Scientia Agricultura Sinica ›› 2016, Vol. 49 ›› Issue (11): 2222-2233.doi: 10.3864/j.issn.0578-1752.2016.11.018

• RESEARCH NOTES • Previous Articles     Next Articles

Effect of Sulphur Availability on Nitrate Accumulation and Expression of Nitrogen and Sulphur Assimilation Related Genes in Non-Heading Chinese Cabbage

XU Yao, MU Jian-mei, ZHANG Guo-qin, MA Jia-jia, XU Jun, LI Jun, LIU Feng-jun, SHE Xu-dong   

  1. Institute of Agricultural Sciences in Taihu Lake District, Suzhou 215155, Jiangsu
  • Received:2015-11-16 Online:2016-06-01 Published:2016-06-01

Abstract: 【Objective】The objective of this paper is to identify the best sulfate to reduce nitrate accumulation in non-heading Chinese cabbage, and analyze the key genes involved in nitrogen and sulphur assimilation. The results of this study will provide new insights into sulphur fertilization and investigation of the molecular mechanisms of nitrate accumulation with the goal of molecular breeding.【Method】Nitrate content of non-heading Chinese cabbage leaves and petioles were measured under treatments of 4 forms of sulphur with 3 concentrations. The expression of 30 nitrogen and sulphur assimilation related genes were analyzed by semi-quantitative RT-PCR. 【Result】Sulphur treatments were significantly increased the aboveground biomass of non-heading Chinese cabbage, and the treatments of Na2SO4 had the best effect, and 30 mg·kg-1 Na2SO4 was the most effective treatment as the aboveground biomass increased by 49.76% compared with the control. Na2SO4 and Na2S2O3 reduced nitrate content of non-heading Chinese cabbage more significantly than others. Na2SO4 decreased nitrate content by 12.23%-23.55% in leaves and by 33.08%-41.98% in petioles compared with the control, and it was also found a positive correlation between the reduction and concentration of Na2SO4, and 30 mg·kg-1 Na2SO4 also had the best effect. Na2S2O3 decreased nitrate content by 15.34%-33.08% compared with the control in leaves and by 11.95%-19.68% in petioles. Sulphur promoted nitrogen assimilation, and the expression of NR-1, NADH-GOGAT-1, NADH-GOGAT-2, Cytoplasm-GS-4, Cytoplasm-GS-5, and GDH-3 were higher than the control in leaves, and the expression of NR-1, NADH-GOGAT-2, Cytoplasm-GS-1, and GDH-2 were higher than the control in petioles. The expression of NADH-GOGAT-2 was correlated with nitrate levels. Sulphur treatments also had an effect on sulphur assimilation genes, and the expressions of ATPS-2, ATPS-3, ATPS-4, APSR-3, SIR, SAT1.1, and SAT2.1 were higher than the control in leaves, and only the expressions of SIR and OASTL-A were higher than the control in petioles. 【Conclusion】 Na2SO4 had the best effect in reducing nitrate content and increasing yield of non-heading Chinese cabbage, and 30 mg·kg-1 Na2SO4 was the most effective treatment. The expression of NADH-GOGAT-2 was correlated with nitrate levels. The data suggested that NADH-GOGAT-2 may be the key gene in nitrogen assimilation.

Key words: non-heading Chinese cabbage, sulphur, nitrate, nitrogen and sulphur assimilation, gene expression

[1]    谢国祥, 郭宝福, 赵士权, 王艳莉, 陈辉. 南京市市售蔬菜硝酸盐含量及居民暴露量评估. 现代预防医学, 2013, 40(7): 1236-1238.
Xiu G Q, Guo F B, Zhao S Q, Wang Y L, Chen H. The nitrate contents in commercial vegetables and assessment of nitrate exposure in Nanjing residents. Modern Preventive Medicine, 2013, 40(7): 1236-1238. (in Chinese)
[2]    郭开秀, 姚春霞, 陈亦, 杨业凤, 陆利民. 上海市秋季蔬菜硝酸盐含量及风险摄入评估. 环境科学, 2011, 32(4): 1177-1181.
