Abstract
Metabolites in maize kernels are associated not only with nutritional value but also physiological properties such as maturation, desiccation, and germination. However, comprehensive information concerning the metabolome of maize kernels is limited. In this study, we identified 210 metabolites in mature kernels of 14 representative maize lines using a non-targeted metabolomic profiling approach. Further statistical analysis revealed that 75 metabolites were significantly variable among those tested lines, and certain metabolites out of the detected 210 metabolites played critical roles in distinguishing one line from another. Additionally, metabolite–metabolite correlation analysis dissected key regulatory elements or pathways involved in metabolism of lipids, amino acids and carbohydrates. Furthermore, an integrated metabolic map constructed with transcriptomic, proteomic and metabolic data uncovered characteristic regulatory mechanisms of maize kernel metabolism. Altogether, this work provides new insights into the maize kernel metabolome that would be useful for metabolic engineering and/or molecular breeding to improve maize kernel quality and yield.
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Ali, Q., Ashraf, M., Anwar, F., & Al-Qurainy, F. (2012). Trehalose-induced changes in seed oil composition and antioxidant potential of maize grown under drought stress. Journal of the American Oil Chemists Society, 89, 1485–1493.
Angelovici, R., Galili, G., Fernie, A. R., et al. (2010). Seed desiccation: A bridge between maturation and germination. Trends in Plant Science, 15(4), 211–218.
Benjamini, Y., & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Annals of Statistics, 29, 1165–1188.
Cañas, R. A., Amiour, N., Quilleré, I., et al. (2011). An integrated statistical analysis of the genetic variability of nitrogen metabolism in the ear of three maize inbred lines (Zea mays L.). Journal of Experimental Botany, 62, 2309–2318.
Chang, Y., Zhao, C., Zhu, Z., et al. (2012). Metabolic profiling based on LC/MS to evaluate unintended effects of transgenic rice with cry1Ac and sck genes. Plant Molecular Biology, 78, 477–487.
Chen, Y., & Burris, J. S. (1990). Role of carbohydrates in desiccation tolerance and membrane behavior in maturing maize seed. Crop Science, 30, 971–975.
Chen, R., Xue, G., Chen, P., et al. (2008). Transgenic maize plants expressing a fungal phytase gene. Transgenic Research, 17, 633–643.
Dierking, E. C., & Bilyeu, K. D. (2009). Raffinose and stachyose metabolism are not required for efficient soybean seed germination. Journal of Plant Physiology, 166, 1329–1335.
Evans, A. M., DeHaven, C. D., Barrett, T., et al. (2009). Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Analytical Chemistry, 81(16), 6656–6667.
Fait, A., Angelovici, R., Less, H., et al. (2006). Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiology, 142(3), 839–854.
Fernández-Bañares, F., Esteve, M., & Viver, J. M. (2009). Fructose-sorbitol malabsorption. Current Gastroenterology Reports, 11(5), 368–374.
Fernie, A. R., & Schauer, N. (2009). Metabolomics-assisted breeding: A viable option for crop improvement? Trends in Genetics, 25, 39–48.
Frank, T., Röhlig, R. M., Davies, H. V., Barros, E., & Engel, K. H. (2012). Metabolite profiling of maize kernels–genetic modification versus environmental influence. Journal of Agriculture and Food Chemistry, 60, 3005–3012.
Fu, Z., Jin, X., Ding, D., Li, Y., Fu, Z., & Tang, J. (2011). Proteomic analysis of heterosis during maize seed germination. Proteomics, 118, 1462–1472.
Fu, J., Thiemann, A., Schrag, T., Melchinger, A., Scholten, S., & Frisch, M. (2010). Dissecting grain yield pathways and their interactions with grain dry matter content by a two-step correlation approach with maize seedling transcriptome. BMC Plant Biology, 10, 63.
Handley, L. W., Pharr, D. M., & McFeeters, R. F. (1983). Carbohydrate changes during maturation of cucumber fruit: Implications for sugar metabolism and transport. Plant Physiology, 72, 498–502.
Harrigan, G. G., Stork, L. G., Riordan, S. G., et al. (2007). Impact of genetics and environment on nutritional and metabolite components of maize grain. Journal of Agriculture and Food Chemistry, 55, 6177–6185.
Islam, M. S., & Sakaguchi, E. (2006). Sorbitol-based osmotic diarrhea: Possible causes and mechanism of prevention investigated in rats. World Journal of Gastroenterology, 12, 7635–7641.
