Synthetic botany

Cold Spring Harbor Perspectives in Biology

Volumn 9, Issue 7, 2017, Pages

  Boehm, Christian R ^a   Pollak, Bernardo ^a   Purswani, Nuri ^b   Patron, Nicola ^c   Haseloff, Jim ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b The IBM Place I ^*  (Singapore)

^c EARLHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOTANY; CHLOROPLAST; GENETIC ENGINEERING; GENETIC TRANSFORMATION; GENETICS; METABOLISM; PLANT; PROCEDURES; SYNTHETIC BIOLOGY; TRANSGENIC PLANT;

BOTANY; CHLOROPLASTS; GENETIC ENGINEERING; PLANTS; PLANTS, GENETICALLY MODIFIED; SYNTHETIC BIOLOGY; TRANSFORMATION, GENETIC;

EID: 85022083710     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a023887     Document Type: Article

References (184)

1. Adachi T, Takase H, Tomizawa K. 2007. Introduction of a 50 kbp DNA fragment into the plastid genome. Biosci Biotechnol Biochem 71: 2266–2273.
2. Annaluru N, Muller H, Mitchell LA, Ramalingam S, Strac-quadanio G, Richardson SM, Dymond JS, Kuang Z, Scheifele LZ, Cooper EM, et al. 2014. Total synthesis of a functional designer eukaryotic chromosome. Science 344: 55–58.
3. Anthony PC, Perez CF, Garcia-Garcia C, Block SM. 2012. Folding energy landscape of the thiamine pyrophosphate riboswitch aptamer. Proc Natl Acad Sci 109: 1485–1489.
4. Antunes MS, Morey KJ, Tewari-Singh N, Bowen TA, Smith JJ, Webb CT, Hellinga HW, Medford JI. 2009. Engineering key components in a synthetic eukaryotic signal transduction pathway. Mol Syst Biol 5: 270.
5. Antunes MS, Morey KJ, Smith JJ, Albrecht KD, Bowen TA, Zdunek JK, Troupe JF, Cuneo MJ, Webb CT, Hellinga HW, et al. 2011. Programmable ligand detection system in plants through a synthetic signal transduction pathway. PLoS ONE 6: e16292.
6. Aoyama T, Chua N-H. 1997. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11: 605–612.
7. Apel W, Bock R. 2009. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol 151: 59–66.
8. Bates SL, Zhao JZ, Roush RT, Shelton AM. 2005. Insect resistance management in GM crops: Past, present and future. Nat Biotechnol 23: 57–62.
9. Beadle G. 1939. Teosinte and the origin of maize. J Hered 30: 245–247.
10. Beemster GTS, Fiorani F, Inzé D. 2003. Cell cycle: The key to plant growth control? Trends Plant Sci 8: 154–158.
11. Beisel CL, Smolke CD. 2009. Design Principles for riboswitch function. PLoS Comput Biol 5: e1000363.
12. Bendich AJ. 1987. Why do chloroplasts and mitochondria contain so many copies of their genome? BioEssays 6: 279–282.
13. Besson S, Dumais J. 2011. Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci 108: 6294– 6299.
14. Binder A, Lambert J, Morbitzer R, Popp C, Ott T, Lahaye T, Parniske M. 2014. A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLoS ONE 9: e88218.
15. Blowers AD, Bogorad L, Shark KB, Sanford JC. 1989. Studies on Chlamydomonas chloroplast transformation: Foreign DNA can be stably maintained in the chromosome. Plant Cell 1: 123–132.
16. Bock R. 2015. Engineering plastid genomes: Methods, tools, and applications in basic research and biotechnology. Annu Rev Plant Biol 66: 211–241.
17. Boehm CR, Ueda M, Nishimura Y, Shikanai T, Haseloff J. 2016. A cyan fluorescent reporter expressed from the chloroplast genome of Marchantia polymorpha. Plant Cell Physiol 57: 291–299.
18. Bohmert-Tatarev K, McAvoy S, Daughtry S, Peoples OP, Snell KD. 2011. High levels of bioplastic are produced in fertile transplastomic tobacco plants engineered with a synthetic operon for the production of polyhydroxybu-tyrate. Plant Physiol 155: 1690–1708.
