Omics Technologies Reveal Abundant Natural Variation in Metabolites and Transcripts among Conventional Maize Hybrids

Xiaofeng S. Yang, Jeffrey M. Staub, Anand Pandravada, Susan G. Riordan, Yongpan Yan, Gary A. Bannon, Susan J. Martino-Catt

DuPont Pioneer, Thondhebhavi, India..
Monsanto Company, St. Louis, USA.

DOI: 10.4236/fns.2013.43044                

Abstract

In this report we have evaluated metabolite and RNA profiling technologies to begin to understand the natural variation in these biomolecules found in commercial-quality, conventional (non-GM) maize hybrids. Our analyses focus on mature grain, the article of commerce that is most typically subjected to the rigorous studies involved in the comparative safety assessment of GM products. We have used a population of conventionally-bred maize hybrids that derive from closely related inbred parents grown under standard field conditions across geographically similar locations. This study highlights the large amount of natural variation in metabolites and transcripts across conventional maize germplasm grown under normal field conditions, and underscores the critical need for further extensive studies before these technologies can be seriously considered for utility in the comparative safety assessment of GM crops.

Keywords

Metabolite Profiling; RNA Profiling; Maize; Conventional Hybrids; GM Crops; Natural Variation; Omics-Technologies; Safety Assessment

