The Multiplanetary Future of Plant Synthetic Biology
Abstract
:1. Taking Full Advantage of Plants on Extraterrestrial Human Outposts
2. Refactoring Plants for Enhanced Performance on Mars
2.1. Enhancing Photosynthesis and Photoprotection
2.2. Improving Drought and Cold Tolerance
2.3. Engineering High Yield and Functional Food
3. Tailoring Microorganisms to Complement and Facilitate Plant Life on Mars
3.1. Conditioning Martian Soil for Plant Growth Using Microbes
3.2. Microbes for Metabolite and Protein Production from Plant Material
4. A Roadmap for Research on Adapting Life to Mars
5. From Earth to Mars and Back to Earth
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Cichan, T.; Bailey, S.A.; Antonelli, T.; Jolly, S.D.; Chambers, R.P.; Clark, B.; Ramm, S.J. Mars Base Camp: An architecture for sending humans to Mars. New Space 2017, 5, 203–218. [Google Scholar] [CrossRef]
- Vernikos, J.; Walter, N.; Worms, J.C.; Blanc, S. THESEUS: The European research priorities for human exploration of space. NPJ Microgravity 2016, 2, 16034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Musk, E. Making humans a multi-planetary species. New Space 2017, 5, 46–61. [Google Scholar] [CrossRef]
- Fu, Y.; Li, L.; Xie, B.; Dong, C.; Wang, M.; Jia, B.; Shao, L.; Dong, Y.; Deng, S.; Liu, H.; et al. How to establish a Bioregenerative Life Support System for long-term crewed missions to the Moon or Mars. Astrobiology 2016, 16, 925–936. [Google Scholar] [CrossRef] [PubMed]
- Wolff, S.A.; Coelho, L.H.; Karoliussen, I.; Jost, A.I. Effects of the extraterrestrial environment on plants: Recommendations for future space experiments for the MELiSSA higher plant compartment. Life 2014, 4, 189–204. [Google Scholar] [CrossRef] [PubMed]
- Wheeler, R.M. Agriculture for space: People and places paving the way. Open Agric. 2017, 2, 14–32. [Google Scholar] [CrossRef]
- Zabel, P.; Bamsey, M.; Schubert, D.; Tajmar, M. Review and analysis of over 40 years of space plant growth systems. Life Sci. Space Res. 2016, 10, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Menezes, A.A.; Cumbers, J.; Hogan, J.A.; Arkin, A.P. Towards synthetic biological approaches to resource utilization on space missions. J. R. Soc. Interface 2015, 12, 20140715. [Google Scholar] [CrossRef] [PubMed]
- Verseux, C.; Baque, M.; Lehto, K.; de Vera, J.P.P.; Rothschild, L.J.; Billi, D. Sustainable life support on Mars—The potential roles of cyanobacteria. Int. J. Astrobiol. 2016, 15, 65–92. [Google Scholar] [CrossRef]
- Way, J.C.; Silver, P.A.; Howard, R.J. Sun-driven microbial synthesis of chemicals in space. Int. J. Astrobiol. 2011, 10, 359–364. [Google Scholar] [CrossRef]
- Rothschild, L.J. Synthetic biology meets bioprinting: Enabling technologies for humans on Mars (and Earth). Biochem. Soc. Trans. 2016, 44, 1158–1164. [Google Scholar] [CrossRef] [PubMed]
- Menezes, A.A.; Montague, M.G.; Cumbers, J.; Hogan, J.A.; Arkin, A.P. Grand challenges in space synthetic biology. J. R. Soc. Interface 2015, 12, 20150803. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Perchonok, M.H.; Cooper, M.R.; Catauro, P.M. Mission to Mars: Food production and processing for the final frontier. Annu. Rev. Food Sci. Technol. 2012, 3, 311–330. [Google Scholar] [CrossRef] [PubMed]
- Hublitz, I.; Henninger, D.L.; Drake, B.G.; Eckart, P. Engineering concepts for inflatable Mars surface greenhouses. Adv. Space Res. 2004, 34, 1546–1551. [Google Scholar] [CrossRef] [PubMed]
- Furfaro, R.; Gellenbeck, S.; Giacomelli, G.; Sadler, P. Mars-Lunar Greehouse (MLGH) prototype for bioregenerative life support systems: Current status and future efforts. In Proceedings of the 47th International Conference on Environmental Systems, Charleston, SC, USA, 16–20 July 2017. [Google Scholar]
