Can the world’s favorite fruit, tomato, provide an effective biosynthetic chassis for high-value metabolites?

Plant Cell Reports

Volumn 37, Issue 10, 2018, Pages 1443-1450

  Li, Yan ^a   Wang, Hsihua ^a   Zhang, Yang ^a   Martin, Cathie ^b  

^a SICHUAN UNIVERSITY   (China)

^b NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

Chassis; Metabolic engineering; Scale up production; Specialized metabolites; Tomato

Indexed keywords

BIOTECHNOLOGY; CROP; GENETICS; METABOLIC ENGINEERING; METABOLISM; PROCEDURES; TOMATO; TRANSGENIC PLANT;

BIOTECHNOLOGY; CROPS, AGRICULTURAL; LYCOPERSICON ESCULENTUM; METABOLIC ENGINEERING; PLANTS, GENETICALLY MODIFIED;

EID: 85044449213     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-018-2283-8     Document Type: Review

References (72)

1. Baud S, Bourrellier ABF, Azzopardi M, Berger A, Dechorgnat J, Danielvedele F, Lepiniec L, Miquel M, Rochat C, Hodges M (2010) PII is induced by WRINKLED1 and fine-tunes fatty acid composition in seeds of Arabidopsis thaliana. Plant J Cell Mol Biol 64:291–303
2. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84
3. Blancquaert D, Van DJ, Strobbe S, Kiekens F, Storozhenko S, De SH, Gellynck X, Lambert W, Stove C, Van DSD (2015) Improving folate (vitamin B9) stability in biofortified rice through metabolic engineering. Nat Biotechnol 33:1076–1078
4. Bovy A, De VR, Kemper M, Schijlen E, Almenar PM, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 14:2509–2526
5. Brooks C, Nekrasov V, Lippman ZB, Van EJ (2014) Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol 166:1292–1297
6. Broun P, Liu Y, Queen E, Schwarz Y, Abenes ML, Leibman M (2006) Importance of transcription factors in the regulation of plant secondary metabolism and their relevance to the control of terpenoid accumulation. Phytochem Rev 5:27–38
7. Butelli E, Titta L, Giorgio M, Mock HP, Matros A, Peterek S, Schijlen E, Hall RD, Bovy AG, Luo J (2008) Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat Biotechnol 26:1301–1308
8. Cárdenas PD, Sonawane PD, Pollier J, Vanden Bossche R, Dewangan V, Weithorn E, Tal L, Meir S, Rogachev I, Malitsky S, Giri AP, Goossens A, Burdman S, Aharoni A (2016) GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nat Commun 7:1–16
9. Carrillo L, Herrero I, Cambra I, Sánchez-Monge R, Diaz I, Martinez M (2011) Differential in vitro and in vivo effect of barley cysteine and serine protease inhibitors on phytopathogenic microorganisms. Plant Physiol Biochem 49:1191–1200
10. Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29
11. Che P, Zhao ZY, Glassman K, Dolde D, Hu TX, Jones TJ, Obukosia S, Wambugu F, Albertsen MC (2016) Elevated vitamin E content improves all-trans β-carotene accumulation and stability in biofortified sorghum. Proc Natl Acad Sci USA 113:11040–11045
12. Consortium TG (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
13. Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, Armstrong CL (2006) MicroTom—a high-throughput model transformation system for functional genomics. Plant Cell Rep 25:432–441
14. Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162
15. Farré G, Blancquaert D, Capell T, Van DSD, Christou P, Zhu C (2014) Engineering complex metabolic pathways in plants. Annu Rev Plant Biol 65:187–223
16. Fischer R, Vaquero-Martin C, Sack M, Drossard J, Emans N, Commandeur U (1999) Towards molecular farming in the future: transient protein expression in plants. Biotechnol Appl Biochem 30:113–116
17. Frary A, Nesbitt TC, Frary A, Grandillo S, Van Der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2. 2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
18. Fridman E, Pleban T, Zamir D (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97:4718–4723
19. Fu R, Martin C, Zhang Y (2018) Next-generation plant metabolic engineering, inspired by an ancient Chinese irrigation system. Mol Plant 11:47–57
20. Georgiev V, Ilieva M, Bley T, Pavlov A (2008) Betalain production in plant in vitro systems. Acta Physiol Plant 30:581–593
21. Gonzali S, Mazzucato A, Perata P (2009) Purple as a tomato: towards high anthocyanin tomatoes. Trends Plant Sci 14:237–241
22. Hannon GJ (2002) RNA interference. Nature 418:244–251
23. Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R (2013) Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341:175–179
