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Metabolomics

, 15:47 | Cite as

Recent developments in metabolomics-based research in understanding transgenic grass metabolism

  • Siriwat Boonchaisri
  • Simone Rochfort
  • Trevor Stevenson
  • Daniel A. DiasEmail author
Review Article
Part of the following topical collections:
  1. Topical Collection: Plant Metabolomics and Lipidomics

Abstract

Background

Transgenic herbicide-resistant (HR) turfgrass together with its associated, broad spectrum herbicides promise cheap, selective and efficient weed control by excluding infested weeds resulting in turf lawn with high uniformity and aesthetic value. The concept of this “weeding program” initiated from modern biotechnology has been widely implemented in several principal crops including maize, soybean, canola and cotton as early as the 1990s. Transgenic HR turfgrass classified as a genetically modified organism (GMO) has undoubtedly caused public concern with respect to its biosafety and legalities similar to well-established HR crops. Nevertheless, applying metabolomics-based approaches which focuses on the identification of the global metabolic state of a biological system in response to either internal or external stimuli can also provide a comprehensive characterization of transgenic grass metabolism and its involvement in biosecurity and public perception.

Aim of review

This review summaries the recent applications of metabolomics applied to HR crops to predict the molecular and physiological phenotypes of HR turfgrass species, glyphosate-resistant Kentucky bluegrass (Poa pratensis L.) and glufosinate-resistant creeping bentgrass (Agrotis stonifera L.). Additionally, this review also presents background knowledge with respect to the application of metabolomics, transformation of HR crops and its biosafety concerns, turfgrass botanical knowledge and its economic and aesthetic value.

Key scientific concepts of review

The purpose of this review is to demonstrate the molecular and physiological phenotypes of HR turfgrass based on several lines of evidence primarily derived from metabolomics data applied to HR crops to identify alterations on HR turfgrass metabolism as a result of genetic modification that confers resistant traits.

Keywords

Herbicide-resistance Turfgrass Kentucky bluegrass Creeping bentgrass Glufosinate Glyphosate Metabolomics 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abbasi, A.-R., Hajirezaei, M., Hofius, D., Sonnewald, U., & Voll, L. M. (2007). Specific roles of α- and γ-tocopherol in abiotic stress responses of transgenic tobacco. Plant Physiology, 143(4), 1720–1738.  https://doi.org/10.1104/pp.106.094771.CrossRefPubMedPubMedCentralGoogle Scholar
  2. AHTEG (2016). Guidance document on risk assessment of living modified organisms. United Nations Environment Programme Convention for Biodiversity.Google Scholar
  3. Aliferis, K. A., & Jabaji, S. (2011). Metabolomics: A robust bioanalytical approach for the discovery of the modes-of-action of pesticides: A review. Pesticide Biochemistry and Physiology, 100(2), 105–117.  https://doi.org/10.1016/j.pestbp.2011.03.004.CrossRefGoogle Scholar
  4. Asano, Y., Ito, Y., Fukami, M., Sugiura, K., & Fujiie, A. (1998). Herbicide-resistant transgenic creeping bentgrass plants obtained by electroporation using an altered buffer. Plant Cell Reports, 17(12), 963–967.  https://doi.org/10.1007/s002990050518.CrossRefPubMedGoogle Scholar
  5. Banks, P., Branham, B., Harrison, K., Whitson, T., & Heap, I. (2003). Determination of the potential impact from the release of glyphosate- and glufosinate-resistant Agrostis stolonifera L. in various crop and non-crop ecosystems. https://www.aphis.usda.gov/brs/pdf/Resistant_Bentgrass_Final_Report.pdf. Accessed 18 January 2019.
