Synthetic biology approaches for improving photosynthesis

Journal of Experimental Botany

Volumn 70, Issue 5, 2019, Pages 1425-1433

  Kubis, Armin ^a   Bar Even, Arren ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

C 4 metabolism; Calvin cycle; carbon fixation; carbon concentrating mechanisms; photorespiration; Rubisco

Indexed keywords

EID: 85062874159     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erz029     Document Type: Review

References (112)

1. Aigner H, Wilson RH, Bracher A, Calisse L, Bhat JY, Hartl FU, Hayer-Hartl M. 2017. Plant RuBisCo assembly in E. coli with fve chloroplast chap-erones including BSD2. Science 358, 1272-1278.
2. Ainsworth EA. 2008. Rice production in a changing climate: a meta-analy-sis of responses to elevated carbon dioxide and elevated ozone concentration. Global Change Biology 14, 1642-1650.
3. Anderson LE. 1971. Chloroplast and cytoplasmic enzymes. II. Pea leaf triose phosphate isomerases. Biochimica et Biophysica Acta 235, 237-244.
4. Atkinson N, Feike D, Mackinder LC, Meyer MT, Griffths H, Jonikas MC, Smith AM, McCormick AJ. 2016. Introducing an algal car-bon-concentrating mechanism into higher plants: location and incorpora-tion of key components. Plant Biotechnology Journal 14, 1302-1315.
5. 4 pathway. Journal of Experimental Botany 62, 3049-3059.
6. Bar-Even A. 2018. Daring metabolic designs for enhanced plant carbon fxation. Plant Science 273, 71-83.
7. Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, Tawfk DS, Milo R. 2011. The moderately effcient enzyme: evolutionary and physico-chemical trends shaping enzyme parameters. Biochemistry 50, 4402-4410.
8. Boehm CR, Bock R. 2018. Recent advances and current challenges in synthetic biology of the plastid genetic system and metabolism. Plant Physiology 3, 00767.2018.
9. Borland AM, Barrera Zambrano VA, Ceusters J, Shorrock K. 2011. The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytologist 191, 619-633.
10. Borland AM, Griffths H, Hartwell J, Smith JA. 2009. Exploiting the potential of plants with crassulacean acid metabolism for bioenergy pro-duction on marginal lands. Journal of Experimental Botany 60, 2879-2896.
11. Borland AM, Hartwell J, Weston DJ, Schlauch KA, Tschaplinski TJ, Tuskan GA, Yang X, Cushman JC. 2014. Engineering crassulacean acid metabolism to improve water-use effciency. Trends in Plant Science 19, 327-338.
12. 3 species Arabidopsis thaliana, and are important in sugar and amino acid metabolism. The Plant Journal 61, 122-133.
13. Campbell WJ, Ogren WL. 1990. Glyoxylate inhibition of ribulosebisphos-phate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynthesis Research 23, 257-268.
14. Chastain CJ, Ogren WL. 1989. Glyoxylate inhibition of ribulosebi-sphosphate carboxylase/oxygenase activation state in vivo. Plant & Cell Physiology 30, 937-944.
15. Cummins PL, Kannappan B, Gready JE. 2018. Directions for optimization of photosynthetic carbon fxation: RuBisCO's effciency may not be so constrained after all. Frontiers in Plant Science 9, 183.
16. Dalal J, Lopez H, Vasani NB, et al. 2015. A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa. Biotechnology for Biofuels 8, 175.
17. DePaoli HC, Borland AM, Tuskan GA, Cushman JC, Yang X. 2014. Synthetic biology as it relates to CAM photosynthesis: challenges and opportunities. Journal of Experimental Botany 65, 3381-3393.
18. Eisenhut M, Bauwe H, Hagemann M. 2007. Glycine accumulation is toxic for the cyanobacterium Synechocystis sp. strain PCC 6803, but can be compensated by supplementation with magnesium ions. FEMS Microbiology Letters 277, 232-237.
