1932

Abstract

Synthetic signaling is a branch of synthetic biology that aims to understand native genetic regulatory mechanisms and to use these insights to engineer interventions and devices that achieve specified design parameters. Applying synthetic signaling approaches to plants offers the promise of mitigating the worst effects of climate change and providing a means to engineer crops for entirely novel environments, such as those in space travel. The ability to engineer new traits using synthetic signaling methods will require standardized libraries of biological parts and methods to assemble them; the decoupling of complex processes into simpler subsystems; and mathematical models that can accelerate the design-build-test-learn cycle. The field of plant synthetic signaling is relatively new, but it is poised for rapid advancement. Translation from the laboratory to the field is likely to be slowed, however, by the lack of constructive dialogue between researchers and other stakeholders.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081519-035852
2020-04-29
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-081519-035852.html?itemId=/content/journals/10.1146/annurev-arplant-081519-035852&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abudayyeh OO, Gootenberg JS, Essletzbichler P, Han S, Joung J et al. 2017. RNA targeting with CRISPR-Cas13. Nature 550:7675280–84
    [Google Scholar]
  2. 2. 
    Agapakis CM. 2014. Designing synthetic biology. ACS Synth. Biol. 3:3121–28
    [Google Scholar]
  3. 3. 
    Andres J, Blomeier T, Zurbriggen MD 2019. Synthetic switches and regulatory circuits in plants. Plant Physiol 179:3862–84
    [Google Scholar]
  4. 4. 
    Antunes MS, Morey KJ, Smith JJ, Albrecht KD, Bowen TA et al. 2011. Programmable ligand detection system in plants through a synthetic signal transduction pathway. PLOS ONE 6:1e16292
    [Google Scholar]
  5. 5. 
    Aoyama T, Chua N-H. 1997. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11:3605–12
    [Google Scholar]
  6. 6. 
    Bachmair A, Varshavsky A. 1989. The degradation signal in a short-lived protein. Cell 56:61019–32
    [Google Scholar]
  7. 7. 
    Band LR, Wells DM, Fozard JA, Ghetiu T, French AP et al. 2014. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell 26:3862–75
    [Google Scholar]
  8. 8. 
    Bashor CJ, Helman NC, Yan S, Lim WA 2008. Using engineered scaffold interactions to reshape MAP kinase pathway signaling dynamics. Science 319:58691539–43
    [Google Scholar]
  9. 9. 
    Basu S, Mehreja R, Thiberge S, Chen M-T, Weiss R 2004. Spatiotemporal control of gene expression with pulse-generating networks. PNAS 101:176355–60
    [Google Scholar]
  10. 10. 
    Deleted in proof
  11. 11. 
    Bernabé-Orts JM, Quijano-Rubio A, Mancheño-Bonillo J, Moles-Casas V, Selma S et al. 2019. A reversible memory switch for plant synthetic biology based on the phage PhiC31 integration system. bioRxiv 656223. https://doi.org/10.1101/656223
    [Crossref]
  12. 12. 
    Bick MJ, Greisen PJ, Morey KJ, Antunes MS, La D et al. 2017. Computational design of environmental sensors for the potent opioid fentanyl. eLife 6:e28909
    [Google Scholar]
  13. 13. 
    Binder A, Lambert J, Morbitzer R, Popp C, Ott T et al. 2014. A modular plasmid assembly kit for multigene expression, gene silencing and silencing rescue in plants. PLOS ONE 9:2e88218
    [Google Scholar]
  14. 14. 
    Boehm CR, Pollak B, Purswani N, Patron N, Haseloff J 2017. Synthetic botany. Cold Spring Harb. Perspect. Biol. 9:7a023887
    [Google Scholar]
  15. 15. 
    Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M 2014. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J 78:131–43
    [Google Scholar]
  16. 16. 
    Borchert R, Honda H. 1984. Control of development in the bifurcating branch system of Tabebuia rosea: a computer simulation. Bot. Gaz. 145:2184–95
    [Google Scholar]
  17. 17. 
    Boudon F, Chopard J, Ali O, Gilles B, Hamant O et al. 2015. A computational framework for 3D mechanical modeling of plant morphogenesis with cellular resolution. PLOS Comput. Biol. 11:1e1003950
    [Google Scholar]
  18. 18. 