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. Bruinsma, “World Agriculture: Towards 2015/2030: An FAO Perspective,” FAO (Food and Agriculture Organization), Rome, 2003.
[2]	C. James, “ISAAA Brief No. 41: Global Status of Commercialized Biotech/GM Crops: 2009,” ISAAA (International Service for the Acquisition of Agri-biotech Applications), Ithaca, 2009.
[3]	F. J. Perlak, R. L. Fuchs, D. A. Dean, S. L. McPherson and D. A. Fischhoff, “Modification of the Coding Sequence Enhances Plant Expression of Insect Control Protein Genes,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 88, No. 8, 1991, pp. 3324-3328. doi:10.1073/pnas.88.8.3324
[4]	S. R. Padgette, K. H. Kolacz, X. Delannay, D. B. Re, B. J. LaVallee, C. N. Tinius, W. K. Rhodes, Y. I. Otero, G. F. Barry, D. A. Eichholtz, V. M. Peschke, D. L. Nida, N. B. Taylor and G. M. Kishore, “Development, Identification, and Characterization of a Glyphosate-Tolerant Soybean Line,” Crop Science, Vol. 35, No. 5, 1995, pp. 1451-1461. doi:10.2135/cropsci1995.0011183X003500050032x
[5]	P. Castiglioni, D. Warner, R. J. Bensen, D. C. Anstrom, J. Harrison, M. Stoecker, M. Abad, G. Kumar, S. Salvador, R. D'Ordine, S. Navarro, S. Back, M. Fernandes, J. Targolli, S. Dasgupta, C. Bonin, M. H. Luethy and J. E. Heard, “Bacterial RNA Chaperones Confer Abiotic Stress Tolerance in Plants and Improved Grain Yield in Maize under Water-Limited Conditions,” Plant Physiology, Vol. 147, No. 2, 2008, pp. 446-455. doi:10.1104/pp.108.118828
[6]	C. Paoletti, E. Flamm, W. Yan, S. Meek, S. Renckens, M. Fellous and H. Kuiper, “GMO Risk Assessment around the World: Some Examples,” Trends in Food Science & Technology, Vol. 19, No. S1, 2008, pp. S70-S78. doi:10.1016/j.tifs.2008.07.007
[7]	C. James, “ISAAA Brief No. 37: Global Status of Commercialized Biotech/GM Crops: 2007,” ISAAA (International Service for the Acquisition of Agri-biotech Applications), Ithaca, 2007.
[8]	B. M. Chassy, “Food Safety Evaluation of Crops Produced through Biotechnology,” Journal of the American College of Nutrition, Vol. 21, No. 3, 2002, pp. 166S-173S.
[9]	A. Cockburn, “Assuring the Safety of Genetically Modified (GM) Foods: The Importance of a Holistic, Integrative Approach,” Journal of Biotechnology, Vol. 98, No.1, 2002, pp. 79-106. doi:10.1016/S0168-1656(02)00088-3
[10]	M. A. Martens, “Safety Evaluation of Genetically Modified Foods,” International Archives of Occupational and Environmental Health, Vol. 73, No. 1, 2000, pp. S14-S18. doi:10.1007/PL00014618
[11]	S. B. Metzdorff, E. J. Kok, P. Knuthsen and J. Pedersen, “Evaluation on a Non-Targeted ‘Omic’ Approach in the Safety Assessment of Genetically Modified Plants,” Plant Biology, Vol. 8, No. 5, 2006, pp. 662-672. doi:10.1055/s-2006-924151
[12]	P. R. Shewry, M. Baudo, A. Lovegrove, S. Powers, J. A. Napier, J. L. Ward, J. M. Baker and M. H. Beale, “Are GM and Conventionally Bred Cereals Really Different?” Trends in Food Science and Technology, Vol. 18, No. 4, 2007, pp. 201-209. doi:10.1016/j.tifs.2006.12.010
[13]	D. Corpillo, G. Gardini, A. M. Vaira, M. Basso, S. Aime, G. P. Accotto and M. Fasano, “Proteomics as a Tool to Improve Investigation of Substantial Equivalence in Genetically Modified Organisms: The Case of a Virus-Resistant Tomato,” Proteomics, Vol. 4, No. 1, 2004, pp. 193-200. doi:10.1002/pmic.200300540
[14]	F. Cellini, A. Chesson, I. Colquhoun, A. Constable, H. V. Davies, K. H. Engel, A. M. R. Gatehouse, S. K?renlampi, E. J. Kok, J. J. S. Leguay, H. P. Lehesranta, J. M. Noteborn, J. Pedersen and M. Smith, “Unintended Effects and Their Detection in Genetically Modified Crops,” Food and Chemical Toxicology, Vol. 42, No. 7, 2004, pp. 1089-1125. doi:10.1016/j.fct.2004.02.003
