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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Metabolomics: A Powerful Tool to Study the Complexity of Wheat Metabolome

Author(s): Ali Razzaq, Wajiha Guul, Muhammad Sarwar Khan and Fozia Saleem*

Volume 28, Issue 8, 2021

Published on: 27 January, 2021

Page: [878 - 895] Pages: 18

DOI: 10.2174/0929866528666210127153532

Price: $65

Abstract

Wheat is a widely cultivated cereal, consumed by nearly 80% of the total population in the world. Although wheat is growing on 215 million hectares annually, its production is still inadequate to meet the future demand of feeding the 10 billion human population. Global food security is the biggest challenge as climate change is threatening crop production. There is a need to fast-- track the wheat breeding by devising modern biotechnological tools. Climate-smart wheat having greater stress resilience, better adaptability and improved agronomic traits are vital to guarantee food security. Substantial understanding and knowledge of vital biochemical pathways and regulatory networks is required for achieving stress resilience in wheat. Metabolomics has emerged as a fascinating technology to speed up the crop improvement programs by deciphering unique metabolic pathways for abiotic/biotic stress tolerance. State-of-the-art metabolomics tools such as nuclear magnetic resonance (NMR) and advanced mass spectrometry (MS) has opened new horizons for detailed analysis of wheat metabolome. The identification of unique metabolic pathways offers various types of stress tolerance and helps to screen the elite wheat cultivars. In this review, we summarize the applications of metabolomics to probe the stress-responsive metabolites and stress-inducive regulatory pathways that govern abiotic/biotic stress tolerance in wheat and highlight the significance of metabolic profiling to characterize wheat agronomics traits. Furthermore, we also describe the potential of metabolomics-assisted speed breeding for wheat improvement and propose future directions.

Keywords: Metabolomics, wheat, climate change, metabolic profiling, metabolites, abiotic stress, biotic stress, agronomics traits, metabolomics-assisted breeding.

Graphical Abstract

[1]
Ray, D.K.; Mueller, N.D.; West, P.C.; Foley, J.A. Yield trends are insufficient to double global crop production by 2050. PLoS One, 2013, 8(6), e66428.
[http://dx.doi.org/10.1371/journal.pone.0066428] [PMID: 23840465]
[2]
FAO statistical database: food and agriculture organization of the united nations. 2020. Available from: http://faostat3.fao.org/home/E
[3]
Raza, A.; Razzaq, A.; Mehmood, S.S.; Zou, X.; Zhang, X.; Lv, Y.; Xu, J. Impact of climate change on crops adaptation and strategies to tackle its outcome: A review. Plants (Basel), 2019, 8(2), 34.
[http://dx.doi.org/10.3390/plants8020034] [PMID: 30704089]
[4]
Xu, Y.; Ramanathan, V.; Victor, D.G. Global warming will happen faster than we think; Nature Publishing Group, 2018.
[http://dx.doi.org/10.1038/d41586-018-07586-5]
[5]
Hisas, L. The food gap: The impacts of climate change on food production: A 2020 perspective; FEU-US Universal Ecological Fund: United States of America, 2011, p. 55.
[6]
Emergency Events Database (EM-DAT). 2020. Available from: https://www.emdat.be/
[7]
Nations, U. World population prospects: the 2012 revision, highlights and advance tables; New York United Nations Department of Economic & Social Affairs, 2013.
[8]
Wu, H.; Shi, N.; An, X.; Liu, C.; Fu, H.; Cao, L.; Feng, Y.; Sun, D.; Zhang, L. Candidate genes for yellow leaf color in common wheat (Triticum aestivum L.) and major related metabolic pathways according to transcriptome profiling. Int. J. Mol. Sci., 2018, 19(6), 1594.
[http://dx.doi.org/10.3390/ijms19061594] [PMID: 29843474]
[9]
Hemdane, S.; Jacobs, P.J.; Dornez, E.; Verspreet, J.; Delcour, J.A.; Courtin, C.M. Wheat (Triticum aestivum L.) bran in bread making: a critical review. Compr. Rev. Food Sci. Food Saf., 2016, 15(1), 28-42.
[http://dx.doi.org/10.1111/1541-4337.12176]
[10]
Shewry, P.R. Wheat. J. Exp. Bot., 2009, 60(6), 1537-1553.
[http://dx.doi.org/10.1093/jxb/erp058] [PMID: 19386614]
[11]
Nussbaumer, T.; Warth, B.; Sharma, S.; Ametz, C.; Bueschl, C.; Parich, A.; Pfeifer, M.; Siegwart, G.; Steiner, B.; Lemmens, M.; Schuhmacher, R.; Buerstmayr, H.; Mayer, K.F.; Kugler, K.G.; Schweiger, W. Joint transcriptomic and metabolomic analyses reveal changes in the primary metabolism and imbalances in the subgenome orchestration in the bread wheat molecular response to Fusarium graminearum. G3 (Bethesda), 2015, 5(12), 2579-2592.
[http://dx.doi.org/10.1534/g3.115.021550] [PMID: 26438291]
[12]
Selim, D.A.H.; Nassar, R.M.A.; Boghdady, M.S.; Bonfill, M. Physiological and anatomical studies of two wheat cultivars irrigated with magnetic water under drought stress conditions. Plant Physiol. Biochem., 2019, 135, 480-488.