  6. Barros, E., Lezar, S., Anttonen, M. J., van Dijk, J. P., Rohlig, R. M., Kok, E. J., et al. (2010). Comparison of two GM maize varieties with a near-isogenic non-GM variety using transcriptomics, proteomics and metabolomics. Plant Biotechnology Journal, 8(4), 436–451.  https://doi.org/10.1111/j.1467-7652.2009.00487.x.CrossRefPubMedGoogle Scholar
  7. Beard, J., & Green, R. L. (1994). The role of turf in environmental protection. Journal of Environmental Quality, 23, 452–460.CrossRefGoogle Scholar
  8. Beckie, H. J., & Hall, L. M. (2014). Genetically-modified herbicide-resistant (GMHR) crops a two-edged sword? An Americas perspective on development and effect on weed management. Crop Protection, 66, 40–45.  https://doi.org/10.1016/j.cropro.2014.08.014.CrossRefGoogle Scholar
  9. Bhuiyan, N. H., Selvaraj, G., Wei, Y., & King, J. (2009). Role of lignification in plant defense. Plant Signaling & Behavior, 4(2), 158–159.CrossRefGoogle Scholar
  10. Blume, C. J., Fei, S.-Z., & Christians, N. E. (2010). Field evaluation of reduced-growth, glyphosate-resistant Kentucky Bluegrass in a noncompetitive setting. Crop Science, 50(3), 1048.  https://doi.org/10.2135/cropsci2009.05.0262.CrossRefGoogle Scholar
  11. Bolton, M. D. (2009). Primary metabolism and plant defense-fuel for the fire. Molecular Plant–Microbe Interactions, 22(5), 487–497.  https://doi.org/10.1094/mpmi-22-5-0487.CrossRefPubMedGoogle Scholar
  12. Brookes, G., & Barfoot, P. (2017). GM crops: Global socio-economic and environmental impacts 1996–2015. Dorchester: PG Economics Ltd.Google Scholar
  13. Brosnan, J. T., & Breeden, G. K. (2013). Herbicide resistance in turfgrass: An emerging problem? Outlooks on Pest Management, 24(4), 164–168.  https://doi.org/10.1564/v24_aug_05.CrossRefGoogle Scholar
  14. Bush, T. (2002). Plant fact sheet: Kentucky bluegrass Poa pratensis L. Rose Lake Plant Materials Center: USDA NRCS.Google Scholar
  15. Cardi, T. (2016). Cisgenesis and genome editing: combining concepts and efforts for a smarter use of genetic resources in crop breeding. Plant Breeding, 135(2), 139–147.  https://doi.org/10.1111/pbr.12345.CrossRefGoogle Scholar
  16. Carey, R. O., Hochmuth, G. J., Martinez, C. J., Boyer, T. H., Nair, V. D., Dukes, M. D., et al. (2012). A review of turfgrass fertilizer management practices: Implications for urban water quality. Horttechnology, 22(3), 280–291.Google Scholar
  17. Casler, M. D., & Duncan, R. R. (2003). Origins of the turfgrasses. In M. D. Casler & R. R. Duncan (Eds.), Turfgrass biology, genetics, and breeding (pp. 5–26). New Jersey: Wiley.Google Scholar
  18. Cela, J., Chang, C., & Munne-Bosch, S. (2011). Accumulation of gamma-rather than alpha-tocopherol alters ethylene signaling gene expression in the vte4 mutant of Arabidopsis thaliana. Plant and Cell Physiology, 52(8), 1389–1400.  https://doi.org/10.1093/pcp/pcr085. doi.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Choi, H., Moon, J.-K., Park, B.-S., Park, H.-W., Park, S.-Y., Kim, T.-S., et al. (2012). Comparative nutritional analysis for genetically modified rice, Iksan483 and Milyang204, and nontransgenic counterparts. Journal of the Korean Society for Applied Biological Chemistry, 55(1), 19–26.  https://doi.org/10.1007/s13765-012-0004-5.CrossRefGoogle Scholar
  20. Christ, B., Hochstrasser, R., Guyer, L., Francisco, R., Aubry, S., Hörtensteiner, S., et al. (2017). Non-specific activities of the major herbicide-resistance gene BAR. Nature Plants, 3(12), 937–945.  https://doi.org/10.1038/s41477-017-0061-1.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Christians, N. E., Patton, A. J., & Law, Q. D. (2016). Introduction to the grasses. In N. E. Christians, A. J. Patton & Q. D. Law (Eds.), Fundamentals of turfgrass management (5th ed., pp. 9–39). Hoboken: Wiley.Google Scholar
  22. Clarke, J. D., Alexander, D. C., Ward, D. P., Ryals, J. A., Mitchell, M. W., Wulff, J. E., et al. (2013). Assessment of genetically modified soybean in relation to natural variation in the soybean seed metabolome. Scientific Reports, 3, 3082.  https://doi.org/10.1038/srep03082.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Clayton, W. D., Vorontsova, M. S., Harman, K. T., & Williamson, H. (2006). Grassbase—The online world grass flora. http://www.kew.org/data/grasses-db.html. Accessed 08 November 2006.
