO scavenger cPTIO (carboxy-PTIO) and 150 U·mL^-1 H₂O₂ scavenger CAT (catalase) reversed the alleviating effect. Furthermore, the results indicated that exogenous NO promoted the accumulation of H₂O₂ in root apexes, while exogenous H₂O₂ did not significantly affect NO content in root apexes. All of these results suggested that the rise of NO and H₂O₂were in accordance with defense response in root apexes and RBCs to Al toxicity in soybean, and the increase of NO may regulate the H₂O₂ production to protect soybean from Al toxicity.

Key words: Al toxicity, hydrogen peroxide, nitric oxide, root apex, root border cells, soybean

WANG Fang-Mei, CAI Miao-Zhen, ZHANG Shu-Na, WANG Ning, LI Hua-Fei, HU Xue-Na, YU Shu-Hang. Effects of nitric oxide and hydrogen peroxide on induction of a defense response in the root tips and root border cells of soybean plants to Al toxicity[J]. Chin J Plant Ecol, 2011, 35(9): 981-989.

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URL: https://www.plant-ecology.com/EN/10.3724/SP.J.1258.2011.00981

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Figures/Tables 8

Fig. 1 Time-dependent effects of Al toxicity on root elongation of soybean (mean ± SE). Different small letters mean significant differences (p < 0.05).

Fig. 2 Effects of Al toxicity on Al content in soybean root apex (mean ± SE). Different small letters mean significant differences (p < 0.05).

Fig. 3 Effects of Al toxicity on endogenous NO and H2O2 contents in soybean root apex (mean ± SE). Different small letters mean significant differences (p < 0.05).

Fig. 4 The in situ observation of NO and H2O2 accumulation in root apex of soybean under Al toxicity. A, B, the in situ observation of NO accumulation (A, -Al; B, Al). C, D, the in situ observation of H2O2 accumulation (C, -Al; D, Al).

Fig. 5 Effects of NO and H2O2 on relative root elongation in soybean under Al toxicity (mean ± SE). A, NO. B, H2O2. CAT, catalase; cPTIO, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyllimidazoline-1-oxyl-3-oxyde, potassium salt; SNP, sodium nitroprusside. Different small letters mean significant differences (p < 0.05).

Fig. 6 Effects of NO and H2O2 on Al content in root apex of soybean under Al toxicity (mean ± SE). A, NO. B, H2O2. CAT, catalase; cPTIO, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyllimidazoline-1-oxyl-3-oxyde, potassium salt; SNP, sodium nitroprusside. Different small letters mean significant differences (p < 0.05).

Fig. 7 Effects of NO and H2O2 on root border cells (RBCs) viability in root apex of soybean under Al toxicity(mean ± SE). A, NO. B, H2O2. CAT, catalase; cPTIO, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyllimidazoline-1-oxyl-3-oxyde, potassium salt; SNP, sodium nitroprusside. Different small letters mean significant differences (p < 0.05).

Fig. 8 Effects of exogenous NO and H2O2 contents in root apex of soybean under Al toxicity (mean ± SE). A, NO. B, H2O2. CAT, catalase; cPTIO, 2-(4-carboxyphenyl)-4,4,5,5-tetramethyllimidazoline-1-oxyl-3-oxyde, potassium salt; SNP, sodium nitroprusside. Different small letters mean significant differences (p < 0.05).