[http://dx.doi.org/10.1016/j.plaphy.2018.11.012] [PMID: 30463800]
[13]
Shewry, P.R.; Hawkesford, M.J.; Piironen, V.; Lampi, A-M.; Gebruers, K.; Boros, D.; Andersson, A.A.; Åman, P.; Rakszegi, M.; Bedo, Z.; Ward, J.L. Natural variation in grain composition of wheat and related cereals. J. Agric. Food Chem., 2013, 61(35), 8295-8303.
[http://dx.doi.org/10.1021/jf3054092] [PMID: 23414336]
[14]
Rasheed, A.; Xia, X.; Yan, Y.; Appels, R.; Mahmood, T.; He, Z. Wheat seed storage proteins: advances in molecular genetics, diversity and breeding applications. J. Cereal Sci., 2014, 60(1), 11-24.
[http://dx.doi.org/10.1016/j.jcs.2014.01.020]
[15]
Curtis, T.; Halford, N.G. Food security: the challenge of increasing wheat yield and the importance of not compromising food safety. Ann. Appl. Biol., 2014, 164(3), 354-372.
[http://dx.doi.org/10.1111/aab.12108] [PMID: 25540461]
[16]
Long, S.P.; Marshall-Colon, A.; Zhu, X-G. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 2015, 161(1), 56-66.
[http://dx.doi.org/10.1016/j.cell.2015.03.019] [PMID: 25815985]
[17]
Kanwal, M.; Razzaq, A.; Maqbool, A. Characterization of phytase transgenic wheat under salt stress. Biol. Bull., 2019, 46(4), 371-380.
[http://dx.doi.org/10.1134/S106235901904006X]
[18]
Lavergne, F.D.; Broeckling, C.D.; Brown, K.J.; Cockrell, D.M.; Haley, S.D.; Peairs, F.B.; Pearce, S.; Wolfe, L.M.; Jahn, C.E.; Heuberger, A.L. Differential stem proteomics and metabolomics profiles for four wheat cultivars in response to the insect pest Wheat Stem Sawfly. J. Proteome Res., 2020, 19(3), 1037-1051.
[http://dx.doi.org/10.1021/acs.jproteome.9b00561] [PMID: 31995381]
[19]
Thomason, K.; Babar, M.A.; Erickson, J.E.; Mulvaney, M.; Beecher, C.; MacDonald, G. Comparative physiological and metabolomics analysis of wheat (Triticum aestivum L.) following post-anthesis heat stress. PLoS One, 2018, 13(6), e0197919.
[http://dx.doi.org/10.1371/journal.pone.0197919] [PMID: 29897945]
[20]
Asseng, S.; Ewert, F.; Martre, P.; Rötter, R.P.; Lobell, D.B.; Cammarano, D. Rising temperatures reduce global wheat production. Nat. Clim. Chang., 2015, 5(2), 143-147.
[http://dx.doi.org/10.1038/nclimate2470]
[21]
Marček, T.; Hamow, K.Á.; Végh, B.; Janda, T.; Darko, E. Metabolic response to drought in six winter wheat genotypes. PLoS One, 2019, 14(2), e0212411.
[http://dx.doi.org/10.1371/journal.pone.0212411] [PMID: 30779775]
[22]
Dai, A. Increasing drought under global warming in observations and models. Nat. Clim. Chang., 2013, 3(1), 52-58.
[http://dx.doi.org/10.1038/nclimate1633]
[23]
Conforti, P; Ahmed, S; Markova, G. Impact of disasters and crises on agriculture and food security, 2017. Food and Agriculture Organization: Rome: Italy, 2018.
[24]
Abdelrahman, M.; Burritt, D.J.; Gupta, A.; Tsujimoto, H.; Tran, L.P. Heat stress effects on source-sink relationships and metabolome dynamics in wheat. J. Exp. Bot., 2020, 71(2), 543-554.
[http://dx.doi.org/10.1093/jxb/erz296] [PMID: 31232445]
[25]
Saito, K.; Matsuda, F. Metabolomics for functional genomics, systems biology, and biotechnology. Annu. Rev. Plant Biol., 2010, 61, 463-489.
[http://dx.doi.org/10.1146/annurev.arplant.043008.092035] [PMID: 19152489]
[26]
Fernie, A.R.; Schauer, N. Metabolomics-assisted breeding: a viable option for crop improvement? Trends Genet., 2009, 25(1), 39-48.
[http://dx.doi.org/10.1016/j.tig.2008.10.010] [PMID: 19027981]
[27]
Bino, R.J.; Hall, R.D.; Fiehn, O.; Kopka, J.; Saito, K.; Draper, J.; Nikolau, B.J.; Mendes, P.; Roessner-Tunali, U.; Beale, M.H.; Trethewey, R.N.; Lange, B.M.; Wurtele, E.S.; Sumner, L.W. Potential of metabolomics as a functional genomics tool. Trends Plant Sci., 2004, 9(9), 418-425.
[http://dx.doi.org/10.1016/j.tplants.2004.07.004] [PMID: 15337491]
[28]
Farahbakhsh, F.; Hamzehzarghani, H.; Massah, A.; Tortosa, M.; Yassaie, M.; Rodriguez, V.M. Comparative metabolomics of temperature sensitive resistance to wheat streak mosaic virus (WSMV) in resistant and susceptible wheat cultivars. J. Plant Physiol., 2019, 237, 30-42.