  24. Dai, S., Zheng, P., Marmey, P., Zhang, S., Tian, W., Chen, S., Beachy, R. N., & Fauquet, C. (2001). Comparative analysis of transgenic rice plants obtained by Agrobacterium-mediated transformation and particle bombardment. Molecular Breeding, 7(1), 25–33.  https://doi.org/10.1023/a:1009687511633.CrossRefGoogle Scholar
  25. Dias, D. A., Jones, O. A. H., Beale, D. J., Boughton, B. A., Benheim, D., Kouremenos, K. A., et al. (2016). Current and future perspectives on the structural identification of small molecules in biological systems. Metabolites, 6(4), 46.  https://doi.org/10.3390/metabo6040046.CrossRefPubMedCentralGoogle Scholar
  26. Dias, D. A., & Koal, T. (2016). Progress in metabolomics standardisation and its significance in future clinical laboratory medicine. The Journal of the International Federation of Clinical Chemistry and Laboratory Medicine, 27(4), 331–343.PubMedGoogle Scholar
  27. Du, H. M., Wang, Z. L., Yu, W. J., & Huang, B. R. (2012). Metabolic responses of hybrid bermudagrass to short-term and long-term drought stress. Journal of the American Society for Horticultural Science, 137(6), 411–420.CrossRefGoogle Scholar
  28. Du, H. M., Wang, Z. L., Yu, W. J., Liu, Y. M., & Huang, B. R. (2011). Differential metabolic responses of perennial grass Cynodon transvaalensis × Cynodon dactylon (C4) and Poa Pratensis (C3) to heat stress. Physiologia Plantarum, 141(3), 251–264.  https://doi.org/10.1111/j.1399-3054.2010.01432.x.CrossRefPubMedGoogle Scholar
  29. Duke, S. O. (2012). Why have no new herbicide modes of action appeared in recent years? Pest Management Science, 68(4), 505–512.  https://doi.org/10.1002/ps.2333.CrossRefPubMedGoogle Scholar
  30. Frank, T., & Engel, K.-H. (2013). Metabolomics of genetically modified crops. In B. M. Lange & V. D. Daygon (Eds.), Hot topics in metabolomics: Food and nutrition (pp. 18–28). London: Future Science Ltd.CrossRefGoogle Scholar
  31. Frank, T., Rohlig, R. M., Davies, H. V., Barros, E., & Engel, K. H. (2012). Metabolite profiling of maize kernels-genetic modification versus environmental influence. Journal of Agricultural and Food Chemistry, 60(12), 3005–3012.  https://doi.org/10.1021/jf204167t.CrossRefPubMedGoogle Scholar
  32. Garcia-Villalba, R., Leon, C., Dinelli, G., Segura-Carretero, A., Fernandez-Gutierrez, A., Garcia-Canas, V., et al. (2008). Comparative metabolomic study of transgenic versus conventional soybean using capillary electrophoresis-time-of-flight mass spectrometry. Journal of Chromatography A, 1195(1–2), 164–173.  https://doi.org/10.1016/j.chroma.2008.05.018.CrossRefPubMedGoogle Scholar
  33. Geel, T. M., Ruiters, M. H. J., Cool, R. H., Halby, L., Voshart, D. C., Ruiz, L. A., et al. (2018). The past and presence of gene targeting: from chemicals and DNA via proteins to RNA. Philosophical Transactions of the Royal Society B-Biological Sciences.  https://doi.org/10.1098/rstb.2017.0077.CrossRefGoogle Scholar
  34. Gerdes, S., Lerma-Ortiz, C., Frelin, O., Seaver, S. M., Henry, C. S., de Crecy-Lagard, V., et al. (2012). Plant B vitamin pathways and their compartmentation: a guide for the perplexed. Journal of Experimental Botany, 63(15), 5379–5395.  https://doi.org/10.1093/jxb/ers208.CrossRefPubMedGoogle Scholar
  35. Gertz, J. M., Vencill, W. K., & Hill, N. S. (1999). Tolerance of transgenic soybean (Glycine max) to heat stress. In The 1999 Brighton Conference: Weeds, Brighton Metrole Hotel, Brighton, UK, 15–18 November 1999 (pp. 835–840). Surrey: British Crop Protection Council.Google Scholar
  36. Gillaspy, G. E. (2011). The cellular language of myo-inositol signaling. New Phytologist, 192(4), 823–839.  https://doi.org/10.1111/j.1469-8137.2011.03939.x.CrossRefPubMedGoogle Scholar
  37. GMO compass (2006). Crop specific safety concerns: Sugar Beet. http://www.gmo-compass.org/eng/safety/environmental_safety/184.sugar_beet.html. Accessed 11 July 2016.
  38. Green, J. M. (2012). The benefits of herbicide-resistant crops. Pest Management Science, 68(10), 1323–1331.  https://doi.org/10.1002/ps.3374.CrossRefPubMedGoogle Scholar
  39. Green, J. M. (2014). Current state of herbicides in herbicide-resistant crops. Pest Management Science, 70(9), 1351–1357.  https://doi.org/10.1002/ps.3727.CrossRefPubMedGoogle Scholar
  40. Green, J. M. (2018). The rise and future of glyphosate and glyphosate-resistant crops. Pest Management Science, 74(5), 1035–1039.  https://doi.org/10.1002/ps.4462.CrossRefPubMedGoogle Scholar
  41. Gregoire, M. C. (2011). Re: Confirmation regulartory status/Kentucky bluegrass (Poa pratensis L.) https://www.aphis.usda.gov/brs/aphisdocs/scotts_kbg_resp.pdf. Accessed 18 January 2019.