19. Bohn-Courseau I. 2010. Auxin: A major regulator of organogenesis. C R Biol 333: 290–296.
20. Bortesi L, Fischer R. 2015. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol Adv 33: 41–52.
21. Briggs G, Osmont K, Shindo C, Sibout R, Hardtke C. 2006. Unequal genetic redundancies in Arabidopsis—A neglected phenomenon? Trends Plant Sci 11: 492–498.
22. Brixey PJ, Guda C, Daniell H. 1997. The chloroplast psbA promoter is more efficient in Escherichia coli than the T7 promoter for hyperexpression of a foreign protein. Biotechnol Lett 19: 395–400.
23. Bruce W, Folkerts O, Garnaat C, Crasta O, Roth B, Bowen B. 2000. Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell 12: 65–80.
24. Brückner K, Schäfer P, Weber E, Grützner R, Marillonnet S, Tissier A. 2015. A library of synthetic transcription acti-vator-like effector-activated promoters for coordinated orthogonal gene expression in plants. Plant J 82: 707– 716.
25. Brunner S, Hurni S, Herren G, Kalinina O, von Burg S, Zeller SL, Schmid B, Winzeler M, Keller B. 2011. Transgenic Pm3b wheat lines show resistance to powdery mildew in the field. Plant Biotechnol J 9: 897–910.
26. Caddick MX, Greenland AJ, Jepson L, Krause KP, Qu N, Riddell KV, Salter MG, Schuch W, Sonnewald U, Tomsett AB. 1998. An ethanol inducible gene switch for plants used to manipulate carbon metabolism. Nat Biotechnol 16: 177–180.
27. Casini A, MacDonald JT, de Jonghe J, Christodoulou G, Freemont PS, Baldwin GS, Ellis T. 2014. One-pot DNA construction for synthetic biology: The modular overlap-directed assembly with linkers (MODAL) strategy. Nucleic Acids Res 42: e7.
28. Chakraborti D, Sarkar A, Mondal HA, Schuermann D, Hohn B, Sarmah BK, Das S. 2008. Cre/lox system to develop selectable marker free transgenic tobacco plants conferring resistance against sap sucking homopteran insect. Plant Cell Rep 27: 1623–1633.
29. Chiyoda S, Linley PJ, Yamato KT, Fukuzawa H, Yokota A, Kohchi T. 2007. Simple and efficient plastid transformation system for the liverwort Marchantia polymorpha L. suspension-culture cells. Transgenic Res 16: 41–49.
30. Chiyoda S, Yamato KT, Kohchi T. 2014. Plastid transformation of sporelings and suspension-cultured cells from the liverwort Marchantia polymorpha L. Methods Mol Biol 1132: 439–447.
31. Comai L, Facciotti D, Hiatt WR, Thompson G, Rose RE, Stalker DM. 1985. Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature 317: 741–744.
32. Cove D. 2005. The moss Physcomitrella patens. Annu Rev Genet 39: 339–358.
33. Craft J, Samalova M, Baroux C, Townley H, Martinez A, Jepson I, Tsiantis M, Moore I. 2005. New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41: 899–918.
34. Craig W, Lenzi P, Scotti N, De Palma M, Saggese P, Carbone V, McGrath Curran N, Magee AM, Medgyesy P, Kavanagh TA, et al. 2008. Transplastomic tobacco plants expressing a fatty acid desaturase gene exhibit altered fatty acid profiles and improved cold tolerance. Transgenic Res 17: 769–782.
35. Daniell H, Khan MS, Allison L. 2002. Milestones in chloroplast genetic engineering: An environmentally friendly era in biotechnology. Trends Plant Sci 7: 84–91.
36. D’Aoust MA, Lavoie PO, Couture MMJ, Trépanier S, Guay JM, Dargis M, Mongrand S, Landry N, Ward BJ, Vézina LP. 2008. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol J 6: 930–940.
37. Dean RE, Dahlberg JA, Hopkins MS, Mitchell SE, Kresovich S. 1999. Genetic redundancy and diversity among “Orange” accessions in the U.S. National Sorghum Collection as assessed with simple sequence repeat (SSR) markers. Crop Sci 39: 1215–1221.
38. De Cosa B, Moar W, Lee SB, Miller M, Daniell H. 2001. Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19: 71–74.
39. De Kok S, Stanton LH, Slaby T, Durot M, Holmes VF, Patel KG, Platt D, Shapland EB, Serber Z, Dean J, et al. 2014. Rapid and reliable DNA assembly via ligase cycling reaction. ACS Synth Biol 3: 97–106.