[http://dx.doi.org/10.1016/j.jplph.2019.03.011] [PMID: 31005806]
[29]
Razzaq, A.; Sadia, B.; Raza, A.; Khalid Hameed, M.; Saleem, F. Metabolomics: a way forward for crop improvement. Metabolites, 2019, 9(12), 303.
[http://dx.doi.org/10.3390/metabo9120303] [PMID: 31847393]
[30]
Weckwerth, W. Metabolomics in systems biology. Annu. Rev. Plant Biol., 2003, 54(1), 669-689.
[http://dx.doi.org/10.1146/annurev.arplant.54.031902.135014] [PMID: 14503007]
[31]
Abbiss, H.; Gummer, J.P.; Francki, M.; Trengove, R.D. Untargeted liquid chromatography-mass spectrometry-based metabolomics analysis of wheat grain. JoVE (Journal of Visualized Experiments), 2020.
[http://dx.doi.org/10.3791/60851]
[32]
Jorge, T.F.; Rodrigues, J.A.; Caldana, C.; Schmidt, R.; van Dongen, J.T.; Thomas-Oates, J.; António, C. Mass spectrometry-based plant metabolomics: metabolite responses to abiotic stress. Mass Spectrom. Rev., 2016, 35(5), 620-649.
[http://dx.doi.org/10.1002/mas.21449] [PMID: 25589422]
[33]
Ribbenstedt, A.; Ziarrusta, H.; Benskin, J.P. Development, characterization and comparisons of targeted and non-targeted metabolomics methods. PLoS One, 2018, 13(11), e0207082.
[http://dx.doi.org/10.1371/journal.pone.0207082] [PMID: 30439966]
[34]
Kong, L.; Xie, Y.; Hu, L.; Si, J.; Wang, Z. Excessive nitrogen application dampens antioxidant capacity and grain filling in wheat as revealed by metabolic and physiological analyses. Sci. Rep., 2017, 7, 43363.
[http://dx.doi.org/10.1038/srep43363] [PMID: 28233811]
[35]
Francki, M.G.; Hayton, S.; Gummer, J.P.; Rawlinson, C.; Trengove, R.D. Metabolomic profiling and genomic analysis of wheat aneuploid lines to identify genes controlling biochemical pathways in mature grain. Plant Biotechnol. J., 2016, 14(2), 649-660.
[http://dx.doi.org/10.1111/pbi.12410] [PMID: 26032167]
[36]
Hong, J.; Yang, L.; Zhang, D.; Shi, J. Plant metabolomics: an indispensable system biology tool for plant science. Int. J. Mol. Sci., 2016, 17(6), 767.
[http://dx.doi.org/10.3390/ijms17060767] [PMID: 27258266]
[37]
Zhen, S.; Dong, K.; Deng, X.; Zhou, J.; Xu, X.; Han, C.; Zhang, W.; Xu, Y.; Wang, Z.; Yan, Y. Dynamic metabolome profiling reveals significant metabolic changes during grain development of bread wheat (Triticum aestivum L.). J. Sci. Food Agric., 2016, 96(11), 3731-3740.
[http://dx.doi.org/10.1002/jsfa.7561] [PMID: 26676564]
[38]
Hill, C.B.; Taylor, J.D.; Edwards, J.; Mather, D.; Langridge, P.; Bacic, A.; Roessner, U. Detection of QTL for metabolic and agronomic traits in wheat with adjustments for variation at genetic loci that affect plant phenology. Plant Sci., 2015, 233, 143-154.
[http://dx.doi.org/10.1016/j.plantsci.2015.01.008] [PMID: 25711822]
[39]
Thorwarth, P.; Liu, G.; Ebmeyer, E.; Schacht, J.; Schachschneider, R.; Kazman, E.; Reif, J.C.; Würschum, T.; Longin, C.F.H. Dissecting the genetics underlying the relationship between protein content and grain yield in a large hybrid wheat population. Theor. Appl. Genet., 2019, 132(2), 489-500.
[http://dx.doi.org/10.1007/s00122-018-3236-x] [PMID: 30456718]
[40]
Saia, S.; Fragasso, M.; De Vita, P.; Beleggia, R. Metabolomics provides valuable insight for the study of durum wheat: a review. J. Agric. Food Chem., 2019, 67(11), 3069-3085.
[http://dx.doi.org/10.1021/acs.jafc.8b07097] [PMID: 30829031]
[41]
Heyneke, E.; Watanabe, M.; Erban, A.; Duan, G.; Buchner, P.; Walther, D. Effect of senescence phenotypes and nitrate availability on wheat leaf metabolome during grain filling. Agronomy (Basel), 2019, 9(6), 305.
[http://dx.doi.org/10.3390/agronomy9060305]
[42]
Bellesi, F.J.; Arata, A.F.; MartÝnez, M.; Arrigoni, A.C.; Stenglein, S.A.; Dinolfo, M.I. Degradation of gluten proteins by Fusarium species and their impact on the grain quality of bread wheat. J. Stored Prod. Res., 2019, 83, 1-8.
[http://dx.doi.org/10.1016/j.jspr.2019.05.007]
[43]
Barros Santos, M.C.; Ribeiro da Silva Lima, L.; Ramos Nascimento, F.; Pimenta do Nascimento, T.; Cameron, L.C.; Simões Larraz Ferreira, M. Metabolomic approach for characterization of phenolic compounds in different wheat genotypes during grain development. Food Res. Int., 2019, 124, 118-128.
