Biology:Genetically modified tomato

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Plant physiologist Athanasios Theologis with tomatoes that contain the bioengineered ACC synthase gene

A genetically modified tomato, or transgenic tomato, is a tomato that has had its genes modified, using genetic engineering. The first trial genetically modified food was a tomato engineered to have a longer shelf life (the Flavr Savr), which was on the market briefly beginning on May 21, 1994.[1] The first direct consumption tomato was approved in Japan in 2021.[2] Primary work is focused on developing tomatoes with new traits like increased resistance to pests or environmental stresses.[3] Other projects aim to enrich tomatoes with substances that may offer health benefits or be more nutritious. As well as aiming to produce novel crops, scientists produce genetically modified tomatoes to understand the function of genes naturally present in tomatoes.

Agrobacterium-mediated genetic engineering techniques were developed in the late 1980s that could successfully transfer genetic material into the nuclear genome of tomatoes.[4] Genetic material can also be inserted into a tomato cell's chloroplast and chromoplast plastomes using biolistics. Tomatoes were the first food crop with an edible fruit where this was possible.[5]

Examples

Delayed ripening

Tomatoes have been used as a model organism to study the fruit ripening of climacteric fruit. To understand the mechanisms involved in the process of ripening, scientists have genetically engineered tomatoes.[6]

In 1994, the Flavr Savr became the first commercially grown genetically engineered food to be granted a license for human consumption. A second copy of the tomato gene polygalacturonase was inserted into the tomato genome in the antisense direction.[7] The polygalacturonase enzyme degrades pectin, a component of the tomato cell wall, causing the fruit to soften. When the antisense gene is expressed it interferes with the production of the polygalacturonase enzyme, delaying the ripening process. The Flavr Savr failed to achieve commercial success and was withdrawn from the market in 1997. Similar technology, but using a truncated version of the polygalacturonase gene, was used to make a tomato paste.[8]

DNA Plant Technology (DNAP), Agritope and Monsanto developed tomatoes that delayed ripening by preventing the production of ethylene,[8] a hormone that triggers ripening of fruit.[9] All three tomatoes inhibited ethylene production by reducing the amount of 1-aminocyclopropane-1-carboxylic acid (ACC), the precursor to ethylene. DNAP's tomato, called Endless Summer, inserted a truncated version of the ACC synthase gene into the tomato that interfered with the endogenous ACC synthase.[8] Monsanto's tomato was engineered with the ACC deaminase gene from the soil bacterium Pseudomonas chlororaphis that lowered ethylene levels by breaking down ACC.[10] Agritope introduced an S-adenosylmethionine hydrolase (SAMase) encoding gene derived from the E. coli bacteriophage T3, which reduced the levels of S-adenosylmethionine, a precursor to ACC.[11] Endless Summer was briefly tested in the marketplace, but patent arguments forced its withdrawal.[12]

Scientists in India have delayed the ripening of tomatoes by silencing two genes encoding N-glycoprotein modifying enzymes, α-mannosidase and β-D-N-acetylhexosaminidase. The fruits produced were not visibly damaged after being stored at room temperature for 45 days, whereas unmodified tomatoes had gone rotten.[13] In India, where 30% of fruit is wasted before it reaches the market due to a lack of refrigeration and poor road infrastructure, the researchers hope genetic engineering of the tomato may decrease wastage.[14]

Environmental stress tolerance

Abiotic stresses like frost, drought and increased salinity are a limiting factor to the growth of tomatoes.[15] While no genetically modified stress-tolerant plants are currently[when?] commercialised, transgenic approaches have been researched. An early tomato was developed that contained an antifreeze gene (afa3) from the winter flounder with the aim of increasing the tomato's tolerance to frost, which became an icon in the early years of the debate over genetically modified foods, especially in relation to the perceived ethical dilemma of combining genes from different species. This tomato gained the moniker "fish tomato".[16] The antifreeze protein was found to inhibit ice recrystallization in the flounder blood, but had no effect when expressed in transgenic tobacco.[17] The resulting tomato was never commercialized, possibly because the transgenic plant did not perform well in its frost-tolerance or other agronomic characteristics.[17] Another failed cold tolerant is the E. coli GR transgenic: Others had successfully produced cold tolerant Nicotiana tabacum by inserting various enzymes into the plastids that had already been observed to be more active under cold stress in the donor organism. Brüggemann et al. 1999 thus assumed the same would hold for a transfer of E. coli's glutathione reductase → the chloroplasts of S. lycopersicum and S. peruvianum. They overexpressed the donated GR – and this was supplementing the endogenous GR. Although total GR activity was increased, no improvement in cold tolerance did obtain.[18]