19. Eisenhut M, Kahlon S, Hasse D, Ewald R, Lieman-Hurwitz J, Ogawa T, Ruth W, Bauwe H, Kaplan A, Hagemann M. 2006. The plantlike C2 glycolate cycle and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiology 142, 333-342.
20. Ellis RJ. 1979. The most abundant protein in the world. Trends in Biochemical Sciences 4, 241-244.
21. FAO. 2018. FAOSTAT database. http://www.fao.org/faostat. (last accessed 1 October 2018)
22. Fletcher AL, Brown HE, Johnstone PR, de Ruiter JM, Zyskowski RF. 2011. Making sense of yield trade-offs in a crop sequence: a New Zealand case study. Field Crops Research 124, 149-156.
23. Flügel F, Timm S, Arrivault S, Florian A, Stitt M, Fernie AR, Bauwe H. 2017. The photorespiratory metabolite 2-phosphoglycolate regulates pho-tosynthesis and starch accumulation in Arabidopsis. The Plant Cell 29, 2537-2551.
24. Galmés J, Kapralov MV, Andralojc PJ, Conesa MÀ, Keys AJ, Parry MA, Flexas J. 2014. Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant, Cell & Environment 37, 1989-2001.
25. Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C. 2010. Food security: the challenge of feeding 9 billion people. Science 327, 812-818.
26. Haber F, Le Rossignol R. 1909. Production of ammonia. Patent no. US1202995A, fled 13 August 1909, issued 31 October 1916.
27. Hausler RE, Bailey KJ, Lea PJ, Leegood RC. 1996. Control of photosynthesis in barley mutants with reduced activities of glutamine synthetase and glutamate synthase III. Aspects of glyoxylate metabolism and effects of glyoxylate on the activation. Planta 44, 388-396.
28. 2 assimilation using a cyanobacterial membrane protein, ictB. Journal of Plant Physiology 212, 58-68.
29. Heineke D, Bykova N, Gardeström P, Bauwe H. 2001. Metabolic response of potato plants to an antisense reduction of the P-protein of gly-cine decarboxylase. Planta 212, 880-887.
30. 3 fowering plants. Nature 415, 451-454.
31. Hibberd JM, Sheehy JE, Langdale JA. 2008. Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. Current Opinion in Plant Biology 11, 228-231.
32. 4 photosynthesis: a model describing the inorganic carbon pool in bundle sheath cells. Plant Physiology 91, 1372-1381.
33. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C. 2007. Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nature Biotechnology 25, 593-599.
34. Khush GS. 2001. Green revolution: the way forward. Nature Reviews. Genetics 2, 815-822.
35. Koester RP, Nohl BM, Diers BW, Ainsworth EA. 2016. Has photosyn-thetic capacity increased with 80 years of soybean breeding? An examination of historical soybean cultivars. Plant, Cell & Environment 39, 1058-1067.
36. Kumar A, Li C, Portis AR Jr. 2009. Arabidopsis thaliana expressing a ther-mostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynthesis Research 100, 143-153.
37. 2-concentrating mechanism in cyanobacterial photosynthesis: organization, physiological role, and evolutionary origin. Photosynthesis Research 117, 133-146.
38. Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G. 2007. Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. The Plant Cell 19, 3230-3241.
39. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA, Fryer M. 2005. Increased sedoheptulose-1, 7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiology 138, 451-460.
40. Lieman-Hurwitz J, Asipov L, Rachmilevitch S, Marcus Y, Kaplan A. 2005. Expression of cyanobacterial ictB in higher plants enhanced pho-tosynthesis and growth. In: Omasa K, Nouchi I, De Kok LJ, eds. Plant responses to air pollution and global change. Tokyo: Springer Japan, 133-139.
41. - accumulation in cyanobacteria. Plant Biotechnology Journal 1, 43-50.
