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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (9): 1779-1790.doi: 10.3724/SP.J.1006.2021.04151

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Regulation of carbon and nitrogen metabolism in leaf of soybean cultivar Suinong 26 at seed-filling stage under drought stress by exogenous melatonin

CAO Liang(), DU Xin, YU Gao-Bo, JIN Xi-Jun, ZHANG Ming-Cong, REN Chun-Yuan, WANG Meng-Xue*(), ZHANG Yu-Xian*()   

  1. College of Agronomy, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang, China
  • Received:2020-07-10 Accepted:2021-01-21 Online:2021-09-12 Published:2021-03-01
  • Contact: WANG Meng-Xue,ZHANG Yu-Xian E-mail:miss9877@126.com;wangmengxue1978@163.com;zyx_lxy@126.com
  • Supported by:
    National Key Research and Development Program of China “Physiological Basis and Agronomic Management for High-quality and High-yield of Field Cash Crops”(2018YFD1000905);Heilongjiang Application Technology Research and Development Projects(GA19B101-02);Heilongjiang Provincial Land Reclamation Bureau Key Research Project(HKKY190206-01)

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Abstract:

The grain-filling stage is the most complex stage of carbon and nitrogen metabolism. Drought stress inevitably inhibits the assimilation, distribution, and transition of carbon and nitrogen at grain-filling stage in soybean, resulting in less soybean yield. The objective of this study was to investigate the effects of exogenous melatonin on the carbon and nitrogen metabolism genes and pathways under drought stress in soybean. Transcriptome analysis showed that, compared with drought stress treatment, 37 and 493 genes were jointly up-regulated and down-regulated in soybean leaves treated with normal water supply and treated with exogenous melatonin under drought stress, respectively. The up-regulated genes included functional genes directly and indirectly involved in carbon and nitrogen metabolism, such as the key genes involved in the cysteine synthesis pathway, photosynthesis, carbohydrate metabolism, and glucose metabolism. Metabolomic analysis revealed that, compared with drought stress treatment, 17 and 43 metabolites were jointly up-regulated and down-regulated in soybean leaves treated with normal water supply and treated with exogenous melatonin under drought stress, respectively. Most (14/17) of up-regulated metabolites were amino acids, lipids, organic acids, and carbohydrates, which further indicated that exogenous melatonin could improve soybean carbon and nitrogen metabolism and drought resistance in soybean. Combined with transcriptome and metabolomic profile, melatonin promoted the relative expression level of β-D-Glucosidase gene due to regulate the pathway of amino acid metabolism and starch and sucrose metabolism, improved the contents of L-Asparagine and D-glucose-6P metabolites, and ultimately improves the ability of drought resistance in soybean.

Key words: melatonin, soybean, drought at grain-filling stage, carbon and nitrogen metabolism, metabolome and transcriptome

Fig. 1

Comparisons of differentially expressed genes in WW/D and DM/D Grey dots represent genes without significant differential expressions, red and blue dots denote significantly up-regulated and down-regulated genes in the WW/D and DM/D comparisons, respectively. WW is the normal water supply group, D is the drought stress group, and DM is the foliar application of melatonin under drought stress group."

Fig. 2

Effects of exogenous melatonin on leave transcriptome under drought stress in soybean A: Venn diagram of the differentially expressed genes between WW/D and DM/D. B: the heat maps of the common differentially expressed genes between WW/D and DM/D. Treatments are the same as those given in Fig. 1. "

Fig. 3

GO biological process enrichment of up-regulated differentially expressed genes under melatonin treatment in WW/D and DM/D A: the heatmap of the up-regulated expressed genes between the WW/D and DM/D. B: GO biological process enrichment on common up-regulated expressed genes between the WW/D and DM/D. Treatments are the same as those given in Fig. 1. "

Fig. 4

KEGG pathway enrichment for differentially up-regulated and down-regulated expressed genes both in WW/D and DM/D A: up-regulated. B: down-regulated. The rich factor is calculated as the differentially expressed genes number divided by the base number of any given pathway. Dot size denotes the number of genes and dot color denotes the range of adjusted P-value. Treatments are the same as those given in Fig. 1. "

Fig. 5

RT-PCR validation of relative expression levels of DEGs White bar signifies transcriptomic data of the differentially expressed genes, and black bar denotes qRT-PCR results of the differentially expressed genes. Treatments are the same as those given in Fig. 1. "

Fig. 6

PCA analysis of metabolomics Treatments are the same as those given in Fig. 1. "

Fig. 7

Effects of drought stress and exogenous melatonin treatment on the metabolome in soybean A: the venn diagram shows the overlapped differentially-accumulated metabolites between the WW/D and DM/D comparisons. B: the histogram of KEGG pathway enrichment for differentially-accumulated metabolites both in WW/D and DM/D comparison. X-axis is the number of differentially expressed genes. Treatments are the same as those given in Fig. 1. "

Fig. 8

KEGG pathway of starch sucrose metabolism and cyanoamino acid metabolism A: starch and sucrose metabolism. B: cyanoamino acid metabolism. Red and pink denote up-regulated metabolites and genes both in WW/D and DM/D."