- Kiss, J.Z. Plant biology in reduced gravity on the Moon and Mars. Plant Biol. 2014, 16, 12–17. [Google Scholar] [CrossRef] [PubMed]
- Blankenship, R.E.; Tiede, D.M.; Barber, J.; Brudvig, G.W.; Fleming, G.; Ghirardi, M.; Gunner, M.R.; Junge, W.; Kramer, D.M.; Melis, A.; et al. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 2011, 332, 805–809. [Google Scholar] [CrossRef] [PubMed]
- Dutta, P.K.; Lin, S.; Loskutov, A.; Levenberg, S.; Jun, D.; Saer, R.; Beatty, J.T.; Liu, Y.; Yan, H.; Woodbury, N.W. Reengineering the optical absorption cross-section of photosynthetic reaction centers. J. Am. Chem. Soc. 2014, 136, 4599–4604. [Google Scholar] [CrossRef] [PubMed]
- Grayson, K.J.; Faries, K.M.; Huang, X.; Qian, P.; Dilbeck, P.; Martin, E.C.; Hitchcock, A.; Vasilev, C.; Yuen, J.M.; Niedzwiedzki, D.M.; et al. Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre. Nat. Commun. 2017, 8, 13972. [Google Scholar] [CrossRef] [PubMed]
- Ort, D.R.; Merchant, S.S.; Alric, J.; Barkan, A.; Blankenship, R.E.; Bock, R.; Croce, R.; Hanson, M.R.; Hibberd, J.M.; Long, S.P.; et al. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA 2015, 112, 8529–8536. [Google Scholar] [CrossRef] [PubMed]
- Cockell, C.S.; Catling, D.C.; Davis, W.L.; Snook, K.; Kepner, R.L.; Lee, P.; McKay, C.P. The ultraviolet environment of Mars: Biological implications past, present, and future. Icarus 2000, 146, 343–359. [Google Scholar] [CrossRef] [PubMed]
- Tohge, T.; Fernie, A.R. Leveraging natural variance towards enhanced understanding of phytochemical sunscreens. Trends Plant Sci. 2017, 22, 308–315. [Google Scholar] [CrossRef] [PubMed]
- Llorente, B. Regulation of carotenoid biosynthesis in photosynthetic organs. Subcell. Biochem. 2016, 79, 141–160. [Google Scholar] [PubMed]
- Kromdijk, J.; Glowacka, K.; Leonelli, L.; Gabilly, S.T.; Iwai, M.; Niyogi, K.K.; Long, S.P. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 2016, 354, 857–861. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Erb, T.J.; Zarzycki, J. Biochemical and synthetic biology approaches to improve photosynthetic CO2-fixation. Curr. Opin. Chem. Biol. 2016, 34, 72–79. [Google Scholar] [CrossRef] [PubMed]
- Giessen, T.W.; Silver, P.A. Engineering carbon fixation with artificial protein organelles. Curr. Opin. Biotechnol. 2017, 46, 42–50. [Google Scholar] [CrossRef] [PubMed]
- Liu, D.; Ramya, R.C.S.; Mueller-Cajar, O. Surveying the expanding prokaryotic Rubisco multiverse. FEMS Microbiol. Lett. 2017, 364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xin, C.P.; Tholen, D.; Devloo, V.; Zhu, X.G. The benefits of photorespiratory bypasses: How can they work? Plant Physiol. 2015, 167, 574–585. [Google Scholar] [CrossRef] [PubMed]
- Erb, T.J.; Jones, P.R.; Bar-Even, A. Synthetic metabolism: Metabolic engineering meets enzyme design. Curr. Opin. Chem. Biol. 2017, 37, 56–62. [Google Scholar] [CrossRef] [PubMed]
- Schwander, T.; Schada von Borzyskowski, L.; Burgener, S.; Cortina, N.S.; Erb, T.J. A synthetic pathway for the fixation of carbon dioxide in vitro. Science 2016, 354, 900–904. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ralphs, M.; Franz, B.; Baker, T.; Howe, S. Water extraction on Mars for an expanding human colony. Life Sci. Space Res. 2015, 7, 57–60. [Google Scholar] [CrossRef] [PubMed]
- Dundas, C.M.; Bramson, A.M.; Ojha, L.; Wray, J.J.; Mellon, M.T.; Byrne, S.; McEwen, A.S.; Putzig, N.E.; Viola, D.; Sutton, S.; et al. Exposed subsurface ice sheets in the Martian mid-latitudes. Science 2018, 359, 199–201. [Google Scholar] [CrossRef] [PubMed]
- Barbosa, G.L.; Gadelha, F.D.; Kublik, N.; Proctor, A.; Reichelm, L.; Weissinger, E.; Wohlleb, G.M.; Halden, R.U. Comparison of land, water, and energy requirements of lettuce grown using hydroponic vs. conventional agricultural methods. Int. J. Environ. Res. Public Health 2015, 12, 6879–6891. [Google Scholar] [CrossRef] [PubMed]
