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Acta Agronomica Sinica ›› 2018, Vol. 44 ›› Issue (8): 1221-1228.doi: 10.3724/SP.J.1006.2018.01221

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Relationship between Lipid and Flag Leaf Senescence Induced by Low Nitrogen Stress during Grain Filling of Wheat

Qian LI1,2(),Ling-Yun QI3,4,Li-Na YIN1,2,3,4,*(),Shi-Wen WANG1,2,3,4,Xi-Ping DENG1,2,4   

  1. 1 College of Natural Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
    2 State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau / Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resource, Yangling 712100, Shaanxi, China
    3 Institute of Soil and Water Conservation, College of Life Science, Northwest A&F University, Yangling 712100, Shaanxi, China;
    4 College of Natural Resources and Environment, Northwest A&F University, Yangling 712100, Shaanxi, China;
  • Received:2017-11-09 Accepted:2018-04-11 Online:2018-08-10 Published:2018-05-14
  • Contact: Li-Na YIN E-mail:liqian515@mails.ucas.edu.cn;linayin@nwsuaf.edu.cn
  • Supported by:
    This study was funded by the National Natural Science Foundation of China(31200206);the National Key Technology R&D Program of China(2015BAD22B01);the Program for Scientific and Technological Star of Shaanxi Province(2016KJXX-66);the Youth Innovation Promotion Association of the Chinese Academy of Sciences(2015389)

Abstract:

Nitrogen (N) deficiency induces flag leaf senescence at the grain-filling stage of wheat resulting in yield decrease. In this study, we carried out a field experiment to investigate the relationship between N-deficiency-induced flag leaf senescence and lipid change using wheat variety ‘Changhan 58’. Under the low-N (120 kg ha -1) condition, the photosynthetic rate, chlorophyll content, total N content, and contents of all lipid components of flag leaf at 14 days after flowering were significantly lower than those under normal-N (180 kg ha -1) condition, while the DGDG/MGDG ratio in low-N treatment increased. The content of unsaturated fatty acids, such as C18:3 and C18:2 decreased significantly, whereas the contents of saturated fatty acids, such as C16:0, increased significantly, leading to the reduction of index of unsaturated double bounds. In addition, thylakoid protein packing density also decreased under N-deficiency condition. These results indicate that N-deficiency-induced leaf senescence is characterized with lipid degradation and components changes, which result in negative effects on reductions of membrane permeability, chlorophyll content and photosynthetic rate. Simultaneously, the DGDG/MGDG ratio of plants is adjusted in response to N deficiency to alleviate damages of membrane function caused bby lipid degradation.

Key words: wheat, flag leaf, nitrogen deficiency, membrane lipids, senescence

Fig. 1

Effects of nitrogen deficiency on Pn and chlorophyll content of wheat leaves Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference among treatments (P < 0.05)."

Fig. 2

Effects of nitrogen deficiency on nitrogen content and nitrogen/chlorophyll ratio of wheat leaves Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference among treatments (P < 0.05)."

Fig. 3

Effects of nitrogen deficiency on lipid content (A) and DGDG/MGDG ratio (B) in wheat leaves MGDG: monogalactosyldiacylglycerol; DGDG: digalactosyldiacylglycerol; PL: phospholipid. Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference between NN and LN treatments (P < 0.05)."

Fig. 4

Effects of nitrogen deficiency on main fatty acid compositions of various lipids in wheat leaves A: fatty acid compositions of monogalactosyldiacylglycerol; DGDG: fatty acid compositions of digalactosyldiacylglycerol; PL: fatty acid compositions of phospholipid; D: fatty acid compositions of total lipids. Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference among fatty acid compositions (P < 0.05)."

Fig. 5

Effects of nitrogen deficiency on DBI of lipids in wheat leaves DBI: double-bond index; MGDG: monogalactosyldiacylglycerol; DGDG: digalactosyldiacylglycerol; PL: phospholipid. Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference between the NN and LN treatments (P < 0.05)."

Fig. 6

Effects of nitrogen deficiency on lipid-to-chlorophyll content ratios in wheat leaves MGDG: monogalactosyldiacylglycerol; DGDG: digalactosyldiacylglycerol; PL: phospholipid. Columns represent mean ± SE (n = 3) and different letters above columns mean significant difference between NN and LN treatments (P < 0.05)."