  42. Grossmann, K., Christiansen, N., Looser, R., Tresch, S., Hutzler, J., Pollmann, S., et al. (2012). Physionomics and metabolomics—two key approaches in herbicidal mode of action discovery. Pest Management Science, 68(4), 494–504.  https://doi.org/10.1002/ps.2300.CrossRefPubMedGoogle Scholar
  43. Halfhill, M. D., Sutherland, J. P., Moon, H. S., Poppy, G. M., Warwick, S. I., Weissinger, A. K., et al. (2005). Growth, productivity, and competitiveness of introgressed weedy Brassica rapa hybrids selected for the presence of Bt cry1Ac and gfp transgenes. Molecular Ecology, 14(10), 3177–3189.  https://doi.org/10.1111/j.1365-294X.2005.02649.x.CrossRefPubMedGoogle Scholar
  44. Han, N., Chen, D., Bian, H.-W., Deng, M.-J., & Zhu, M.-Y. (2005). Production of transgenic creeping bentgrass Agrostis stolonifera var. palustris plants by Agrobacterium tumefaciens-mediated transformation using hygromycin selection. Plant Cell, Tissue and Organ Culture, 81(2), 131–138.  https://doi.org/10.1007/s11240-004-4042-5.CrossRefGoogle Scholar
  45. Harriman, R. W., Lee, L., Stalker, D., & Torisky, R. (2015a). Methods for detecting Kentucky bluegrass plant transgenic events Pp009-401, Pp009-415, and Pp009-469 comprising EPSPS gene from Arabidopsis and GA2OX from spinach with improved glyphosate tolerance and enhanced turfgrass quality. (Patent no: WO 2015/006774 A l). USA: Oms Investments, Inc.Google Scholar
  46. Harriman, R. W., Lee, L., Stalker, D., & Torisky, R. (2015b). Plants comprising events pp009-401, pp009-415, and pp009-469, compositions, sequences, and methods for detection thereof. USA: (Patent no: WO 2015/006774 A l). Oms Investments, Inc.Google Scholar
  47. Hartman, C. L., Lee, L., Day, P. R., & Tumer, N. E. (1994). Herbicide resistant turfgrass (Agrostis palustris huds.) by biolistic transformation. Nature Biotechnology, 12(9), 919–923.CrossRefGoogle Scholar
  48. Hathaway, A., & Frank, K. (2016). Crabgrass control during a hot summer. http://msue.anr.msu.edu/news/crabgrass_control_during_a_hot_summer. Accessed 6 January 2017.
  49. Heap, I. (2017). The international survey of herbicide resistant weeds. http://www.weedscience.org. Accessed 17 January 2017.
  50. Heap, I., & Duke, S. O. (2018). Overview of glyphosate-resistant weeds worldwide. Pest Management Science, 74(5), 1040–1049.  https://doi.org/10.1002/ps.4760.CrossRefPubMedGoogle Scholar
  51. Heckart, D. L., Schwartz, B. M., Raymer, P. L., & Parrott, W. A. (2016). Synonymous mutation gene design to overexpress ACCase in creeping bentgrass to obtain resistance to ACCase-inhibiting herbicides. Transgenic Research, 25(4), 465–476.  https://doi.org/10.1007/s11248-016-9942-8.CrossRefPubMedGoogle Scholar
  52. Horticulture Innovation Australia Ltd. (2017). Australian turf industry snapshot report 2016/17. Sydney: Western Research Institute Ltd.Google Scholar
  53. Hoyle, J. (2017). Turfgrass selection (MF2032). K-State Research and Extension, 1–4.Google Scholar
  54. Huang, B., DaCosta, M., & Jiang, Y. (2014). Research advances in mechanisms of turfgrass tolerance to abiotic stresses: From physiology to molecular biology. Critical Reviews in Plant Sciences, 33(2–3), 141–189.  https://doi.org/10.1080/07352689.2014.870411.CrossRefGoogle Scholar
  55. ISAAA (2013a). GM crop events list: ASR368. http://www.isaaa.org/gmapprovaldatabase/event/default.asp?EventID=240. Accessed 14 April 2018.
  56. ISAAA (2013b). Pocket K no. 4: GM crops and the environment. http://www.isaaa.org/resources/publications/pocketk/4/default.asp. Accessed 11 July 2016.