24. Kunzler A, Kolling EA, da Silva-Jr JD, Gasparotto J, de Bittencourt Pasquali MA, Moreira JC, Gelain DP (2017) Retinol (vitamin A) increases α-synuclein, β-amyloid peptide, tau phosphorylation and RAGE content in human SH-SY5Y neuronal cell line. Neurochem Res 42:2788–2797
25. Kushibiki T, Tabata Y (2005) Preparation of poly(ethylene glycol)-introduced cationized gelatin as a non-viral gene carrier. J Biomater Sci Polym Ed 16:1447–1461
26. Lin T, Zhu G, Zhang J, Xu X, Yu Q, Zheng Z, Zhang Z, Lun Y, Li S, Wang X (2014) Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46:1220–1226
27. Liu X, Ding W, Jiang H (2017a) Engineering microbial cell factories for the production of plant natural products: from design principles to industrial-scale production. Microb Cell Fact 16:125–134
28. Liu Y, Zhong Y, Chen H, Wang D, Wang M, Ou JS, Xia M (2017b) Retinol binding protein-dependent cholesterol uptake regulates macrophage foam cell formation and promotes atherosclerosis. Circulation 135:1339–1354
29. Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R (2013) Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proc Natl Acad Sci USA 110:623–632
30. Luo J (2015) Metabolite-based genome-wide association studies in plants. Curr Opin Plant Biol 24:31–38
31. Luo J, Butelli E, Hill L, Parr A, Niggeweg R, Bailey P, Weisshaar B, Martin C (2008) AtMYB12 regulates caffeoyl quinic acid and flavonol synthesis in tomato: expression in fruit results in very high levels of both types of polyphenol. Plant J 56:316–326
32. Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K (2009) An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J Cell Mol Biol 60:476–487
33. Marchive C, Nikovics K, To A, Lepiniec L, Baud S (2015) Transcriptional regulation of fatty acid production in higher plants: molecular bases and biotechnological outcomes. Eur J Lipid Sci Technol 116:1332–1343
34. Martin C (1996) Transcription factors and the manipulation of plant traits. Curr Opin Biotechnol 7:130–138
35. Martin C, Li J (2017) Medicine is not health care, food is health care: plant metabolic engineering, diet and human health. New Phytol 216:699–719
36. Mène-Saffrané L, Pellaud S (2017) Current strategies for vitamin E biofortification of crops. Curr Opin Biotechnol 44:189–197
37. Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, De Vos CR, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474
38. Nogueira M, Enfissi E, Martínez MV, Menard GN, Driller RL, Eastmond PJ, Schuch W, Sandmann G, Fraser PD (2017) Engineering of tomato for the sustainable production of ketocarotenoids and its evaluation in aquaculture feed. Proc Natl Acad Sci USA 114:10876–10881
39. O’Neill EC, Kelly S (2016) Engineering biosynthesis of high-value compounds in photosynthetic organisms. Crit Rev Biotechnol 37:779–802
40. Olmedilla B, Granado F, Blanco I, Vaquero M (2003) Lutein, but not alpha-tocopherol, supplementation improves visual function in patients with age-related cataracts: a 2-y double-blind, placebo-controlled pilot study. Nutrition 19:21–24
41. Orzaez D, Medina A, Torrez S, Fernandez-Moreno JP, Rambla JL, Fernandez-Del-Carmen A, Butelli E, Martin C, Granell A (2009) A visual reporter system for virus-induced gene silencing in tomato fruit based on anthocyanin accumulation. Plant Physiol 150:1122–1134
42. Pan C, Ye L, Qin L, Liu X, He Y, Wang J, Chen L, Lu G (2016) CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci Rep 6:24765
43. Peixoto JV, Neto CM, Campos LF, Dourado WS, Nogueira AP, Nascimento AD (2017) Industrial tomato lines: morphological properties and productivity. Genet Mol Res 16:1–15
44. Polturak G, Grossman N, Vela-Corcia D, Dong Y, Nudel A, Pliner M, Levy M, Rogachev I, Aharoni A (2017) Engineered gray mold resistance, antioxidant capacity, and pigmentation in betalain-producing crops and ornamentals. Proc Natl Acad Sci USA 114:9062–9067
45. Potrykus I (1991) Gene transfer to plants assessment of published approaches and results. Annu Rev Plant Physiol Plant Mol Biol 42:205–225
46. Powell ALT, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernández-Muñoz R, Vicente A, Lopez-Baltazar J, Barry CS, Liu Y, Chetelat R, Granell A, Deynze AV, Giovannoni JJ, Bennett AB (2012) Uniform ripening encodes a golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336:1711–1715
47. Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, B.Lippman Z (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:1–11
