Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-17T17:59:13.518Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of wheat powdery mildew on grain nitrogen metabolism

Published online by Cambridge University Press:  21 April 2021

H. Y. Gao Open the ORCID record for H. Y. Gao [Opens in a new window] ,
J. S. Niu ,
W. Q. Liu ,
D. L. Zhang  and
S. P. Li
H. Y. Gao
Affiliation:
School of Life Sciences of Henan University, Kaifeng475004, China School of Life Sciences of Zhengzhou Normal University, Zhengzhou450044, China
J. S. Niu
Affiliation:
National Centre of Engineering and Technological Research for Wheat, Henan Agricultural University, Zhengzhou450046, China
W. Q. Liu
Affiliation:
Zhengzhou City Fulun Foreign Language School, Zhengzhou450000, China
D. L. Zhang
Affiliation:
School of Life Sciences of Henan University, Kaifeng475004, China
S. P. Li*
Affiliation:
School of Life Sciences of Henan University, Kaifeng475004, China
*
Author for correspondence: S. P. Li, E-mail: lisuopingzznu@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Glutamine synthetase (GS) and glutamate synthase (GOGAT) play a central role in plant nitrogen (N) metabolism. In order to study the effect of powdery mildew (Blumeria graminis f. sp. tritici, Bgt) on N metabolism, field experiments were carried out to evaluate GS and GOGAT activity, GS expression and grain protein content (GPC) in susceptible (Xi'nong 979) and resistant (Zhengmai 103) wheat cultivars under three treatments. The three treatments were no inoculation (CK), inoculated once with Bgt (MP) and inoculated nine times with Bgt (HP). For Xi'nong 979, the activities of GS and GOGAT in grains as well as GS activity in flag leaves increased at 10–15 days after anthesis (DAA), and decreased significantly at 15 or 20–30 DAA in HP and MP. However, GS activity in grains decreased from 20 DAA, which was later than that of flag leaves (15 DAA). At the same time, GS expression in grains was up-regulated at early stage, with GS1 at 10 DAA and GS2 at 15 DAA, followed by a continuous down-regulation. This result indicated that GS and GOGAT activity as well as GS expression were inhibited by powdery mildew, indicating that N metabolism in grains was inhibited at 20–30 DAA. The current study also found out that the yield of the susceptible cultivar decreased significantly, while its GPC increased obviously in HP. It was shown that the increase of GPC was not due to the enhancement of N metabolism, but due to the passive increase caused by yield reduction.

Keywords

ActivityBlumeria graminis f. sp. tritici (Bgt)gene expressionglutamate synthaseglutamine synthetase
Type
Crops and Soils Research Paper
Information
The Journal of Agricultural Science , Volume 159 , Issue 1-2 , January 2021 , pp. 128 - 138
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bernard, SM and Habash, DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist 182, 608–620.10.1111/j.1469-8137.2009.02823.xCrossRefGoogle Scholar
Bernard, SM, Møller, ALB, Dionisio, G, Kichey, T, Jahn, TP, Dubois, F, Baudo, M, Lopes, MS, Tercé-Laforgue, T, Foyer, CH, Parry, MAJ, Forde, BG, Araus, JL, Hirel, B, Schjoerring, JK and Habash, DZ (2008) Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Molecular Biology 67, 89–105.10.1007/s11103-008-9303-yCrossRefGoogle Scholar
Cervilla, LM, Blasco, B, Ríos, JJ, Rosales, MA, Rubio-Wilhelmi, MM, Sánchez-Rodríguez, E, Romero, L and Ruiz, JM (2009) Response of nitrogen metabolism to boron toxicity in tomato plants. Plant Biology 11, 671–677.10.1111/j.1438-8677.2008.00167.xCrossRefGoogle ScholarPubMed
Gadaleta, A, Nigro, D, Giancaspro, A and Blanco, A (2011) The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Functional & Integrative Genomics 11, 665–670.CrossRefGoogle ScholarPubMed
Gadaleta, A, Nigro, D, Marcotuli, I, Giancaspro, A, Giove, SL and Blanco, A (2014) Isolation and characterisation of cytosolic glutamine synthetase (GSe) genes and association with grain protein content in durum wheat. Crop & Pasture Science 65, 38–45.10.1071/CP13140CrossRefGoogle Scholar