    Bradley RW, Wang B. 2015. Designer cell signal processing circuits for biotechnology. New Biotechnol 32:6635–43
    [Google Scholar]
  19. 19. 
    Busov VB, Brunner AM, Meilan R, Filichkin S, Ganio L et al. 2005. Genetic transformation: a powerful tool for dissection of adaptive traits in trees. New Phytol 167:19–18
    [Google Scholar]
  20. 20. 
    Campbell MEM, Palfreyman JW, Preston CM 1984. Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. J. Mol. Biol. 180:11–19
    [Google Scholar]
  21. 21. 
    Cantó-Pastor A, Mollá-Morales A, Ernst E, Dahl W, Zhai J et al. 2015. Efficient transformation and artificial miRNA gene silencing in Lemna minor. Plant Biol 17:Suppl. 159–65
    [Google Scholar]
  22. 22. 
    Chang C, Bowman JL, Meyerowitz EM 2016. Field guide to plant model systems. Cell 167:2325–39
    [Google Scholar]
  23. 23. 
    Chatelle C, Ochoa-Fernandez R, Engesser R, Schneider N, Beyer HM et al. 2018. A green-light-responsive system for the control of transgene expression in mammalian and plant cells. ACS Synth. Biol. 7:51349–58
    [Google Scholar]
  24. 24. 
    Chickarmane V, Roeder AHK, Tarr PT, Cunha A, Tobin C, Meyerowitz EM 2010. Computational morphodynamics: a modeling framework to understand plant growth. Annu. Rev. Plant Biol. 61:65–87
    [Google Scholar]
  25. 25. 
    Chung HK, Zou X, Bajar BT, Brand VR, Huo Y et al. 2019. A compact synthetic pathway rewires cancer signaling to therapeutic effector release. Science 364:6439eaat6982
    [Google Scholar]
  26. 26. 
    Collier R, Thomson JG, Thilmony R 2018. A versatile and robust Agrobacterium-based gene stacking system generates high-quality transgenic Arabidopsis plants. Plant J 95:573–83
    [Google Scholar]
  27. 27. 
    Cosentino C, Alberio L, Gazzarrini S, Aquila M, Romano E et al. 2015. Engineering of a light-gated potassium channel. Science 348:6235707–10
    [Google Scholar]
  28. 28. 
    de Lange O, Klavins E, Nemhauser J 2018. Synthetic genetic circuits in crop plants. Curr. Opin. Biotechnol. 49:16–22
    [Google Scholar]
  29. 29. 
    Delépine B, Duigou T, Carbonell P, Faulon J-L 2018. RetroPath2.0: a retrosynthesis workflow for metabolic engineers. Metab. Eng. 45:158–70
    [Google Scholar]
  30. 30. 
    Dey N, Sarkar S, Acharya S, Maiti IB 2015. Synthetic promoters in planta. Planta 242:51077–94
    [Google Scholar]
  31. 31. 
    Eisenstein M. 2014. Biotechnology: against the grain. Nature 514:7524S55–57
    [Google Scholar]
  32. 32. 
    Elowitz M, Lim WA. 2010. Build life to understand it. Nature 468:889–90
    [Google Scholar]
  33. 33. 
    Endy D. 2005. Foundations for engineering biology. Nature 438:7067449–53
    [Google Scholar]
  34. 34. 
    Engler C, Youles M, Gruetzner R, Ehnert T-M, Werner S et al. 2014. A Golden Gate modular cloning toolbox for plants. ACS Synth. Biol. 3:11839–43
    [Google Scholar]
  35. 35. 
    Erb TJ, Jones PR, Bar-Even A 2017. Synthetic metabolism: Metabolic engineering meets enzyme design. Curr. Opin. Chem. Biol. 37:56–62
    [Google Scholar]
  36. 36. 
    Faden F, Mielke S, Dissmeyer N 2019. Modulating protein stability to switch toxic protein function on and off in living cells. Plant Physiol 179:3929–42
    [Google Scholar]
  37. 37. 
    Farzadfard F, Lu TK. 2014. Genomically encoded analog memory with precise in vivo DNA writing in living cell populations. Science 346:62111256272
    [Google Scholar]
  38. 38. 
    Fendrych M, Akhmanova M, Merrin J, Glanc M, Hagihara S et al. 2018. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 4:7453–59
    [Google Scholar]
  39. 39. 