[1] 宫丽娟, 李秀芬, 田宝星, 王萍, 姜蓝齐, 赵慧颖. 黑龙江省大豆不同生育阶段干旱时空特征. 应用气象学报, 2020, 31:95-104.
Gong L J, Li X F, Tian B X, Wang P, Jiang L Q, Zhao H Y. Spatio-temporal characteristics drought in different growth stages of soybean in heilongjiang. J Appl Meteorol Sci, 2020, 31:95-104 (in Chinese with English abstract).
[2] 王秋京, 李秀芬, 闫平, 吕佳佳, 王晾晾, 马国忠. 黑龙江省主要农业气象灾害时序特征及其对大豆产量影响的灰色关联分析. 中国农学通报, 2020, 36(3):81-87.
Wang Q J, Li X F, Yan P, Lyu J J, Wang L L, Ma G Z. Main agro-meteorological disasters Heilongjiang: sequential characteristics and grey correlation analysis of their effects on soybean yield. Chin Agric Sci Bull, 2020, 36(3):81-87 (in Chinese with English abstract).
[3] Harrison M T, Tardieu F, Dong Z, Carlos D, Graeme L. Characterizing drought stress and trait influence on maize yield under current and future conditions. Global Change Biol, 2014, 20:867-878.
doi: 10.1111/gcb.12381 pmid: 24038882
[4] Lobell D B, Roberts M J, Schlenker W, Noah B, Bertis B L, Roderick M R, Graeme L H. Greater sensitivity to drought accompanies maize yield increase in the U.S. midwest. Science, 2014, 344:516-519.
doi: 10.1126/science.1251423
[5] Mayank A G, Jelli V, Lam-Son P T. Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant, 2015, 8:1304-1320.
doi: 10.1016/j.molp.2015.05.005
[6] Chaves M M, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot, 2009, 103:551-560.
doi: 10.1093/aob/mcn125
[7] 屈春媛, 张玉先, 金喜军, 任春元, 张明聪, 王孟雪, 王彦宏, 李菁华, 郑浩宇, 邹京南. 干旱胁迫下外源ABA对鼓粒期大豆产量及氮代谢关键酶活性的影响. 中国农学通报, 2017, 33(34):26-31.
Qu C Y, Zhang Y X, Jin X J, Ren C Y, Zhang M C, Wang M X, Wang Y H, Li J H, Zheng H Y, Zou J N. Effect of exogenous ABA on yield and key enzyme activities of nitrogen metabolism of soybean under drought stress. Chin Agric Sci Bull, 2017, 33(34):26-31 (in Chinese with English abstract).
[8] Arnao M B, Hernández R J. Melatonin: plant growth regulator and/or biostimulator during stress. Trends Plant Sci, 2014, 19:789-797.
doi: 10.1016/j.tplants.2014.07.006
[9] Reiter R J, Tan D X, Zhou Z C, Maria H C C, Lorena F B, Annia G. Phytomelatonin: assisting plants to survive and thrive. Molecules, 2015, 20:7396-7437.
doi: 10.3390/molecules20047396
[10] Zhang N, Sun Q, Zhang H J, Cao Y Y, Sarah W, Ren S X, Guo Y D. Roles of melatonin in abiotic stress resistance in plants. J Exp Bot, 2015, 66:647-656.
doi: 10.1093/jxb/eru336 pmid: 25124318
[11] 邹京南. 外源褪黑素对干旱胁迫下大豆光合及生长的影响. 黑龙江八一农垦大学硕士学位论文, 黑龙江大庆, 2019.
Zou J N. Effects of Exogenous Melatonin on Photosynthesis and Growth of Soybean under Drought Stress. MS Thesis of Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang, China, 2019 (in Chinese with English abstract).
[12] 邹京南, 曹亮, 王梦雪, 金喜军, 任春元, 王明瑶, 于奇, 张玉先. 外源褪黑素对干旱胁迫下大豆结荚期光合及生理的影响. 生态学杂志, 2019, 38:2709-2718.
Zou J N, Cao L, Wang M X, Jin X J, Ren C Y, Wang M Y, Yu Q, Zhang Y X. Effects of exogenous melatonin on photosynthesis and physiology of soybean seedlings under drought stress. Chin J Ecol, 2019, 38:2709-2718 (in Chinese with English abstract).
[13] 邹京南, 于奇, 金喜军, 王明瑶, 秦彬, 任春元, 王孟雪, 张玉先. 外源褪黑素对干旱胁迫下大豆鼓粒期生理和产量的影响. 作物学报, 2020, 46:745-758.
Zou J N, Yu Q, Jin X J, Wang M Y, Qin B, Ren C Y, Wang M X, Zhang Y X. Effects of exogenous melatonin on physiology and yield of soybean during seed filling stage under drought stress. Acta Agron Sin, 2020, 46:745-758 (in Chinese with English abstract).