- Glowacka, K.; Kromdijk, J.; Kucera, K.; Xie, J.; Cavanagh, A.P.; Leonelli, L.; Leakey, A.D.B.; Ort, D.R.; Niyogi, K.K.; Long, S.P. Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop. Nat. Commun. 2018, 9, 868. [Google Scholar] [CrossRef] [PubMed]
- Cabello, J.V.; Lodeyro, A.F.; Zurbriggen, M.D. Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr. Opin. Biotechnol. 2014, 26, 62–70. [Google Scholar] [CrossRef] [PubMed]
- Paul, M.J.; Nuccio, M.L.; Basu, S.S. Are GM crops for yield and resilience possible? Trends Plant Sci. 2018, 23, 10–16. [Google Scholar] [CrossRef] [PubMed]
- Albert, R.; Acharya, B.R.; Jeon, B.W.; Zanudo, J.G.T.; Zhu, M.; Osman, K.; Assmann, S.M. A new discrete dynamic model of ABA-induced stomatal closure predicts key feedback loops. PLoS Biol. 2017, 15, e2003451. [Google Scholar] [CrossRef] [PubMed]
- Yang, X.; Cushman, J.C.; Borland, A.M.; Edwards, E.J.; Wullschleger, S.D.; Tuskan, G.A.; Owen, N.A.; Griffiths, H.; Smith, J.A.; De Paoli, H.C.; et al. A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytol. 2015, 207, 491–504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Costa, M.C.D.; Farrant, J.M.; Oliver, M.J.; Ligterink, W.; Buitink, J.; Hilhorst, H.M.W. Key genes involved in desiccation tolerance and dormancy across life forms. Plant Sci. 2016, 251, 162–168. [Google Scholar] [CrossRef] [PubMed]
- Giarola, V.; Hou, Q.; Bartels, D. Angiosperm plant desiccation tolerance: Hints from transcriptomics and genome sequencing. Trends Plant Sci. 2017, 22, 705–717. [Google Scholar] [CrossRef] [PubMed]
- Mazin, P.V.; Shagimardanova, E.; Kozlova, O.; Cherkasov, A.; Sutormin, R.; Stepanova, V.V.; Stupnikov, A.; Logacheva, M.; Penin, A.; Sogame, Y.; et al. Cooption of heat shock regulatory system for anhydrobiosis in the sleeping chironomid Polypedilum vanderplanki. Proc. Natl. Acad. Sci. USA 2018, 115, E2477–E2486. [Google Scholar] [CrossRef] [PubMed]
- Yoshida, Y.; Koutsovoulos, G.; Laetsch, D.R.; Stevens, L.; Kumar, S.; Horikawa, D.D.; Ishino, K.; Komine, S.; Kunieda, T.; Tomita, M.; et al. Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol. 2017, 15, e2002266. [Google Scholar] [CrossRef] [PubMed]
- Schofield, J.T.; Barnes, J.R.; Crisp, D.; Haberle, R.M.; Larsen, S.; Magalhaes, J.A.; Murphy, J.R.; Seiff, A.; Wilson, G. The Mars Pathfinder atmospheric structure investigation/meteorology (ASI/MET) experiment. Science 1997, 278, 1752–1758. [Google Scholar] [CrossRef] [PubMed]
- Bredow, M.; Walker, V.K. Ice-binding proteins in plants. Front. Plant Sci. 2017, 8, 2153. [Google Scholar] [CrossRef] [PubMed]
- Megha, S.; Basu, U.; Kay, N.N.V. Metabolic engineering of cold tolerance in plants. Biocatal. Agric. Biotechnol. 2014, 3, 88–95. [Google Scholar] [CrossRef]
- Krasensky, J.; Jonak, C. Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot. 2012, 63, 1593–1608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harmer, S.L. The circadian system in higher plants. Annu. Rev. Plant Biol. 2009, 60, 357–377. [Google Scholar] [CrossRef] [PubMed]
- Dodd, A.N.; Salathia, N.; Hall, A.; Kevei, E.; Toth, R.; Nagy, F.; Hibberd, J.M.; Millar, A.J.; Webb, A.A. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 2005, 309, 630–633. [Google Scholar] [CrossRef] [PubMed]
- Kyriacou, M.C.; De Pascale, S.; Kyratzis, A.; Rouphael, Y. Microgreens as a component of space life support systems: A cornucopia of functional food. Front. Plant Sci. 2017, 8, 1587. [Google Scholar] [CrossRef] [PubMed]
- Boccalandro, H.E.; Ploschuk, E.L.; Yanovsky, M.J.; Sanchez, R.A.; Gatz, C.; Casal, J.J. Increased phytochrome B alleviates density effects on tuber yield of field potato crops. Plant Physiol. 2003, 133, 1539–1546. [Google Scholar] [CrossRef] [PubMed]
