Please wait a minute...
Journal of Integrative Agriculture  2021, Vol. 20 Issue (5): 1216-1228    DOI: 10.1016/S2095-3119(20)63216-6
Special Issue: 麦类耕作栽培合辑Triticeae Crops Physiology · Biochemistry · Cultivation · Tillage
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Changes of oxidative metabolism in the roots of wheat (Triticum aestivum L.) seedlings in response to elevated ammonium concentrations
LIU Yang1, 2*, LI Yu-xiang2*, LI Yi-xiang1, TIAN Zhong-wei1, HU Jin-ling1, Steve ADKINS3, DAI Ting-bo1
1 Key Laboratory of Crop Physiology and Ecology in Southern China/College of Agriculture, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 College of Agriculture, Shihezi University, Shihezi 823003, P.R.China
3 School of Agriculture and Food Sciences, the University of Queensland, Gatton QLD 4343, Australia
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

试验采用温室水培的方式,以豫麦49(高铵迟钝型)和鲁麦15(高铵敏感型)为材料,设置了5.0 mM NH4+-N(EAC)和NO3--N(CON)两个处理,研究了小麦幼苗根系氧化代谢对高铵胁迫的响应机制。结果表明,高铵胁迫下,两个小麦品种根系生长显著降低,其中鲁麦15降低程度高于豫麦49。高铵胁迫增加了两个小麦品种根系单脱氢抗坏血酸还原酶活性和脱氢抗坏血酸还原酶活性,但降低了处理12天后的根系抗坏血酸(ASA)含量和GDP-甘露糖焦磷酸酶(GMPase)活性,其中鲁麦15根系ASA含量和GMPase活性分别降低了62.0和71.4%,豫麦49根系ASA含量和GMPase活性分别降低了38.8和62.2%,说明高铵胁迫提高了ASA再生,但减少了ASA合成。此外,EAC增加了两个小麦品种根系DHA/ASA,活性氧(ROS)含量,丙二醛含量和抗氧化物酶活性。与豫麦49相比,鲁麦15根系中ROS含量和可溶性糖含量相对增加较多,而抗氧化物酶活性增加较少,说明鲁麦15根系氧化代谢紊乱更严重。结果表明,高铵胁迫下,GMPase活性降低导致ASA生物合成的减少可能是ROS过量积累和氧化还原失衡的原因之一,进而抑制小麦幼苗根系生长。与高铵敏感型品种鲁麦15相比,豫麦49具有较强的氧化胁迫保护能力,维持较低水平DHA/ASA,进而保持较好的氧化还原平衡状态,因此更耐高铵。




Abstract  
To elucidate the response of oxidative metabolism, triggered by elevated ammonium (NH4+) concentrations, on root growth of wheat seedlings, Yumai 49 (NH4+-tolerant) and Lumai 15 (NH4+-sensitive) cultivars were supplied with either 5.0 mmol L–1 NH4+-N (EAC) or 5.0 mmol L–1 NO3-N (CON) under hydroponic conditions.  Root growth in both cultivars was significantly reduced under EAC, and the negative effect was greater in Lumai 15.  EAC enhanced the activities of monodehydroascorbate reductase and dehydroascorbate reductase in the roots of both cultivars, while it decreased ascorbic acid (ASA) content and GDP-mannose pyrophosphorylase (GMPase) activity at the 12th day after treatment in Lumai 15 by 62.0 and 71.4%; and in Yumai 49 by 38.8 and 62.2%, respectively, indicating that the regeneration of ASA was increased, but the biosynthesis of ASA was reduced under EAC treatment.  Moreover, EAC increased DHA/ASA, reactive oxygen species (ROS), and malondialdehyde contents, as well as antioxidant enzyme activities in the roots of both cultivars.  Relatively greater increases in ROS and soluble sugar, and lower antioxidant enzyme activities in Lumai 15 indicate severe disruption of oxidative metabolism when compared to Yumai 49.  Results reveal that the reduction of ASA biosynthesis via decreased GMPase activity under the EAC condition probably acts as a trigger for accumulated ROS and imbalanced redox status, resulting in root growth inhibition during wheat seedling growth stage.  Yumai 49, being an NH4+-tolerant cultivar, had the stronger capacity to protect itself from oxidative stress, which allowed it to retain a lower DHA to ASA ratio by maintaining a better redox homeostasis than could be maintained in the NH4+-sensitive cultivar Lumai 15.
Keywords:  elevated ammonium concentrations        oxidative metabolism        redox homeostasis        root morphology        wheat  
Received: 11 November 2019   Accepted:
Fund: This study was funded by a project of the National Natural Science Foundation of China (31471443), the Jiangsu Collaborative Innovation Center for Modern Crop Production, China (JCIC-MCP) and the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD).
Corresponding Authors:  Correspondence DAI Ting-bo, Tel: +86-25-84396466, E-mail: tingbod@njau.edu.cn    
About author:  * These authors contributed equally to this study.