Jacobson, E. L., Lange, R. A., & Jacobson, M. K. (1979). Pyridine nucleotide synthesis in 3T3 cells. Journal of Cellular Physiology, 99, 417–425.
Jiao, Y., Zhao, H., Ren, L., et al. (2012). Genome-wide genetic changes during modern breeding of maize. Nature Genetics, 44, 812–815.
Kametani, T., & Furuyama, H. (1987). Synthesis of vitamin D3 and related compounds. Medicinal Research Reviews, 7, 147–171.
Keurentjes, J. J., Fu, J., De Vos, C. R., et al. (2006). The genetics of plant metabolism. Nature Genetics, 38, 842–849.
Kusano, M., Fukushima, A., Redestig, H., & Saito, K. (2011). Metabolomic approaches toward understanding nitrogen metabolism in plants. Journal of Experimental Botany, 62(4), 1439–1453.
Lai, J., Li, R., Xu, X., et al. (2010). Genome-wide patterns of genetic variation among elite maize inbred lines. Nature Genetics, 42, 1027–1030.
Lawton, K. A., Berger, A., Mitchell, M., et al. (2008). Analysis of the adult human plasma metabolome. Pharmacogenomics, 9(4), 383–397.
Li, H., Peng, Z., Yang, X., et al. (2012a). Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nature Genetics, 45, 43–50.
Li, Q., Yang, X., Xu, S., et al. (2012b). Genome-wide association studies identified three independent polymorphisms associated with α-tocopherol content in maize kernels. PLoS ONE, 7, e36807.
Lisec, J., Römisch-Margl, L., Nikoloski, Z., et al. (2011). Corn hybrids display lower metabolite variability and complex metabolite inheritance patterns. Plant Journal, 68, 326–336.
Liu, K., Goodman, M., Muse, S., Smith, J. S., Buckler, E., & Doebley, J. (2003). Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics, 165, 2117–2128.
Liu, Q., Majdi, M., Cankar, K., et al. (2011). Reconstitution of the costunolide biosynthetic pathway in yeast and Nicotianabenthamiana. PLoS ONE, 6, e23255.
Matsuoka, Y., Vigouroux, Y., Goodman, M. M., Sanchez, J., Buckler, E., & Doebley, J. (2002). A single domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the National Academy of Sciences of the United States of America, 99, 6080–6084.
Moussaieff, A., Rogachev, I., Brodsky, L., et al. (2013). High-resolution metabolic mapping of cell types in plant roots. Proceedings of the National Academy of Sciences of the United States of America, 110, E1232–E1241.
Nambara, E., & Nonogaki, H. (2012). Seed biology in the 21st century: Perspectives and new directions. Plant and Cell Physiology, 53, 1–4.
Nowacki, J., & Bandurski, R. S. (1980). Myo-inositol esters of indole-3-acetic acid as seed auxin precursors of Zea mays L. Plant Physiology, 65, 422–427.
Ohta, T., Masutomi, N., Tsutsui, N., et al. (2009). Untargeted metabolomic profiling as an evaluative tool of fenofibrate-induced toxicology in Fischer 344 male rats. Toxicologic Pathology, 37(4), 521–535.
Oliver, M. J., Guo, L., Alexander, D. C., Ryals, J. A., Wone, B. W., & Cushman, J. C. (2011). A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell, 23, 1231–1248.
Raboy, V., Gerbasi, P. F., Young, K. A., et al. (2000). Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1. Plant Physiology, 124, 355–368.
Raboy, V., Young, K. A., Dorsch, J. A., & Cook, A. (2001). Genetics and breeding of seed phosphorus and phytic acid. Journal of Plant Physiology, 158, 489–497.
Rao, J., Yang, L., Wang, C., Zhang, D., & Shi, J. (2013). Digital gene expression analysis of mature seeds of transgenic maize overexpressing Aspergillus niger phyA2 and its non-transgenic counterpart. GM Crops and Food: Biotechnology in Agriculture and the Food Chain, 4(2), 1–11.
Redzynia, I., Ziółkowska, N. E., Majzner, W. R., et al. (2009). Structural investigation of biologically active phenolic compounds isolated from European tree species. Molecules, 14, 4147–4158.
Reumann, S., Quan, S., Aung, K., et al. (2009). In-depth proteome analysis of Arabidopsis leaf peroxisomes combined with in vivo subcellular targeting verification indicates novel metabolic and regulatory functions of peroxisomes. Plant Physiology, 150, 125–143.