- Lopez Pereira, M.; Sadras, V.O.; Batista, W.; Casal, J.J.; Hall, A.J. Light-mediated self-organization of sunflower stands increases oil yield in the field. Proc. Natl. Acad. Sci. USA 2017, 114, 7975–7980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martinez-Garcia, J.F.; Gallemi, M.; Molina-Contreras, M.J.; Llorente, B.; Bevilaqua, M.R.; Quail, P.H. The shade avoidance syndrome in Arabidopsis: The antagonistic role of phytochrome a and B differentiates vegetation proximity and canopy shade. PLoS ONE 2014, 9, e109275. [Google Scholar] [CrossRef] [PubMed]
- Ganesan, M.; Lee, H.Y.; Kim, J.I.; Song, P.S. Development of transgenic crops based on photo-biotechnology. Plant Cell Environ. 2017, 40, 2469–2486. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez-Leal, D.; Lemmon, Z.H.; Man, J.; Bartlett, M.E.; Lippman, Z.B. Engineering quantitative trait variation for crop improvement by genome editing. Cell 2017, 171, 470–480. [Google Scholar] [CrossRef] [PubMed]
- Soyk, S.; Lemmon, Z.H.; Oved, M.; Fisher, J.; Liberatore, K.L.; Park, S.J.; Goren, A.; Jiang, K.; Ramos, A.; van der Knaap, E.; et al. Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell 2017, 169, 1142–1155. [Google Scholar] [CrossRef] [PubMed]
- Soyk, S.; Muller, N.A.; Park, S.J.; Schmalenbach, I.; Jiang, K.; Hayama, R.; Zhang, L.; Van Eck, J.; Jimenez-Gomez, J.M.; Lippman, Z.B. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat. Genet. 2017, 49, 162–168. [Google Scholar] [CrossRef] [PubMed]
- Khan, M.A.; Gemenet, D.C.; Villordon, A. Root system architecture and abiotic stress tolerance: Current knowledge in root and tuber crops. Front. Plant Sci. 2016, 7, 1584. [Google Scholar] [CrossRef] [PubMed]
- Kong, X.; Zhang, M.; De Smet, I.; Ding, Z. Designer crops: Optimal root system architecture for nutrient acquisition. Trends Biotechnol. 2014, 32, 597–598. [Google Scholar] [CrossRef] [PubMed]
- Heppell, J.; Talboys, P.; Payvandi, S.; Zygalakis, K.C.; Fliege, J.; Withers, P.J.; Jones, D.L.; Roose, T. How changing root system architecture can help tackle a reduction in soil phosphate (P) levels for better plant P acquisition. Plant Cell Environ. 2015, 38, 118–128. [Google Scholar] [CrossRef] [PubMed]
- Pasek, M. Early Mars: Without phosphate limits. Nat. Geosci. 2013, 6, 806–807. [Google Scholar] [CrossRef]
- Adcock, C.T.; Hausrath, E.M.; Forster, P.M. Readily available phosphate from minerals in early aqueous environments on Mars. Nat. Geosci. 2013, 6, 824–827. [Google Scholar] [CrossRef]
- Stern, J.C.; Sutter, B.; Freissinet, C.; Navarro-Gonzalez, R.; McKay, C.P.; Archer, P.D., Jr.; Buch, A.; Brunner, A.E.; Coll, P.; Eigenbrode, J.L.; et al. Evidence for indigenous nitrogen in sedimentary and aeolian deposits from the Curiosity rover investigations at Gale crater, Mars. Proc. Natl. Acad. Sci. USA 2015, 112, 4245–4250. [Google Scholar] [CrossRef] [PubMed]
- Allen, R.S.; Tilbrook, K.; Warden, A.C.; Campbell, P.C.; Rolland, V.; Singh, S.P.; Wood, C.C. Expression of 16 nitrogenase proteins within the plant mitochondrial matrix. Front. Plant Sci. 2017, 8, 287. [Google Scholar] [CrossRef] [PubMed]
- Buren, S.; Young, E.M.; Sweeny, E.A.; Lopez-Torrejon, G.; Veldhuizen, M.; Voigt, C.A.; Rubio, L.M. Formation of nitrogenase NifDK tetramers in the mitochondria of Saccharomyces cerevisiae. ACS Synth. Biol. 2017, 6, 1043–1055. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Xie, X.; Yang, M.; Dixon, R.; Wang, Y.P. Modular electron-transport chains from eukaryotic organelles function to support nitrogenase activity. Proc. Natl. Acad. Sci. USA 2017, 114, E2460–E2465. [Google Scholar] [CrossRef] [PubMed]
- Buren, S.; Rubio, L.M. State of the art in eukaryotic nitrogenase engineering. FEMS Microbiol. Lett. 2018, 365. [Google Scholar] [CrossRef] [PubMed]