42. Lin MT, Occhialini A, Andralojc PJ, Parry MA, Hanson MR. 2014. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513, 547-550.
43. Liu W, Stewart CN Jr. 2015. Plant synthetic biology. Trends in Plant Science 20, 309-317.
44. 2-fxing enzyme Rubisco in tobacco chloroplasts. Nature Communications 9, 3570.
45. 2-concentrating mechanism components: function and prospects for plant metabolic engineering. Current Opinion in Plant Biology 31, 1-8.
46. Long SP, Zhu XG, Naidu SL, Ort DR. 2006. Can improvement in pho-tosynthesis increase crop yields? Plant, Cell & Environment 29, 315-330.
47. López-Calcagno PE, Fisk S, Brown KL, Bull SE, South PF, Raines CA. 2019. Overexpressing the H-protein of the glycine cleavage system increases biomass yield in glasshouse and feld-grown transgenic tobacco plants. Plant Biotechnology Journal 17, 141-151.
48. 2+. Biochemistry 19, 5321-5328.
49. 13C fux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation. Proceedings of the National Academy of Sciences, USA 111, 16967-16972.
50. 2-concentrating mech-anism and its potential for engineering photosynthesis in plants. New Phytologist 217, 54-61.
51. Maier A, Fahnenstich H, von Caemmerer S, Engqvist MK, Weber AP, Flügge UI, Maurino VG. 2012. Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Frontiers in Plant Science 3, 38.
52. 2 concentrating mechanism. Proceedings of the National Academy of Sciences, USA 113, E5354-E5362.
53. 2 concentration on growth and nitrogen use in tobacco (Nicotiana tabacum) plants transformed with an antisense gene to the small subunit of ribulose-1, 5-bis-phosphate carboxylase/oxygenase. Plant Physiology 103, 1075-1088.
54. McGrath JM, Long SP. 2014. Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiology 164, 2247-2261.
55. Miyagawa Y, Tamoi M, Shigeoka S. 2001. Overexpression of a cyano-bacterial fructose-1, 6-/sedoheptulose-1, 7-bisphosphatase in tobacco enhances photosynthesis and growth. Nature Biotechnology 19, 965-969.
56. 4 intermediate photosynthesis in plants. BioScience 34, 563-574.
57. Monteith JL, Moss CJ. 1977. Climate and the effciency of crop production in Britain. Philosophical Transactions of the Royal Society B: Biological Sciences 281, 277-294.
58. Nölke G, Houdelet M, Kreuzaler F, Peterhänsel C, Schillberg S. 2014. The expression of a recombinant glycolate dehydrogenase polyprotein in potato (Solanum tuberosum) plastids strongly enhances photosynthesis and tuber yield. Plant Biotechnology Journal 12, 734-742.
59. 2. The Plant Journal 85, 148-160.
60. Oliver DJ. 1980. The effect of glyoxylate on photosynthesis and photores-piration by isolated soybean mesophyll cells. Plant Physiology 65, 888-892.
61. Oliver DJ, Zelitch I. 1977. Increasing photosynthesis by inhibiting pho-torespiration with glyoxylate. Science 196, 1450-1451.
62. Orr DJ, Alcântara A, Kapralov MV, Andralojc PJ, Carmo-Sasilva E, Parry MA. 2016. Surveying rubisco diversity and temperature response to improve crop photosynthetic effciency. Plant Physiology 172, 707-717.
63. Ort DR, Merchant SS, Alric J, et al. 2015. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proceedings of the National Academy of Sciences, USA 112, 8529-8536.
64. Parry MA, Keys AJ, Madgwick PJ, Carmo-Silva AE, Andralojc PJ. 2008. Rubisco regulation: a role for inhibitors. Journal of Experimental Botany 59, 1569-1580.
65. Peng S, Tang Q, Zou Y. 2009. Current status and challenges of rice production in China. Plant Production Science 12, 3-8.