Gao, HY, He, DX, Niu, JS, Wang, CY and Yang, XW (2014a) The effect and molecular mechanism of powdery mildew on wheat grain prolamins. Journal of Agricultural Science 152, 239–253.CrossRefGoogle Scholar
Gao, HY, Niu, JS, Yang, XW, Wang, CY and He, DX (2014b) Impacts of powdery mildew on wheat grain sugar metabolism and starch accumulation in developing grains. Starch/Stärke 66, 947–958.10.1002/star.201400047CrossRefGoogle Scholar
Goodall, AJ, Kumar, P and Tobin, AK (2013) Identification and expression analyses of cytosolic glutamine synthetase genes in barley (Hordeum vulgare L.). Plant and Cell Physiology 54, 492–505.CrossRefGoogle Scholar
Habash, DZ, Massiah, AJ, Rong, HL, Wallsgrove, RM and Leigh, RA (2001) The role of cytosolic glutamine synthetase in wheat. Annals of Applied Biology 138, 83–89.10.1111/j.1744-7348.2001.tb00087.xCrossRefGoogle Scholar
Habash, DZ, Bernard, S, Schondelmaier, J, Weyen, J and Quarrie, SA (2007) The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theoretical and Applied Genetics 114, 403–419.CrossRefGoogle ScholarPubMed
Hu, MY, Zhao, XQ, Liu, Q, Hong, X, Zhang, W, Zhang, YJ, Sun, LJ, Li, H and Tong, YP (2018) Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnology Journal 16, 1858–1867.10.1111/pbi.12921CrossRefGoogle ScholarPubMed
Imagawa, F, Minagawa, H, Nakayama, Y, Kanno, K, Hayakawa, T and Kojima, S (2018) Tos17 insertion in NADH-dependent glutamate synthase genes leads to an increase in grain protein content in rice. Journal of Cereal Science 84, 38–43.CrossRefGoogle Scholar
Jenner, CF, Ugalde, TD and Aspinall, D (1991) The physiology of starch and protein deposition in the endosperm of wheat. Australian Journal of Plant Physiology 18, 211–226.Google Scholar
Kaur, B, Asthir, B and Bains, NS (2017) Enzymatic efficiency and genotypic differences for nitrogen assimilation in wheat. Proceedings of the National Academy of Sciences India Section B – Biological Sciences 87, 985–995.10.1007/s40011-015-0661-3CrossRefGoogle Scholar
Lam, HM, Coschigano, KT, Oliveira, IC, Melo-Oliveira, R and Coruzzi, GM (1996) The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 569–593.10.1146/annurev.arplant.47.1.569CrossRefGoogle ScholarPubMed
Li, XP, Zhao, XQ, He, X, Zhao, GY, Li, B, Liu, DC, Zhang, AM, Zhang, XY, Tong, YP and Li, ZS (2011) Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytologist 189, 449–458.10.1111/j.1469-8137.2010.03490.xCrossRefGoogle ScholarPubMed
Li, D, Li, Q, Guan, Zhang WD XZ and Tian, JC (2012) Proteomic analyses of the early Pm21 wheat near isogenic lines and their parents affected by powdery mildew. Acta Agriculturae Boreali-Sinica 27, 5–11.Google Scholar
Li, J, Yang, XW, Li, YC, Niu, JS and He, DX (2017) Proteomic analysis of developing wheat grains infected by powdery mildew (Blumeriagraminis f. sp. tritici). Journal of Plant Physiology 215, 140–153.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods (San Diego, Calif.) 25, 402–408.10.1006/meth.2001.1262CrossRefGoogle Scholar
Martino, C, Palumbo, G, Vitullo, D, Santo, P and Fuggi, A (2018) Regulation of mycorrhiza development in durum wheat by P fertilization: effect on plant nitrogen metabolism. Journal of Plant Nutrition and Soil Science 181, 429–440.10.1002/jpln.201700110CrossRefGoogle Scholar
Masclaux-Daubresse, C, Daniel-Vedele, F, Dechorgnat, J, Chardon, F, Gaufichon, L and Suzuki, A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 1141–1157.CrossRefGoogle ScholarPubMed
Masclaux, C, Valadier, MH, Brugière, N, Morot-Gaudry, JF and Hirel, B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510–518.CrossRefGoogle ScholarPubMed
Németh, E, Nagy, Z and Pécsváradi, A (2018) Chloroplast glutamine synthetase, the key regulator of nitrogen metabolism in wheat, performs its role by fine regulation of enzyme activity via negative cooperativity of its subunits. Frontiers in Plant Science 9, 191.CrossRefGoogle ScholarPubMed