Other genes from various species have been inserted into the tomato with the hope of increasing their resistance to various environmental factors. A gene from rice (Osmyb4), which codes for a transcription factor, that was shown to increase cold and drought tolerance in transgenic Arabidopsis thaliana plants, was inserted into the tomato. This resulted in increased drought tolerance, but did not appear to have any effect on cold tolerance.[19] Overexpressing a vacuolar Na+/H+ antiport (AtNHX1) from A. thaliana lead to salt accumulating in the leaves of the plants, but not in the fruit and allowed them to grow more in salt solutions than wildtype plants.[20][21] Tobacco osmotic genes overexpressed in tomatoes produced plants that held a higher water content than wildtype plants increasing tolerance to drought and salt stress.[22]

Pest resistance

The insecticidal toxin from the bacterium Bacillus thuringiensis has been inserted into a tomato plant.[23] When field tested they showed resistance to the tobacco hornworm (Manduca sexta), tomato fruitworm (Heliothis zea), the tomato pinworm (Keiferia lycopersicella) and the tomato fruit borer (Helicoverpa armigera).[24][25] A 91-day feeding trial in rats showed no adverse effects,[26] but the Bt tomato has never been commercialised. Tomatoes resistant to a root knot nematode have been created by inserting a cysteine proteinase inhibitor gene from taro.[27] A chemically synthesised cecropin B gene, usually found in the giant silk moth (Hyalophora cecropia), has been introduced into tomato plants and in vivo studies show significant resistance to bacterial wilt and bacterial spot.[28] When the cell wall proteins, polygalacturonase and expansin are prevented from being produced in fruits, they are less susceptible to the fungus Botrytis cinerea than normal tomatoes.[29][30] Pest resistant tomatoes can reduce the ecological footprint of tomato production while at the same time increase farm income.[31]

Improved nutrition

Tomatoes have been altered in attempts to add nutritional content. In 2000, the concentration of pro-vitamin A was increased by adding a bacterial gene encoding phytoene desaturase, although the total amount of carotenoids remained equal.[32] The researchers admitted at the time that it had no prospect of being grown commercially due to the anti-GM climate. Sue Meyer of the pressure group Genewatch, told The Independent that she believed, "If you change the basic biochemistry, you could alter the levels of other nutrients very important for health".[33] More recently, scientists created blue tomatoes that have increased the production of anthocyanin, an antioxidant in tomatoes in several ways. One group added a transcription factor for the production of anthocyanin from Arabidopsis thaliana[34] whereas another used transcription factors from snapdragon (Antirrhinum).[35] When the snapdragon genes were used, the fruits had similar anthocyanin concentrations to blackberries and blueberries.[36] The inventors of the GMO blue tomato using snapdragon genes, Jonathan Jones and Cathie Martin of the John Innes Centre, founded a company called Norfolk Plant Sciences[37] to commercialize the blue tomato. They partnered with a company in Canada called New Energy Farms to grow a large crop of blue tomatoes, from which to create juice to test in clinical trials on the way to obtaining regulatory approval.[38][39]

Another group has tried to increase the levels of isoflavone, known for its potential cancer preventive properties, by introducing the soybean isoflavone synthase into tomatoes.[40]

In 2021 Japanese Sanatech Seed issued Sicilian Rouge High GABA tomato variety with increased GABA levels.[2]