Guo K X, Yao C X, Chen Y, Yang Y F, Lu L M. Nitrate contents in autumn vegetables and assessment of nitrate intake in Shanghai. Environmental Science, 2011, 32(4): 1177-1181. (in Chinese)
[3]    Koprivova A, Suter M, Opden C R, Brunold C, Kopriva S. Regulation of sulfate assimilation by nitrogen in Arabidopsis. Plant Physiology, 2000, 122: 737-746.
[4]    Mario G, John A R. Nitrogen and sulfur assimilation in plants and algae. Aquatic Botany, 2014, 118: 45-61.
[5]    Hoefgen R, Nikiforova V. Metabolomics integrated with transcriptomics: assessing systems response to sulfur-de?ciency stress. Plant Physiology, 2008, 132: 190-198.
[6]    Carfagna S, Vona V, Di Martino V, Esposito S, Rigano C. Nitrogen assimilation and cysteine biosynthesis in barley: evidence for root sulphur assimilation upon recovery from N deprivation. Environmental and Experimental Botany, 2011, 71: 18-24.
[7]    Donna M K, Joshua N, Nancy L E, Timothy J T, David E G. Nitrogen and sulfur requirements for Clostridium thermocellum and Caldicellulosiruptor bescii on cellulosic substrates in minimal nutrient media. Bioresource Technology, 2013, 130: 125-135.
[8]    Hesse H, Nikiforova V, Gakiere B, Hoefge R. Molecular analysis and control of cysteine biosynthesis, integration of nitrogen and sulphur metabolism. Journal of Experimental Botany, 2004, 55: 1283-1292.
[9]    Imamura S, Terashita M, Ohnuma M, Maruyama S, Minoda A, Weber A P M, Inouye T, Sekine Y, Fujita Y, Omata T, Tanaka K. Nitrate assimilatory genes and their transcriptional regulation in a unicellular red alga Cyanidioschyzon merolae: genetic evidence for nitrite reduction by a sul?te reductase- like enzyme. Plant Cell Physiology, 2010, 51(5): 707-717.
[10]   Aleksandra K, Peter B, Elisabeth E S, Freek S P, Stanislav K, Malcolm J H, Luit J D K. Expression and activity of sulfate transporters and APS reductase in curly kale in response to sulfate deprivation and re-supply. Journal of Plant Physiology, 2009, 166: 168-179.
[11]   Zhang Q, Bok-Rye L, Sang-Hyun P, Rashed Z, Jean-Christophe A, Alain O, Tae-Hwan K. Sulfate resupply accentuates protein synthesis in coordination with nitrogen metabolism in sulfur deprived Brassica napus. Plant Physiology and Biochemistry, 2015, 87: 1-8.
[12]   Muhammad S, Mei H T, Elisabeth E S, Aleksandra K, Freek S, Posthumus, Jan H V, Saroj P, Henk S, Malcolm J H, Luit J D K. Copper exposure interferes with the regulation of the uptake, distribution and metabolism of sulfate in Chinese cabbage. Journal of Plant Physiology, 2010, 167: 438-446.
[13]   Abdallaha M, Etienne P, Ourry A, Meuriot F. Do initial S reserves and mineral S availability alter leaf S-N mobilization and leaf senescence in oilseed rape? Plant Science, 2011, 180: 511-520.
[14]   Anne H, Mikiko K, Richard H, Wolfgang F, Hitoshi S, Cornelia H, Heinz R. Sulphur limitation and early sulphur de?ciency responses in poplar: signi?cance of gene expression, metabolites, and plant hormones. Journal of Experimental Botany, 2012, 63(5): 1873-1893.
[15]   李晓峰, 王俊玲, 李林妍, 谢鑫, 高志奎. 硫磺与水杨酸配施对韭菜硝酸盐累积及氮代谢的影响. 植物营养与肥料学报, 2013, 19(5): 1264 -1271.
Li X F, Wang J L, Li L Y, Xie X, Gao Z K. Effects of sulfur and salicylic acid on nitrate accumulation and nitrogen metabolism in leaves of Chinese chive. Journal of Plant Nutrition and Fertilizer, 2013, 19(5): 1264-1271. (in Chinese)
[16]   孔灵君, 徐坤, 张永征, 何平. 硫对大葱生长及氮硫同化关键酶活性的影响. 园艺学报, 2013, 40(12): 2505-2512. 
