Creating plant molecular factories for industrial and nutritional isoprenoid production

Current Opinion in Biotechnology

Volumn 49, Issue , 2018, Pages 80-87

  Nogueira, Marilise ^a   Enfissi, Eugenia MA ^a   Almeida, Juliana ^a   Fraser, Paul D ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGY;

CHEMICAL DIVERSITY; CHEMICAL REFINING; CLIMATIC FLUCTUATIONS; ECONOMIC CHALLENGES; EFFICIENT PROCESS; INDUSTRIAL SECTOR; INDUSTRIALISATION; MANUFACTURING OUTPUT;

LIPIDS;

FRAGRANCE; ISOPRENOID; NATURAL PRODUCT; BIOLOGICAL PRODUCT; TERPENE;

CRISPR CAS SYSTEM; DIETARY SUPPLEMENT; DRUG MANUFACTURE; FEEDING; FOOD INDUSTRY; GENE EDITING; INDUSTRIAL PRODUCTION; METABOLIC ENGINEERING; MOLECULAR DYNAMICS; NONHUMAN; NUTRIGENOMICS; NUTRITION; PLANT BIOTECHNOLOGY; PRIORITY JOURNAL; REVIEW; METABOLISM; PLANT;

BIOLOGICAL PRODUCTS; METABOLIC ENGINEERING; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PLANTS; TERPENES;

EID: 85027569054     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2017.08.002     Document Type: Review

References (58)