Improved taste

When geraniol synthase from lemon basil (Ocimum basilicum) was expressed in tomato fruits under a fruit-specific promoter, 60% of untrained taste testers preferred the taste and smell of the transgenic tomatoes. The fruits contained around half the amount of lycopene.[41]

Vaccines

Tomatoes (along with potatoes, bananas and other plants) are being investigated as vehicles for delivering edible vaccines. Clinical trials have been conducted on mice using tomatoes expressing antibodies or proteins that stimulate antibody production targeted to norovirus, hepatitis B, rabies, HIV, anthrax and respiratory syncytial virus.[42] Korean scientists are looking at using the tomato to express a vaccine against Alzheimer's disease.[43] Hilary Koprowski, who was involved in the development of the polio vaccine, led a group of researchers in developing a tomato expressing a recombinant vaccine to SARS.[44]

Basic research

Tomatoes are used as a model organism in scientific research and they are frequently genetically modified to further understanding of particular processes. Tomatoes have been used as a model in map-based cloning, where transgenic plants must be created to prove that a gene has been successfully isolated.[45] The plant peptide hormone, systemin was first identified in tomato plants and genetic modification has been used to demonstrate its function, by adding antisense genes to silence the native gene or by adding extra copies of the native gene.[46][47]

References

  1. ↑ Martineau, B., "First Fruit", McGraw Hill Book Co., p191
  2. ↑ 2.0 2.1 "Sanatech Seed launches world's first GE tomato". http://www.fruitnet.com/eurofruit/article/184662/sanatech-seed-launches-worlds-first-ge-tomato. 
  3. ↑ Nowicki, Marcin (11 October 2013), "Late Blight of Tomato", Translational Genomics for Crop Breeding, pp. 241–265, doi:10.1002/9781118728475.ch13, ISBN 9781118728475 
  4. ↑ Jeroen S. C. van Roekel, Brigitte Damm, Leo S. Melchers, and Andr Hoekema (1993). "Factors influencing transformation frequency of tomato (Lycopersicon esculentum)". Plant Cell Reports 12 (11): 644–647. doi:10.1007/bf00232816. PMID 24201880. 
  5. ↑ Ruf, S.; Hermann, M.; Berger, I.; Carrer, H.; Bock, R. (2001). "Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit". Nature Biotechnology 19 (9): 870–875. doi:10.1038/nbt0901-870. PMID 11533648. 
  6. ↑ Alexander, L.; Grierson, D (October 2002). "Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening". Journal of Experimental Botany 53 (377): 2039–55. doi:10.1093/jxb/erf072. PMID 12324528. 
  7. ↑ Redenbalpolollolneau, Matthew Kramer, Ray Sheehy, Rick Sanders, Cathy Houck and Don Emlay (1992). Safety Assessment of Genetically Engineered Fruits and Vegetables: A Case Study of the Flavr Savr Tomato. CRC Press. p. 288. 
  8. ↑ 8.0 8.1 8.2 Center for Environmental Risk Assessment. "GM Crop Database: Event 1345-4". International Life Sciences Institute. http://cera-gmc.org/index.php?action=gm_crop_database&mode=ShowProd&data=1345-4. 
  9. ↑ Marcia Wood (July 1995). "Bioengineered Tomatoes Taste Great". Agricultural Research Magazine. http://www.ushrl.saa.ars.usda.gov/is/ar/archive/jul95/tomatoes0795.htm?pf=1. Retrieved 2010-08-20. 