[15]	E. Barros, S. Lezar, M. J. Anttonen, J. P. Van Dijk, R. M. Rohlig, E. J. Kok and K. H. Engel, “Comparison of Two GM Maize Varieties with a New-Isogenic Non-GM Variety Using Transcriptomics, Proteomics and Metabolomics,” Plant Biotechnology Journal, Vol. 8, No. 4, 2010, pp. 436-451. doi:10.1111/j.1467-7652.2009.00487.x
[16]	A. Brazma, P. Hingamp, J. Quackenbush, G. Sherlock, P. Spellman, C. Stoeckert, J. Aach, W. Ansorge, C. A. Ball, H. C. Causton, T. Gaasterland, P. Glenisson, F. C. Holstege, I. F. Kim, V. Markowitz, J. C. Matese, H. Parkinson, A. Robinson, U. Sarkans, S. Schulze-Kremer, J. Stewart, R. Taylor, J. Vilo and M. Vingron, “Minimum Information about a Microarray Experiment (MIAME)Toward Standards for Microarray Data,” Nature Genetics, Vol. 29, No. 4, 2001, pp. 365-371. doi:10.1038/ng1201-365
[17]	J. E. Larkin, B. C. Frank, H. Gavras, R. Sultana and J. Quackenbush, “Independence and Reproducibility across Microarray Platforms,” Nature Methods, Vol. 2, No. 5, 2005, pp. 337-343. doi:10.1038/nmeth757
[18]	D. A. Nettleton, “Discussion of Statistical Methods for Design and Analysis of Microarray Experiments for Plant Scientists,” The Plant Cell, Vol. 18, No. 9, 2006, pp. 2112-2121. doi:10.1105/tpc.106.041616
[19]	C. F. Taylor, N. W. Paton, K. S. Lilley, P. A. Binz, R. K. Julian, A. R. Jones, W. Zhu, R. Apweiler, R. Aebersold, E. W. Deutsch, M. J. Dunn, A. J. Heck, A. Leitner, M. Macht, M. Mann, L. Martens, T. A. Neubert, S. D. Patterson, P. Ping, S. L. Seymour, P. Souda, A. Tsugita, J. Vandekerckhove, T. M. Vondriska, J. P. Whitelegge, M. R. Wilkins, I. Xenarios, J. R. Yates and H. Hermjakob, “The Minimum Information about a Proteomics Experiment (MIAPE),” Nature Biotechnology, Vol. 25, No. 8, 2007, pp. 887-893. doi:10.1038/nbt1329
[20]	H. Jenkins, N. Hardy, M. Beckmann, J. Draper, A. R. Smith, J. Taylor, O. Fiehn, R. Goodacre, R. J. Bino, R. Hall, J. Kopka, G. A. Lane, B. M. Lange, J. R. Liu, P. Mendes, B. J. Nikolau, S. G. Oliver, N. W. Paton, S. Rhee, U. Roessner-Tunali, K. Saito, J. Smedsgaard, L. W. Sumner, T. Wang, S. Walsh, E. S. Wurtele and D. B. Kell, “A Proposed Framework for the Description of Plant Metabolomics Experiments and Their Results,” Nature Biotechnology, Vol. 22, No. 12, 2004, pp. 1601-1606. doi:10.1038/nbt1041
[21]	W. P. Ridley, R. D. Shillito, I. Coats, H-Y Steiner, M. Shawgo, A. Phillips, P. Dussold and L. Kurtyka, “Development of the International Life Sciences Institute Crop Composition Database,” Journal of Food Composition and Analysis, Vol. 17, No. 3-4, 2004, pp. 423-438. doi:10.1016/j.jfca.2004.03.006
[22]	W. P. Ridley, R. S. Sidhu, P. D. Pyla, M. A. Nemeth, M. L. Breeze and J. D. Astwood, “Comparison of the Nutritional Profile of Glyphosate-Tolerant Corn Event NK603 with That of Conventional Corn (Zea mays L. ),” Journal of Agricultural and Food Chemistry, Vol. 50, No. 25, 2002, pp. 7235-7243. doi:10.1021/jf0205662
[23]	J. C. Obert, W. P. Ridley, R. W. Schneider, S. G. Riordan, M. A. Nemeth, W. A. Trujillo, M. L. Breeze, R. Sorbet, and J. D. Astwood, “The Composition of Grain and Forage from Glyphosate Tolerant Wheat MON 71800 Is Equivalent to That of Conventional Wheat (Triticum aestivum L. ),” Journal of Agricultural and Food Chemistry, Vol. 52, No. 5, 2004, pp. 1375-1384. doi:10.1021/jf035218u
[24]	S. M. Drury, T. L. Reynolds, W. P. Ridley, N. Bogdanova, S. G. Riordan, M. A. Nemeth, R. Sorbet, A. W. A. Trujillo and M. L. Breeze, “Composition of Forage and Grain from Second-Generation Insect-Protected Corn MON 89034 is Equivalent to That of Conventional Corn (Zea mays L. ),” Journal of Agricultural and Food Chemistry, Vol. 56, No. 12, 2008, pp. 4623-4630. doi:10.1021/jf800011u