1. Bouvier, F., Rahier, A., Camara, B., Biogenesis, molecular regulation and function of plant isoprenoids. Prog Lipid Res 44 (2005), 357–429.
2. Wurtzel, E.T., Kutchan, T.M., Plant metabolism, the diverse chemistry set of the future. Science 353 (2016), 1232–1236.
3. Wake, H., Oil refineries: a review of their ecological impacts on the aquatic environment. Estuar Coast Shelf Sci 62 (2005), 131–140.
4. Bensley, L., Van Eenwyk, J., Bruemmer, B.A., Measuring fruit and vegetable consumption: providing serving size information doubles estimated percent eating five per day. J Am Diet Assoc 103 (2003), 1530–1532.
5. Phillips, M.A., Leon, P., Boronat, A., Rodriguez-Concepcion, M., The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13 (2008), 619–623.
6. Fray, R.G., Wallace, A., Fraser, P.D., Valero, D., Hedden, P., Bramley, P.M., Grierson, D., Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Plant J 8 (1995), 693–701.
7. Busch, M., Seuter, A., Hain, R., Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiol 128 (2002), 439–453.
8. Masferrer, A., Arro, M., Manzano, D., Schaller, H., Fernandez-Busquets, X., Moncalean, P., Fernandez, B., Cunillera, N., Boronat, A., Ferrer, A., Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J 30 (2002), 123–132.
9. Fraser, P.D., Romer, S., Shipton, C.A., Mills, P.B., Kiano, J.W., Misawa, N., Drake, R.G., Schuch, W., Bramley, P.M., Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci U S A 99 (2002), 1092–1097.
10. Emanuelli, F., Battilana, J., Costantini, L., Le Cunff, L., Boursiquot, J.M., This, P., Grando, M.S., A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.). BMC Plant Biol, 10, 2010, 17.
11. Zamir, D., Improving plant breeding with exotic genetic libraries. Nat Rev Genet 2 (2001), 983–989.
12. Beyer, P., Al-Babili, S., Ye, X.D., Lucca, P., Schaub, P., Welsch, R., Potrykus, I., Golden rice: introducing the beta-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J Nutr 132 (2002), 506S–510S.
13. Bai, C., Rivera, S.M., Medina, V., Alves, R., Vilaprinyo, E., Sorribas, A., Canela, R., Capell, T., Sandmann, G., Christou, P., et al. An in vitro system for the rapid functional characterization of genes involved in carotenoid biosynthesis and accumulation. Plant J 77 (2014), 464–475 This article reports an interesting development with the potential to act as a synthetic biology platform to rapidly evaluated genes/products of interest and holistic metabolic changes.
14. Paine, J.A., Shipton, C.A., Chaggar, S., Howells, R.M., Kennedy, M.J., Vernon, G., Wright, S.Y., Hinchliffe, E., Adams, J.L., Silverstone, A.L., et al. Improving the nutritional value of golden rice through increased pro-vitamin A content. Nat Biotechnol 23 (2005), 482–487.
15. Diretto, G., Al-Babili, S., Tavazza, R., Papacchioli, V., Beyer, P., Giuliano, G., Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial mini-pathway. PLoS ONE, 2, 2007, e350.
16. Robertson, B.H., Grubman, M.J., Weddell, G.N., Moore, D.M., Welsh, J.D., Fischer, T., Dowbenko, D.J., Yansura, D.G., Small, B., Kleid, D.G., Nucleotide and amino-acid sequence coding for polypeptides of foot-and-mouth-disease virus type-a12. J Virol 54 (1985), 651–660.
17. Donnelly, M.L.L., Luke, G., Mehrotra, A., Li, X.J., Hughes, L.E., Gani, D., Ryan, M.D., Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal ‘skip’. J Gen Virol 82 (2001), 1013–1025.
18. Ralley, L., Enfissi, E.M., Misawa, N., Schuch, W., Bramley, P.M., Fraser, P.D., Metabolic engineering of ketocarotenoid formation in higher plants. Plant J 39 (2004), 477–486.
19. Ha, S.H., Liang, Y.S., Jung, H., Ahn, M.J., Suh, S.C., Kweon, S.J., Kim, D.H., Kim, Y.M., Kim, J.K., Application of two bicistronic systems involving 2A and IRES sequences to the biosynthesis of carotenoids in rice endosperm. Plant Biotechnol J 8 (2010), 928–938.
20. Van Moerkercke, A., Steensma, P., Schweizer, F., Pollier, J., Gariboldi, I., Payne, R., Bossche, R.V., Miettinen, K., Espoz, J., Purnama, P.C., et al. The bHLH transcription factor BIS1 controls the iridoid branch of the monoterpenoid indole alkaloid pathway in Catharanthus roseus. Proc Natl Acad Sci U S A 112 (2015), 8130–8135.