  10. ↑ H. J. Klee; M. B. Hayford; K. A. Kretzmer; G. F. Barry; G. M. Kishore (1991). "Control of Ethylene Synthesis by Expression of a Bacterial Enzyme in Transgenic Tomato Plants". The Plant Cell 3 (11): 1187–1193. doi:10.2307/3869226. PMID 1821764. PMC 160085. http://www.plantcell.org/cgi/content/abstract/3/11/1187. 
  11. ↑ Good, X.; Kellogg, J. A.; Wagoner, W.; Langhoff, D.; Matsumura, W.; Bestwick, R. K. (1994). "Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase". Plant Molecular Biology 26 (3): 781–790. doi:10.1007/BF00028848. PMID 7999994. 
  12. ↑ Craig Freudenrich; Dora Barlaz; Jane Gardner (2009). AP Environmental Science. Kaplen inc. pp. 189–190. ISBN 978-1-4277-9816-9. https://books.google.com/books?id=gT7Saz64Bs4C&q=Endless+summer+tomato&pg=PA190. 
  13. ↑ Meli, V.; Ghosh, S.; Prabha, T.; Chakraborty, N.; Chakraborty, S.; Datta, A. (2010). "Enhancement of fruit shelf life by suppressing N-glycan processing enzymes". Proceedings of the National Academy of Sciences of the United States of America 107 (6): 2413–2418. doi:10.1073/pnas.0909329107. PMID 20133661. Bibcode: 2010PNAS..107.2413M. 
  14. ↑ Buncombe, Andrew (2010-02-09). "India's new delicacy: a 45-day-old tomato - Asia, World". The Independent (London). https://www.independent.co.uk/news/world/asia/indias-new-delicacy-a-45dayold-tomato-1893333.html. 
  15. ↑ Foolad, M. R. (2007). "Current Status of Breeding Tomatoes for Salt and Drought Tolerance". Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. pp. 669–700. doi:10.1007/978-1-4020-5578-2_27. ISBN 978-1-4020-5577-5. 
  16. ↑ Mchugen, Alan (2000). Pandora's Picnic Basket. Oxford University Press, UK. ISBN 978-0-19-850674-4. https://books.google.com/books?id=UkAAZPNS9b4C&q=alan+mchughen+fish+tomato&pg=PA15. 
  17. ↑ 17.0 17.1 Lemaux, P. (2008). "Genetically Engineered Plants and Foods: A Scientist's Analysis of the Issues (Part I)". Annual Review of Plant Biology 59: 771–812. doi:10.1146/annurev.arplant.58.032806.103840. PMID 18284373. 
  18. ↑ Iba, Koh (2002). "Acclimative Response to Temperature Stress in Higher Plants: Approaches of Gene Engineering for Temperature Tolerance". Annual Review of Plant Biology (Annual Reviews) 53 (1): 225–245. doi:10.1146/annurev.arplant.53.100201.160729. ISSN 1543-5008. PMID 12221974. 
  19. ↑ Vannini, C.; Campa, M.; Iriti, M.; Genga, A.; Faoro, F.; Carravieri, S.; Rotino, G. L.; Rossoni, M. et al. (2007). "Evaluation of transgenic tomato plants ectopically expressing the rice Osmyb4 gene". Plant Science 173 (2): 231–239. doi:10.1016/j.plantsci.2007.05.007. 
  20. ↑ Zhang, H. X.; Blumwald, E. (2001). "Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit". Nature Biotechnology 19 (8): 765–768. doi:10.1038/90824. PMID 11479571. 
  21. ↑ "Gene-modified tomato revels in salty soils - 31 July 2001". New Scientist. https://www.newscientist.com/article/dn1092-gene-modified-tomato-revels-in-salty-soils/. 
  22. ↑ Goel, D.; Singh, A. K.; Yadav, V.; Babbar, S. B.; Bansal, K. C. (2010). "Overexpression of osmotin gene confers tolerance to salt and drought stresses in transgenic tomato (Solanum lycopersicum L.)". Protoplasma 245 (1–4): 133–141. doi:10.1007/s00709-010-0158-0. PMID 20467880. 
  23. ↑ Fischhoff, D. A.; Bowdish, K. S.; Perlak, F. J.; Marrone, P. G.; McCormick, S. M.; Niedermeyer, J. G.; Dean, D. A.; Kusano-Kretzmer, K. et al. (1987). "Insect Tolerant Transgenic Tomato Plants". Bio/Technology 5 (8): 807–813. doi:10.1038/nbt0887-807. 