[1] 李世清, 王瑞军, 张兴昌, 伍维模, 邵明安 . 小麦氮素营养与籽粒灌浆期氮素转移的研究进展. 水土保持学报, 2001,18:106-111
doi: 10.3321/j.issn:1009-2242.2004.03.027
Li S Q, Wang R J, Zhang X C, Wu W M, Shao M A . Research advancement of wheat nitrogen nutrition and nitrogen transportation in wheat grain filling. J Soil Water Conserv, 2001,18:106-111 (in Chinese with English abstract)
doi: 10.3321/j.issn:1009-2242.2004.03.027
[2] Hashimoto H, Kura Hotta M, Katoh S . Changes in protein content and in the structure and number of Chloroplasts during leaf senescence in rice seedlings. Plant Cell Physiol, 1989,30:705-707
[3] Barton R . The production and behavior of phytoferritin particles during senescence of phasolusleave. Planta, 1970,94:73-77
doi: 10.1007/BF00386610 pmid: 24496818
[4] Kolber Z, Falkowski P G . Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion photosystem II. Plant Physiol, 1988,88:923-929
doi: 10.1104/pp.88.3.923
[5] 孙虎 . 氮肥对番茄衰老调控及产量的影响. 北方园艺, 2016,40(24):35-37
Sun H . Effect of nitrogen fertilizer on tomato aging control and production. Northern Hort, 2016,40(24):35-37 (in Chinese with English abstract)
[6] 曾建敏, 崔克辉, 黄见良, 贺帆, 彭少兵 . 水稻生理生化特性对氮肥的反应及与氮利用效率的关系. 作物学报, 2007,33:1168-1176
Zeng J M, Cui K H, Huang J L, He F, Peng S B . Responses of physio-biochemical properties to N-fertilizer application and its relationship with nitrogen use efficiency in rice (Oryza sativa L.). Acta Agron Sin, 2007,33:1168-1176 (in Chinese with English abstract)
[7] 张绪成, 于显枫, 高世铭 . 氮素对高大气CO2浓度下小麦叶片光合功能的影响. 作物学报, 2010,36:1362-1370
doi: 10.3724/SP.J.1006.2010.01362
Zhang X C, Yu X F, Gao S M . Effects of nitrogen nutrition on photosynthetic function of wheat leaves under elevated atmospheric CO2 concentration. Acta Agron Sin, 2010,36:1362-1370 (in Chinese with English abstract)
doi: 10.3724/SP.J.1006.2010.01362
[8] Halliwell B. Chloroplast Metablism: The Structure and Function of Chloroplasts in Green Leaf Cells. Oxford: Charenden Press, 1981
[9] 许长成, 邹琦 . 大豆叶片早促衰老及其与膜质过氧化的关系. 作物学报, 1993,19:359-364
Xu C C, Zou Q . The acceleration of senescence of soybean leaves induced by drought and its relation to membrane lipid peroxidation. Acta Agron Sin, 1993,19:359-364 (in Chinese with English abstract)
[10] Chen D, Wang S, Xiong B, Deng X . Carbon/nitrogen imbalance associated with drought-induced leaf senescence in sorghum bicolor. PLoS One, 2015,10:e0137026
doi: 10.1371/journal.pone.0137026 pmid: 4552878
[11] 曹蓓蓓, 王仕稳, 齐凌云, 陈道钳, 殷俐娜, 邓西平 . 小麦苗期叶片碳氮平衡与低氮诱导的叶片衰老的关系. 麦类作物学报, 2017,37:1-7
doi: 10.7606/j.issn.1009-1041.2017.05.14
Cao B B, Wang S W, Qi L Y, Chen D Q, Yin L N, Deng X P . Carbon/nitrogen balance involved in nitrogen deficiency induced leaf senescence in wheat seedling. J Triticeae Crops, 2017,37:1-7 (in Chinese with English abstract)
doi: 10.7606/j.issn.1009-1041.2017.05.14
[12] Sinclair T R, de Wit C T . Comparative analysis of photosynthate and nitrogen requirements in the production of seeds by various crops. Science, 1975,189:565-567
doi: 10.1126/science.189.4202.565 pmid: 17798304
[13] Wanda Y, Miura K, Wantanabe K . Effect of source to sink ratio on carbohydrate production and senescence of rice flag leaves during the ripening period. Jpn J Crop Sci, 1993,62:547-553
doi: 10.1626/jcs.62.547