[http://dx.doi.org/10.1016/j.foodres.2018.08.034] [PMID: 31466630]
[44]
Vergara-Diaz, O.; Vatter, T.; Vicente, R.; Obata, T.; Nieto-Taladriz, M.T.; Aparicio, N.; Carlisle Kefauver, S.; Fernie, A.; Araus, J.L. Metabolome profiling supports the key role of the spike in wheat yield performance. Cells, 2020, 9(4), 1025.
[http://dx.doi.org/10.3390/cells9041025] [PMID: 32326207]
[45]
Chen, J.; Hu, X.; Shi, T.; Yin, H.; Sun, D.; Hao, Y.; Xia, X.; Luo, J.; Fernie, A.R.; He, Z.; Chen, W. Metabolite-based genome-wide association study enables dissection of the flavonoid decoration pathway of wheat kernels. Plant Biotechnol. J., 2020, 18(8), 1722-1735.
[http://dx.doi.org/10.1111/pbi.13335] [PMID: 31930656]
[46]
Shi, T.; Zhu, A.; Jia, J.; Hu, X.; Chen, J.; Liu, W.; Ren, X.; Sun, D.; Fernie, A.R.; Cui, F.; Chen, W. Metabolomics analysis and metabolite-agronomic trait associations using kernels of wheat (Triticum aestivum) recombinant inbred lines. Plant J., 2020, 103(1), 279-292.
[http://dx.doi.org/10.1111/tpj.14727] [PMID: 32073701]
[47]
Wang, Z.; Shi, H.; Yu, S.; Zhou, W.; Li, J.; Liu, S.; Deng, M.; Ma, J.; Wei, Y.; Zheng, Y.; Liu, Y. Comprehensive transcriptomics, proteomics, and metabolomics analyses of the mechanisms regulating tiller production in low-tillering wheat. Theor. Appl. Genet., 2019, 132(8), 2181-2193.
[http://dx.doi.org/10.1007/s00122-019-03345-w] [PMID: 31020386]
[48]
Longin, F.; Beck, H.; Gütler, H.; Heilig, W.; Kleinert, M.; Rapp, M.; Philipp, N.; Erban, A.; Brilhaus, D.; Mettler-Altmann, T.; Stich, B. Aroma and quality of breads baked from old and modern wheat varieties and their prediction from genomic and flour-based metabolite profiles. Food Res. Int., 2020, 129, 108748.
[http://dx.doi.org/10.1016/j.foodres.2019.108748] [PMID: 32036907]
[49]
Tang, H.; Song, Y.; Guo, J.; Wang, J.; Zhang, L.; Niu, N.; Ma, S.; Zhang, G.; Zhao, H. Physiological and metabolome changes during anther development in wheat (Triticum aestivum L.). Plant Physiol. Biochem., 2018, 132, 18-32.
[http://dx.doi.org/10.1016/j.plaphy.2018.08.024] [PMID: 30172190]
[50]
Yu, Y.; Peng, Z.S.; Qu, J.P.; Chen, Z.Y.; Wei, S.H.; Liao, M.L. Comparative metabolomics and transcriptomics of pistils, stamens and pistilloid stamens widen key knowledge of pistil and stamen development in wheat. Czech J. Genet. Plant Breed., 2019, 56(1), 24-33.
[http://dx.doi.org/10.17221/70/2019-CJGPB]
[51]
Jones, OA Assessing pre-harvest sprouting in cereals using near-infrared spectroscopy-based metabolomics. NIR news, 2017, 28(1), 15-9.
[http://dx.doi.org/10.1177/0960336016687945]
[52]
Lavergne, F.D.; Broeckling, C.D.; Cockrell, D.M.; Haley, S.D.; Peairs, F.B.; Jahn, C.E.; Heuberger, A.L. GC-MS metabolomics to evaluate the composition of plant cuticular waxes for four Triticum aestivum cultivars. Int. J. Mol. Sci., 2018, 19(2), 249.
[http://dx.doi.org/10.3390/ijms19020249] [PMID: 29360745]
[53]
Chen, W.; Wang, W.; Peng, M.; Gong, L.; Gao, Y.; Wan, J.; Wang, S.; Shi, L.; Zhou, B.; Li, Z.; Peng, X.; Yang, C.; Qu, L.; Liu, X.; Luo, J. Comparative and parallel genome-wide association studies for metabolic and agronomic traits in cereals. Nat. Commun., 2016, 7(1), 12767.
[http://dx.doi.org/10.1038/ncomms12767] [PMID: 27698483]
[54]
Kim, H.K.; Verpoorte, R. Sample preparation for plant metabolomics. Phytochem. Anal., 2010, 21(1), 4-13.
[http://dx.doi.org/10.1002/pca.1188] [PMID: 19904733]
[55]
Li, N.; Song, Yp.; Tang, H.; Wang, Y. Recent developments in sample preparation and data pre-treatment in metabonomics research. Arch. Biochem. Biophys., 2016, 589, 4-9.