    Feng J, Jester BW, Tinberg CE, Mandell DJ, Antunes MS et al. 2015. A general strategy to construct small molecule biosensors in eukaryotes. eLife 4:e10606This paper presents a potential pipeline for engineering a small molecule detector for diverse ligands that is able to trigger changes in transcription upon binding.
    [Google Scholar]
  40. 40. 
    Fu W, Wichuk K, Brynjólfsson S 2015. Developing diatoms for value-added products: challenges and opportunities. New Biotechnol 32:6547–51
    [Google Scholar]
  41. 41. 
    Gallego-Bartolomé J, Gardiner J, Liu W, Papikian A, Ghoshal B et al. 2018. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. PNAS 115:9E2125–34
    [Google Scholar]
  42. 42. 
    Gander MW, Vrana JD, Voje WE, Carothers JM, Klavins E 2017. Digital logic circuits in yeast with CRISPR-dCas9 NOR gates. Nat. Commun. 8:15459
    [Google Scholar]
  43. 43. 
    García-Arenal F, Zerbini FM. 2019. Life on the edge: geminiviruses at the interface between crops and wild plant hosts. Annu. Rev. Virol. 6:411–33
    [Google Scholar]
  44. 44. 
    Gilbert LA, Larson MH, Morsut L, Liu Z, Brar GA et al. 2013. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:2442–51
    [Google Scholar]
  45. 45. 
    Gómez-Gómez L, Boller T. 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:61003–11
    [Google Scholar]
  46. 46. 
    Gonneau M, Desprez T, Martin M, Doblas VG, Bacete L et al. 2018. Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in Arabidopsis. Curr. Biol 28:152452–58.e4
    [Google Scholar]
  47. 47. 
    Gordley RM, Williams RE, Bashor CJ, Toettcher JE, Yan S, Lim WA 2016. Engineering dynamical control of cell fate switching using synthetic phospho-regulons. PNAS 113:4713528–33
    [Google Scholar]
  48. 48. 
    Gorochowski TE. 2016. Agent-based modelling in synthetic biology. Essays Biochem 60:4325–36
    [Google Scholar]
  49. 49. 
    Groves B, Khakhar A, Nadel CM, Gardner RG, Seelig G 2016. Rewiring MAP kinases in Saccharomyces cerevisiae to regulate novel targets through ubiquitination. eLife 5:e15200
    [Google Scholar]
  50. 50. 
    Guiziou S, Mayonove P, Bonnet J 2019. Hierarchical composition of reliable recombinase logic devices. Nat. Commun. 10:1456
    [Google Scholar]
  51. 51. 
    Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR 2014. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:6169408–11
    [Google Scholar]
  52. 52. 
    Haseloff J. 1999. GFP variants for multispectral imaging of living cells. Methods Cell Biol 58:139–51
    [Google Scholar]
  53. 53. 
    Hay Mele B, Giannino F, Vincenot CE, Mazzoleni S, Cartení F 2015. Cell-based models in plant developmental biology: insights into hybrid approaches. Front. Environ. Sci. 3:73
    [Google Scholar]
  54. 54. 
    Hillson N, Caddick M, Cai Y, Carrasco JA, Chang MW et al. 2019. Building a global alliance of biofoundries. Nat. Commun. 10:12040
    [Google Scholar]
  55. 55. 
    Hochreiter B, Garcia AP, Schmid JA 2015. Fluorescent proteins as genetically encoded FRET biosensors in life sciences. Sensors 15:1026281–314
    [Google Scholar]
  56. 56. 
    Iacopino S, Jurinovich S, Cupellini L, Piccinini L, Cardarelli F et al. 2019. A synthetic oxygen sensor for plants based on animal hypoxia signaling. Plant Physiol 179:3986–1000
    [Google Scholar]
  57. 57. 
    Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:318–56
    [Google Scholar]
  58. 58. 
    Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J 2013. RNA-programmed genome editing in human cells. eLife 2:e00471
    [Google Scholar]
  59. 59. 
    Jones AM, Danielson JA, Manojkumar SN, Lanquar V, Grossmann G, Frommer WB 2014. Abscisic acid dynamics in roots detected with genetically encoded FRET sensors. eLife 3:e01741
    [Google Scholar]
  60. 60. 
    Kamisugi Y, Schlink K, Rensing SA, Schween G, von Stackelberg M et al. 2006. The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res 34:216205–14
    [Google Scholar]
  61. 61. 