  57. James, C. (2015). Brief 51: 20th anniversary (1996 to 2015) of the global commercialization of biotech crops and biotech crop highlights in 2015. http://www.isaaa.org/resources/publications/briefs/51/default.asp. Accessed 10 July 2016.
  58. Jimenez, J. J., Bernal, J. L., Nozal, M. J., Toribio, L., & Bernal, J. (2009). Profile and relative concentrations of fatty acids in corn and soybean seeds from transgenic and isogenic crops. Journal of Chromatography A, 1216(43), 7288–7295.  https://doi.org/10.1016/j.chroma.2009.08.015.CrossRefPubMedGoogle Scholar
  59. Johnson, P. G., & Riordan, T. P. (1999). A review of issues pertaining to transgenic turfgrasses. HortScience, 34(4), 594–598.CrossRefGoogle Scholar
  60. Jones, O. A. H., Maguire, M. L., Griffin, J. L., Dias, D. A., Spurgeon, D. J., & Svendsen, C. (2013). Metabolomics and its use in ecology. Austral Ecology, 38(6), 713–720.  https://doi.org/10.1111/aec.12019.CrossRefGoogle Scholar
  61. Katsuta, K., Matsuo, K., Yoshimura, Y., & Ohsawa, R. (2015). Long-term monitoring of feral genetically modified herbicide-tolerant Brassica napus populations around unloading Japanese ports. Breeding Science, 65(3), 265–275.  https://doi.org/10.1270/jsbbs.65.265.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kim, J. K., Park, S.-Y., Lee, S. M., Lim, S.-H., Kim, H. J., Oh, S.-D., et al. (2013). Unintended polar metabolite profiling of carotenoid-biofortified transgenic rice reveals substantial equivalence to its non-transgenic counterpart. Plant Biotechnology Reports, 7(1), 121–128.  https://doi.org/10.1007/s11816-012-0231-6.CrossRefGoogle Scholar
  63. Kim, S. J., Lee, J. Y., Kim, Y. M., Yang, S. S., Hwang, O. J., Hong, N. J., et al. (2007). Agrobacterium-mediated high-efficiency transformation of creeping bentgrass with herbicide resistance. Journal of Plant Biology, 50(5), 577–585.  https://doi.org/10.1007/bf03030712.CrossRefGoogle Scholar
  64. Kusano, M., Baxter, I., Fukushima, A., Oikawa, A., Okazaki, Y., Nakabayashi, R., et al. (2014). Assessing metabolomic and chemical diversity of a soybean lineage representing 35 years of breeding. Metabolomics, 11(2), 261–270.  https://doi.org/10.1007/s11306-014-0702-6.CrossRefGoogle Scholar
  65. Kusonmano, K., Vongsangnak, W., & Chumnanpuen, P. (2016). Informatics for metabolomics. Advances in Experimental Medicine and Biology, 939, 91–115.  https://doi.org/10.1007/978-981-10-1503-8_5.CrossRefPubMedGoogle Scholar
  66. Lee, L., Popham, P., & Berg, B. (2002). Transgenic Poa grasses (Patent no: WO2002022838A2). USA: The Scotts Company.Google Scholar
  67. Lee, S. H., Kim, J. S., Kim, G. Y., Park, H. S., Lim, Y. C., Lee, G. W., et al. (2011). Antibiotic marker-free transformed creeping bentgrass resistant to two herbicides. (Patent no: KR2011124606A). South Korea: Rural Development Administration.Google Scholar
  68. Liu, C. A., Zhong, H., Vargas, J., Penner, D., & Sticklen, M. (1998). Prevention of fungal diseases in transgenic, bialaphos- and glufosinate-resistant creeping bentgrass (Agrostis palustris). Weed Science, 46(1), 139–146.Google Scholar
  69. Liu, Q., Luo, L., & Zheng, L. (2018). Lignins: Biosynthesis and biological functions in plants. International Journal of Molecular Sciences.  https://doi.org/10.3390/ijms19020335.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Loewus, F. A., & Loewus, M. W. (1983). myo-Inositol: Its biosynthesis and metabolism. Annual Review of Plant Physiology and Plant Molecular Biology, 34, 137–161.  https://doi.org/10.1146/annurev.pp.34.060183.001033.CrossRefGoogle Scholar
  71. Loewus, F. A., & Murthy, P. P. N. (2000). myo-Inositol metabolism in plants. Plant Science, 150(1), 1–19.  https://doi.org/10.1016/S0168-9452(99)00150-8.CrossRefGoogle Scholar
  72. Lowry, B. J., Whitesides, R. E., Dewey, S. A., Ransom, C. V., & Banner, R. E. (2011). Creeping bentgrass. In B. J. Lowry, R. E. Whitesides, S. A. Dewey, C. V. Ransom, & R. E. Banner (Eds.), Common weeds of the yard and garden a guidebook (pp. 69–72): Utah State University Cooperate Extension.Google Scholar
  73. Luo, H., Hu, Q., Nelson, K., Longo, C., Kausch, A. P., Chandlee, J. M., et al. (2004). Agrobacterium tumefaciens-mediated creeping bentgrass (Agrostis stolonifera L.) transformation using phosphinothricin selection results in a high frequency of single-copy transgene integration. Plant Cell Reports, 22(9), 645–652.  https://doi.org/10.1007/s00299-003-0734-2.CrossRefPubMedGoogle Scholar
  74. Madsen, K. H., & Streibig, J. C. (2003). Benefits and risks of the use of herbicide-resistant crops. In R. Labrada (Ed.), Weed management for developing countries. Rome: FAO.Google Scholar
  75. Mahmood, S., Wahid, A., Rasheed, R., Hussain, I., & Basra, S. M. A. (2012). Possible antioxidative role of endogenous vitamins biosynthesis in heat stressed maize (Zea mays). International Journal of Agriculture and Biology, 14, 705–712.Google Scholar
  76. Manning, J. (2017). GMO grass that ‘escaped’ defies eradication, divides grass seed industry. http://www.oregonlive.com/business/index.ssf/2017/01/grass_seed_industry_fearful_ab.html. Accessed 2 March 2018.