- Li, X.X.; Liu, Q.; Liu, X.M.; Shi, H.W.; Chen, S.F. Using synthetic biology to increase nitrogenase activity. Microb. Cell Fact. 2016, 15, 43. [Google Scholar] [CrossRef] [PubMed]
- Temme, K.; Zhao, D.; Voigt, C.A. Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. Proc. Natl. Acad. Sci. USA 2012, 109, 7085–7090. [Google Scholar] [CrossRef] [PubMed]
- Rogers, C.; Oldroyd, G.E. Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. J. Exp. Bot. 2014, 65, 1939–1946. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geddes, B.A.; Ryu, M.H.; Mus, F.; Costas, A.G.; Peters, J.W.; Voigt, C.A.; Poole, P. Use of plant colonizing bacteria as chassis for transfer of N2-fixation to cereals. Curr. Opin. Biotechnol. 2015, 32, 216–222. [Google Scholar] [CrossRef] [PubMed]
- Mus, F.; Crook, M.B.; Garcia, K.; Garcia Costas, A.; Geddes, B.A.; Kouri, E.D.; Paramasivan, P.; Ryu, M.H.; Oldroyd, G.E.D.; Poole, P.S.; et al. Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl. Environ. Microbiol. 2016, 82, 3698–3710. [Google Scholar] [CrossRef] [PubMed]
- Bergouignan, A.; Stein, T.P.; Habold, C.; Coxam, V.; O’ Gorman, D.; Blanc, S. Towards human exploration of space: The THESEUS review series on nutrition and metabolism research priorities. NPJ Microgravity 2016, 2, 16029. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rodriguez-Concepcion, M.; Avalos, J.; Bonet, M.L.; Boronat, A.; Gomez-Gomez, L.; Hornero-Mendez, D.; Limon, M.C.; Melendez-Martinez, A.J.; Olmedilla-Alonso, B.; Palou, A.; et al. A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health. Prog. Lipid Res. 2018, 70, 62–93. [Google Scholar] [CrossRef] [PubMed]
- Cohu, C.M.; Lombardi, E.; Adams, W.W.; Demmig-Adams, B. Increased nutritional quality of plants for long-duration spaceflight missions through choice of plant variety and manipulation of growth conditions. Acta Astronaut. 2014, 94, 799–806. [Google Scholar] [CrossRef]
- Llorente, B.; D’Andrea, L.; Rodriguez-Concepcion, M. Evolutionary recycling of light signaling components in fleshy fruits: New insights on the role of pigments to monitor ripening. Front. Plant Sci. 2016, 7, 263. [Google Scholar] [CrossRef] [PubMed]
- Llorente, B.; Martinez-Garcia, J.F.; Stange, C.; Rodriguez-Concepcion, M. Illuminating colors: Regulation of carotenoid biosynthesis and accumulation by light. Curr. Opin. Plant Biol. 2017, 37, 49–55. [Google Scholar] [CrossRef] [PubMed]
- Sun, T.; Yuan, H.; Cao, H.; Yazdani, M.; Tadmor, Y.; Li, L. Carotenoid metabolism in plants: The role of plastids. Mol. Plant 2018, 11, 58–74. [Google Scholar] [CrossRef] [PubMed]
- D’Andrea, L.; Simon-Moya, M.; Llorente, B.; Llamas, E.; Marro, M.; Loza-Alvarez, P.; Li, L.; Rodriguez-Concepcion, M. Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening. J. Exp. Bot. 2018, 69, 1557–1568. [Google Scholar] [CrossRef] [PubMed]
- Llorente, B.; D’Andrea, L.; Ruiz-Sola, M.A.; Botterweg, E.; Pulido, P.; Andilla, J.; Loza-Alvarez, P.; Rodriguez-Concepcion, M. Tomato fruit carotenoid biosynthesis is adjusted to actual ripening progression by a light-dependent mechanism. Plant J. 2016, 85, 107–119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Majer, E.; Llorente, B.; Rodriguez-Concepcion, M.; Daros, J.A. Rewiring carotenoid biosynthesis in plants using a viral vector. Sci. Rep. 2017, 7, 41645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, X.; Welsch, R.; Yang, Y.; Alvarez, D.; Riediger, M.; Yuan, H.; Fish, T.; Liu, J.; Thannhauser, T.W.; Li, L. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc. Natl. Acad. Sci. USA 2015, 112, 3558–3563. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.; Butelli, E.; Alseekh, S.; Tohge, T.; Rallapalli, G.; Luo, J.; Kawar, P.G.; Hill, L.; Santino, A.; Fernie, A.R.; et al. Multi-level engineering facilitates the production of phenylpropanoid compounds in tomato. Nat. Commun. 2015, 6, 8635. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Naqvi, S.; Zhu, C.; Farre, G.; Ramessar, K.; Bassie, L.; Breitenbach, J.; Perez Conesa, D.; Ros, G.; Sandmann, G.; Capell, T.; et al. Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc. Natl. Acad. Sci. USA 2009, 106, 7762–7767. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Butelli, E.; Titta, L.; Giorgio, M.; Mock, H.P.; Matros, A.; Peterek, S.; Schijlen, E.G.; Hall, R.D.; Bovy, A.G.; Luo, J.; et al. Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors. Nat. Biotechnol. 2008, 26, 1301–1308. [Google Scholar] [CrossRef] [PubMed]
- Llorente, B.; Alonso, G.D.; Bravo-Almonacid, F.; Rodriguez, V.; Lopez, M.G.; Carrari, F.; Torres, H.N.; Flawia, M.M. Safety assessment of nonbrowning potatoes: Opening the discussion about the relevance of substantial equivalence on next generation biotech crops. Plant Biotechnol. J. 2011, 9, 136–150. [Google Scholar] [CrossRef] [PubMed]
- Llorente, B.; Rodriguez, V.; Alonso, G.D.; Torres, H.N.; Flawia, M.M.; Bravo-Almonacid, F.F. Improvement of aroma in transgenic potato as a consequence of impairing tuber browning. PLoS ONE 2010, 5, e14030. [Google Scholar] [CrossRef] [PubMed]
- Morris, J.; Hawthorne, K.M.; Hotze, T.; Abrams, S.A.; Hirschi, K.D. Nutritional impact of elevated calcium transport activity in carrots. Proc. Natl. Acad. Sci. USA 2008, 105, 1431–1435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- 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. 2016, 34, 950–952. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chakraborty, S.; Chakraborty, N.; Agrawal, L.; Ghosh, S.; Narula, K.; Shekhar, S.; Naik, P.S.; Pande, P.C.; Chakrborti, S.K.; Datta, A. Next-generation protein-rich potato expressing the seed protein gene AmA1 is a result of proteome rebalancing in transgenic tuber. Proc. Natl. Acad. Sci. USA 2010, 107, 17533–17538. [Google Scholar] [CrossRef] [PubMed]
- Gallo, M.; Sayre, R. Removing allergens and reducing toxins from food crops. Curr. Opin. Biotechnol. 2009, 20, 191–196. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Butelli, E.; De Stefano, R.; Schoonbeek, H.J.; Magusin, A.; Pagliarani, C.; Wellner, N.; Hill, L.; Orzaez, D.; Granell, A.; et al. Anthocyanins double the shelf life of tomatoes by delaying overripening and reducing susceptibility to gray mold. Curr. Biol. 2013, 23, 1094–1100. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Leon, S.; Gil-Humanes, J.; Ozuna, C.V.; Gimenez, M.J.; Sousa, C.; Voytas, D.F.; Barro, F. Low-gluten, nontransgenic wheat engineered with CRISPR/Cas9. Plant Biotechnol. J. 2018, 16, 902–910. [Google Scholar] [CrossRef] [PubMed]
- Wamelink, G.W.; Frissel, J.Y.; Krijnen, W.H.; Verwoert, M.R.; Goedhart, P.W. Can plants grow on Mars and the moon: A growth experiment on Mars and moon soil simulants. PLoS ONE 2014, 9, e103138. [Google Scholar] [CrossRef] [PubMed]
- Maggi, F.; Pallud, C. Martian base agriculture: The effect of low gravity on water flow, nutrient cycles, and microbial biomass dynamics. Adv. Space Res. 2010, 46, 1257–1265. [Google Scholar] [CrossRef]
- Cary, S.C.; McDonald, I.R.; Barrett, J.E.; Cowan, D.A. On the rocks: The microbiology of Antarctic Dry Valley soils. Nat. Rev. Microbiol. 2010, 8, 129–138. [Google Scholar] [CrossRef] [PubMed]
- Marchant, D.R.; Head, J.W. Antarctic dry valleys: Microclimate zonation, variable geomorphic processes, and implications for assessing climate change on Mars. Icarus 2007, 192, 187–222. [Google Scholar] [CrossRef] [Green Version]
- Ji, M.; Greening, C.; Vanwonterghem, I.; Carere, C.R.; Bay, S.K.; Steen, J.A.; Montgomery, K.; Lines, T.; Beardall, J.; van Dorst, J.; et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 2017, 552, 400–403. [Google Scholar] [CrossRef] [PubMed]