Cite this article: 

LIU Yang, LI Yu-xiang, LI Yi-xiang, TIAN Zhong-wei, HU Jin-ling, Steve ADKINS, DAI Ting-bo. 2021. Changes of oxidative metabolism in the roots of wheat (Triticum aestivum L.) seedlings in response to elevated ammonium concentrations. Journal of Integrative Agriculture, 20(5): 1216-1228.


Barrameda-Medina Y, Montesinos-Pereira D, Romero L, Blasco B, Ruiz J M. 2014. Role of GSH homeostasis under Zn toxicity in plants with different Zn tolerance. Plant Science, 227, 110–121.
Barth C, Gouzd Z A, Steele H P, Imperio R M. 2010. A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. Journal of Experimental Botany, 61, 379–394.
Bittsánszky A, Pilinszky K, Gyulai G, Komives T. 2015. Overcoming ammonium toxicity. Plant Science, 231, 184–190.
Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.
Britto D T, Kronzucker H J. 2002. Review NH4+ toxicity in higher plants: A critical review. Journal of Plant Physiology, 584, 567–584.
Conklin P L, Norris S R, Wheeler G L, Williams E H, Smirnoff N, Last R L. 1999. Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C ) biosynthesis. Proceedings of the National Academy of Sciences of United States of America, 96, 4198–4203.
Conklin P L, Pallanca E, Last R, Smirnoff N. 1997. L-Ascorbic acid metabolism in the ascorbate-deficient Arabidopsis mutant vtc1. Plant Physiology, 115, 1277–1285.
Domínguez-Valdivia M D, Aparicio-Tejo P M, Lamsfus C, Cruz C, Maria A M, Moran J F. 2008. Nitrogen nutrition and antioxidant metabolism in ammonium-tolerant and -sensitive plants. Physiologia Plantarum, 132, 359–369.
Doulis A G, Debian N, Kingston-Smith A H, Foyer C H. 1997. Differential localization of antioxidants in maize leaves. Plant Physiology, 114, 1031–1037.
Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N. 2007. Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. The Plant Journal, 52, 673–689.
Fales F W. 1951. The assimilation and degradation of carbohydrates by yeast cells. Journal of Biological Chemistry, 193, 113–124.
Fotopoulos V, Kanellis A K. 2013. Altered apoplastic ascorbate redox state in tobacco plants via ascorbate oxidase overexpression results in delayed dark-induced senescence in detached leaves. Plant Physiology Biochemistry, 73, 154–160.
Hossain M A, Nakano Y, Asada K. 1984. Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant and Cell Physiology, 25, 385–395.
Leleu O, Vuylsteker C, Sn Ã, Sciences Â. 2004. Unusual regulatory nitrate reductase activity in cotyledons of Brassica napus seedlings: Enhancement of nitrate reductase activity by ammonium supply. Journal of Experimental Botany, 55, 815–823.
Li B H, Li G J, Kronzucker J H, Baluška F, Shi W M. 2014. Ammonium stress in Arabidopsis: Signaling, genetic loci, and physiological targets. Trends in Plant Science, 19, 107–114.
Li G J, Li B H, Dong G Q, Feng X Y, Kronzucker H J, Shi W M. 2013. Ammonium-induced shoot ethylene production is associated with the inhibition of lateral root formation in Arabidopsis. Journal of Experimental Botany, 64, 1413–1425.
Li Q, Li B H, Kronzucker H J, Shi W M. 2010. Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity. Plant Cell and Environment, 33, 1529–1542.
Li S, Di D W, Kronzucker H J, Shi W M. 2017. Spatio-temporal dynamics in global rice gene expression (Oryza sativa L.) in response to high ammonium stress. Journal of Plant Physiology, 212, 94–104.
Lin L L, Shi Q H, Wang H S, Qin A G, Yu X C. 2011. Over-expression of tomato gdp-mannose pyrophosphorylase (GMPase) in potato increases ascorbate content and delays plant senescence. Agricultural Sciences in China, 10, 534–543.
Liu X, Zhang Y, Han W, Tang A, Shen J L , Cui Z L, Vitousek P, Erisman J W, Goulding K, Christie P, Fangmeier A, Zhang F S. 2013. Enhanced nitrogen deposition over China. Nature, 494, 459–462.
Liu Y, Sun J Y, Tian Z W, Hakeem A, Wang F, Steve A, Dong J, Dai T B. 2017. Physiological responses of wheat (Triticum aestivum L.) germination to elevated ammonium concentrations: Reserve mobilization, sugar utilization, and antioxidant metabolism. Plant Growth Regulation, 81, 209–220.
Moore S, Stein W. 1954. A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. Journal of Biological Chemistry, 211, 907–913.
Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson A G, Escobar M A. 2010. Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell and Environment, 33, 1486–1501.
Pinto M C, Francis D, Gara L D. 1999. The redox state of the ascorbate dehydroascorbate pair as aspeci?c sensor of cell division in tobacco BY-2 cells. Protoplasma, 209, 90–97.
Polesskaya O G, Kashirina E I, Alekhina N D. 2004. Changes in the activity of antioxidant enzymes in wheat leaves and roots as a function of nitrogen source and supply. Russian Journal of Plant Physiology, 51, 615–620.
Potters G, Horemans N,Bellone S, Caubergs R L. 2004. Dehydroascorbate in?uences the plant cell cycle through a glutathioneindependent reduction mechanism. Plant Physiology, 134, 1479–1487.
Qin C, Qian W Q, Wang W F, Wu Y, Yu C M, Jiang X H, Wang D W, Wu P. 2008. GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of United States of America, 105, 18308–18313.
Raquel E, Idoia A, Cristina C, eMoran J F. 2016. Review: Mechanisms of ammonium toxicity and the quest for tolerance. Plant Science, 248, 92–101.
Sakihama Y, Cohen M F, Grace S C, Yamasaki H. 2002. Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology, 177, 67–80.
Skopelitis D S, Paranychianakis N V, Paschalidis K A, Pilakonis E D, Delis I D, Yakoumakis D I, Kouvarakis A, Papadakis A, Sephanou E G, Roubelakis-Angelakis K A. 2006. Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. The Plant Cell, 18, 2767–2781.
Szumilo T, Darke R R, York J L, Elbein A D. 1993. GDP-Mannose pyrophosphorylase purification to homogenety, properties, and utilization to prepare photoaffiniy analogs. The Journal of Biological and Chemistry, 268, 17943–17950.
Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D. 2008. Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica, 46, 21–27.
Tanaka H, Maruta T, Ogawa T, Tanabe N, Tamoi M, Yoshimura K, Shigeoka S. 2015. Identification and characterization of Arabidopsis AtNUDX9 as a GDP-d-mannose pyrophosphohydrolase: Its involvement in root growth inhibition in response to ammonium. Journal of Experimental Botany, 66, 5797–5808.
Truffault V, Gest N, Garchery C, Florian A, Fernie A R, Gautier H, Stevens R. 2016. Reduction of MDHAR activity in cherry tomato suppresses growth and yield and MDHAR activity is correlated with sugar levels under high light. Plant Cell and Environment, 39, 1279–1292.
Wang C, Zhang S H, Wang P F, Li w, Lu J. 2010. Effects of ammonium on the antioxidative response in Hydrilla verticillata (L.f.) Royle plants. Ecotoxicology and Environmental Safety, 73, 189–195.
Wang F, Gao J W, Shi S M, He X H, Dai T B. 2019. Impaired electron transfer accounts for the photosynthesis inhibition in wheat seedlings (Triticum aestivum L.) subjected to ammonium stress. Physiologia Plantarum, 167, 159–172.
Wang F, Gao J W, Tian Z W, Liu Y, Abid M, Jiang D, Cao W X, Dai T B. 2016. Adaptation to rhizosphere acidification is a necessary prerequisite for wheat (Triticum asetivum L.) seelding resistance to ammonium stress. Plant Physiology and Biochemistry, 108, 447–455.
Wang H S, Zhu Z J, Feng Z, Zhang S G, Yu C. 2012. Antisense-mediated depletion of GMPase gene expression in tobacco decreases plant tolerance to temperature stresses and alters plant development. Molecular Biology Reports, 39, 10413–10420.
Wang W G, Li R, Zhu Q, Tang X Y, Zhao Q. 2016. Transcriptomic and physiological analysis of common duckweed Lemna minor responses to NH4+ toxicity. BMC Plant Biology, 16, 92.
Wang X. 2006. Principle and Techniques of Plant Physiological Biochemical Experiment. 2nd ed. Higher Education Press, Beijing, China. (in Chinese)
Xie Y, Mao Y, Zhou H, Duan X L, Cui W T, Zhang J, Xu G H. 2014. Heme-heme oxygenase 1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa. Plant Cell and Environment, 38, 129–143.
Zhang J X, Kirkham M B. 1996. Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytologist, 132, 361–373.
Zhang Y Y, Li H X, Shu W B, Zhang W, Ye Z B. 2011. Suppressed expression of ascorbate oxidase gene promotes ascorbic acid accumulation in tomato fruit. Plant Molecular Biology Reports, 29, 638–645.
[1] Changqin Yang, Xiaojing Wang, Jianan Li, Guowei Zhang, Hongmei Shu, Wei Hu, Huanyong Han, Ruixian Liu, Zichun Guo.