  24. ↑ Delannay, X.; Lavallee, B. J.; Proksch, R. K.; Fuchs, R. L.; Sims, S. R.; Greenplate, J. T.; Marrone, P. G.; Dodson, R. B. et al. (1989). "Field Performance of Transgenic Tomato Plants Expressing the Bacillus Thuringiensis Var. Kurstaki Insect Control Protein". Nature Biotechnology 7 (12): 1265–1269. doi:10.1038/nbt1289-1265. 
  25. ↑ Kumar, H.; Kumar, V. (2004). "Tomato expressing Cry1A(b) insecticidal protein from Bacillus thuringiensis protected against tomato fruit borer, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) damage in the laboratory, greenhouse and field". Crop Protection 23 (2): 135–139. doi:10.1016/j.cropro.2003.08.006. 
  26. ↑ Noteborn, H. P. J. M.; Bienenmann-Ploum, M. E.; Van Den Berg, J. H. J.; Alink, G. M.; Zolla, L.; Reynaerts, A.; Pensa, M.; Kuiper, H. A. (1995). "Safety Assessment of theBacillus thuringiensisInsecticidal Crystal Protein CRYIA(b) Expressed in Transgenic Tomatoes". Safety Assessment of the Bacillus thuringiensis Insecticidal Crystal Protein CRYIA(b) Expressed in Transgenic Tomatoes. ACS Symposium Series. 605. pp. 134. doi:10.1021/bk-1995-0605.ch012. ISBN 978-0-8412-3320-1. 
  27. ↑ Chan, Y.; Yang, A.; Chen, J.; Yeh, K.; Chan, M. (2010). "Heterologous expression of taro cystatin protects transgenic tomato against Meloidogyne incognita infection by means of interfering sex determination and suppressing gall formation". Plant Cell Reports 29 (3): 231–238. doi:10.1007/s00299-009-0815-y. PMID 20054551. http://ntur.lib.ntu.edu.tw/bitstream/246246/243272/-1/59.pdf. 
  28. ↑ Jan, P.; Huang, H.; Chen, H. (2010). "Expression of a synthesized gene encoding cationic peptide cecropin B in transgenic tomato plants protects against bacterial diseases". Applied and Environmental Microbiology 76 (3): 769–775. doi:10.1128/AEM.00698-09. PMID 19966019. Bibcode: 2010ApEnM..76..769J. 
  29. ↑ "Fruit Cell Wall Proteins Help Fungus Turn Tomatoes From Ripe To Rotten". Science Daily. Jan 31, 2008. https://www.sciencedaily.com/releases/2008/01/080126172454.htm. 
  30. ↑ Cantu, D.; Vicente, A.; Greve, L.; Dewey, F.; Bennett, A.; Labavitch, J.; Powell, A. (2008). "The intersection between cell wall disassembly, ripening, and fruit susceptibility to Botrytis cinerea". Proceedings of the National Academy of Sciences of the United States of America 105 (3): 859–864. doi:10.1073/pnas.0709813105. PMID 18199833. Bibcode: 2008PNAS..105..859C. 
  31. ↑ Groeneveld, Rolf, Erik Ansink, Clemens van de Wiel, and Justus Wesseler (2011) Benefits and costs of biologically contained GM tomatoes and eggplants in Italy and Spain. Sustainability. 2011, 3, 1265-1281
  32. ↑ Römer, S.; Fraser, P. D.; Kiano, J. W.; Shipton, C. A.; Misawa, N.; Schuch, W.; Bramley, P. M. (2000). "Elevation of the provitamin a content of transgenic tomato plants". Nature Biotechnology 18 (6): 666–669. doi:10.1038/76523. PMID 10835607. 
  33. ↑ Connor, Steve (2000-05-31). "No market for the GM tomato that fights cancer - Science, News". The Independent (London). https://www.independent.co.uk/news/science/no-market-for-the-gm-tomato-that-fights-cancer-716980.html. [|permanent dead link|dead link}}]