Nigro, D, Blanco, A, Anderson, OD and Gadaleta, A (2014) Characterization of ferredoxin-dependent glutamine-oxoglutarate amidotransferase (Fd-GOGAT) genes and their relationship with grain protein content QTL in wheat. PLoS ONE 9, e103869.CrossRefGoogle ScholarPubMed
Nigro, D, Fortunato, S, Giove, SL, Paradiso, A, Gu, YQ, Blanco, A, de Pinto, MC and Gadaleta, A (2016) Glutamine synthetase in durum wheat: genotypic variation and relationship with grain protein content. Frontiers in Plant Science 7, 971.CrossRefGoogle ScholarPubMed
Nigro, D, Fortunato, S, Giove, SL, Mangini, G, Yacoubi, I, Simeone, R, Blanco, A and Gadaleta, A (2017) Allelic variants of glutamine synthetase and glutamate synthase genes in a collection of durum wheat and association with grain protein content. Diversity 9, 52.10.3390/d9040052CrossRefGoogle Scholar
Obara, M, Kajiura, M, Fukuta, Y, Yano, M, Hayashi, M, Yamaya, T and Sato, T (2001) Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). Journal of Experimental Botany 52, 1209–1217.Google Scholar
Pageau, K, Reisdorf-Cren, M, Morot-Gaudry, JF and Masclaux-Daubresse, C (2006) The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. Journal of Experimental Botany 57, 547–557.CrossRefGoogle Scholar
Pérez-García, A, Pereira, S, Pissarra, J, Gutiérrez, AG, Cazorla, FM, Salema, Vicente A R and Cánovas, FM (1998) Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment. Planta 206, 426–434.Google Scholar
Shi, WM, Xu, WF, Li, SM, Zhao, XQ and Dong, GQ (2010) Responses of two rice cultivars differing in seedling-stage nitrogen use efficiency to growth under low-nitrogen conditions. Plant and Soil 326, 291–302.CrossRefGoogle Scholar
Silveira, APD, Sala, VMR, Cardoso, EJBN, Labanca, EG and Cipriano, MAP (2016) Nitrogen metabolism and growth of wheat plant under diazotrophic endophytic bacteria inoculation. Applied Soil Ecology 107, 313–319.CrossRefGoogle Scholar
Singh, RP and Srivastava, HS (1986) Increase in glutamate synthase (NADH) activity in maize seedlings in response to nitrate and ammonium nitrogen. Physiologia Plantarum 66, 413–416.CrossRefGoogle Scholar
Sutton, PN, Gilbert, MJ, Williams, LE and Hall, JL (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiologia Plantarum 129, 787–795.CrossRefGoogle Scholar
Tabuchi, M, Abiko, T and Yamaya, T (2007) Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). Journal of Experimental Botany 58, 2319–2327.CrossRefGoogle Scholar
Tao, ZQ, Chang, XH, Wang, DM, Wang, YJ, Ma, SK, Yang, YS and Zhao, GC (2018) Effects of sulfur fertilization and short-term high temperature on wheat grain production and wheat flour proteins. The Crop Journal 6, 413–425.CrossRefGoogle Scholar
Tavernier, V, Cadiou, S, Pageau, K, Lauge, R, Reisdorf-Cren, M, Langin, T and Masclaux-Daubresse, C (2007) The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. Journal of Experimental Botany 58, 3351–3360.CrossRefGoogle ScholarPubMed
Thomsen, HC, Eriksson, D, Møller, IS and Schjoerring, JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends in Plant Science 19, 656–663.CrossRefGoogle ScholarPubMed
Yamaya, T, Hayakawa, T, Tanasawa, K, Kamachi, K, Mae, T and Ojima, K (1992) Tissue distribution of glutamate synthase and glutamine synthetase in rice leaves: occurrence of NADH-dependent glutamate synthase protein and activity in the unexpanded, nongreen leaf blades. Plant Physiology 100, 1427–1432.CrossRefGoogle ScholarPubMed
Zadoks, JC, Chang, TT and Konzak, CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.CrossRefGoogle Scholar
Zhang, MW, Ma, DY, Ma, G, Wang, CY, Xie, XD and Kang, GZ (2017) Responses of glutamine synthetase activity and gene expression to nitrogen levels in winter wheat cultivars with different grain protein content. Journal of Cereal Science 74, 187–193.CrossRefGoogle Scholar
Zhang, J, Khan, S, Sun, M, Gao, ZQ, Liang, YF, Yang, QS, Zhang, HY and Li, NN (2018) Coordinated improvement of grain yield and protein content in dryland wheat by subsoiling and optimum planting density. Applied Ecology and Environmental Research 16, 7847–7866.CrossRefGoogle Scholar