    Kaplan DR. 1992. The relationship of cells to organisms in plants: problem and implications of an organismal perspective. Int. J. Plant Sci. 153:3S28–37
    [Google Scholar]
  62. 62. 
    Kapusi E, Kempe K, Rubtsova M, Kumlehn J, Gils M 2012. phiC31 integrase-mediated site-specific recombination in barley. PLOS ONE 7:9e45353
    [Google Scholar]
  63. 63. 
    Katsir L, Chung HS, Koo AJK, Howe GA 2008. Jasmonate signaling: a conserved mechanism of hormone sensing. Curr. Opin. Plant Biol. 11:4428–35
    [Google Scholar]
  64. 64. 
    Kausch AP, Nelson-Vasilchik K, Hague J, Mookkan M, Quemada H et al. 2019. Edit at will: genotype independent plant transformation in the era of advanced genomics and genome editing. Plant Sci 281:186–205
    [Google Scholar]
  65. 65. 
    Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J et al. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat. Biotechnol 25:5593–99
    [Google Scholar]
  66. 65a. 
    Keller B, Vrana J, Miller A, Newman G, Klavins E 2019. klavinslab/aquarium: protocol images and bug fixes for invoices and imports.. Zenodo https://zenodo.org/record/2880352#.XdV5kldKiUk
    [Google Scholar]
  67. 66. 
    Kessler SA, Lindner H, Jones DS, Grossniklaus U 2015. Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception. EMBO Rep 16:1107–15
    [Google Scholar]
  68. 67. 
    Khakhar A, Leydon AR, Lemmex AC, Klavins E, Nemhauser JL 2018. Synthetic hormone-responsive transcription factors can monitor and re-program plant development. eLife 7:e34702
    [Google Scholar]
  69. 68. 
    Kim BH, Kim SY, Nam KH 2013. Assessing the diverse functions of BAK1 and its homologs in Arabidopsis, beyond BR signaling and PTI responses. Mol. Cells 35:17–16
    [Google Scholar]
  70. 69. 
    Kim H, Bojar D, Fussenegger M 2019. A CRISPR/Cas9-based central processing unit to program complex logic computation in human cells. PNAS 116:157214–19
    [Google Scholar]
  71. 70. 
    Kitada T, DiAndreth B, Teague B, Weiss R 2018. Programming gene and engineered-cell therapies with synthetic biology. Science 359:6376eaad1067
    [Google Scholar]
  72. 71. 
    Koschmann J, Machens F, Becker M, Niemeyer J, Schulze J et al. 2012. Integration of bioinformatics and synthetic promoters leads to the discovery of novel elicitor-responsive cis-regulatory sequences in Arabidopsis. Plant Physiol 160:1178–91
    [Google Scholar]
  73. 72. 
    Lampropoulos A, Sutikovic Z, Wenzl C, Maegele I, Lohmann JU, Forner J 2013. GreenGate—a novel, versatile, and efficient cloning system for plant transgenesis. PLOS ONE 8:12e83043
    [Google Scholar]
  74. 73. 
    Lapin A, Klann M, Reuss M 2010. Multi-scale spatio-temporal modeling: lifelines of microorganisms in bioreactors and tracking molecules in cells. Adv. Biochem. Eng. Biotechnol. 121:23–43
    [Google Scholar]
  75. 74. 
    Lavarenne J, Guyomarc'h S, Sallaud C, Gantet P, Lucas M 2018. The spring of systems biology-driven breeding. Trends Plant Sci 23:8706–20
    [Google Scholar]
  76. 75. 
    Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM et al. 2012. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26:2126–36
    [Google Scholar]
  77. 76. 
    Li Z, Zhang D, Xiong X, Yan B, Xie W et al. 2017. A potent Cas9-derived gene activator for plant and mammalian cells. Nat. Plants 3:12930–36
    [Google Scholar]
  78. 77. 
    Lim WA. 2010. Designing customized cell signalling circuits. Nat. Rev. Mol. Cell Biol. 11:6393–403
    [Google Scholar]
  79. 78. 
    Liu W, Stewart CN. 2015. Plant synthetic biology. Trends Plant Sci 20:5309–17
    [Google Scholar]
  80. 79. 