  34. ↑ Zuluaga, D. L.; Gonzali, S.; Loreti, E.; Pucciariello, C.; Degl'Innocenti, E.; Guidi, L.; Alpi, A.; Perata, P. (2008). "Arabidopsis thaliana MYB75/PAP1transcription factor induces anthocyanin production in transgenic tomato plants". Functional Plant Biology 35 (7): 606–618. doi:10.1071/FP08021. PMID 32688816. 
  35. ↑ "Purple Tomatoes, Rich In Health-Protecting Anthocyanins, Developed With Help Of Snapdragons". Sciencedaily.com. 2008-10-27. https://www.sciencedaily.com/releases/2008/10/081026150149.htm. 
  36. ↑ Butelli, E.; Titta, L.; Giorgio, M.; Mock, H.; Matros, A.; Peterek, S.; Schijlen, E.; Hall, R. et al. (2008). "Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors". Nature Biotechnology 26 (11): 1301–1308. doi:10.1038/nbt.1506. PMID 18953354. 
  37. ↑ Norfolk Plant Sciences About Norfolk Plant Sciences
  38. ↑ Clive Cookson for the Financial Times. January 24, 2014 Purple tomato juice from Canadian GM crop heads for trial in UK
  39. ↑ John Innes Centre 25 January 2014 Press Release: Bumper harvest for GM purple tomatoes
  40. ↑ Shih, C. H.; Chen, Y.; Wang, M.; Chu, I. K.; Lo, C. (2008). "Accumulation of Isoflavone Genistin in Transgenic Tomato Plants Overexpressing a Soybean Isoflavone Synthase Gene". Journal of Agricultural and Food Chemistry 56 (14): 5655–5661. doi:10.1021/jf800423u. PMID 18540614. 
  41. ↑ Davidovich-Rikanati, R.; Sitrit, Y.; Tadmor, Y.; Iijima, Y.; Bilenko, N.; Bar, E.; Carmona, B.; Fallik, E. et al. (2007). "Enrichment of tomato flavor by diversion of the early plastidial terpenoid pathway". Nature Biotechnology 25 (8): 899–901. doi:10.1038/nbt1312. PMID 17592476. 
  42. ↑ Goyal, R.; Ramachandran, R.; Goyal, P.; Sharma, V. (2007). "Edible vaccines: Current status and future". Indian Journal of Medical Microbiology 25 (2): 93–102. doi:10.1016/S0255-0857(21)02165-4. PMID 17582177. 
  43. ↑ Youm, J.; Jeon, J.; Kim, H.; Kim, Y.; Ko, K.; Joung, H.; Kim, H. (2008). "Transgenic tomatoes expressing human beta-amyloid for use as a vaccine against Alzheimer's disease". Biotechnology Letters 30 (10): 1839–1845. doi:10.1007/s10529-008-9759-5. PMID 18604480. 
  44. ↑ Pogrebnyak, N.; Golovkin, M.; Andrianov, V.; Spitsin, S.; Smirnov, Y.; Egolf, R.; Koprowski, H. (2005). "Severe acute respiratory syndrome (SARS) S protein production in plants: development of recombinant vaccine". Proceedings of the National Academy of Sciences of the United States of America 102 (25): 9062–9067. doi:10.1073/pnas.0503760102. PMID 15956182. Bibcode: 2005PNAS..102.9062P. 
  45. ↑ Wing, R.; Zhang, H. B.; Tanksley, S. (1994). "Map-based cloning in crop plants. Tomato as a model system: I. Genetic and physical mapping of jointless". MGG Molecular & General Genetics 242 (6): 681–688. doi:10.1007/BF00283423. PMID 7908716. 
  46. ↑ Orozco-Cardenas, M; McGurl, B; Ryan, CA (September 1993). "Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae". Proceedings of the National Academy of Sciences of the United States of America 90 (17): 8273–6. doi:10.1073/pnas.90.17.8273. PMID 11607423. Bibcode: 1993PNAS...90.8273O. 
  47. ↑ McGurl, B; Orozco-Cardenas, M; Pearce, G; Ryan, CA (October 1994). "Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis". Proceedings of the National Academy of Sciences of the United States of America 91 (21): 9799–802. doi:10.1073/pnas.91.21.9799. PMID 7937894. Bibcode: 1994PNAS...91.9799M. 



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