- Hecht, M.H.; Kounaves, S.P.; Quinn, R.C.; West, S.J.; Young, S.M.M.; Ming, D.W.; Catling, D.C.; Clark, B.C.; Boynton, W.V.; Hoffman, J.; et al. Detection of perchlorate and the soluble chemistry of Martian soil at the Phoenix Lander site. Science 2009, 325, 64–67. [Google Scholar] [CrossRef] [PubMed]
- Bardiya, N.; Bae, J.H. Dissimilatory perchlorate reduction: A review. Microbiol. Res. 2011, 166, 237–254. [Google Scholar] [CrossRef] [PubMed]
- Davila, A.F.; Willson, D.; Coates, J.D.; Mckay, C.P. Perchlorate on Mars: A chemical hazard and a resource for humans. Int. J. Astrobiol. 2013, 12, 321–325. [Google Scholar] [CrossRef]
- Martin-Torres, F.J.; Zorzano, M.P.; Valentin-Serrano, P.; Harri, A.M.; Genzer, M.; Kemppinen, O.; Rivera-Valentin, E.G.; Jun, I.; Wray, J.; Madsen, M.B.; et al. Transient liquid water and water activity at Gale crater on Mars. Nat. Geosci. 2015, 8, 357–361. [Google Scholar] [CrossRef]
- Maestre, F.T.; Sole, R.; Singh, B.K. Microbial biotechnology as a tool to restore degraded drylands. Microb. Biotechnol. 2017, 10, 1250–1253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vickers, C.E.; Williams, T.C.; Peng, B.; Cherry, J. Recent advances in synthetic biology for engineering isoprenoid production in yeast. Curr. Opin. Chem. Biol. 2017, 40, 47–56. [Google Scholar] [CrossRef] [PubMed]
- Paddon, C.J.; Westfall, P.J.; Pitera, D.J.; Benjamin, K.; Fisher, K.; McPhee, D.; Leavell, M.D.; Tai, A.; Main, A.; Eng, D.; et al. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496, 528–532. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xia, X.X.; Qian, Z.G.; Ki, C.S.; Park, Y.H.; Kaplan, D.L.; Lee, S.Y. Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber. Proc. Natl. Acad. Sci. USA 2010, 107, 14059–14063. [Google Scholar] [CrossRef] [PubMed]
- Marcellin, E.; Behrendorff, J.B.; Nagaraju, S.; DeTissera, S.; Segovia, S.; Palfreyman, R.W.; Daniell, J.; Licona-Cassani, C.; Quek, L.E.; Speight, R.; et al. Low carbon fuels and commodity chemicals from waste gases- systematic approach to understand energy metabolism in a model acetogen. Green Chem. 2016, 18, 3020–3028. [Google Scholar] [CrossRef] [Green Version]
- Schuchmann, K.; Muller, V. Autotrophy at the thermodynamic limit of life: A model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 2014, 12, 809–821. [Google Scholar] [CrossRef] [PubMed]
- Valgepea, K.; Lemgruber, R.D.P.; Meaghan, K.; Palfreyman, R.W.; Abdalla, T.; Heijstra, B.D.; Behrendorff, J.B.; Tappel, R.; Kopke, M.; Simpson, S.D.; et al. Maintenance of ATP homeostasis triggers metabolic shifts in gas-fermenting acetogens. Cell Syst. 2017, 4, 505–515. [Google Scholar] [CrossRef] [PubMed]
- Du, B.; Daniels, V.R.; Vaksman, Z.; Boyd, J.L.; Crady, C.; Putcha, L. Evaluation of physical and chemical changes in pharmaceuticals flown on space missions. AAPS J. 2011, 13, 299–308. [Google Scholar] [CrossRef] [PubMed]
- Loh, H.S.; Green, B.J.; Yusibov, V. Using transgenic plants and modified plant viruses for the development of treatments for human diseases. Curr. Opin. Virol. 2017, 26, 81–89. [Google Scholar] [CrossRef] [PubMed]
- Zhang, B.; Shanmugaraj, B.; Daniell, H. Expression and functional evaluation of biopharmaceuticals made in plant chloroplasts. Curr. Opin. Chem. Biol. 2017, 38, 17–23. [Google Scholar] [CrossRef] [PubMed]
- Cao, J.C.; Perez-Pinera, P.; Lowenhaupt, K.; Wu, M.R.; Purcell, O.; de la Fuente-Nunez, C.; Lu, T.K. Versatile and on-demand biologics co-production in yeast. Nat. Commun. 2018, 9, 77. [Google Scholar] [CrossRef] [PubMed]
- Perez-Pinera, P.; Han, N.R.; Cleto, S.; Cao, J.C.; Purcell, O.; Shah, K.A.; Lee, K.; Ram, R.; Lu, T.K. Synthetic biology and microbioreactor platforms for programmable production of biologics at the point-of-care. Nat. Commun. 2016, 7, 12211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pardee, K.; Slomovic, S.; Nguyen, P.Q.; Lee, J.W.; Donghia, N.; Burrill, D.; Ferrante, T.; McSorley, F.R.; Furuta, Y.; Vernet, A.; et al. Portable, on-demand biomolecular manufacturing. Cell 2016, 167, 248–259. [Google Scholar] [CrossRef] [PubMed]