Riedelsheimer, C., Czedik-Eysenberg, A., Grieder, C., et al. (2012a). Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nature Genetics, 44, 217–220.
Riedelsheimer, C., Lisec, J., Czedik-Eysenberg, A., et al. (2012b). Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proceedings of the National Academy of Sciences of the United States of America, 109, 8872–8877.
Schmid, M., Davison, T. S., Henz, S. R., et al. (2005). A gene expression map of Arabidopsis thaliana development. Nature Genetics, 37, 501–506.
Schmid, K. M., & Ohlrogge, J. B. (2002). Lipid metabolism in plants. New Comprehensive Biochemistry, 36, 93–126.
Serna-Saldivar, S. O., Gomez, M. H., & Rooney, L. W. (1994). Food uses of regular and specialty corns and their dry-milled fractions. In A. R. Hallauer (Ed.), Specialty corns (pp. 263–298). Boca Raton: CRC Press.
Skogerson, K., Harrigan, G. G., Reynolds, T. L., et al. (2010). Impact of genetics and environment on the metabolite composition of maize grain. Journal of Agriculture and Food Chemistry, 58, 3600–3610.
Takaha, T., & Smith, S. M. (1999). The functions of 4-alpha-glucanotransferases and their use for the production of cyclic glucans. Biotechnology and Genetic Engineering Reviews, 16, 257–280.
Toubiana, D., Semel, Y., Tohge, T., et al. (2012). Metabolic profiling of a mapping population exposes new insights in the regulation of seed metabolism and seed, fruit, and plant relations. PLoS Genetics, 8, e1002612.
Ueda, M., & Bandurski, R. S. (1969). A quantitative estimation of alkali-labile indole-3-acetic acid compounds in dormant and germinating maize kernels. Plant Physiology, 44, 1175–1181.
Van Der Maarel, M. J., Van Der Veen, B., Uitdehaag, J., Leemhuis, H., & Dijkhuizen, L. (2002). Properties and applications of starch-converting enzymes of the alpha-amylase family. Journal of Biotechnology, 94, 137–155.
Voelker, T., & Kinney, A. J. (2001). Variations in the biosynthesis of seed-storage lipids. Annual Review of Plant Biology, 52, 335–361.
Wang, G., Wang, G., Wang, F., & Song, R. (2012). A transcriptional roadmap for seed development in maize. In G. K. Agrawal & R. Rakwal (Eds.), Seed development: Omics technologies toward improvement of seed quality and crop yield (pp. 81––97). Netherlands: Springer.
Weber, H., Heim, U., Golombek, S., Borisjuk, L., & Wobus, U. (1998). Assimilate uptake and the regulation of seed development. Seed Science Research, 8, 331–345.
Weckwerth, W., & Fiehn, O. (2002). Can we discover novel pathways using metabolomic analysis? Current Opinion in Biotechnology, 13, 156–160.
Xu, Y. Z., De la Rosa Santamaria, R., Virdi, K. S., et al. (2012). The chloroplast triggers developmental reprogramming when MUTS HOMOLOG1 is suppressed in plants. Plant Physiology, 159, 710–720.
Yang, X. S., Staub, J. M., Pandravada, A., et al. (2013). Omics technologies reveal abundant natural variation in metabolites and transcripts among conventional maize hybrids. Food Nutrients, 4, 335–341.
Zachariou, M., & Scopes, R. K. (1986). Glucose-fructose oxidoreductase, a new enzyme isolated from Zymomonas mobilis that is responsible for sorbitol production. Journal of Bacteriology, 167, 863–869.
Zheng, Z. L. (2009). Carbon and nitrogen nutrient balance signaling in plants. Plant Signaling and Behaviour, 4, 584–591.
Acknowledgments
We thank Mrs. Qian Luo, Mrs. Jin Zhou, and Dr. Guorun Qu for their assistance in the metabolomic analysis. This work was supported by the China National Transgenic Plant Special Fund (2011ZX08012-002 and 2013ZX08012-002), China Innovative Research Team, Ministry of Education, and 111 Project (B14016).
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Rao, J., Cheng, F., Hu, C. et al. Metabolic map of mature maize kernels. Metabolomics 10, 775–787 (2014). https://doi.org/10.1007/s11306-014-0624-3
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DOI: https://doi.org/10.1007/s11306-014-0624-3