48. Ru M, Wang K, Bai Z, Peng L, He S, Pei T, Jia Y, Li H, Liang Z (2016) Molecular cloning and characterisation of two enzymes involved in the rosmarinic acid biosynthesis pathway of Prunella vulgaris L. Plant Cell Tissue Organ Culture 128:381–390
49. Sato S, Frederiksen R, Cornwall MC, Kefalov VJ (2017) The retina visual cycle is driven by cis retinol oxidation in the outer segments of cones. Vis Neurosci 34:1–8
50. Scarano A, Butelli E, De Santis S, Cavalcanti E, Hill L, De Angelis M, Giovinazzo G, Chieppa M, Martin C, Santino A (2017) Combined dietary anthocyanins, flavonols and stilbenoids alleviate inflammatory bowel disease symptoms in mice. Front Nutr 4:75
51. Schijlen E, Ch RDV, Jonker H, Van Den Broeck H, Molthoff J, Van TA, Martens S, Bovy A (2006) Pathway engineering for healthy phytochemicals leading to the production of novel flavonoids in tomato fruit. Plant Biotechnol J 4:433–444
52. Schwinn KE (2016) The dope on l-DOPA formation for betalain pigments. New Phytol 210:269–283
53. Siddiqui MW, Ayalazavala JF, Dhua RS (2015) Genotypic variation in tomatoes affecting processing and antioxidant attributes. Crit Rev Food Sci Nutr 55:1819–1835
54. Sonawane PD, Pollier J, Panda S, Szymanski J, Massalha H, Yona M, Unger T, Malitsky S, Arendt P, Pauwels L (2016) Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism. Nat Plants 3:16205–16218
55. Soyk S, Lemmon ZH, Oved M, Fisher J, Liberatore KL, Park SJ, Goren A, Jiang K, Ramos A Van dKE (2017) Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell 169:1142–1155
56. Sprink T, Metje J, Hartung F (2015) Plant genome editing by novel tools: TALEN and other sequence specific nucleases. Curr Opin Biotechnol 32:47–53
57. Suresh BV, Roy R, Sahu K, Misra G, Chattopadhyay D (2014) Tomato genomic resources database: an integrated repository of useful tomato genomic information for basic and applied research. PLoS One 9:e86387
58. Tieman D, Zhu G, Resende M Jr, Lin T, Nguyen C, Bies D, Rambla JL, Beltran KS, Taylor M, Zhang B (2017) A chemical genetic roadmap to improved tomato flavor. Science 355:391–394
59. Tzin V, Rogachev I, Meir S, Moyal Ben Zvi M, Masci T, Vainstein A, Aharoni A, Galili G (2013) Tomato fruits expressing a bacterial feedback-insensitive 3-deoxy-d-arabino-heptulosonate 7-phosphate synthase of the shikimate pathway possess enhanced levels of multiple specialized metabolites and upgraded aroma. J Exp Bot 64:4441–4452
60. USDA (2017) National Agricultural Statistics Service - Vegetables 2016 Summary
61. Van EH, Kelly AA, Menard G, Eastmond PJ (2014) Multigene engineering of triacylglycerol metabolism boosts seed oil content in Arabidopsis. Plant Physiol 165:30–36
62. Vanhercke T, El TA, Liu Q, Zhou XR, Shrestha P, Divi UK, Ral JP, Mansour MP, Nichols PD, James CN (2014) Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J 12:231–239
63. Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20 (Oxford University Press/USA)
64. Wang D, Seymour G (2017) Tomato flavor: lost and found? Mol Plant 10:782–784
65. Yin LH, Xu LN, Wang XN, Lu BN, Liu YT, Peng JY (2010) An economical method for isolation of dioscin from Dioscorea nipponica Makino by HSCCC coupled with ELSD, and a computer-aided UNIFAC mathematical model. Chromatographia 71:15–23
66. Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated. QTL Genet 141:1147–1162
67. Zamir D (2001) Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2:983–989
68. Zhang Y, Butelli E, Alseekh S, Tohge T, Rallapalli G, Luo J, Kawar PG, Hill L, Santino A, Fernie AR, Martin C (2015) Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat Commun 6:8635–8655
69. Zhang PC, Wu CR, Wang ZL, Wang LY, Han Y, Sun SL, Li QS, Ma L (2017) Effect of lutein supplementation on visual function in nonproliferative diabetic retinopathy. Asia Pac J Clin Nutr 26:406–411
70. Zhu CF, Bai C, Sanahuja G, Yuan DW, Farré G, Naqvi S, Shi LX, Capell T, Christou P, Landrum JT (2010) The regulation of carotenoid pigmentation in flowers. Arch Biochem Biophys 504:132–141
71. Zhu G, Wang S, Huang Z, Zhang S, Liao Q, Zhang C, Lin T, Qin M, Peng M, Yang C, Cao X (2018) Rewiring of the fruit metabolome in tomato breeding. Cell 172:249–261
72. Zsögön A, Cermak T, Dan V, Peres LEP (2017) Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: case study in tomato. Plant Sci Int J Exp Plant Biol 256:120–130