21. Paul, P., Singh, S.K., Patra, B., Sui, X.Y., Pattanaik, S., Yuan, L., A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus. New Phytol 213 (2017), 1107–1123.
22. Li, L., Paolillo, D.J., Parthasarathy, M.V., DiMuzio, E.M., Garvin, D.F., A novel gene mutation that confers abnormal patterns of beta-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26 (2001), 59–67.
23. Zhou, X.J., Welsch, R., Yang, Y., Alvarez, D., Riediger, M., Yuan, H., Fish, T., Liu, J.P., Thannhauser, T.W., Li, L., Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci U S A 112 (2015), 3558–3563.
24. Chayut, N., Yuan, H., Ohali, S., Meir, A., Sa'ar, U., Tzuri, G., Zheng, Y., Mazourek, M., Gepstein, S., Zhou, X.J., et al. Distinct mechanisms of the ORANGE protein in controlling carotenoid flux. Plant Physiol 173 (2017), 376–389.
25. Bock, R., Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Merchant, S.S., (eds.) Annual Review of Plant Biology, Vol 66. Annual Reviews, 2015, 211–241.
26. Stegemann, S., Bock, R., Exchange of genetic material between cells in plant tissue grafts. Science 324 (2009), 649–651.
27. Stegemann, S., Keuthe, M., Greiner, S., Bock, R., Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci U S A 109 (2012), 2434–2438.
28. Fuentes, I., Stegemann, S., Golczyk, H., Karcher, D., Bock, R., Horizontal genome transfer as an asexual path to the formation of new species. Nature, 511, 2014 232-+ The report describes a new plant breeding technique that can be exploited to generate new plant species that could contain novel compounds or different abundances. In combination with Stegemann et al., 2012 the potential exists to transfer transformed plastid genomes into crops plants where plastid transformation is not routine.
29. Fuentes, P., Zhou, F., Erban, A., Karcher, D., Kopka, J., Bock, R., A new synthetic biology approach allows transfer of an entire metabolic pathway from a medicinal plant to a biomass crop. Elife, 5, 2016, 26 The first report of COSTEREL a combinatorial super transformation approach that combines both nuclear and plastomic transformation for complex synthetic biology approaches. In this case artemisinin formation in tobacco was used to illustrate the technique.
30. Enfissi, E.M., Barneche, F., Ahmed, I., Lichtle, C., Gerrish, C., McQuinn, R.P., Giovannoni, J.J., Lopez-Juez, E., Bowler, C., Bramley, P.M., et al. Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22 (2010), 1190–1215.
31. Yen, H.C., Shelton, B.A., Howard, L.R., Lee, S., Vrebalov, J., Giovannoni, J.J., The tomato high-pigment (hp) locus maps to chromosome 2 and influences plastome copy number and fruit quality. Theor Appl Genet 95 (1997), 1069–1079.
32. Galpaz, N., Wang, Q., Menda, N., Zamir, D., Hirschberg, J., Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53 (2008), 717–730.
33. Simkin, A.J., Gaffe, J., Alcaraz, J.P., Carde, J.P., Bramley, P.M., Fraser, P.D., Kuntz, M., Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68 (2007), 1545–1556.
34. Fraser, P.D., Enfissi, E.M., Halket, J.M., Truesdale, M.R., Yu, D., Gerrish, C., Bramley, P.M., Manipulation of phytoene levels in tomato fruit: effects on isoprenoids, plastids, and intermediary metabolism. Plant Cell 19 (2007), 3194–3211.
35. Maass, D., Arango, J., Wust, F., Beyer, P., Welsch, R., Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS ONE, 4, 2009, 12.
36. Nogueira, M., Mora, L., Enfissi, E.M., Bramley, P.M., Fraser, P.D., Subchromoplast sequestration of carotenoids affects regulatory mechanisms in tomato lines expressing different carotenoid gene combinations. Plant Cell 25 (2013), 4560–4579.
37. Bai, C., Capell, T., Berman, J., Medina, V., Sandmann, G., Christou, P., Zhu, C.F., Bottlenecks in carotenoid biosynthesis and accumulation in rice endosperm are influenced by the precursor-product balance. Plant Biotechnol J 14 (2016), 195–205.
38. Rivas, F., Parra, A., Martinez, A., Garcia-Granados, A., Enzymatic glycosylation of terpenoids. Phytochem Rev 12 (2013), 327–339.