  77. Maroli, A. S., Nandula, V. K., Dayan, F. E., Duke, S. O., Gerard, P., & Tharayil, N. (2015). Metabolic profiling and enzyme analyses indicate a potential role of antioxidant systems in complementing glyphosate resistance in an Amaranthus palmeri biotype. Journal of Agricultural and Food Chemistry, 63(41), 9199–9209.  https://doi.org/10.1021/acs.jafc.5b04223.CrossRefPubMedGoogle Scholar
  78. McGrath, M., & Strasser, F. (2012). Superweeds pose GM-resistant challenge for farmers. http://www.bbc.com/news/magazine-19594335. Accessed 11 July 2016.
  79. Meï, C., Michaud, M., Cussac, M., Albrieux, C., Gros, V., Maréchal, E., et al. (2015). Levels of polyunsaturated fatty acids correlate with growth rate in plant cell cultures. Scientific Reports, 5, 15207.  https://doi.org/10.1038/srep15207.CrossRefPubMedPubMedCentralGoogle Scholar
  80. Mesnage, R., Agapito-Tenfen, S. Z., Vilperte, V., Renney, G., Ward, M., Seralini, G. E., et al. (2016). An integrated multi-omics analysis of the NK603 Roundup-tolerant GM maize reveals metabolism disturbances caused by the transformation process. Scientific Reports, 6, 37855.  https://doi.org/10.1038/srep37855.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Miedes, E., Vanholme, R., Boerjan, W., & Molina, A. (2014). The role of the secondary cell wall in plant resistance to pathogens. Frontiers in Plant Science, 5, 358.  https://doi.org/10.3389/fpls.2014.00358.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Miquel, M., James, D. Jr., Dooner, H., & Browse, J. (1993). Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proceedings of the National Academy of Sciences of the United States of America, 90(13), 6208–6212.CrossRefGoogle Scholar
  83. Mittal, R. D. (2015). Tandem mass spectroscopy in diagnosis and clinical research. Indian Journal of Clinical Biochemistry, 30(2), 121–123.  https://doi.org/10.1007/s12291-015-0498-9.CrossRefPubMedPubMedCentralGoogle Scholar
  84. National Turfgrass Federation (n.d.). The turfgrass industry—present and future. http://www.turfresearch.org/pdf/Industry%20Turf%20Initiative.pdf. Accessed March 2 2018.
  85. Neal, J. C. (2000). Hercide resistant turfgrasses-panacea or problem? Turfgrass Trends, 4–7.Google Scholar
  86. Park, S., Seo, Y. S., & Hegeman, A. D. (2014). Plant metabolomics for plant chemical responses to belowground community change by climate change. Journal of Plant Biology, 57(3), 137–149.  https://doi.org/10.1007/s12374-014-0110-5.CrossRefGoogle Scholar
  87. Rao, V. S. (2015). Transgenic herbicide resistance in plants. Boca Raton: CRC Press.Google Scholar
  88. RDA. (2007). Studies on the environmental safety assessment of herbicide tolerant genetically modified rice, Iksan483 & Milyang204. Suwon: Rural Development Administration, National Institute of Agricultural Biotechnology.Google Scholar
  89. Roessner, U., & Beckles, D. M. (2012). Metabolomics for salinity research. Methods in Molecular Biology, 913, 203–215.  https://doi.org/10.1007/978-1-61779-986-0_13.CrossRefPubMedGoogle Scholar
  90. Roessner, U., & Dias, D. A. (2013). Plant tissue extraction for metabolomics. In U. Roessner & D. A. Dias (Eds.), Metabolomics tools for natural product discovery: Methods and protocols (pp. 21–28). New York: Humana Press.CrossRefGoogle Scholar
  91. Santero, E., Hervás, A. B., Canosa, I., & Govantes, F. (2012). Glutamate dehydrogenases: Enzymology, physiological role and biotechnological relevance. In R. A. Canuto (Ed.), Dehydrogenases (pp. 289–309). InTechOpen,  https://doi.org/10.5772/47767.