[14] 李淑文, 文宏达, 薛宝民, 齐永清, 肖凯 . 小麦高效吸收利用氮素的生理生化特性研究进展, 麦类作物学报, 2003,23(4):131-135
doi: 10.3969/j.issn.1009-1041.2003.04.032
Li S W, Wen H D, Xue B M, Qi Y Q, Xiao K . Advances on the physiological and biochemical characteristics of high nitrogen use efficiency in wheat. J Triticeae Crops, 2003,23(4):131-135 (in Chinese with English abstract)
doi: 10.3969/j.issn.1009-1041.2003.04.032
[15] 赵平, 林克惠, 郑毅 . 氮钾营养对烟叶衰老过程中内源激素与叶绿素含量的影响. 植物营养与肥料学报, 2005,11:379-384
doi: 10.3321/j.issn:1008-505X.2005.03.016
Zhao P, Lin K H, Zheng Y . Effect of N and K nutrition on chlorophyll content and endogenous hormones in the process of tobacco senescence. Plant Nutr Fert Sci, 2005,11:379-384 (in Chinese with English abstract)
doi: 10.3321/j.issn:1008-505X.2005.03.016
[16] 王汉忠, 赵福庚, 张国珍 . 多胺延缓植物衰老的机制. 山东农业大学学报, 1995,26:227-232
Wang H Z, Zhao F G, Zhang G Z . Retardation of plant senescence by polyamines. J Shandong Agric Univ, 1995,26:227-232 (in Chinese with English abstract)
[17] Zhang M, Deng X, Yin L, Qi L, Wang X, Wang S, Li H . Regulation of galactolipid biosynthesis by overexpression of the rice MGD gene contributes to enhanced aluminum tolerance in tobacco. Front Plant Sci, 2016,7:337
[18] Block M A, Dorne A J, Joyard J, Douce R . Preparation and characterization of membrane-fractions enriched in outer and inner envelope membranes from spinach-chloroplasts II biochemical-characterization. J Biol Chem, 1983,258:13281-13286
[19] Ohlrogge J, Browse J . Lipid biosynthesis. Plant Cell, 1995,7:957-970
doi: 10.1105/tpc.7.7.957
[20] Harwood J L . Recent advances in the biosynthesis of plant fatty acids. Biochim Biophys Acta, 1996,1301:7-56
doi: 10.1016/0005-2760(95)00242-1 pmid: 8652653
[21] Shimojima M, Watanabe T, Madoka Y, Koizumi R, Masuda K, Yamada K, Masuda S, Ohta H . Differential regulation of two types of monogalactosyldiacylglycerol synthase in membrane lipid remodeling under phosphate-limited conditions in sesame plants. Front Plant Sci, 2013,469:1-10
[22] Wang S, Uddin M I, Tanaka K, Yin L, Shi Z, Qi Y, Mano J, Matsui K, Shimomura N, Sakaki T, Deng X, Zhang S . Maintenance of chloroplast structure and function by overexpression of the rice MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE gene leads to enhanced salt tolerance in tobacco. Plant Physiol, 2014,165:1144-1155
[23] 史中惠, 王仕稳, 殷俐娜, 张梅娟, 邓西平 . 超表达水稻MGD基因(OsMGD)烟草植株的耐低磷胁迫能力. 西北农林科技大学学报(自然科学版) . 2013,41(10):97-104
Shi Z H, Wang S W, Yin L N, Zhang M J, Deng X P . Tolerance of tobacco plants with OsMGD gene to low phosphorus stress. J Northwest A&F Univ(Nat Sci Edn), 2013,41(10):97-104 (in Chinese with English abstract)
[24] Sakaki T, Saito K, Kawaguchi A, Kondo N, Yamada M . Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol, 1990,94:766-772
doi: 10.1104/pp.94.2.766
[25] 齐凌云, 张梅娟, 曹蓓蓓, 殷俐娜, 王仕稳, 邓西平 . 小麦苗期叶片膜质组成对低氮胁迫的响应及其与耐低氮的关系. 植物生理学报, 2017,53:1039-1050
Qi L Y, Zhang M J, Cao B B, Yin L N, Wang S W, Deng X P . Effect of nitrogen deficiency on leaf lipid composition in different nitrogen deficiency tolerant wheat (Triticum aestivum) cultivars during seedling stage. Plant Physiol J, 2017,53:1039-1050 (in Chinese with English abstract)
[26] 高俊凤 . 植物生理学试验指导. 北京: 高等教育出版社, 2006. pp 74-77
Gao J F. Experimental Guidance for Plant Physiology. Beijing: Higher Education Press, 2006. pp 74-77(in Chinese)