40. De Vos D, Dzhurakhalov A, Draelants D, Bogaerts I, Kalve S, Prinsen E, Vissenberg K, Vanroose W, Broeckhove J, Beemster GTS. 2012. Towards mechanistic models of plant organ growth. J Exp Bot 63: 3325–3337.
41. Doebley J. 2004. The genetics of maize evolution. Annu Rev Genet 38: 37–59.
42. Dupuy L, Mackenzie J, Haseloff J. 2010. Coordination of plant cell division and expansion in a simple morphogenetic system. Proc Natl Acad Sci 107: 2711–2716.
43. Ellis T, Wang X, Collins JJ. 2009. Diversity-based, model-guided construction of synthetic gene networks with predicted functions. Nat Biotechnol 27: 465–471.
44. Emadpour M, Karcher D, Bock R. 2015. Boosting riboswitch efficiency by RNA amplification. Nucleic Acids Res 43: e66.
45. Emami S, Yee MC, Dinneny JR. 2013. A robust family of Golden Gate Agrobacterium vectors for plant synthetic biology. Front Plant Sci 4: 339.
46. Endy D. 2005. Foundations for engineering biology. Nature 438: 449–453.
47. Engler C, Kandzia R, Marillonnet S. 2008. A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3: e3647.
48. Engler C, Gruetzner R, Kandzia R, Marillonnet S. 2009. Golden gate shuffling: A one-pot DNA shuffling method based on type IIs restriction enzymes. PLoS ONE 4: e5553.
49. Engler C, Youles M, Gruetzner R, Ehnert TM, Werner S, Jones JDG, Patron NJ, Marillonnet S. 2014. A golden gate modular cloning toolbox for plants. ACS Synth Biol 3: 839–843.
50. Federici F, Dupuy L, Laplaze L, Heisler M, Haseloff J. 2012. Integrated genetic and computation methods for in planta cytometry. Nat Methods 9: 483–485.
51. Fethe MH, Liu W, Burris JN, Millwood RJ, Mazarei M, Rudis MR, Yeaman DG, Dubosquielle M, Stewart CN. 2014. The performance of pathogenic bacterial phytosensing transgenic tobacco in the field. Plant Biotechnol J 12: 755–764.
52. Field B, Fiston-Lavier AS, Kemen A, Geisler K, Quesneville H, Osbourn AE. 2011. Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc Natl Acad Sci 108: 16116–16121.
53. Fitting H. 1935. Untersuchungen über die induktion der dorsiventralität bei den keimenden brutkörpern Marchantia und Lunularia. Jahrb Wiss Bot 82: 333.
54. Flavell R. 2009. Role of model plant species. Methods Mol Biol 513: 1–18.
55. Fromm M, Taylor LP, Walbot V. 1985. Expression of genes transferred into monocot and dicot plant cells by electroporation. Proc Natl Acad Sci 82: 5824–5828.
56. Gardner MJ, Baker AJ, Assie JM, Poethig RS, Haseloff JP, Webb AA. 2009. GAL4 GFP enhancer trap lines for anal- ysis of stomatal guard cell development and gene expression. J Exp Bot 60: 213–226.
57. Gelvin SB. 2003. Agrobacterium-mediated plant transformation: The biology behind the “Gene-Jockeying” Tool. Microbiol Mol Biol Rev 67: 16–37.
58. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, Smith HO. 2009. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343– 345.
59. Goffinet B, Shaw AJ. 2009. Bryophyte biology, 2nd ed. Cambridge University Press, Cambridge.
60. Goh HH, Sloan J, Dorca-Fornell C, Fleming A. 2012. Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol 159: 1759–1770.
61. Golds T, Maliga P, Koop HU. 1993. Stable plastid transformation in PEG-treated protoplasts of Nicotiana tabacum. Nat Biotechnol 11: 95–97.
62. Graham IA, Besser K, Blumer S, Branigan CA, Czechowski T, Elias L, Guterman I, Harvey D, Isaac PG, Khan AM, et al. 2010. The genetic map of Artemisia annua L. identifies loci affecting yield of the antimalarial drug artemisinin. Science 327: 328–331.
63. Green PB. 1980. Organogenesis—A biophysical view. Annu Rev Plant Physiol 31: 51–82.
64. Green CE, Phillips RL. 1975. PPlant regeneration from tissue cultures of maize. Crop Sci 15: 417–421.
65. Hasunuma T, Miyazawa SI, Yoshimura S, Shinzaki Y, Tomizawa KI, Shindo K, Choi SK, Misawa N, Miyake C. 2008. Biosynthesis of astaxanthin in tobacco leaves by transplastomic engineering. Plant J 55: 857–868.