    Liu W, Stewart CN. 2016. Plant synthetic promoters and transcription factors. Curr. Opin. Biotechnol. 37:36–44
    [Google Scholar]
  81. 80. 
    Lowder LG, Paul JW, Qi Y 2017. Multiplexed transcriptional activation or repression in plants using CRISPR-dCas9-based systems. Methods Mol. Biol. 1629:167–84
    [Google Scholar]
  82. 81. 
    Lowder LG, Zhang D, Baltes NJ, Paul JW, Tang X et al. 2015. A CRISPR/Cas9 toolbox for multiplexed plant genome editing and transcriptional regulation. Plant Physiol 169:2971–85
    [Google Scholar]
  83. 82. 
    Lowder LG, Zhou J, Zhang Y, Malzahn A, Zhong Z et al. 2018. Robust transcriptional activation in plants using multiplexed CRISPR-Act2.0 and mTALE-Act systems. Mol. Plant 11:2245–56Expansion of dCAS9 transcription factor recruitment through interaction with MS2-protein fusions in plants.
    [Google Scholar]
  84. 83. 
    Macia J, Manzoni R, Conde N, Urrios A, de Nadal E et al. 2016. Implementation of complex biological logic circuits using spatially distributed multicellular consortia. PLOS Comput. Biol. 12:2e1004685
    [Google Scholar]
  85. 84. 
    Mahas A, Neal Stewart C Jr., Mahfouz MM 2018. Harnessing CRISPR/Cas systems for programmable transcriptional and post-transcriptional regulation. Biotechnol. Adv. 36:1295–310
    [Google Scholar]
  86. 85. 
    Maier A, Fahnenstich H, von Caemmerer S, Engqvist MKM, Weber APM et al. 2012. Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Front. Plant Sci. 3:38
    [Google Scholar]
  87. 86. 
    Malik MR, Tang J, Sharma N, Burkitt C, Ji Y et al. 2018. Camelina sativa, an oilseed at the nexus between model system and commercial crop. Plant Cell Rep 37:101367–81
    [Google Scholar]
  88. 87. 
    Martin K, Kopperud K, Chakrabarty R, Banerjee R, Brooks R, Goodin MM 2009. Transient expression in Nicotiana benthamiana fluorescent marker lines provides enhanced definition of protein localization, movement and interactions in planta. Plant J 59:1150–62
    [Google Scholar]
  89. 88. 
    Martinez A, Sparks C, Hart CA, Thompson J, Jepson I 1999. Ecdysone agonist inducible transcription in transgenic tobacco plants. Plant J 19:197–106
    [Google Scholar]
  90. 89. 
    Mendoza L, Thieffry D, Alvarez-Buylla ER 1999. Genetic control of flower morphogenesis in Arabi-dopsis thaliana: a logical analysis. Bioinformatics 15:7–8593–606
    [Google Scholar]
  91. 90. 
    Merks R. 2015. Cell-based modeling. Encyclopedia of Applied and Computational Mathematics B Engquist 195–201 Berlin: Springer
    [Google Scholar]
  92. 91. 
    Morris RJ 2018. Mathematical Modelling in Plant Biology Cham, Switz.: Springer
  93. 92. 
    Morsut L, Roybal KT, Xiong X, Gordley RM, Coyle SM et al. 2016. Engineering customized cell sensing and response behaviors using synthetic notch receptors. Cell 164:4780–91
    [Google Scholar]
  94. 93. 
    Moss BL, Mao H, Guseman JM, Hinds TR, Hellmuth A et al. 2015. Rate motifs tune auxin/indole-3-acetic acid degradation dynamics. Plant Physiol 169:1803–13
    [Google Scholar]
  95. 94. 
    Muraro D, Byrne HM, King JR, Bennett MJ 2013. Mathematical modelling plant signalling networks. Math. Model. Nat. Phenom. 8:45–24
    [Google Scholar]
  96. 95. 
    Muraro D, Mellor N, Pound MP, Help H, Lucas M et al. 2014. Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. PNAS 111:2857–62
    [Google Scholar]
  97. 96. 
    Murase K, Hirano Y, Sun T, Hakoshima T 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:7221459–63
    [Google Scholar]
  98. 97. 
    Mutalik VK, Guimaraes JC, Cambray G, Lam C, Christoffersen MJ et al. 2013. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods 10:4354–60
    [Google Scholar]
  99. 98. 