References 36

[1]	Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ (2000). NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. The Plant Journal, 24, 667-677. URL PMID
[2]	Delhaize E, Ryan PR (1995). Aluminum toxicity and tolerance in plants. Plant Physiology, 107, 315-321. URL PMID
[3]	Delledonne M, Zeier J, Marocco A, Lamb C (2001). Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proceedings of the National Academy of Sciences of the United States of America, 98, 13454-13459. DOI URL PMID
[4]	Fan B, Shen L, Liu KL, Zhao DY, Yu MM, Sheng JP (2008). Interaction between nitric oxide and hydrogen peroxide in postharvest tomato resistance response to Rhizopus nigricans. Journal of the Science of Food and Agriculture, 88, 1238-1244. DOI URL
[5]	Hawes MC, Gunawardena U, Miyasaka S, Zhao XW (2000). The role of root border cells in plant defense. Trends in Plant Science, 5, 128-133. DOI URL PMID
[6]	Horst WJ, Wang YX, Eticha D (2010). The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Annals of Botany, 106, 185-197. URL PMID
[7]	Jia ZQ ( 贾芝琪), Yuan HY ( 袁海永), Li YZ ( 李颖章) (2007). Effects of Verticillium dahliae toxin on the NO and H₂O₂ production and the GST gene expression in cotton suspension cells. Chinese Science Bulletin (科学通报), 52, 911-917. (in Chinese)
[8]	Kawai K (1980). The relationship of phosphorus adsorption to amorphous aluminum for characterizing andosols. Soil Science, 129, 186-190. DOI URL
[9]	Kovtun Y, Chiu WL, Tnea G, Sheen J (2000). Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences of the United States of America, 97, 2940-2945. URL PMID
[10]	Li G ( 李刚), Xu FJ ( 徐芳杰), Jiang SS ( 蒋思丝), Zhang YS ( 章永松), Lin XY ( 林咸永) (2010). Effects of aluminum on hydrogen peroxide content and cell wall-bound peroxidase activity in wheat root tips. Plant Nutrition and Fertilizer Science (植物营养与肥料学报), 16, 887-892. (in Chinese with English abstract) DOI URL
[11]	Li RF ( 李荣峰), Cai MZ ( 蔡妙珍), Liu P ( 刘鹏), Xu GD ( 徐根娣), Chen MY ( 陈敏燕), Liang H ( 梁和) (2008). Phytoecological effect of Al ³+ on the inductivity of programmed cell death of border cells in soybean root. Journal of Plant Ecology (Chinese Version)(植物生态学报), 32, 690-697. (in Chinese with English abstract)
[12]	Li ZG ( 李忠光), Song YQ ( 宋玉泉), Long M ( 垄明) (2007). Xylenol orange method used for the measurement of hydrogen peroxide in plant tissue. Journal of Yunnan Normal University (Natural Sciences Edition) (云南师范大学学报(自然科学版)), 27, 50-54. (in Chinese with English abstract)
[13]	Ma JF (2007). Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. International Review of Cytology, 264, 225-252. URL PMID
[14]	Mittle R, Vanderauwera S, Gollery M, Breusegem FV (2004). Reactive oxygen gene network in plants. Trends in Plant Science, 9, 490-498. DOI URL PMID
[15]	Miyasaka SC, Hawes MC (2001). Possible role of root border cells in detection and avoidance of aluminum toxicity. Plant Physiology, 125, 1978-1987. URL PMID
[16]	Murphy ME, Noack E (1994). Nitric oxide assay using hemoglobin method. Methods in Enzymology, 233, 240-250. URL PMID
[17]	Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002). Hydrogen peroxide and nitric oxide as signaling molecules in plants. Journal of Experimental Botany, 53, 1237-1247. URL PMID
[18]	Orozco-Cárdenas ML, Ryan CA (2002). Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiology, 130, 487-493. URL PMID
[19]	Pan JW, Zhu MY, Chen H (2001). Aluminium-induced cell death in root-tip cells of barley. Environmental and Experimental Botany, 46, 71-79. DOI URL PMID
[20]	Pan JW, Zhu MY, Chen H, Han N (2002). Inhibition of cell growth caused by aluminum toxicity results from aluminum-induced cell death in barley suspension cells. Journal of Plant Nutrition, 25, 1063-1073.
[21]	Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003). Nitric oxide-mediated transcrip- tional changes in Arabidopsis thaliana. Molecular Plantmicrobe Interactions, 16, 1094-1105.
[22]	Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río LA, Sandalio LM (2006). Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant, Cell & Environment, 29, 1532-1544. URL PMID
[23]	Tada Y, Mori T, Shinogi T, Yao N, Takahashi S, Betsuyaku S, Sakamoto M, Park P, Nakayashiki H, Tosa Y, Mayama S (2004). Nitric oxide and reactive oxygen species do not elicit hypersensitive cell death but induce apoptosis in the adjacent cells during the defense response of oat. Molecular Plant-Microbe Interactions, 17, 245-253. DOI URL PMID
[24]	Tamás L, Budíková S, Huttová J, Mistrík I, Šimomovičová M, Široká B (2005). Aluminum-induced cell death of barley- root border cells is correlated with peroxidase- and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Reports, 24, 189-194. URL PMID
[25]	Tian QY, Sun DH, Zhao MG, Zhang WH (2007). Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytologist, 174, 322-331.
[26]	Wang HH, Huang JJ, Bi YR (2010). Nitrate reductase- dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Science, 179, 281-288. DOI URL
[27]	Wang J, Higgins VJ (2006). Nitric oxide modulates H₂O₂- mediated defenses in the Colletotrichum coccodes-tomato interaction. Physiological and Molecular Plant Pathology, 67, 131-137.
[28]	Wang YS, Yang ZM (2005). Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant and Cell Physiology, 46, 1915-1923. DOI URL PMID
[29]	Xu MJ ( 徐茂军), Dong JF ( 董菊芳), Zhang XB ( 张新波) (2008). The signal interactions of NO and H₂O₂ in mediating heat shock induced Hypericum monogynum cell synthesis hypericin. Science China (中国科学), 38, 643-653. (in Chinese)
[30]	Xue YJ, Tao L, Yang ZM (2008). Aluminum-induced cell wall peroxidase activity and lignin synthesis are differentially regulated by jasmonate and nitric oxide. Journal of Agricultural and Food Chemistry, 56, 9676-9684. URL PMID
[31]	Yang JL ( 杨建立), He YF ( 何云峰), Zheng SJ ( 郑绍建) (2005). Research progresses in aluminum tolerance mechanisms in plants. Plant Nutrition and Fertilizer Science (植物营养与肥料学报), 11, 836-845. (in Chinese with English abstract) DOI URL
[32]	Yu M, Shen RF, Liu JY, Chen RF, Xu MM, Yang Y, Xiao HD, Wang HZ, Wang HY, Wang CQ (2009). The role of root border cells in aluminum resistance of pea (Pisum sativum) grown in mist culture. Journal of Plant Nutrition and Soil Science, 172, 528-534.
[33]	Yu YH ( 禹艳红), Bin JH ( 宾金华) (2002). The occurrence and biological function of root border cells. Chinese Bulletin of Botany (植物学通报), 19, 756-762. (in Chinese with English abstract)
[34]	Zhang F, Wang YP, Wang D (2007). Role of nitric oxide and hydrogen peroxide during the salt resistance response. Plant Signalling & Behavior, 2, 473-474.
[35]	Zhang WL ( 张文利), Shen WB ( 沈文飚), Ye MB ( 叶茂炳), Xu LC ( 徐朗菜) (2002). Sensitivity of wheat leaf aconitase to nitric oxide and hydrogen peroxide. Journal of Plant Physiology and Molecular Biology (植物生理与分子生物学学报), 28, 99-104. (in Chinese Chinese with English abstract)
[36]	Zhao MG, Tian QY, Zhang WH (2007). Nitric oxide synthase- dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology, 144, 206-217. URL PMID