66. Hauptmann RM, Ozias-Akins P, Vasil V, Tabaeizadeh Z, Rogers SG, Horsch RB, Vasil IK, Fraley RT. 1987. Transient expression of electroporated DNA in monocotyle-donous and dicotyledonous species. Plant Cell Rep 6: 265–270.
67. Heberlein EA. 1929. Morphological studies on a new species of Marchantia. Bot Gaz 88: 417–429.
68. 4 photosynthesis. Annu Rev Plant Biol 61: 181–207.
69. Hoff T, Schnorr KM, Mundy J. 2001. A recombinase-medi-ated transcriptional induction system in transgenic plants. Plant Mol Biol 45: 41–49.
70. Horvath DM, Stall RE, Jones JB, Pauly MH, Vallad GE, Dahlbeck D, Staskawicz BJ, Scott JW. 2012. Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLoS ONE 7: e42036.
71. Ishizaki K, Chiyoda S, Yamato KT, Kohchi T. 2008. Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol 49: 1084–1091.
72. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280: 104–106.
73. Johnson AAT, Hibberd JM, Gay C, Essah PA, Haseloff J, Tester M, Guiderdoni E. 2005. Spatial control of transgene expression in rice (Oryza sativa L.) using the GAL4 enhancer trapping system. Plant J 41: 779–789.
74. Jones H, Ooms G, Jones MGK. 1989. Transient gene expression in electroporated Solanum protoplasts. Plant Mol Biol 13: 503–511.
75. Jones JDG, Witek K, Verweij W, Jupe F, Cooke D, Dorling S, Tomlinson L, Smoker M, Perkins S, Foster S. 2014. Elevating crop disease resistance with cloned genes. Philos Trans R Soc B Biol Sci 369: 20130087.
76. Jönsson H, Krupinski P. 2010. Modeling plant growth and pattern formation. Curr Opin Plant Biol 13: 5–11.
77. Kapila J, De Rycke R, Van Montagu M, Angenon G. 1997. An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122: 101–108.
78. Karunanandaa B, Qi Q, Hao M, Baszis SR, Jensen PK, Wong YHH, Jiang J, Venkatramesh M, Gruys KJ, Moshiri F, et al. 2005. Metabolically engineered oilseed crops with enhanced seed tocopherol. Metab Eng 7: 384–400.
79. Katoh K, Ohta Y, Hirose Y, Iwamura T. 1979. Photoautotro-phic growth of Marchantia polymorpha L. cells in suspension culture. Planta 144: 509–510.
80. Kimura S, Sinha N. 2008. How to grow tomatoes. CSH Protoc 2008: pdb.prot5081.
81. Kindle KL, Richards KL, Stern DB. 1991. Engineering the chloroplast genome: Techniques and capabilities for chloroplast transformation in Chlamydomonas reinhard-tii. Proc Natl Acad Sci 88: 1721–1725.
82. Knight T. 2003. Idempotent vector design for standard assembly of biobricks. MIT Artificial Intelligence Laboratory; MIT Synthetic Biology Working Group.
83. Koo JC, Asurmendi S, Bick J, Woodford-Thomas T, Beachy RN. 2004. Ecdysone agonist-inducible expression of a coat protein gene from tobacco mosaic virus confers viral resistance in transgenic Arabidopsis. Plant J 37: 439–448.
84. Koschmann J, Machens F, Becker M, Niemeyer J, Schulze J, Bulow L, Stahl DJ, Hehl R. 2012. Integration of bioinfor-matics and synthetic promoters leads to the discovery of novel elicitor-responsive cis-regulatory sequences in Arabidopsis. Plant Physiol 160: 178–191.
85. Krens FA, Molendijk L, Wullems GJ, Schilperoort RA. 1982. In vitro transformation of plant protoplasts with Ti-plas-mid DNA. Nature 296: 72–74.
86. Ku MS, Cho D, Li X, Jiao DM, Pinto M, Miyao M, Matsuoka M. 2001. Introduction of genes encoding C4 photosynthesis enzymes into rice plants: Physiological consequences. Novartis Found Symp 236: 100–116.