Straw return increases crop production by improving soil organic carbon sequestration and soil aggregation in a long-term wheat–cotton cropping system [J]. >Journal of Integrative Agriculture, 2024, 23(2): 669-679.

[2] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[3] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
[4] ZHANG Guang-xin, ZHAO De-hao, FAN Heng-zhi, LIU Shi-ju, LIAO Yun-cheng, HAN Juan. Combining controlled-release urea and normal urea with appropriate nitrogen application rate to reduce wheat stem lodging risk and increase grain yield and yield stability[J]. >Journal of Integrative Agriculture, 2023, 22(10): 3006-3021.
[5] HUANG Feng, LI Xuan-shuang, DU Xiao-yu, LI Shun-cheng, LI Nan-nan, LÜ Yong-jun, ZOU Shao-kui, ZHANG Qian, WANG Li-na, NI Zhong-fu, HAN Yu-lin, XING Jie-wen. SNP-based identification of QTLs for thousand-grain weight and related traits in wheat 8762/Keyi 5214 DH lines[J]. >Journal of Integrative Agriculture, 2023, 22(10): 2949-2960.
[6] LI Si-ping, ZENG Lu-sheng, SU Zhong-liang. Wheat growth, photosynthesis and physiological characteristics under different soil Zn levels[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1927-1940.
[7] ZHANG Hai-feng, Tofazzal ISLAM, LIU Wen-de. Integrated pest management programme for cereal blast fungus Magnaporthe oryza[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3420-3433.
[8] ZHAO Lai-bin, XIE Die, HUANG Lei, ZHANG Shu-jie, LUO Jiang-tao, JIANG Bo, NING Shun-zong, ZHANG Lian-quan, YUAN Zhong-wei, WANG Ji-rui, ZHENG You-liang, LIU Deng-cai, HAO Ming. Integrating the physical and genetic map of bread wheat facilitates the detection of chromosomal rearrangements[J]. >Journal of Integrative Agriculture, 2021, 20(9): 2333-2342.
[9] SHAO Ze-qiang, ZHENG Cong-cong, Johannes A. POSTMA, LU Wen-long, GAO Qiang, GAO Ying-zhi, ZHANG Jin-jing. Nitrogen acquisition, fixation and transfer in maize/alfalfa intercrops are increased through root contact and morphological responses to interspecies competition[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2240-2254.
[10] LI Si-nan, CHEN Wen, MA Xin-yao, TIAN Xia-xia, LIU Yao, HUANG Li-li, KANG Zhen-sheng, ZHAO Jie. Identification of eight Berberis species from the Yunnan-Guizhou plateau as aecial hosts for Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1563-1569.
[11] LIU Hang, TANG Hua-ping, LUO Wei, MU Yang, JIANG Qian-tao, LIU Ya-xi, CHEN Guo-yue, WANG Ji-rui, ZHENG Zhi, QI Peng-fei, JIANG Yun-feng, CUI Fa, SONG Yin-ming, YAN Gui-jun, WEI Yuming, LAN Xiu-jin, ZHENG You-liang, MA Jian. Genetic dissection of wheat uppermost-internode diameter and its association with agronomic traits in five recombinant inbred line populations at various field environments[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2849-2861.
[12] LIU Da-zhong, YANG Fei-fei, LIU Sheng-ping. Estimating wheat fractional vegetation cover using a density peak k-means algorithm based on hyperspectral image data[J]. >Journal of Integrative Agriculture, 2021, 20(11): 2880-2891.
[13] XIAO Jing-xiu, ZHU Ying-an, BAI Wen-lian, LIU Zhen-yang, TANG Li, ZHENG Yi. Yield performance and optimal nitrogen and phosphorus application rates in wheat and faba bean intercropping[J]. >Journal of Integrative Agriculture, 2021, 20(11): 3012-3025.
[14] PAN Li-jun, LU Lin, LIU Yu-ping, WEN Sheng-xian, ZHANG Zeng-yan. The M43 domain-containing metalloprotease RcMEP1 in Rhizoctonia cerealis is a pathogenicity factor during the fungus infection to wheat[J]. >Journal of Integrative Agriculture, 2020, 19(8): 2044-2055.
[15] ZHOU Chun-yun, XIONG Hong-chun, LI Yu-ting, GUO Hui-jun, XIE Yong-dun, ZHAO Lin-shu, GU Jiayu, ZHAO Shi-rong, DING Yu-ping, SONG Xi-yun, LIU Lu-xiang. Genetic analysis and QTL mapping of a novel reduced height gene in common wheat (Triticum aestivum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1721-1730.
No Suggested Reading articles found!