Kong L J, Xu K, Zhang Y Z, He P. Effects of sulfur on growth and key enzyme activities involved in nitrogen and sulfur assimilation in Chinese spring onion. Acta Horticulturae Sinica, 2013, 40(12): 2505-2512. (in Chinese)
[17]   霍捷, 王俊玲, 薛占军, 王梅, 高志奎. 亚硫酸氢钠对白菜叶片硝酸盐还原及光合能力的影响. 园艺学报, 2012, 39(4): 669-676.
Huo J, Wang J L, Xue Z J, Wang M, Gao Z K. Effects of sodium bisulfite on nitrate reduction and photosynthetic capacity in the leaves of non-heading Chinese cabbage. Acta Horticulturae Sinica, 2012, 39(4): 669-676. (in Chinese) 
[18]   付雪清, 王俊玲, 高志奎. NaHSO3和Na2SO4配施对小白菜叶片硝酸盐含量及营养品质的影响. 河北农业大学学报, 2013, 36(6): 43-47.
Fu X Q, Wang J L, Gao Z K. Effects of NaHSO3 and Na2SO4 combination on the nitrate and nutritional quality non-heading Chinese cabbage. Journal of agricultural university of Hebei, 2013, 36(6): 43-47. (in Chinese)
[19]   李合生. 植物生理生化实验原理和技术. 北京: 高等教育出版社, 2000, 123-137.
Li H S. Theory and Technology of Plant Physiology and Biochemistry Experiments. Beijing: Higher Education Press, 2000: 123-137. (in Chinese)
[20]   Ren J, Chen Z W, Duan W K, Song X M, Zhou J, Liu T K, Wang J J, Hou X L, Li Y. Comparison of ascorbic acid biosynthesis in different tissues of three non-heading Chinese cabbage cultivars. Plant Physiology and Biochemistry, 2013, 73: 229-236.
[21]   Takahashi H, Kopriva S, Giordano M, Saito K, Hell R. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annual Review of Plant Biology, 2011, 62: 157-184.
[22]   Dubousset L, Abdallah M, Desfeux A S, Etienne P, Meuriot F, Hawkesford M J, Gombert J, Segura R, Bataille M P, Reze S, Bonnefoy J, Ameline1 A F, Ourry A, Dily F L, Avice J C. Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. Journal of Experimental Botany, 2009, 60(11): 3239-3253.
[23]   Ruslan Y, Sarah G M, Colette M, Tamara G, Henning  F, Sean D, Anna K, Ulf-Ingo F Stanislav K. Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. The Plant Journal, 2010, 62: 1-11.
[24]   Riemenschneider A, Nikiforova V, Hoefgen R, De K, Kok L J D, Papenbrock J. Impact of elevated H2S onmetabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiology and Biochemistry, 2005, 43: 473-483.
[25]   Davidian J C, Kopriva S. Regulation of sulfate uptake and assimilation—the same or not the same? Molecular Plant, 2010, 3(2): 314-325.
[26]   Giordano M, Norici A, Hell R. Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytologist, 2005, 166(2): 371-382.
[27]   Abdallah M, Dubousset L, Meuriot F, Etienne P, Avice J C, Ourry A. Effect of mineral sulphur availability on nitrogen and sulphur uptake and remobilization during the vegetative growth of Brassica napus L.. Journal of Experimental Botany, 2010, 61(10): 2635-2646.
[28]   Zhang B, Pasini R, Hanbin D, Naveen J, Zhao Y H, Thoma, Zheng Z. Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. The Plant Journal, 2014, 77: 185-197.
[29]   Simona C, Vincenza V, Vittoria D M, Sergio E, Carmelo R. Nitrogen assimilation and cysteine biosynthesis in barley: Evidence for root sulphur assimilation upon recovery from N deprivation. Environmental and Experimental Botany, 2011, 71: 18-24.
[30]   Lee B R, Muneer S, Kim K Y, Avice J C, Ourry A, Kim T H. S-deciency responsive accumulation of amino acids is mainly due to hydrolysis of the previously synthesized proteins not to de novo synthesis in Brassica napus. Physiologia Plantarum, 2013, 147: 369-380.