- Kwon, K.C.; Daniell, H. Low-cost oral delivery of protein drugs bioencapsulated in plant cells. Plant Biotechnol. J. 2015, 13, 1017–1022. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pena, D.A.; Gasser, B.; Zanghellini, J.; Steiger, M.G.; Mattanovich, D. Metabolic engineering of Pichia pastoris. Metab. Eng. 2018. [Google Scholar] [CrossRef]
- Chao, R.; Mishra, S.; Si, T.; Zhao, H. Engineering biological systems using automated biofoundries. Metab. Eng. 2017, 42, 98–108. [Google Scholar] [CrossRef] [PubMed]
- Shih, P.M.; Vuu, K.; Mansoori, N.; Ayad, L.; Louie, K.B.; Bowen, B.P.; Northen, T.R.; Loque, D. A robust gene-stacking method utilizing yeast assembly for plant synthetic biology. Nat. Commun. 2016, 7, 13215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, Y.; You, L.; Li, S.; Ma, M.; Wu, M.; Ma, L.; Bock, R.; Chang, L.; Zhang, J. In vivo assembly in Escherichia coli of transformation vectors for plastid genome engineering. Front. Plant Sci. 2017, 8, 1454. [Google Scholar] [CrossRef] [PubMed]
- Altpeter, F.; Springer, N.M.; Bartley, L.E.; Blechl, A.E.; Brutnell, T.P.; Citovsky, V.; Conrad, L.J.; Gelvin, S.B.; Jackson, D.P.; Kausch, A.P.; et al. Advancing crop transformation in the era of genome editing. Plant Cell 2016, 28, 1510–1520. [Google Scholar] [CrossRef] [PubMed]
- Dann, M.; Leister, D. Enhancing (crop) plant photosynthesis by introducing novel genetic diversity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2017, 372. [Google Scholar] [CrossRef] [PubMed]
- Nemhauser, J.L.; Torii, K.U. Plant synthetic biology for molecular engineering of signalling and development. Nat. Plants 2016, 2, 16010. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leister, D. Experimental evolution in photoautotrophic microorganisms as a means of enhancing chloroplast functions. Essays Biochem. 2018, 62, 77–84. [Google Scholar] [CrossRef] [PubMed]
- Boehm, C.R.; Pollak, B.; Purswani, N.; Patron, N.; Haseloff, J. Synthetic botany. Cold Spring Harb. Perspect. Biol. 2017, 9, a023887. [Google Scholar] [CrossRef] [PubMed]
- Reski, R.; Bae, H.; Simonsen, H.T. Physcomitrella patens, a versatile synthetic biology chassis. Plant Cell Rep. 2018. [Google Scholar] [CrossRef] [PubMed]
- Food and Agriculture Organization of the United Nations. The Future of Food and Agriculture—Trends and Challenges; Food and Agriculture Organization of the United Nations: Rome, Italy, 2017. [Google Scholar]
- Mueller, N.D.; Gerber, J.S.; Johnston, M.; Ray, D.K.; Ramankutty, N.; Foley, J.A. Closing yield gaps through nutrient and water management. Nature 2012, 490, 254–257. [Google Scholar] [CrossRef] [PubMed]
- Hunter, M.C.; Smith, R.G.; Schipanski, M.E.; Atwood, L.W.; Mortensen, D.A. Recalibrating targets for sustainable intensification. Bioscience 2017, 67, 386–391. [Google Scholar] [CrossRef]
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Llorente, B.; Williams, T.C.; Goold, H.D. The Multiplanetary Future of Plant Synthetic Biology. Genes 2018, 9, 348. https://doi.org/10.3390/genes9070348
Llorente B, Williams TC, Goold HD. The Multiplanetary Future of Plant Synthetic Biology. Genes. 2018; 9(7):348. https://doi.org/10.3390/genes9070348
Chicago/Turabian StyleLlorente, Briardo, Thomas C. Williams, and Hugh D. Goold. 2018. "The Multiplanetary Future of Plant Synthetic Biology" Genes 9, no. 7: 348. https://doi.org/10.3390/genes9070348
APA StyleLlorente, B., Williams, T. C., & Goold, H. D. (2018). The Multiplanetary Future of Plant Synthetic Biology. Genes, 9(7), 348. https://doi.org/10.3390/genes9070348