[http://dx.doi.org/10.1016/j.abb.2015.08.024] [PMID: 26342458]
[56]
Zhang, Y.; Ma, X.M.; Wang, X.C.; Liu, J.H.; Huang, B.Y.; Guo, X.Y.; Xiong, S.P.; La, G.X. UPLC-QTOF analysis reveals metabolomic changes in the flag leaf of wheat (Triticum aestivum L.) under low-nitrogen stress. Plant Physiol. Biochem., 2017, 111, 30-38.
[http://dx.doi.org/10.1016/j.plaphy.2016.11.009] [PMID: 27894005]
[57]
Nguyen, V.L.; Palmer, L.; Roessner, U.; Stangoulis, J. Genotypic variation in the root and shoot metabolite profiles of wheat (Triticum aestivum L.) indicate sustained, preferential carbon allocation as a potential mechanism in phosphorus efficiency. Front. Plant Sci., 2019, 10, 995.
[http://dx.doi.org/10.3389/fpls.2019.00995] [PMID: 31447867]
[58]
Beleggia, R.; Platani, C.; Nigro, F.; De Vita, P.; Cattivelli, L.; Papa, R. Effect of genotype, environment and genotype-by-environment interaction on metabolite profiling in durum wheat (Triticum durum Desf.) grain. J. Cereal Sci., 2013, 57(2), 183-192.
[http://dx.doi.org/10.1016/j.jcs.2012.09.004]
[59]
Kage, U.; Karre, S.; Kushalappa, A.C.; McCartney, C. Identification and characterization of a fusarium head blight resistance gene TaACT in wheat QTL-2DL. Plant Biotechnol. J., 2017, 15(4), 447-457.
[http://dx.doi.org/10.1111/pbi.12641] [PMID: 27663684]
[60]
Bernardo, L.; Carletti, P.; Badeck, F.W.; Rizza, F.; Morcia, C.; Ghizzoni, R.; Rouphael, Y.; Colla, G.; Terzi, V.; Lucini, L. Metabolomic responses triggered by Arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol. Biochem., 2019, 137, 203-212.
[http://dx.doi.org/10.1016/j.plaphy.2019.02.007] [PMID: 30802803]
[61]
Borrelli, G.M.; Fragasso, M.; Nigro, F.; Platani, C.; Papa, R.; Beleggia, R.; Trono, D. Analysis of metabolic and mineral changes in response to salt stress in durum wheat (Triticum turgidum ssp. durum) genotypes, which differ in salinity tolerance. Plant Physiol. Biochem., 2018, 133, 57-70.
[http://dx.doi.org/10.1016/j.plaphy.2018.10.025] [PMID: 30390432]
[62]
Yadav, A.K.; Carroll, A.J.; Estavillo, G.M.; Rebetzke, G.J.; Pogson, B.J. Wheat drought tolerance in the field is predicted by amino acid responses to glasshouse-imposed drought. J. Exp. Bot., 2019, 70(18), 4931-4948.
[http://dx.doi.org/10.1093/jxb/erz224] [PMID: 31189018]
[63]
Piasecka, A.; Kachlicki, P.; Stobiecki, M. Analytical methods for detection of plant metabolomes changes in response to biotic and abiotic stresses. Int. J. Mol. Sci., 2019, 20(2), 379.
[http://dx.doi.org/10.3390/ijms20020379] [PMID: 30658398]
[64]
Wishart, D.S. Advances in metabolite identification. Bioanalysis, 2011, 3(15), 1769-1782.
[http://dx.doi.org/10.4155/bio.11.155] [PMID: 21827274]
[65]
Cuperlovic-Culf, M.; Vaughan, M.M.; Vermillion, K.; Surendra, A.; Teresi, J.; McCormick, S.P. Effects of atmospheric CO2 level on the metabolic response of resistant and susceptible wheat to Fusarium graminearum infection. Mol. Plant Microbe Interact., 2019, 32(4), 379-391.
[http://dx.doi.org/10.1094/MPMI-06-18-0161-R] [PMID: 30256178]
[66]
Kim, H.K.; Choi, Y.H.; Verpoorte, R. NMR-based plant metabolomics: where do we stand, where do we go? Trends Biotechnol., 2011, 29(6), 267-275.
[http://dx.doi.org/10.1016/j.tibtech.2011.02.001] [PMID: 21435731]
[67]
Boiteau, R.M.; Hoyt, D.W.; Nicora, C.D.; Kinmonth-Schultz, H.A.; Ward, J.K.; Bingol, K. Structure elucidation of unknown metabolites in metabolomics by combined NMR and MS/MS prediction. Metabolites, 2018, 8(1), 8.
[http://dx.doi.org/10.3390/metabo8010008] [PMID: 29342073]
[68]
Shewry, P.R.; Corol, D.I.; Jones, H.D.; Beale, M.H.; Ward, J.L. Defining genetic and chemical diversity in wheat grain by 1H-NMR spectroscopy of polar metabolites. Mol. Nutr. Food Res., 2017, 61(7), 1600807.
[http://dx.doi.org/10.1002/mnfr.201600807] [PMID: 28087883]
[69]
Kang, Z.; Babar, M.A.; Khan, N.; Guo, J.; Khan, J.; Islam, S.; Shrestha, S.; Shahi, D. Comparative metabolomic profiling in the roots and leaves in contrasting genotypes reveals complex mechanisms involved in post-anthesis drought tolerance in wheat. PLoS One, 2019, 14(3), e0213502.