[25]	J. Ryals, K. Lawton, D. Stevens and M. Milburn, “Metabolon, Inc.,” Pharmacogenomics, Vol. 8, No. 7, 2007, pp. 863-866. doi:10.2217/14622416.8.7.863
[26]	K. A. Lawton, A. Berger, M. Mitchell, K. E. Milgram, A. M. Evans, L. Guo, R. W. Hanson, S. C. Kalhan, J. A. Ryals and M. V. Milburn, “Analysis of the Adult Human Plasma Metabolome,” Pharmacogenomics, Vol. 9, No. 4, 2008, pp. 383-397. doi:10.2217/14622416.9.4.383
[27]	R. M. Stupar, J. M. Gardiner, A. G. Oldre, W. J. Haun, V. L. Chandler and N. M. Springer, “Gene Expression Analyses in Maize Inbreds and Hybrids with Varying Levels of Heterosis,” BMC Plant Biology, Vol. 8, 2008, p. 33. doi:10.1186/1471-2229-8-33
[28]	M. Vuylsteke, F. van Eeuwijk, P. Van Hummelen, M. Kuiper and M. Zabeau, “Genetic Analysis of Variation in Gene Expression in Arabidopsis thaliana,” Genetics, Vol. 171, No. 3, 2005, pp. 1267-1275. doi:10.1534/genetics.105.041509
[29]	Y. Huang, L. Zhang, J. Zhang, D. Yuan, C. Xu, X. Li, D. Zhou, S. Wang and Q. Zhang, “Heterosis and Polymorphisms of Gene Expression in an Elite Rice Hybrid as Revealed by a Microarray Analysis of 9198 Unique ESTs,” Plant Molecular Biology, Vol. 62, No. 4-5, 2006, pp. 579-591. doi:10.1007/s11103-006-9040-z
[30]	R. Batista, N. Saibo, T. Lourenco and M. M. Oliveira, “Microarray Analyses Reveal that Plant Mutagenesis May Induce More Transcriptomic Changes than Transgene Insertion,” Proceedings of the National Academy of Sciences, Vol. 105, No. 9, 2008, pp. 3640-3645. doi:10.1073/pnas.0707881105
[31]	A. Frizzi, R. A. Caldo, J. A. Morrell, M. Wang, L. L. Lutfiyya, W. E. Brown, T. M. Malvar and S. Huang, “Compositional and Transcriptional Analyses of Reduced Zein Kernels Derived from the opaque2 Mutation and RNAi Suppression,” Plant Molecular Biology, Vol. 73, No. 4-5, 2010, pp. 569-585. doi:10.1007/s11103-010-9644-1
[32]	E. Ottaviano and A. Camussi, “Phenotypic and Genetic Relationships between Yield Components in Maize,” Euphytica, Vol. 30, No. 3, 1981, pp. 601-609. doi:10.1007/BF00038787
[33]	M. Tollenaar and J. Wu, “Yield Improvement in Temperate Maize Is Attributable to Greater Stress Tolerance,” Crop Science Society of America, Vol. 39, Vol. 6, 1998, pp. 1597-1604.
[34]	M. M. Baudo, R. Lyons, S. Powers, G. M. Pastori, K. J. Edwards, M. J. Holdsworth and P. R. Shewry, “Transgenesis Has Less Impact on the Transcriptome of Wheat Grain than Conventional Breeding,” Plant Biotechnology Journal, Vol. 4, No. 4, 2006, pp. 369-380. doi:10.1111/j.1467-7652.2006.00193.x
[35]	S. J. Lehesranta, H. V. Davies, L. V. T. Shepherd, N. Nunan, J. W. McNicol, S. Auriola, K. M. Koistinen, S. Suomalainen, H. I. Kokko and S. O. Karenlampi, “Comparison of Tuber Proteomes of Potato Varieties, Landraces, and Genetically Modified Lines,” Plant Physiology, Vol.138, No. 3, 2005, pp. 1690-1699. doi:10.1104/pp.105.060152
[36]	A. Coll, A. Nadal, M. Palaudelmàs, J. Messeguer, E. Melé, P. Puigdomènech and M. Pla, “Lack of Repeatable Differential Expression Patterns between MON810 and Comparable Commercial Varieties of Maize,” Plant Molecular Biology, Vol. 68, No. 1-2, 2008, pp. 105-117. doi:10.1007/s11103-008-9355-z
[37]	K. C. Cheng, J. Beaulieu, E. Iquira, F. J. Belzile, M. G. Fortin and M. V. Str?mvik, “Effect of Transgenes on Global Gene Expression in Soybean Is within the Natural Range of Variation of Conventional Cultivars,” Journal of Agricultural and Food Chemistry, Vol. 56, No. 9, 2008, pp. 3057-3067. doi:10.1021/jf073505i
[38]	A. E. Ricroch, J. B. Bergé and M. Kuntz, “Evaluation of Genetically Engineered Crops Using Transcriptomic, Proteomic and Metabolomic Profiling Techniques,” Plant Physiology, Vol. 155, Vol. 4, 2011, pp. 1752-1761.