    Myers CJ, Beal J, Gorochowski TE, Kuwahara H, Madsen C et al. 2017. A standard-enabled workflow for synthetic biology. Biochem. Soc. Trans. 45:3793–803
    [Google Scholar]
  100. 99. 
    Nielsen AAK, Der BS, Shin J, Vaidyanathan P, Paralanov V et al. 2016. Genetic circuit design automation. Science 352:6281aac7341
    [Google Scholar]
  101. 100. 
    Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M 2009. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat. Methods 6:12917–22
    [Google Scholar]
  102. 101. 
    Oborny B. 2004. External and internal control in plant development. Complexity 9:322–28
    [Google Scholar]
  103. 102. 
    Ohme-Takagi M, Taylor CB, Newman TC, Green PJ 1993. The effect of sequences with high AU content on mRNA stability in tobacco. PNAS 90:2411811–15
    [Google Scholar]
  104. 103. 
    O'Shaughnessy EC, Palani S, Collins JJ, Sarkar CA 2011. Tunable signal processing in synthetic MAP kinase cascades. Cell 144:1119–31
    [Google Scholar]
  105. 104. 
    Palm MM, Merks RMH. 2015. Large-scale parameter studies of cell-based models of tissue morphogenesis using CompuCell3D or VirtualLeaf. Methods Mol. Biol 1189:301–22
    [Google Scholar]
  106. 105. 
    Papanatsiou M, Petersen J, Henderson L, Wang Y, Christie JM, Blatt MR 2019. Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science 363:64341456–59The authors implemented a blue-light optogenetic signaling module called BLINK1 that augments stomatal dynamics and enhances water use efficiency.
    [Google Scholar]
  107. 106. 
    Papikian A, Liu W, Gallego-Bartolomé J, Jacobsen SE 2019. Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat. Commun. 10:1729
    [Google Scholar]
  108. 107. 
    Park J-J, Dempewolf E, Zhang W, Wang Z-Y 2017. RNA-guided transcriptional activation via CRISPR/dCas9 mimics overexpression phenotypes in Arabidopsis. PLOS ONE 12:6e0179410
    [Google Scholar]
  109. 108. 
    Park S-Y, Peterson FC, Mosquna A, Yao J, Volkman BF, Cutler SR 2015. Agrochemical control of plant water use using engineered abscisic acid receptors. Nature 520:7548545–48Saturation mutagenesis was used to engineer an orthogonal abscisic acid receptor, PYR1MANDI, that perceives the fungicide mandipropamid instead of ABA.
    [Google Scholar]
  110. 109. 
    Patron NJ, Orzaez D, Marillonnet S, Warzecha H, Matthewman C et al. 2015. Standards for plant synthetic biology: a common syntax for exchange of DNA parts. New Phytol 208:113–19
    [Google Scholar]
  111. 110. 
    Pérez-Ruiz RV, García-Ponce B, Marsch-Martínez N, Ugartechea-Chirino Y, Villajuana-Bonequi M et al. 2015. XAANTAL2 (AGL14) is an important component of the complex gene regulatory network that underlies Arabidopsis shoot apical meristem transitions. Mol. Plant 8:5796–813
    [Google Scholar]
  112. 111. 
    Peterhansel C, Horst I, Niessen M, Blume C, Kebeish R et al. 2010. Photorespiration. Arabidopsis Book 8:e0130
    [Google Scholar]
  113. 112. 
    Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A et al. 2015. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnol. J. 13:4578–89
    [Google Scholar]
  114. 113. 
    Pierre-Jerome E, Jang SS, Havens KA, Nemhauser JL, Klavins E 2014. Recapitulation of the forward nuclear auxin response pathway in yeast. PNAS 111:269407–12
    [Google Scholar]
  115. 114. 
    Pollak B, Cerda A, Delmans M, Álamos S, Moyano T et al. 2019. Loop assembly: a simple and open system for recursive fabrication of DNA circuits. New Phytol 222:1628–40
    [Google Scholar]
  116. 115. 
    Prusinkiewicz P, Runions A. 2012. Computational models of plant development and form. New Phytol 193:3549–69
    [Google Scholar]
  117. 116. 
    Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS et al. 2013. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:51173–83
    [Google Scholar]
  118. 117. 
    Refahi Y, Brunoud G, Farcot E, Jean-Marie A, Pulkkinen M et al. 2016. A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis. eLife 5:e14093
    [Google Scholar]
  119. 118. 