  92. Sato, H., Takamizo, T., Shimizu, T., Kawai, K., & Kaku, K. (2009). Conferred resistance to an acetolactate synthase-inhibiting herbicide in transgenic tall fescue (Festuca arundinacea Schreb.). HortScience, 44(5), 1254–1257.CrossRefGoogle Scholar
  93. Scheben, A., Wolter, F., Batley, J., Puchta, H., & Edwards, D. (2017). Towards CRISPR/Cas crops – bringing together genomics and genome editing. New Phytologist, 216(3), 682–698.  https://doi.org/10.1111/nph.14702.CrossRefPubMedGoogle Scholar
  94. Schneider, C. (2005). Chemistry and biology of vitamin E. Molecular Nutrition & Food Research, 49(1), 7–30.  https://doi.org/10.1002/mnfr.200400049.CrossRefGoogle Scholar
  95. Shanks, R. (2012). Re: Enhanced turfgrass quality Kentucky bluegrass. https://www.aphis.usda.gov/biotechnology/downloads/reg_loi/Scotts_KBG_013112.pdf. Accessed 18 January 2019.
  96. Shin, J. S., Kim, K. M., Lee, D. J., Lee, S. B., Burgos, N. R., & Kuk, Y. I. (2011). Resistance levels and fitness of glufosinate-resistant transgenic sweet potato in field experiments. Field Crops Research, 121(3), 324–332.  https://doi.org/10.1016/j.fcr.2010.12.020.CrossRefGoogle Scholar
  97. Shukla, V. K., Doyon, Y., Miller, J. C., DeKelver, R. C., Moehle, E. A., Worden, S. E., et al. (2009). Precise genome modification in the crop species Zea mays using zinc-finger nucleases. Nature, 459(7245), 437–441.  https://doi.org/10.1038/nature07992.CrossRefPubMedGoogle Scholar
  98. Smith, R., Grando, M., Li, Y., Seib, J., & Shatters, R. (2002). Transformation of bahiagrass (Paspalum notatum Flugge). Plant Cell Reports, 20(11), 1017–1021.  https://doi.org/10.1007/s00299-001-0423-y.CrossRefGoogle Scholar
  99. Snow, A. A. (2012). Illegal gene flow from transgenic creeping bentgrass: The saga continues. Molecular Ecology, 21(19), 4663–4664.  https://doi.org/10.1111/j.1365-294X.2012.05695.x.CrossRefPubMedGoogle Scholar
  100. Snyder, G., Cisar, J., & Park, D. (2008). Warm-season turfgrass fertilization. In M. Pessarakli (Ed.), Handbook of turfgrass management and physiology (pp. 47–55). Florida: CRC Press.Google Scholar
  101. Song, I.-J., Bae, T.-W., Ganesan, M., Kim, J.-I., Lee, H.-Y., & Song, P.-S. (2013). Transgenic herbicide-resistant turfgrasses. In A. J. Price, & J. A. Kelton (Eds.), Herbicidescurrent research and case studies in use (pp. 377–395). InTechOpen,  https://doi.org/10.5772/56096.
