The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites
Plant secondary metabolites are protective dietary constituents and <i>rol</i> genes evidently increase the synthesis of these versatile phytochemicals. This study subjected a globally important vegetable, lettuce (<i>Lactuca sativa</i>) to a combination of untargeted metabol...
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| Format: | Article |
| Language: | English |
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MDPI AG
2019-05-01
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| Series: | Metabolites |
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| Online Access: | https://www.mdpi.com/2218-1989/9/5/97 |
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| author | Hammad Ismail Anna L. Gillespie Danielle Calderwood Haroon Iqbal Colene Gallagher Olivier P. Chevallier Christopher T. Elliott Xiaobei Pan Bushra Mirza Brian D. Green |
| author_facet | Hammad Ismail Anna L. Gillespie Danielle Calderwood Haroon Iqbal Colene Gallagher Olivier P. Chevallier Christopher T. Elliott Xiaobei Pan Bushra Mirza Brian D. Green |
| author_sort | Hammad Ismail |
| collection | DOAJ |
| description | Plant secondary metabolites are protective dietary constituents and <i>rol</i> genes evidently increase the synthesis of these versatile phytochemicals. This study subjected a globally important vegetable, lettuce (<i>Lactuca sativa</i>) to a combination of untargeted metabolomics (LC-QTof-MS) and in vitro bioactivity assays. Specifically, we examined the differences between untransformed cultured lettuce (UnT), lettuce transformed with either <i>rolABC</i> (RA) or <i>rolC</i> (RC) and commercially grown (COM) lettuce. Of the 5333 metabolite features aligned, deconvoluted and quantified 3637, 1792 and 3737 significantly differed in RA, RC and COM, respectively, compared with UnT. In all cases the number of downregulated metabolites exceeded the number increased. In vitro bioactivity assays showed that RA and RC (but not COM) significantly improved the ability of <i>L. sativa</i> to inhibit α-glucosidase, inhibit dipeptidyl peptidase-4 (DPP-4) and stimulate GLP-1 secretion. We putatively identified 76 lettuce metabolites (sesquiterpene lactones, non-phenolic and phenolic compounds) some of which were altered by several thousand percent in RA and RC. Ferulic acid levels increased 3033–9777%, aminooxononanoic acid increased 1141–1803% and 2,3,5,4′tetrahydroxystilbene-2-O-β-d-glucoside increased 40,272–48,008%. Compound activities were confirmed using commercially obtained standards. In conclusion, <i>rol</i> gene transformation significantly alters the metabolome of <i>L.sativa</i> and enhances its antidiabetic properties. There is considerable potential to exploit <i>rol</i> genes to modulate secondary metabolite production for the development of novel functional foods. This investigation serves as a new paradigm whereby genetic manipulation, metabolomic analysis and bioactivity techniques can be combined to enable the discovery of novel natural bioactives and determine the functional significance of plant metabolites. |
| first_indexed | 2024-12-21T19:38:02Z |
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| id | doaj.art-aed971824ae140128f74e673f9573c20 |
| institution | Directory Open Access Journal |
| issn | 2218-1989 |
| language | English |
| last_indexed | 2024-12-21T19:38:02Z |
| publishDate | 2019-05-01 |
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| spelling | doaj.art-aed971824ae140128f74e673f9573c202022-12-21T18:52:33ZengMDPI AGMetabolites2218-19892019-05-01959710.3390/metabo9050097metabo9050097The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary MetabolitesHammad Ismail0Anna L. Gillespie1Danielle Calderwood2Haroon Iqbal3Colene Gallagher4Olivier P. Chevallier5Christopher T. Elliott6Xiaobei Pan7Bushra Mirza8Brian D. Green9Department of Biochemistry, Quaid-I-Azam University, 45320 Islamabad, PakistanInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKDepartment of Biochemistry, Quaid-I-Azam University, 45320 Islamabad, PakistanInstitute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, Biological Sciences Building, Chlorine Gardens, Belfast BT9 5DL, UKPlant secondary metabolites are protective dietary constituents and <i>rol</i> genes evidently increase the synthesis of these versatile phytochemicals. This study subjected a globally important vegetable, lettuce (<i>Lactuca sativa</i>) to a combination of untargeted metabolomics (LC-QTof-MS) and in vitro bioactivity assays. Specifically, we examined the differences between untransformed cultured lettuce (UnT), lettuce transformed with either <i>rolABC</i> (RA) or <i>rolC</i> (RC) and commercially grown (COM) lettuce. Of the 5333 metabolite features aligned, deconvoluted and quantified 3637, 1792 and 3737 significantly differed in RA, RC and COM, respectively, compared with UnT. In all cases the number of downregulated metabolites exceeded the number increased. In vitro bioactivity assays showed that RA and RC (but not COM) significantly improved the ability of <i>L. sativa</i> to inhibit α-glucosidase, inhibit dipeptidyl peptidase-4 (DPP-4) and stimulate GLP-1 secretion. We putatively identified 76 lettuce metabolites (sesquiterpene lactones, non-phenolic and phenolic compounds) some of which were altered by several thousand percent in RA and RC. Ferulic acid levels increased 3033–9777%, aminooxononanoic acid increased 1141–1803% and 2,3,5,4′tetrahydroxystilbene-2-O-β-d-glucoside increased 40,272–48,008%. Compound activities were confirmed using commercially obtained standards. In conclusion, <i>rol</i> gene transformation significantly alters the metabolome of <i>L.sativa</i> and enhances its antidiabetic properties. There is considerable potential to exploit <i>rol</i> genes to modulate secondary metabolite production for the development of novel functional foods. This investigation serves as a new paradigm whereby genetic manipulation, metabolomic analysis and bioactivity techniques can be combined to enable the discovery of novel natural bioactives and determine the functional significance of plant metabolites.https://www.mdpi.com/2218-1989/9/5/97Lettuceplantssecondary metabolitesmetabolomicsdiabetes |
| spellingShingle | Hammad Ismail Anna L. Gillespie Danielle Calderwood Haroon Iqbal Colene Gallagher Olivier P. Chevallier Christopher T. Elliott Xiaobei Pan Bushra Mirza Brian D. Green The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites Metabolites Lettuce plants secondary metabolites metabolomics diabetes |
| title | The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites |
| title_full | The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites |
| title_fullStr | The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites |
| title_full_unstemmed | The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites |
| title_short | The Health Promoting Bioactivities of <i>Lactuca sativa</i> can be Enhanced by Genetic Modulation of Plant Secondary Metabolites |
| title_sort | health promoting bioactivities of i lactuca sativa i can be enhanced by genetic modulation of plant secondary metabolites |
| topic | Lettuce plants secondary metabolites metabolomics diabetes |
| url | https://www.mdpi.com/2218-1989/9/5/97 |
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