    Reski R, Bae H, Simonsen HT 2018. Physcomitrella patens, a versatile synthetic biology chassis. Plant Cell Rep 37:101409–17
    [Google Scholar]
  120. 119. 
    Rizza A, Walia A, Tang B, Jones AM 2019. Visualizing cellular gibberellin levels using the nlsGPS1 Förster resonance energy transfer (FRET) biosensor. J. Vis. Exp. 143:e58739
    [Google Scholar]
  121. 120. 
    Roell M-S, Zurbriggen MD. 2020. The impact of synthetic biology for future agriculture and nutrition. Curr. Opin. Biotechnol. 61:102–9
    [Google Scholar]
  122. 121. 
    Rogers C, Oldroyd GED. 2014. Synthetic biology approaches to engineering the nitrogen symbiosis in cereals. J. Exp. Bot. 65:81939–46
    [Google Scholar]
  123. 122. 
    Roybal KT, Rupp LJ, Morsut L, Walker WJ, McNally KA et al. 2016. Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell 164:4770–79
    [Google Scholar]
  124. 123. 
    Ryu J, Park S-H. 2015. Simple synthetic protein scaffolds can create adjustable artificial MAPK circuits in yeast and mammalian cells. Sci. Signal. 8:383ra66
    [Google Scholar]
  125. 124. 
    Sarrion-Perdigones A, Vazquez-Vilar M, Palací J, Castelijns B, Forment J et al. 2013. GoldenBraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiol 162:31618–31GoldenBraid 2.0 is a modular framework to assemble plant biological parts based on type IIS restriction enzymes; the authors include a collection of biological parts.
    [Google Scholar]
  126. 125. 
    Schreiber T, Prange A, Hoppe T, Tissier A 2019. Split-TALE: aTALE-based two-component system for synthetic biology applications in planta. Plant Physiol 179:31001–12
    [Google Scholar]
  127. 126. 
    Schuler ML, Mantegazza O, Weber APM 2016. Engineering C4 photosynthesis into C3 chassis in the synthetic biology age. Plant J 87:151–65
    [Google Scholar]
  128. 127. 
    Schwander T, von Borzyskowski LS, Burgener S, Cortina NS, Erb TJ 2016. A synthetic pathway for the fixation of carbon dioxide in vitro. Science 354:6314900–4
    [Google Scholar]
  129. 128. 
    She J, Han Z, Kim T-W, Wang J, Cheng W et al. 2011. Structural insight into brassinosteroid perception by BRI1. Nature 474:7352472–76
    [Google Scholar]
  130. 129. 
    Shih PM, Vuu K, Mansoori N, Ayad L, Louie KB et al. 2016. A robust gene-stacking method utilizing yeast assembly for plant synthetic biology. Nat. Commun. 7:13215
    [Google Scholar]
  131. 130. 
    Shiu S-H, Bleecker AB. 2001. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. PNAS 98:1910763–68
    [Google Scholar]
  132. 131. 
    South PF, Cavanagh AP, Liu HW, Ort DR 2019. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:6422eaat9077The authors used a model-driven approach to engineer a photorespiration bypass pathway; implementation in plants increases photosynthesis efficiency.
    [Google Scholar]
  133. 132. 
    Sperschneider J, Catanzariti A-M, DeBoer K, Petre B, Gardiner DM et al. 2017. LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell. Sci. Rep. 7:44598
    [Google Scholar]
  134. 133. 
    Takeuchi H, Higashiyama T. 2016. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:7593245–48
    [Google Scholar]
  135. 134. 
    Takaoka Y, Iwahashi M, Chini A, Saito H, Ishimaru Y et al. 2018. A rationally designed JAZ subtype-selective agonist of jasmonate perception. Nat. Commun. 9:13654
    [Google Scholar]
  136. 135. 
    Thomson JG, Chan R, Smith J, Thilmony R, Yau Y-Y et al. 2012. The Bxb1 recombination system demonstrates heritable transmission of site-specific excision in Arabidopsis. BMC Biotechnol 12:9
    [Google Scholar]
  137. 136. 
    Tinberg CE, Khare SD, Dou J, Doyle L, Nelson JW et al. 2013. Computational design of ligand-binding proteins with high affinity and selectivity. Nature 501:7466212–16
    [Google Scholar]
  138. 137. 