87. Kubota A, Ishizaki K, Hosaka M, Kohchi T. 2013. Efficient Agrobacterium-mediated transformation of the liverwort Marchantia polymorpha using regenerating Thalli. Biosci Biotechnol Biochem 77: 167–172.
88. Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP. 2014. Breeding high-yielding drought-tolerant rice: Genetic variations and conventional and molecular approaches. J Exp Bot 65: 6265–6278.
89. Lampropoulos A, Sutikovic Z, Wenzl C, Maegele I, Loh-mann JU, Forner J. 2013. GreenGate– –A novel, versatile, and efficient cloning system for plant transgenesis. PLoS ONE 8: e83043.
90. Laplaze L, Parizot B, Baker A, Ricaud L, Martinière A, Auguy F, Franche C, Nussaume L, Bogusz D, Haseloff J. 2005. GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J Exp Bot 56: 2433–2442.
91. Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun MO, Daniell H. 2003. Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11: 1–13.
92. 4 photosynthesis. J Plant Physiol 170: 378–388.
93. Li MZ, Elledge SJ. 2012. SLIC: A method for sequence- and ligation-independent cloning. Methods Mol Biol 852: 51–59.
94. Li JF, Chung HS, Niu Y, Bush J, McCormack M, Sheen J. 2013. Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell 25: 1507–1522.
95. Li JF, Zhang D, Sheen J. 2014. Cas9-based genome editing in Arabidopsis and tobacco. Methods Enzymol 546: 459– 472.
96. Link KH, Breaker RR. 2009. Engineering ligand-responsive gene-control elements: Lessons learned from natural ri-boswitches. Gene Ther 16: 1189–1201.
97. Liu W, Mazarei M, Rudis MR, Fethe MH, Stewart CN. 2011. Rapid in vivo analysis of synthetic promoters for plant pathogen phytosensing. BMC Biotechnol 11: 108.
98. Liu W, Yuan JS, Stewart CN Jr. 2013. Advanced genetic tools for plant biotechnology. Nat Rev Genet 14: 781–793.
99. Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X, Zheng X, Voytas DF, Hsieh TF, Zhang Y, Qi Y. 2015. A CRISPR/ Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169: 971–985.
100. 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 110: E623.
101. Maliga P. 2004. Plastid transformation in higher plants. Annu Rev Plant Biol 55: 289–313.
102. Mardanova ES, Kotlyarov RY, Kuprianov VV, Stepanova LA, Tsybalova LM, Lomonosoff GP, Ravin NV. 2015. Rapid high-yield expression of a candidate influenza vaccine based on the ectodomain of M2 protein linked to flagellin in plants using viral vectors. BMC Biotechnol 15: 42.
103. Martinez A, Sparks C, Hart CA, Thompson J, Jepson I. 1999. Ecdysone agonist inducible transcription in transgenic tobacco plants. Plant J 19: 97–106.
104. Mayfield SP, Yohn CB, Cohen A, Danon A. 1995. Regulation of chloroplast gene expression. Annu Rev Plant Physiol Plant Mol Biol 46: 147–166.
105. McCaskill D, Croteau R. 1999. Strategies for bioengineering the development and metabolism of glandular tissues in plants. Nat Biotechnol 17: 31–36.
106. McHughen A. 1983. Rapid regeneration of wheat in vitro. Ann Bot 51: 851–853.
107. Mett VL, Lochhead LP, Reynolds PH. 1993. Copper-control-lable gene expression system for whole plants. Proc Natl Acad Sci 90: 4567–4571.
108. Meyerowitz EM. 1989. Arabidopsis, a useful weed. Cell 56: 263–269.
109. Miller MW. 1964. A technique for isolating and culturing gemmae of Marchantia polymorpha L. under aseptic conditions. Bryologist 67: 317–320.
110. Moore I, Galweiler L, Grosskopf D, Schell J, Palme K. 1998. A transcription activation system for regulated gene expression in transgenic plants. Proc Natl Acad Sci 95: 376–381.
111. Mühlbauer SK, Koop H-U. 2005. External control of transgene expression in tobacco plastids using the bacterial lac repressor. Plant J 43: 941–946.
112. Müller B, Sheen J. 2008. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094–1097.
113. Müller K, Siegel D, Rodriguez Jahnke F, Gerrer K, Wend S, Decker EL, Reski R, Weber W, Zurbriggen MD. 2014. A red light-controlled synthetic gene expression switch for plant systems. Mol BioSyst 10: 1679–1688.