[14] Zou J N, Jin X J, Zhang Y X, Ren C Y, Zhang M C, Wang M X. Effects of melatonin on photosynthesis and soybean seed growth during grain filling under drought stress. Photosynthetica, 2019, 57:512-520.
doi: 10.32615/ps.2019.066
[15] Maharaj D S, Anoopkumar D S, Glass B D, Antunes E M, Lack B, Walker R B, Daya S. The identification of the UV degradants of melatonin and their ability to scavenge free radicals. J Pineal Res, 2010, 32:257-261.
doi: 10.1034/j.1600-079X.2002.01866.x
[16] Cao L, Jin X J, Zhang Y X. Melatonin confers drought stress tolerance in soybean ( Glycine max L.) by modulating photosynthesis, osmolytes, and reactive oxygen metabolism. Photosynthetica, 2019, 57:812-829.
doi: 10.32615/ps.2019.100
[17] 倪知游. 外源褪黑素对猕猴桃幼苗干旱胁迫调控机理的研究. 四川农业大学硕士学位论文, 四川成都, 2018.
Ni Z Y. Regulatory Mechanism of Exogenous Melatonin on Kiwifruit under Drought Stress. MS Thesis of Sichuan Agricultural University, Chengdu, Sichuan, China, 2018 (in Chinese with English abstract).
[18] 李超. 外源褪黑素和多巴胺对苹果抗旱耐盐性的调控功能研究. 西北农林科技大学硕士学位论文, 陕西杨凌, 2016.
Li C. Regulatory Function of Exogenous Melatonin and Dopamine on Salt and Drought Tolerance in Malus. MS Thesis of Northwest A&F University, Yangling, Shaanxi, China, 2016 (in Chinese with English abstract).
[19] 魏志为. 褪黑素对光逆境下苹果的保护功能研究. 西北农林科技大学硕士学位论文, 陕西杨凌, 2019.
Wei Z W. The Protective Function of Melatonin in Malus under Light Stress. MS Thesis of Northwest A&F University, Yangling, Shaanxi, China, 2019 (in Chinese with English abstract).
[20] Graham I A. Carbohydrate control of gene expression in higher plants. Res Microbiol, 1996, 147:500-580.
[21] Seki M, Narusaki M, Ishida J. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full length cDNA micro array. Plant J, 2002, 31:279-292.
doi: 10.1046/j.1365-313X.2002.01359.x
[22] Wei W, Li Q T, Chu Y N, Russel J R, Yu X M, Zhu D H, Zhang W K, Ma B, Lin Q, Zhang J S. Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot, 2015, 66:695-707.
doi: 10.1093/jxb/eru392 pmid: 25297548
[23] Hildebrandt T M, Nesi A N, Araújo W L, Hans P B. Amino acid catabolism in plants. Mol Plant, 2015, 8:1563-1579.
doi: 10.1016/j.molp.2015.09.005 pmid: 26384576
[24] Pires M V, Júnior P, Adilson A, Medeiros D B, Daloso D M, Pham P A, Barros K A, Martin K M, Florian A K, Ina M, Veronica G, Araújo W L, Fernie A R. The influence of alternative pathways of respiration that utilize branched-chain amino acids following water shortage in Arabidopsis. Plant Cell Environ, 2016, 39:1304-1319.
doi: 10.1111/pce.12682
[25] Maeda H, Dudareva N. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol, 2012, 63:73-105.
doi: 10.1146/annurev-arplant-042811-105439
[26] Ismail G S M. Roles of hydrogen sulfide and cysteine in alleviation of nickel induced oxidative damages in wheat seedling. Egyptian J Exp Biol, 2013, 9:105-114.
[27] Verslues P E, Sharma S. Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book, 2010, 8:e0140.
doi: 10.1199/tab.0140
[28] Antoniou C, Chatzimichail G, Xenofontos R, Pavlou J J, Panagiotou E, Christou A, Fotopoulos V. Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. J Pineal Res, 2017, 62:e12401.
doi: 10.1111/jpi.2017.62.issue-4
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