    Toda S, Blauch LR, Tang SKY, Morsut L, Lim WA 2018. Programming self-organizing multicellular structures with synthetic cell-cell signaling. Science 361:6398156–62
    [Google Scholar]
  139. 138. 
    Uchida N, Takahashi K, Iwasaki R, Yamada R, Yoshimura M et al. 2018. Chemical hijacking of auxin signaling with an engineered auxin-TIR1 pair. Nat. Chem. Biol. 14:3299–305An orthogonal synthetic ligand-receptor pair that connects to the endogenous auxin response pathway was developed using a bump-and-hole strategy.
    [Google Scholar]
  140. 139. 
    Vain T, Raggi S, Ferro N, Barange DK, Kieffer M et al. 2019. Selective auxin agonists induce specific AUX/IAA protein degradation to modulate plant development. PNAS 116:136463–72
    [Google Scholar]
  141. 140. 
    Vazquez-Vilar M, Quijano-Rubio A, Fernandez-del-Carmen A, Sarrion-Perdigones A, Ochoa-Fernandez R et al. 2017. GB3.0: a platform for plant bio-design that connects functional DNA elements with associated biological data. Nucleic Acids Res 45:42196–209
    [Google Scholar]
  142. 141. 
    Vergunst AC, Jansen LET, Hooykaas PJJ 1998. Site-specific integration of Agrobacterium T-DNA in Arabidopsis thaliana mediated by Cre recombinase. Nucleic Acids Res 26:112729–34
    [Google Scholar]
  143. 142. 
    Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J et al. 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8:161
    [Google Scholar]
  144. 143. 
    Waadt R, Kudla J. 2008. In planta visualization of protein interactions using bimolecular fluorescence complementation (BiFC). CSH Protoc 2008:pdb.prot4995
    [Google Scholar]
  145. 144. 
    Walia A, Waadt R, Jones AM 2018. Genetically encoded biosensors in plants: pathways to discovery. Annu. Rev. Plant Biol. 69:497–524
    [Google Scholar]
  146. 145. 
    Wang T, Liang L, Xue Y, Jia P-F, Chen W et al. 2016. A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:7593241–44
    [Google Scholar]
  147. 146. 
    Weber W, Daoud-El Baba M, Fussenegger M 2007. Synthetic ecosystems based on airborne inter- and intrakingdom communication. PNAS 104:2510435–40
    [Google Scholar]
  148. 147. 
    Weinberg BH, Pham NTH, Caraballo LD, Lozanoski T, Engel A et al. 2017. Large-scale design of robust genetic circuits with multiple inputs and outputs for mammalian cells. Nat. Biotechnol. 35:5453–62
    [Google Scholar]
  149. 148. 
    Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ 2007. An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLOS ONE 2:8e718
    [Google Scholar]
  150. 149. 
    Wu C-Y, Roybal KT, Puchner EM, Onuffer J, Lim WA 2015. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science 350:6258aab4077
    [Google Scholar]
  151. 150. 
    Wullschleger SD, Weston DJ, DiFazio SP, Tuskan GA 2013. Revisiting the sequencing of the first tree genome. Populus trichocarpa. Tree Physiol. 33:4357–64
    [Google Scholar]
  152. 151. 
    Xin C-P, Tholen D, Devloo V, Zhu X-G 2015. The benefits of photorespiratory bypasses: How can they work?. Plant Physiol 167:2574–85
    [Google Scholar]
  153. 152. 
    Zalatan JG, Lee ME, Almeida R, Gilbert LA, Whitehead EH et al. 2015. Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160:1–2339–50
    [Google Scholar]
  154. 153. 
    Zimny T, Sowa S, Tyczewska A, Twardowski T 2019. Certain new plant breeding techniques and their marketability in the context of EU GMO legislation—recent developments. New Biotechnol 51:49–56
    [Google Scholar]
  155. 154. 
    Zúñiga A, Guiziou S, Mayonove P, Meriem ZB, Camacho M et al. 2019. Rational programming of history-dependent logic in cellular populations. bioRxiv 617209. https://doi.org/10.1101/617209
    [Crossref]
  156. 155. 
    Zuo J, Niu QW, Chua N-H 2000. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24:2265–73
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081519-035852
Loading
/content/journals/10.1146/annurev-arplant-081519-035852
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error