114. Nakazato T, Kadota A, Wada M. 1999. Photoinduction of spore germination in Marchantia polymorpha L. is mediated by photosynthesis. Plant Cell Physiol 40: 1014–1020.
115. Negrutiu I, Shillito R, Potrykus I, Biasini G, Sala F. 1987. Hybrid genes in the analysis of transformation conditions. Plant Mol Biol 8: 363–373.
116. Newell CA, Birch-Machin I, Hibberd JM, Gray JC. 2003. Expression of green fluorescent protein from bacterial and plastid promoters in tobacco chloroplasts. Transgenic Res 12: 631–634.
117. Newman DJ, Cragg GM. 2016. Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79: 629–661.
118. Nishiguchi M, Sato T, Motoyoshi F. 1987. An improved method for electroporation in plant protoplasts: Infection of tobacco protoplasts by tobacco mosaic virus particles. Plant Cell Rep 6: 90–93.
119. Nützmann HW, Osbourn A. 2014. Gene clustering in plant specialized metabolism. Curr Opin Biotechnol 26: 91–99.
120. Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, No-zato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, et al. 1992. Complete nucleotide sequence of the mitochondri-al DNA from a liverwort, Marchantia polymorpha. Plant Mol Biol Report 10: 105–163.
121. Oey M, Lohse M, Kreikemeyer B, Bock R. 2009. Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57: 436–445.
122. O’Hanlon ME. 1926. Germination of spores and early stages in development of gametophyte of Marchantia polymorpha. Bot Gaz 82: 215–222.
123. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, et al. 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322: 572–574.
124. Ohyama K, Takemura M, Oda K, Fukuzawa H, Kohchi T, Nakayama S, Ishizaki K, Fujisawa M, Yamato K. 2009. Gene content, organization and molecular evolution of plant organellar genomes and sex chromosomes: Insights from the case of the liverwort Marchantia polymorpha. Proc Jpn Acad Ser B Phys Biol Sci 85: 108–124.
125. Okada S, Fujisawa M, Sone T, Nakayama S, Nishiyama R, Takenaka M, Yamaoka S, Sakaida M, Kono K, Takahama M, et al. 2000. Construction of male and female PAC genomic libraries suitable for identification of Y-chro-mosome-specific clones from the liverwort, Marchantia polymorpha. Plant J 24: 421–428.
126. Ono K, Ohyama K, Gamborg OL. 1979. Regeneration of the liverwort Marchantia polymorpha L. from protoplasts isolated from cell suspension culture. Plant Sci Lett 14: 225–229.
127. Ou-Lee TM, Turgeon R, Wu R. 1986. Expression of a foreign gene linked to either a plant-virus or a Drosophila promoter, after electroporation of protoplasts of rice, wheat, and sorghum. Proc Natl Acad Sci 83: 6815–6819.
128. Padidam M, Gore M, Lu DL, Smirnova O. 2003. Chemical-inducible, ecdysone receptor-based gene expression system for plants. Transgenic Res 12: 101–109.
129. Patron NJ. 2014. DNA assembly for plant biology: Techniques and tools. Curr Opin Plant Biol 19: 14–19.
130. Patron NJ, Orzaez D, Marillonnet S, Warzecha H, Matthew-man C, Youles M, Raitskin O, Leveau A, Farré G, Rogers C, et al. 2015. Standards for plant synthetic biology: A common syntax for exchange of DNA parts. New Phytol 208: 13–19.
131. Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S, Aouida M, Mahfouz MM. 2015. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol J 13: 578–589.
132. Potrykus I, Paszkowski J, Saul MW, Petruska J, Shillito RD. 1985. Molecular and general genetics of a hybrid foreign gene introduced into tobacco by direct gene transfer. MGG Mol Gen Genet 199: 169–177.
133. Prusinkiewicz P, Runions A. 2012. Computational models of plant development and form. New Phytol 193: 549–569.
134. Przibilla E, Heiss S, Johanningmeier U, Trebst A. 1991. Site-specific mutagenesis of the D1 subunit of photosystem II in wild-type Chlamydomonas. Plant Cell 3: 169–174.
135. Quan J, Tian J. 2009. Circular polymerase extension cloning of complex gene libraries and pathways. PLoS ONE 4: e6441.
136. Raitskin O, Patron NJ. 2016. Multi-gene engineering in plants with RNA-guided Cas9 nuclease. Curr Opin Biotechnol 37: 69–75
137. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud P-F, Lindquist EA, Kami-sugi Y, et al. 2008. The physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64–69.