[http://dx.doi.org/10.1371/journal.pone.0213502] [PMID: 30856235]
[70]
Shavit, R.; Batyrshina, Z.S.; Dotan, N.; Tzin, V. Cereal aphids differently affect benzoxazinoid levels in durum wheat. PLoS One, 2018, 13(12), e0208103.
[http://dx.doi.org/10.1371/journal.pone.0208103] [PMID: 30507950]
[71]
Gunnaiah, R.; Kushalappa, A.C.; Duggavathi, R.; Fox, S.; Somers, D.J. Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS One, 2012, 7(7), e40695.
[http://dx.doi.org/10.1371/journal.pone.0040695] [PMID: 22866179]
[72]
Seybold, H.; Demetrowitsch, T.J.; Hassani, M.A.; Szymczak, S.; Reim, E.; Haueisen, J.; Lübbers, L.; Rühlemann, M.; Franke, A.; Schwarz, K.; Stukenbrock, E.H. A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition. Nat. Commun., 2020, 11(1), 1910.
[http://dx.doi.org/10.1038/s41467-020-15633-x] [PMID: 32313046]
[73]
Guo, R.; Yang, Z.; Li, F.; Yan, C.; Zhong, X.; Liu, Q.; Xia, X.; Li, H.; Zhao, L. Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol., 2015, 15(1), 170.
[http://dx.doi.org/10.1186/s12870-015-0546-x] [PMID: 26149720]
[74]
Redestig, H; Szymanski, J; Hirai, MY; Selbig, J; Willmitzer, L; Nikoloski, Z. Data integration, metabolic networks and systems biology. In: Annual Plant Reviews online; Roberts, J.A., Ed.; Wiley Online Library, 2018; pp. 261-316.
[http://dx.doi.org/10.1002/9781119312994.apr0469]
[75]
Liland, K.H. Multivariate methods in metabolomics–from pre-processing to dimension reduction and statistical analysis. Trends Analyt. Chem., 2011, 30(6), 827-841.
[http://dx.doi.org/10.1016/j.trac.2011.02.007]
[76]
Saccenti, E.; Hoefsloot, H.C.; Smilde, A.K.; Westerhuis, J.A.; Hendriks, M.M. Reflections on univariate and multivariate analysis of metabolomics data. Metabolomics, 2014, 10(3), 361-374.
[http://dx.doi.org/10.1007/s11306-013-0598-6]
[77]
Fiehn, O.; Barupal, D.K.; Kind, T. Extending biochemical databases by metabolomic surveys. J. Biol. Chem., 2011, 286(27), 23637-23643.
[http://dx.doi.org/10.1074/jbc.R110.173617] [PMID: 21566124]
[78]
Xu, Y.; Goodacre, R. Multiblock principal component analysis: an efficient tool for analyzing metabolomics data which contain two influential factors. Metabolomics, 2012, 8(1), 37-51.
[http://dx.doi.org/10.1007/s11306-011-0361-9]
[79]
Gardinassi, L.G.; Xia, J.; Safo, S.E.; Li, S. Bioinformatics tools for the interpretation of metabolomics data. Curr. Pharmacol. Rep., 2017, 3(6), 374-383.
[http://dx.doi.org/10.1007/s40495-017-0107-0]
[80]
Wang, X.; Hou, L.; Lu, Y.; Wu, B.; Gong, X.; Liu, M.; Wang, J.; Sun, Q.; Vierling, E.; Xu, S. Metabolic adaptation of wheat grain contributes to a stable filling rate under heat stress. J. Exp. Bot., 2018, 69(22), 5531-5545.
[http://dx.doi.org/10.1093/jxb/ery303] [PMID: 30476278]
[81]
Zhao, Y.; Zhou, M.; Xu, K.; Li, J.; Li, S.; Zhang, S. Integrated transcriptomics and metabolomics analyses provide insights into cold stress response in wheat. Crop J., 2019, 7(6), 857-866.
[http://dx.doi.org/10.1016/j.cj.2019.09.002]
[82]
Koobaz, P.; Reza Ghaffari, M.; Heidari, M.; Mirzaei, M.; Ghanati, F.; Amirkhani, A.; Mortazavi, S.E.; Moradi, F.; Hajirezaei, M.R.; Salekdeh, G.H. Proteomic and metabolomic analysis of desiccation tolerance in wheat young seedlings. Plant Physiol. Biochem., 2020, 146, 349-362.
[http://dx.doi.org/10.1016/j.plaphy.2019.11.017] [PMID: 31786507]
[83]
Cuperlovic-Culf, M.; Wang, L.; Forseille, L.; Boyle, K.; Merkley, N.; Burton, I.; Fobert, P.R. Metabolic biomarker panels of response to fusarium head blight infection in different wheat varieties. PLoS One, 2016, 11(4), e0153642.
[http://dx.doi.org/10.1371/journal.pone.0153642] [PMID: 27101152]
[84]
Özkaya, B.; Turksoy, S.; Özkaya, H.; Baumgartner, B.; Özkeser, İ.; Köksel, H. Changes in the functional constituents and phytic acid contents of firiks produced from wheats at different maturation stages. Food Chem., 2018, 246, 150-155.