[27] Wang Z, Benning C . Arabidopsis thaliana polar glycerolipid profiling by thin layer chromatography (TLC) coupled with gas-liquid chromatography (GLC). J Vis Exp, 2011,49:e2518
[28] Rawyler A, Pavelic D, Gianinazzi C, Oberson J, Braendle R . Membrane lipid integrity relies on a threshold of ATP production rate in potato cell cultures submitted to anoxia. Plant Physiol, 1999,120:293-300
doi: 10.1104/pp.120.1.293
[29] Harwood J L . Fatty acid metabolism. Annu Rev Plant Physiol Plant Mol Biol, 1988,39:101-138
doi: 10.1146/annurev.pp.39.060188.000533
[30] 冯波, 王法宏, 刘延忠, 孔令安, 张宾, 李升东, 司纪升 . 施氮水平对不同栽培模式小麦旗叶衰老及产量的影响. 中国农学通报, 2010,26(8):189-193
Feng B, Wang F H, Liu Y Z, Kong L A, Zhang B, Li S D, Si J S . Effect of nitrogen application on senescence of flag leaf and grain yield in wheat in different planting models. Chin Agric Sci Bull, 2010,26(8):189-193 (in Chinese with English abstract)
[31] 许强, 王彦才, 马宏玮 . 宁夏春小麦缺氮导致减产的生理机理研究. 干旱地区农业研究, 1999,17(3):56-61
Xu Q, Wang Y C, Ma H W . Study on physiological mechanism of the decline in spring wheat production caused by inscofficient nitrogen in Ningxia. Agric Res Arid Areas, 1999,17(3):56-61 (in Chinese with English abstract)
[32] 何萍, 金继运, 林葆 . 氮肥用量对春玉米叶片衰老的影响及其机理研究. 中国农业科学, 1998,31(3):66-71
doi: 10.3321/j.issn:0578-1752.1998.03.012
He P, Jin J Y, Lin B . Effect of n application rates on leaf senescence and its mechanism in spring maize. Sci Agric Sin, 1998,31(3):66-71 (in Chinese with English abstract)
doi: 10.3321/j.issn:0578-1752.1998.03.012
[33] 王亚江, 魏海燕, 颜希亭, 葛梦婕, 孟天瑶, 张洪程, 戴其根, 霍中洋, 许轲, 费新茹 . 光、氮及其互作对超级粳稻产量和氮、磷、钾吸收的影响. 作物学报, 2014,40:1235-1244
Wang Y J, Wei H Y, Yan X T, Ge M J, Meng T Y, Zhang H C, Dai Q G, Huo Z Y, Xu K, Fei X R . Effects of light, nitrogen and their interaction on grain yield and nitrogen, phosphorus and potassium absorption in japonica super rice. Acta Agron Sin, 2014,40:1235-1244 (in Chinese with English abstract)
[34] 禹晓梅, 王荣, 李唯奇 . 拟南芥角果衰老过程中膜脂的变化. 植物分类与资源学报, 2014,36:177-186
doi: 10.7677/ynzwyj201413107
Yu X M, Wang R, Li W Q . Changes in membrane lipids during silique senescence in Arabidopsis. Plant Diversity Resour, 2014,36:177-186 (in Chinese with English abstract)
doi: 10.7677/ynzwyj201413107
[35] Douce R, Joyard J. Lipids: structure and function. New York: Academic Press, 1980. pp 221-225
[36] Gasulla F, vom Dorp K, Dombrink I, Dormann P, Bartels D . The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J, 2013,75:726-741
[37] Kirchhoff H, Sharpe R M, Herbstova M, Yarbrough R, Edwards G E . Differential mobility of pigment-protein complexes in granal and agranal thylakoid membranes of C3 and C4 plants. Plant Physiol, 2013,161:497-507
doi: 10.1104/pp.112.207548
[38] Haferkamp S, Kirchhoff H . Significance of molecular crowding in grana membranes of higher plants for light harvesting by photosystem II. Photosynth Res, 2008,95:129-134
doi: 10.1007/s11120-007-9253-2
[39] 胡锋, 黄俊丽, 秦峰, 岳彩黎, 王贵学 . 植物叶绿体类囊体膜及膜蛋白研究进展. 生命科学, 2011,23:291-198
Hu F, Huang J L, Qin F, Yue C L, Wang G X . Progress in chloroplast thylakoid membrane and membrane proteins. Chin Bull Life Sci, 2011,23:291-198 (in Chinese with English abstract)
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