66. Piatek AA, Lenaghan SC, Neal Stewart C Jr. 2018. Advanced editing of the nuclear and plastid genomes in plants. Plant Science 273, 42-49.
67. Portis AR Jr. 2003. Rubisco activase-Rubisco's catalytic chaperone. Photosynthesis Research 75, 11-27.
68. 2-concentrating mechanism into higher plants. Journal of Experimental Botany 68, 3717-3737.
69. Raven J. 2009. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fuxes in aquatic environments. Aquatic Microbial Ecology 56, 177-192.
70. Raven JA. 2013. Rubisco: still the most abundant protein of Earth? New Phytologist 198, 1-3.
71. 4 intermediate species Moricandia arvensis (L.) DC. Planta 176, 527-532.
72. Ray DK, Ramankutty N, Mueller ND, West PC, Foley JA. 2012. Recent patterns of crop yield growth and stagnation. Nature Communications 3, 1293.
73. Rolland V, Badger MR, Price GD. 2016. Redirecting the cyanobacte-rial bicarbonate transporters BicA and SbtA to the chloroplast envelope: soluble and membrane cargos need different chloroplast targeting signals in plants. Frontiers in Plant Science 7, 185.
74. 2 fumigation (FACE). BMC Plant Biology 11, 123.
75. 4 photosynthesis. Annual Review of Plant Biology 63, 19-47.
76. Salvucci ME, Crafts-Brandner SJ. 2004. Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiology 134, 1460-1470.
77. Savir Y, Noor E, Milo R, Tlusty T. 2010. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. Proceedings of the National Academy of Sciences, USA 107, 3475-3480.
78. 4 photosynthesis: evolution of a complex trait via intermediary states. Plant & Cell Physiology 57, 881-889.
79. 3 chassis in the synthetic biology age. The Plant Journal 87, 51-65.
80. Schwander T, Schada von Borzyskowski L, Burgener S, Cortina NS, Erb TJ. 2016. A synthetic pathway for the fxation of carbon dioxide in vitro. Science 354, 900-904.
81. Servaites JC, Ogren WL 1977. Chemical inhibition of the glycolate pathway in soybean leaf cells. Plant Physiology 60, 461-466.
82. 2-fxing photorespiratory bypass into a cyanobacterium. Journal of Biological Chemistry 289, 9493-9500.
83. 2 fxation and biomass yield in tobacco. Journal of Experimental Botany 66, 4075-4090.
84. Somerville CR, Ogren WL. 1979. A phosphoglycolate phosphatase-def-cient mutant of Arabidopsis. Nature 280, 833-836.
85. Somerville CR, Ogren WL. 1982. Genetic modifcation of photorespira-tion. Trends in Biochemical Sciences 7, 171-174.
86. South PF, Cavanagh AP, Liu HW, Ort DR. 2019. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the feld. Science 363, eaat9077.
87. Spreitzer RJ, Peddi SR, Satagopan S. 2005. Phylogenetic engineering at an interface between large and small subunits imparts land-plant kinetic properties to algal Rubisco. Proceedings of the National Academy of Sciences, USA 102, 17225-17230.
88. Sutton MA, Simpson D, Levy PE, Smith RI, Reis S, van Oijen M, de Vries W. 2008. Uncertainties in the relationship between atmospheric nitrogen deposition and forest carbon sequestration. Global Change Biology 14, 2057-2063.
89. Tcherkez GGB, Farquhar GD, Andrews TJ. 2006. Despite slow catalysis and confused substrate specifcity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences, USA 103, 7246-7251.
90. Tilman D, Balzer C, Hill J, Befort BL. 2011. Global food demand and the sustainable intensifcation of agriculture. Proceedings of the National Academy of Sciences, USA 108, 20260-20264.
91. Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H. 2012. Glycine decarboxylase controls photosynthesis and plant growth. FEBS Letters 586, 3692-3697.
92. Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H. 2015. Mitochondrial dihydrolipoyl dehydro-genase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. The Plant Cell 27, 1968-1984.