[31]   Xu Y, Zhu X, Chen Y, Gong Y Q, Liu L. Expression pro?ling of genes involved in ascorbate biosynthesis and recycling during ?eshy root development in radish. Plant Physiology and Biochemistry, 2013, 70: 269-277.
[32]   Prosser I M, Purves J V, Saker L R, Clarkson D T. Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. Journal of Experimental Botany, 2001, 52: 113-121.
[33]   Nikiforova V J, Bielecka M, Gakiere B, Krueger S, Rinder J, Kempa S R, Morcuende R, Scheible W R, Hesse H, Hoefgen R. Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids, 2006, 30: 173-183.
[34]   Lea P J, Miflin B J. Alternative route for nitrogen assimilation in higher plants. Nature, 1974, 251: 614-616.
[35]   Suárez M F, Avila C, Gallardo F, Cantón F R, García- Gutiérrez A, Claros M G, Cánovas F M. Molecular and enzymatic analysis of ammonium assimilation in woody plants. Journal of Experimental Botany, 2002, 53: 891-904.
[36] Teixeira J, Fidalgo F. Salt stress affects glutamine synthetase activity and mRNA accumulation on potato plants in an organ- dependent manner. Plant Physiology and Biochemistry, 2009, 47: 807-813.
[37] Castro-Rodríguez V, García-Gutiérrez A, Canales J, Avila C, Kirby E G, Cánovas F M. The glutamine synthetase gene family in Populus. BMC Plant Biology, 2011, 11: 119-134.
[38]   Bernard S M, Habash D Z. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist, 2009, 182: 608-620.
[39]   Lam H M, Coschigano K T, Oliveira I C, Melo-Oliveira R, Coruzzi G. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Biology, 1996, 47: 569-593.
[40]   Lu Y E, Luo F, Yang M, Li X H, Lian X M. Suppression of glutamate synthase genes significantly affects carbon and nitrogen metabolism in rice (Oryza sativa L.). Sciences China Life Sciences, 2011, 54(7): 651-663.
[41]   Lancien M, Martin M, Hsieh M H, Leustek T, Goodman H, Coruzzi G M. Arabidopsis glt1-T mutant defines a role for NADH-GOGAT in the non-photorespiratory ammonium assimilatory pathway. The Plant Journal, 2002, 29: 347-358.
[42]   Liang G, Yang F, Yu D. MicroRNA395 mediates regulation of sulphate accumulation and allocation in Arabidopsis thaliana. The Plant Journal, 2010, 62, 1046-1057.
[1] ZHANG KeKun,CHEN KeQin,LI WanPing,QIAO HaoRong,ZHANG JunXia,LIU FengZhi,FANG YuLin,WANG HaiBo. Effects of Irrigation Amount on Berry Development and Aroma Components Accumulation of Shine Muscat Grape in Root-Restricted Cultivation [J]. Scientia Agricultura Sinica, 2023, 56(1): 129-143.
[2] GU LiDan,LIU Yang,LI FangXiang,CHENG WeiNing. Cloning of Small Heat Shock Protein Gene Hsp21.9 in Sitodiplosis mosellana and Its Expression Characteristics During Diapause and Under Temperature Stresses [J]. Scientia Agricultura Sinica, 2023, 56(1): 79-89.
[3] LAI ChunWang, ZHOU XiaoJuan, CHEN Yan, LIU MengYu, XUE XiaoDong, XIAO XueChen, LIN WenZhong, LAI ZhongXiong, LIN YuLing. Identification of Ethylene Synthesis Pathway Genes in Longan and Its Response to ACC Treatment [J]. Scientia Agricultura Sinica, 2022, 55(3): 558-574.
[4] SHU JingTing,SHAN YanJu,JI GaiGe,ZHANG Ming,TU YunJie,LIU YiFan,JU XiaoJun,SHENG ZhongWei,TANG YanFei,LI Hua,ZOU JianMin. Relationship Between Expression Levels of Guangxi Partridge Chicken m6A Methyltransferase Genes, Myofiber Types and Myogenic Differentiation [J]. Scientia Agricultura Sinica, 2022, 55(3): 589-601.