39. Ariizumi, T., Kishimoto, S., Kakami, R., Maoka, T., Hirakawa, H., Suzuki, Y., Ozeki, Y., Shirasawa, K., Bernillon, S., Okabe, Y., et al. Identification of the carotenoid modifying gene PALE YELLOW PETAL 1 as an essential factor in xanthophyll esterification and yellow flower pigmentation in tomato (Solanum lycopersicum). Plant J 79 (2014), 453–465.
40. Che, P., Zhao, Z.Y., Glassman, K., Dolde, D., Hu, T.X., Jones, T.J., Obukosia, S., Wambugu, F., Albertsen, M.C., Elevated vitamin E content improves all-trans beta-carotene accumulation and stability in biofortified sorghum. Proc Natl Acad Sci U S A 113 (2016), 11040–11045 One of the first examples illustrating the importance of reducing non-enzymatic degradation as a means of optimising nutritional carotenoids.
41. Gonzalez-Jorge, S., Ha, S.H., Magallanes-Lundback, M., Gilliland, L.U., Zhou, A.L., Lipka, A.E., Nguyen, Y.N., Angelovici, R., Lin, H.N., Cepela, J., et al. CAROTENOID CLEAVAGE DIOXYGENASE4 is a negative regulator of beta-carotene content in Arabidopsis seeds. Plant Cell 25 (2013), 4812–4826.
42. Stacey, M.G., Cahoon, R.E., Nguyen, H.T., Cui, Y.Y., Sato, S., Nguyen, C.T., Phoka, N., Clark, K.M., Liang, Y., Forrester, J., et al. Identification of homogentisate dioxygenase as a target for Vitamin E biofortification in oilseeds. Plant Physiol 172 (2016), 1506–1518.
43. Baltes, N.J., Voytas, D.F., Enabling plant synthetic biology through genome engineering. Trends Biotechnol 33 (2015), 120–131.
44. Doudna, J.A., Charpentier, E., The new frontier of genome engineering with CRISPR-Cas9. Science, 346, 2014 1077-+.
45. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., Patron, N.J., Nekrasov, V., Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32 (2015), 76–84.
46. Puchta, H., Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr Opin Plant Biol 36 (2017), 1–8.
47. Liu, D., Hu, R., Palla, K.J., Tuskan, G.A., Yang, X., Advances and perspectives on the use of CRISPR/Cas9 systems in plant genomics research. Curr Opin Plant Biol 30 (2016), 70–77.
48. Schiml, S., Puchta, H., Revolutionizing plant biology: multiple ways of genome engineering by CRISPR/Cas. Plant Methods, 12, 2016, 8.
49. Schaart, J.G., van de Wiel, C.C., Lotz, L.A., Smulders, M.J., Opportunities for products of new plant breeding techniques. Trends Plant Sci 21 (2016), 438–449.
50. Nekrasov, V., Wang, C., Win, J., Lanz, C., Weigel, D., Kamoun, S., Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Sci Rep, 7, 2017, 482.
51. Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., Teramura, H., Yamamoto, T., Komatsu, H., Miura, K., et al. Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat Biotechnol 35 (2017), 441–443.
52. Wang, Y.P., Cheng, X., Shan, Q.W., Zhang, Y., Liu, J.X., Gao, C.X., Qiu, J.L., Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32 (2014), 947–951.
53. Zhou, J.H., Peng, Z., Long, J.Y., Sosso, D., Liu, B., Eom, J.S., Huang, S., Liu, S.Z., Cruz, C.V., Frommer, W.B., et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82 (2015), 632–643.
54. Uluisik, S., Chapman, N.H., Smith, R., Poole, M., Adams, G., Gillis, R.B., Besong, T.M., Sheldon, J., Stiegelmeyer, S., Perez, L., et al. Genetic improvement of tomato by targeted control of fruit softening. Nat Biotechnol 34 (2016), 950–952 Highlights the potential of natural variation and emerging technologies such as CRISPR-Cas to deliver consumer output traits into commerical practice.
55. The National Academies of Sciences, Engineering and Medicine, Genetically Engineered Crops: Experiences and Prospects. 2016 www.nas-site.org/ge-crops.
56. Eisenstein, M., Against the grain. Nature 514 (2014), S55–S57.
57. Turck, D., Bresson, J.L., Burlingame, B., Dean, T., Fairweather-Tait, S., Heinonen, M., Ildico Hirsch-Ernst, K., Mangelsdorf, I., McArdle, H.J., Naska, A., Neuhauser-Berthold, M., Nowicka, G., Pentieva, K., Sanz, Y., Sjodin, A., Stern, M., Tome, D., Van Loveren, H., Vinceti, M., Willatts, P., Martin, A., Joseph Strain, J., Heng, L., Valtuena-Martınez, S., Sian, A., Scientific and technical guidance for the preparation and presentation of a health claim application. EFSA J, 15, 2017, 4680.
58. Ausich, R.L., Commercial opportunities for carotenoid production by biotechnology. Pure Appl Chem 69 (1997), 2169–2173.