  102. Soumeh, E. A., Hedemann, M. S., Poulsen, H. D., Corrent, E., van Milgen, J., & Norgaard, J. V. (2016). Nontargeted LC-MS metabolomics approach for metabolic profiling of plasma and urine from pigs fed branched chain amino acids for maximum growth performance. Journal of Proteome Research, 15(12), 4195–4207.  https://doi.org/10.1021/acs.jproteome.6b00184.CrossRefPubMedGoogle Scholar
  103. Svitashev, S., Young, J. K., Schwartz, C., Gao, H., Falco, S. C., & Cigan, A. M. (2015). Targeted mutagenesis, precise gene editing, and site-specific gene insertion in maize using cas9 and guide RNA. Plant Physiology, 169(2), 931–945.  https://doi.org/10.1104/pp.15.00793.CrossRefPubMedPubMedCentralGoogle Scholar
  104. Tang, W., & Tang, A. Y. (2018). Genome engineering technologies for targeted genetic modification in plants. Journal of Forestry Research, 29(4), 875–887.  https://doi.org/10.1007/s11676-017-0588-z.CrossRefGoogle Scholar
  105. Tjellstrom, H., Yang, Z., Allen, D. K., & Ohlrogge, J. B. (2012). Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids. Plant Physiology, 158(2), 601–611.  https://doi.org/10.1104/pp.111.186122.CrossRefPubMedGoogle Scholar
  106. Toyama, K., Bae, C. H., Kang, J. G., Lim, Y. P., Adachi, T., Riu, K. Z., et al. (2003). Production of herbicide-tolerant zoysiagrass by Agrobacterium-mediated transformation. Molecules and Cells, 16(1), 19–27.PubMedGoogle Scholar
  107. Trenholm, L. E., & Unruh, J. B. (2005). Warm-season turfgrass response to fertilizer rates and sources. Journal of Plant Nutrition, 28(6), 991–999.  https://doi.org/10.1081/pln-200058894.CrossRefGoogle Scholar
  108. Van de Water, P. K., Watrud, L. S., Lee, E. H., Burdick, C., & King, G. A. (2007). Long-distance GM pollen movement of creeping bentgrass using modeled wind trajectory analysis. Ecological Applications, 17(4), 1244–1256.CrossRefGoogle Scholar
  109. Wang, Y., Browning, M., Ruemmele, B. A., Chandlee, J. M., Kausch, A. P., & Jackson, N. (2003). Glufosinate reduces fungal diseases in transgenic glufosinate-resistant bentgrasses (Agrostis spp.). Weed Science, 51(1), 130–138.CrossRefGoogle Scholar
  110. Wang, Z., Liu, Y., Wang, Y., Xing, S., Dong, Y., & Li, H. (2006). Culture method for Poa pratensis germ plasm with resistance to glyphosate. (Patent no: CN1799343A). Jilin Academy of Agricultural Sciences, People Republic of China.Google Scholar
  111. Watrud, L. S., Lee, E. H., Fairbrother, A., Burdick, C., Reichman, J. R., Bollman, M., Storm, M., King, G., et al. (2004). Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proceedings of the National Academy of Sciences of the United States of America, 101(40), 14533–14538.  https://doi.org/10.1073/pnas.0405154101.CrossRefPubMedPubMedCentralGoogle Scholar
  112. Wile, R. (2015). The American lawn is now the largest single ‘crop’ in the U.S. https://www.huffingtonpost.com/entry/lawn-largest-crop-america_us_55d0dc06e4b07addcb43435d. Accessed 7 March 2018.
  113. Xin, L., Xiaoyun, H., Yunbo, L., Guoying, X., Xianbin, J., & Kunlun, H. (2008). Comparative analysis of nutritional composition between herbicide-tolerant rice with bar gene and its non-transgenic counterpart. Journal of Food Composition and Analysis, 21(7), 535–539.  https://doi.org/10.1016/j.jfca.2008.06.001.CrossRefGoogle Scholar
  114. Yi, G., Shin, Y. M., Choe, G., Shin, B., Kim, Y. S., & Kim, K. M. (2007). Production of herbicide-resistant sweet potato plants transformed with the bar gene. Biotechnology Letters, 29(4), 669–675.  https://doi.org/10.1007/s10529-006-9278-1.CrossRefPubMedGoogle Scholar
  115. Zhang, X. W., Wang, D. F., Zhao, S. N., & Shen, Z. C. (2014). A double built-in containment strategy for production of recombinant proteins in transgenic rice. PLoS ONE.  https://doi.org/10.1371/journal.pone.0115459.CrossRefPubMedPubMedCentralGoogle Scholar
  116. Zhong, H., Bolyard, M. G., Srinivasan, C., & Sticklen, M. B. (1993). Transgenic plants of turfgrass (Agrostis palustris Huds.) from microprojectile bombardment of embryogenic callus. Plant Cell Reports, 13(1), 1–6.  https://doi.org/10.1007/bf00232305.CrossRefPubMedGoogle Scholar
  117. Zonetti, P. D., Suzuki, L. S., Bonini, E. A., Ferrarese, M. L. L., & Ferrarese, O. (2012). High temperatures on root growth and lignification of transgenic glyphosate-resistant soybean. Agrociencia, 46(6), 557–565.Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of ScienceRMIT UniversityBundooraAustralia
  2. 2.Agriculture Research VictoriaAgriBioBundooraAustralia
  3. 3.School of Applied Systems BiologyLa Trobe UniversityBundooraAustralia
  4. 4.School of Health and Biomedical Sciences, Discipline of Laboratory MedicineRMIT UniversityBundooraAustralia

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