138. Rogers C, Oldroyd GED. 2014. Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. J Exp Bot 65: 1939–1946.
139. Roslan HA, Salter MG, Wood CD, White MRH, Croft KP, Robson F, Coupland G, Doonan J, Laufs P, Tomsett AB, et al. 2001. Characterization of the ethanol-inducible alc gene-expression system in Arabidopsis thaliana. Plant J 28: 225–235.
140. Salter MG, Paine JA, Riddell K V, Jepson I, Greenland AJ, Caddick MX, Tomsett AB. 1998. Characterisation of the ethanol-inducible alc gene expression system for transgenic plants. Plant J 16: 127–132.
141. Samalova M, Brzobohaty B, Moore I. 2005. pOp6/LhGR: A stringently regulated and highly responsive dexametha-sone-inducible gene expression system for tobacco. Plant J 41: 919–935.
142. Sarrion-Perdigones A, Falconi EE, Zandalinas SI, Juárez P, Fernández-del-Carmen A, Granell A, Orzaez D. 2011. GoldenBraid: An iterative cloning system for standard- ized assembly of reusable genetic modules. PLoS ONE 6: e21622.
143. Sasaki G, Katoh K, Hirose N, Suga H, Kuma K, Miyata T, Su ZH. 2007. Multiple receptor-like kinase cDNAs from liverwort Marchantia polymorpha and two charophycean green algae, Closterium ehrenbergii and Nitella axillaris: Extensive gene duplications and gene shufflings in the early evolution of streptophytes. Gene 401: 135–144.
144. Scharff LB, Bock R. 2014. Synthetic biology in plastids. Plant J 78: 783–798.
145. Schaumberg KA, Antunes MS, Kassaw TK, Xu W, Zalewski CS, Medford JI, Prasad A. 2016. Quantitative characterization of genetic parts and circuits for plant synthetic biology. Nat Methods 13: 94–100.
146. Schilmiller AL, Last RL, Pichersky E. 2008. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J 54: 702–711.
147. Schiml S, Puchta H. 2016. Revolutionizing plant biology: Multiple ways of genome engineering by CRISPR/Cas. Plant Methods 12:8
148. Sheen J. 2001. Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol 127: 1466–1475.
149. Shetty RP, Endy D, Knight TF. 2008. Engineering BioBrick vectors from BioBrick parts. J Biol Eng 2: 5.
150. Shimamura M. 2012. An introduction to the taxonomy and morphology of Marchantia polymorpha. BSJ-Review 3: 84–113.
151. Somerville C, Koornneef M. 2002. A fortunate choice: The history of Arabidopsis as a model plant. Nat Rev Genet 3: 883–889.
152. Sparkes IA, Runions J, Kearns A, Hawes C. 2006. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1: 2019–2025.
153. Springer PS. 2000. Gene traps: Tools for plant development and genomics. Plant Cell 12: 1007–1020.
154. Sudarsan N, Barrick JE, Breaker RR. 2003. Metabolite-bind-ing RNA domains are present in the genes of eukaryotes. RNA 9: 644–647.
155. Suire C, Bouvier F, Backhaus RA, Bégu D, Bonneu M, Camara B. 2000. Cellular localization of isoprenoid biosyn-thetic enzymes in Marchantia polymorpha. Uncovering a new role of oil bodies. Plant Physiol 124: 971–978.
156. Svab Z, Hajdukiewicz P, Maliga P. 1990. Stable transformation of plastids in higher plants. Proc Natl Acad Sci 87: 8526–8530.
157. Takenaka M, Yamaoka S, Hanajiri T, Shimizu-Ueda Y, Yamato KT, Fukuzawa H, Ohyama K. 2000. Direct transformation and plant regeneration of the haploid liverwort Marchantia polymorpha L. Transgenic Res 9: 179–185.
158. Thimmappa R, Geisler K, Louveau T, O’Maille P, Osbourn A. 2014. Triterpene biosynthesis in plants. Annu Rev Plant Biol 65: 225–257.
159. Torella JP, Boehm CR, Lienert F, Chen JH, Way JC, Silver PA. 2013. Rapid construction of insulated genetic circuits via synthetic sequence-guided isothermal assembly. Nucleic Acids Res 42: 1–9.