[http://dx.doi.org/10.1016/j.foodchem.2017.11.022] [PMID: 29291833]
[85]
Zhen, S.; Zhou, J.; Deng, X.; Zhu, G.; Cao, H.; Wang, Z. Metabolite profiling of the response to high-nitrogen fertilizer during grain development of bread wheat (Triticum aestivum L.). J. Cereal Sci., 2016, 69, 85-94.
[http://dx.doi.org/10.1016/j.jcs.2016.02.014]
[86]
Corol, D.I.; Ravel, C.; Rakszegi, M.; Charmet, G.; Bedo, Z.; Beale, M.H.; Shewry, P.R.; Ward, J.L. (1)H-NMR screening for the high-throughput determination of genotype and environmental effects on the content of asparagine in wheat grain. Plant Biotechnol. J., 2016, 14(1), 128-139.
[http://dx.doi.org/10.1111/pbi.12364] [PMID: 25816894]
[87]
Das, A.; Kim, D-W.; Khadka, P.; Rakwal, R.; Rohila, J.S. Unraveling key metabolomic alterations in wheat embryos derived from freshly harvested and water-imbibed seeds of two wheat cultivars with contrasting dormancy status. Front. Plant Sci., 2017, 8, 1203.
[http://dx.doi.org/10.3389/fpls.2017.01203] [PMID: 28747920]
[88]
Bowne, J.B.; Erwin, T.A.; Juttner, J.; Schnurbusch, T.; Langridge, P.; Bacic, A.; Roessner, U. Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Mol. Plant, 2012, 5(2), 418-429.
[http://dx.doi.org/10.1093/mp/ssr114] [PMID: 22207720]
[89]
Rahman, M.A.; Akond, M.; Babar, M.A.; Beecher, C.; Erickson, J.; Thomason, K. LC-HRMS based non-targeted metabolomic profiling of Wheat (Triticum aestivum L.) under post-anthesis drought stress. Am. J. Plant Sci., 2017, 8(12), 3024-3061.
[http://dx.doi.org/10.4236/ajps.2017.812205]
[90]
Aidoo, M.K.; Quansah, L.; Galkin, E.; Batushansky, A.; Wallach, R.; Moshelion, M. A combination of stomata deregulation and a distinctive modulation of amino acid metabolism are associated with enhanced tolerance of wheat varieties to transient drought. Metabolomics, 2017, 13(11), 138.
[http://dx.doi.org/10.1007/s11306-017-1267-y]
[91]
Guo, X.; Xin, Z.; Yang, T.; Ma, X.; Zhang, Y.; Wang, Z.; Ren, Y.; Lin, T. Metabolomics response for drought stress tolerance in chinese wheat genotypes (Triticum aestivum). Plants (Basel), 2020, 9(4), 520.
[http://dx.doi.org/10.3390/plants9040520] [PMID: 32316652]
[92]
Guo, R.; Shi, L.; Jiao, Y.; Li, M.; Zhong, X.; Gu, F.; Liu, Q.; Xia, X.; Li, H. Metabolic responses to drought stress in the tissues of drought-tolerant and drought-sensitive wheat genotype seedlings. AoB Plants, 2018, 10(2), ply016.
[http://dx.doi.org/10.1093/aobpla/ply016] [PMID: 29623182]
[93]
Michaletti, A.; Naghavi, M.R.; Toorchi, M.; Zolla, L.; Rinalducci, S. Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Sci. Rep., 2018, 8(1), 5710.
[http://dx.doi.org/10.1038/s41598-018-24012-y] [PMID: 29632386]
[94]
Che-Othman, M.H.; Jacoby, R.P.; Millar, A.H.; Taylor, N.L. Wheat mitochondrial respiration shifts from the tricarboxylic acid cycle to the GABA shunt under salt stress. New Phytol., 2020, 225(3), 1166-1180.
[http://dx.doi.org/10.1111/nph.15713] [PMID: 30688365]
[95]
Woodrow, P.; Ciarmiello, L.F.; Annunziata, M.G.; Pacifico, S.; Iannuzzi, F.; Mirto, A.; D’Amelia, L.; Dell’Aversana, E.; Piccolella, S.; Fuggi, A.; Carillo, P. Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol. Plant., 2017, 159(3), 290-312.
[http://dx.doi.org/10.1111/ppl.12513] [PMID: 27653956]
[96]
Bouthour, D.; Kalai, T.; Chaffei, H.C.; Gouia, H.; Corpas, F.J. Differential response of NADP-dehydrogenases and carbon metabolism in leaves and roots of two durum wheat (Triticum durum Desf.) cultivars (Karim and Azizi) with different sensitivities to salt stress. J. Plant Physiol., 2015, 179, 56-63.
[http://dx.doi.org/10.1016/j.jplph.2015.02.009] [PMID: 25835711]
[97]
Cheong, B.E.; Ho, W.W.H.; Biddulph, B.; Wallace, X.; Rathjen, T.; Rupasinghe, T.W.T.; Roessner, U.; Dolferus, R. Phenotyping reproductive stage chilling and frost tolerance in wheat using targeted metabolome and lipidome profiling. Metabolomics, 2019, 15(11), 144.
[http://dx.doi.org/10.1007/s11306-019-1606-2] [PMID: 31630279]
[98]
Khan, F.; Fuentes, D.; Threthowan, R.; Mohammad, F.; Ahmad, M. Comparative metabolite profiling of two wheat genotypes as affected by nitrogen stress at seedling stage. J. Anim. Plant Sci., 2019, 29, 260-268.