[5] GUO ShaoLei,XU JianLan,WANG XiaoJun,SU ZiWen,ZHANG BinBin,MA RuiJuan,YU MingLiang. Genome-Wide Identification and Expression Analysis of XTH Gene Family in Peach Fruit During Storage [J]. Scientia Agricultura Sinica, 2022, 55(23): 4702-4716.
[6] KANG Chen,ZHAO XueFang,LI YaDong,TIAN ZheJuan,WANG Peng,WU ZhiMing. Genome-Wide Identification and Analysis of CC-NBS-LRR Family in Response to Downy Mildew and Powdery Mildew in Cucumis sativus [J]. Scientia Agricultura Sinica, 2022, 55(19): 3751-3766.
[7] YuXia WEN,Jian ZHANG,Qin WANG,Jing WANG,YueHong PEI,ShaoRui TIAN,GuangJin FAN,XiaoZhou MA,XianChao SUN. Cloning, Expression and Anti-TMV Function Analysis of Nicotiana benthamiana NbMBF1c [J]. Scientia Agricultura Sinica, 2022, 55(18): 3543-3555.
[8] ZHONG JiaLin,XU ZiYan,ZHANG YiYun,LI Jie,LIU XiaoYu,LI LianQing,PAN GenXing. Effects of Feedstock, Pyrolyzing Temperature and Biochar Components on the Growth of Chinese Cabbage [J]. Scientia Agricultura Sinica, 2022, 55(14): 2775-2785.
[9] JIN MengJiao,LIU Bo,WANG KangKang,ZHANG GuangZhong,QIAN WanQiang,WAN FangHao. Light Energy Utilization and Response of Chlorophyll Synthesis Under Different Light Intensities in Mikania micrantha [J]. Scientia Agricultura Sinica, 2022, 55(12): 2347-2359.
[10] YUAN JingLi,ZHENG HongLi,LIANG XianLi,MEI Jun,YU DongLiang,SUN YuQiang,KE LiPing. Influence of Anthocyanin Biosynthesis on Leaf and Fiber Color of Gossypium hirsutum L. [J]. Scientia Agricultura Sinica, 2021, 54(9): 1846-1855.
[11] SHU JingTing,JI GaiGe,SHAN YanJu,ZHANG Ming,JU XiaoJun,LIU YiFan,TU YunJie,SHENG ZhongWei,TANG YanFei,JIANG HuaLian,ZOU JianMin. Expression Analysis of IGF1-PI3K-Akt-Dependent Pathway Genes in Skeletal Muscle and Liver Tissue of Yellow Feather Broilers [J]. Scientia Agricultura Sinica, 2021, 54(9): 2027-2038.
[12] ZHAO Ke,ZHENG Lin,DU MeiXia,LONG JunHong,HE YongRui,CHEN ShanChun,ZOU XiuPing. Response Characteristics of Plant SAR and Its Signaling Gene CsSABP2 to Huanglongbing Infection in Citrus [J]. Scientia Agricultura Sinica, 2021, 54(8): 1638-1652.
[13] ZHAO Le,YANG HaiLi,LI JiaLu,YANG YongHeng,ZHANG Rong,CHENG WenQiang,CHENG Lei,ZHAO YongJu. Expression Patterns of TETs and Programmed Cell Death Related Genes in Oviduct and Uterus of Early Pregnancy Goats [J]. Scientia Agricultura Sinica, 2021, 54(4): 845-854.
[14] HUANG Ming,WU JinZhi,LI YouJun,FU GuoZhan,ZHAO KaiNan,ZHANG ZhenWang,YANG ZhongShuai,HOU YuanQuan. Effects of Tillage Practices and Nitrogen Fertilizer Application Rates on Grain Yield, Protein Content in Winter Wheat and Soil Nitrate Residue in Dryland [J]. Scientia Agricultura Sinica, 2021, 54(24): 5206-5219.
[15] WANG XinYuan,ZHAO SiDa,ZHENG XianFeng,WANG ZhaoHui,HE Gang. Effects of Straw Returning and Nitrogen Application Rate on Grain Yield and Nitrogen Utilization of Winter Wheat [J]. Scientia Agricultura Sinica, 2021, 54(23): 5043-5053.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!