160. Tsuboyama S, Kodama Y. 2014. AgarTrap: A simplified Agrobacterium-mediated transformation method for sporelings of the liverwort Marchantia polymorpha L. Plant Cell Physiol 55: 229–236.
161. Tsukaya H. 2003. Organ shape and size: A lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6: 57–62.
162. Vafaee Y, Staniek A, Mancheno-Solano M, Warzecha H. 2014. A modular cloning toolbox for the generation of chloroplast transformation vectors. PLoS ONE 9: e110222.
163. Valvekens D, Van Lijsebettens M, Van Montagu M. 1992. Arabidopsis regeneration and transformation (Root Explant System). In Plant tissue culture manual, pp. 1–17. Springer, Boston.
164. van Herpen TWJM, Cankar K, Nogueira M, Bosch D, Bouwmeester HJ, Beekwilder J. 2010. Nicotiana benthamiana as a production platform for artemisinin precursors. PLoS ONE 5: e14222.
165. Vaughan DA, Balazs E, Heslop-Harrison JS. 2007. From crop domestication to super-domestication. Ann Bot 100: 893–901.
166. Verhounig A, Karcher D, Bock R. 2010. Inducible gene expression from the plastid genome by a synthetic riboswitch. Proc Natl Acad Sci 107: 6204–6209.
167. Verma D, Kanagaraj A, Jin S, Singh ND, Kolattukudy PE, Daniell H. 2010. Chloroplast-derived enzyme cocktails hydrolyse lignocellulosic biomass and release ferment-able sugars. Plant Biotechnol J 8: 332–350.
168. Vötching H. 1885. Über die regeneration der Marchan-tiaceen. Jahrbuecher fur Wissenschaftliche Bot 16: 367– 414.
169. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR. 2007. Riboswitch control of gene expression in plants by splicing and alternative 3' end processing of mRNAs. Plant Cell 19: 3437–3450.
170. Wani S, Haider N, Kumar HB, Singh N. 2010. Plant plastid engineering. Curr Genomics 11: 500–512.
171. Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S. 2011. a modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6: e16765.
172. Weinmann P, Gossen M, Hillen W, Bujard H, Gatz C. 1994. A chimeric transactivator allows tetracycline-responsive gene expression in whole plants. Plant J 5: 559–569.
173. Wend S, Bosco CD, Kämpf MM, Ren F, Palme K, Weber W, Dovzhenko A, Zurbriggen MD. 2013. A quantitative ra-tiometric sensor for time-resolved analysis of auxin dynamics. Sci Rep 3: 769–782.
174. Werner S, Engler C, Weber E, Gruetzner R, Marillonnet S. 2012. Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system. Bioeng Bugs 3: 38–43.
175. Wijnker E, van Dun K, de Snoo CB, Lelivelt CLC, Keurentjes JJB, Naharudin NS, Ravi M, Chan SWL, de Jong H, Dirks R. 2012. Reverse breeding in Arabidopsis thaliana generates homozygous parental lines from a heterozygous plant. Nat Genet 44: 467–470.
176. Yamato KT, Kohchi T. 2012. The “sneak” preview of the Marchantia polymorpha genome. BSJ Rev 3: 71–83.
177. Yamato KT, Ishizaki K, Fujisawa M, Okada S, Nakayama S, Fujishita M, Bando H, Yodoya K, Hayashi K, Bando T, et al. 2007. Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci 104: 6472–6477.
178. Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcription fac- tor in plants: Improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci 101: 7833–7838.
179. Ye X, Al-Babili S, Klöti A, Zhang J, Lucca P, Beyer P, Potrykus I. 2000. Engineering the provitamin A (β-carotene) bio-synthetic pathway into (carotenoid-free) rice endosperm. Science 287: 303–305.
180. Yu S, Pilot G. 2014. Testing the efficiency of plant artificial microRNAs by transient expression in Nicotiana benthamiana reveals additional action at the translational level. Front Plant Sci 5: 622.
181. * MADS-Box Proteins: Conserved regulators of the game- tophytic generation of land plants. Mol Biol Evol 27: 1201–1211.
182. Zohary D, Hopf M, Weiss E. 2012. Domestication of plants in the old world: The origin and spread of domesticated plants in Southwest Asia, Europe, and the Mediterranean basin. Oxford University Press, New York.
183. Zuo J, Niu QW, Chua NH. 2000. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265–273.
184. Zurcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Muller B. 2013. A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161: 1066–1075.