[99]
Heyneke, E.; Watanabe, M.; Erban, A.; Duan, G.; Buchner, P.; Walther, D.; Kopka, J.; Hawkesford, M.J.; Hoefgen, R. Characterization of the wheat leaf metabolome during grain filling and under varied N-supply. Front. Plant Sci., 2017, 8, 2048.
[http://dx.doi.org/10.3389/fpls.2017.02048] [PMID: 29238358]
[100]
Beleggia, R.; Omranian, N.; Holtz, Y.; Gioia, T.; Fiorani, F.; Nigro, F. Comparative analysis based on transcriptomics and metabolomics data reveal differences between emmer and durum wheat in response to nitrogen starvation. bioRxiv, 2020.
[101]
Balmer, D.; Flors, V.; Glauser, G.; Mauch-Mani, B. Metabolomics of cereals under biotic stress: current knowledge and techniques. Front. Plant Sci., 2013, 4, 82.
[http://dx.doi.org/10.3389/fpls.2013.00082] [PMID: 23630531]
[102]
Batyrshina, Z.S.; Yaakov, B.; Shavit, R.; Singh, A.; Tzin, V. Comparative transcriptomic and metabolic analysis of wild and domesticated wheat genotypes reveals differences in chemical and physical defense responses against aphids. BMC Plant Biol., 2020, 20(1), 19.
[http://dx.doi.org/10.1186/s12870-019-2214-z] [PMID: 31931716]
[103]
Chandrasekhar, K.; Shavit, R.; Distelfeld, A.; Christensen, S.A.; Tzin, V. Exploring the metabolic variation between domesticated and wild tetraploid wheat genotypes in response to corn leaf aphid infestation. Plant Signal. Behav., 2018, 13(6), e1486148.
[http://dx.doi.org/10.1080/15592324.2018.1486148] [PMID: 29944455]
[104]
Vassiliadis, S.; Plummer, K.M.; Powell, K.S.; Rochfort, S.J. Elevated CO2 and virus infection impacts wheat and aphid metabolism. Metabolomics, 2018, 14(10), 133.
[http://dx.doi.org/10.1007/s11306-018-1425-x] [PMID: 30830473]
[105]
Bönnighausen, J.; Schauer, N.; Schäfer, W.; Bormann, J. Metabolic profiling of wheat rachis node infection by Fusarium graminearum - decoding deoxynivalenol-dependent susceptibility. New Phytol., 2019, 221(1), 459-469.
[http://dx.doi.org/10.1111/nph.15377] [PMID: 30084118]
[106]
Kage, U.; Hukkeri, S.; Kushalappa, A.C. Liquid chromatography and high resolution mass spectrometry-based metabolomics to identify quantitative resistance-related metabolites and genes in wheat QTL-2DL against Fusarium head blight. Eur. J. Plant Pathol., 2018, 151(1), 125-139.
[107]
Ye, W.; Liu, T.; Zhang, W.; Li, S.; Zhu, M.; Li, H.; Kong, Y.; Xu, L. Disclosure of the molecular mechanism of wheat leaf spot disease caused by Bipolaris sorokiniana through comparative transcriptome and metabolomics analysis. Int. J. Mol. Sci., 2019, 20(23), 6090.
[http://dx.doi.org/10.3390/ijms20236090] [PMID: 31816858]
[108]
Matros, A.; Liu, G.; Hartmann, A.; Jiang, Y.; Zhao, Y.; Wang, H.; Ebmeyer, E.; Korzun, V.; Schachschneider, R.; Kazman, E.; Schacht, J.; Longin, F.; Reif, J.C.; Mock, H.P. Genome-metabolite associations revealed low heritability, high genetic complexity, and causal relations for leaf metabolites in winter wheat (Triticum aestivum). J. Exp. Bot., 2017, 68(3), 415-428.
[PMID: 28007948]
[109]
Razzaq, A.; Saleem, F.; Kanwal, M.; Mustafa, G.; Yousaf, S.; Imran Arshad, H.M.; Hameed, M.K.; Khan, M.S.; Joyia, F.A. Modern trends in plant genome editing: an inclusive review of the CRISPR/Cas9 toolbox. Int. J. Mol. Sci., 2019, 20(16), 4045.
[http://dx.doi.org/10.3390/ijms20164045] [PMID: 31430902]
[110]
Watson, A.; Ghosh, S.; Williams, M.J.; Cuddy, W.S.; Simmonds, J.; Rey, M-D.; Asyraf Md Hatta, M.; Hinchliffe, A.; Steed, A.; Reynolds, D.; Adamski, N.M.; Breakspear, A.; Korolev, A.; Rayner, T.; Dixon, L.E.; Riaz, A.; Martin, W.; Ryan, M.; Edwards, D.; Batley, J.; Raman, H.; Carter, J.; Rogers, C.; Domoney, C.; Moore, G.; Harwood, W.; Nicholson, P.; Dieters, M.J.; DeLacy, I.H.; Zhou, J.; Uauy, C.; Boden, S.A.; Park, R.F.; Wulff, B.B.H.; Hickey, L.T. Speed breeding is a powerful tool to accelerate crop research and breeding. Nat. Plants, 2018, 4(1), 23-29.
[http://dx.doi.org/10.1038/s41477-017-0083-8] [PMID: 29292376]

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