93. Trudeau DL, Edlich-Muth C, Zarzycki J, et al. 2018. Design and in vitro realization of carbon-conserving photorespiration. Proceedings of the National Academy of Sciences, USA 115, E11455-E11464.
94. Uehara S, Adachi F, Ito-Inaba Y, Inaba T. 2016. Specifc and effcient targeting of cyanobacterial bicarbonate transporters to the inner envelope membrane of chloroplasts in Arabidopsis. Frontiers in Plant Science 7, 16.
95. Uematsu K, Suzuki N, Iwamae T, Inui M, Yukawa H. 2012. Increased fructose 1, 6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. Journal of Experimental Botany 63, 3001-3009.
96. Vazquez-Vilar M, Orzaez D, Patron N. 2018. DNA assembly standards: setting the low-level programming code for plant biotechnology. Plant Science 273, 33-41.
97. Whitney SM, Andrews TJ. 2001. Plastome-encoded bacterial ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO) supports photosynthesis and growth in tobacco. Proceedings of the National Academy of Sciences, USA 98, 14738-14743.
98. 4 catalytic switch that increases ribulose-1, 5-bisphosphate carboxylase/oxygenase (rubisco) carboxylation rate in Flaveria. Proceedings of the National Academy of Sciences, USA 108, 14688-14693.
99. Wilson RH, Alonso H, Whitney SM. 2016. Evolving Methanococcoides burtonii archaeal Rubisco for improved photosynthesis and plant growth. Scientifc Reports 6, 22284.
100. Wingler A, Lea PJ, Leegood RC. 1997. Control of photosynthesis in barley plants with reduced activities of glycine decarboxylase. Planta 202, 171-178.
101. Xin CP, Tholen D, Devloo V, Zhu XG. 2015. The benefts of photorespira-tory bypasses: how can they work? Plant Physiology 167, 574-585.
102. Yamori W, Masumoto C, Fukayama H, Makino A. 2012. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. The Plant Journal 71, 871-880.
103. Yang S-M, Chang C-Y, Yanagisawa M, Park I, Tseng T-H, Ku MSB. 2008. Transgenic rice expressing cyanobacterial bicarbonate transporter exhibited enhanced photosynthesis, growth and grain yield. In: Allen JF, Gantt E, Golbeck JH, Osmond B, eds. Photosynthesis. Energy from the Sun. Dordrecht: Springer Netherlands, 1243-1246.
104. Yang X, Cushman JC, Borland AM, et al. 2015. A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytologist 207, 491-504.
105. Yin X, Struik PC. 2017. Can increased leaf photosynthesis be converted into higher crop mass production? A simulation study for rice using the crop model GECROS. Journal of Experimental Botany 68, 2345-2360.
106. Yokota A. 1991. Carboxylation and detoxifcation of xylulose bisphosphate by spinach ribulose bisphosphate carboxylase/oxygenase. Plant & Cell Physiology 32, 755-762.
107. Young JN, Heureux AM, Sharwood RE, Rickaby RE, Morel FM, Whitney SM. 2016. Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. Journal of Experimental Botany 67, 3445-3456.
108. Yu H, Li X, Duchoud F, Chuang DS, Liao JC. 2018. Augmenting the Calvin-Benson-Bassham cycle by a synthetic malyl-CoA-glycerate carbon fxation pathway. Nature Communications 9, 2008.
109. Zhu G, Jensen RG. 1991. Xylulose 1, 5-bisphosphate synthesized by ribu-lose 1, 5-bisphosphate carboxylase/oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiology 97, 1348-1353.
110. Zhu XG, de Sturler E, Long SP. 2007. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiology 145, 513-526.
111. Zhu XG, Long SP, Ort DR. 2010. Improving photosynthetic effciency for greater yield. Annual Review of Plant Biology 61, 235-261.
112. 3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant, Cell & Environment 27, 155-165.