1932

Abstract

Although cyanobacteria and algae represent a small fraction of the biomass of all primary producers, their photosynthetic activity accounts for roughly half of the daily CO fixation that occurs on Earth. These microorganisms are able to accomplish this feat by enhancing the activity of the CO-fixing enzyme Rubisco using biophysical CO concentrating mechanisms (CCMs). Biophysical CCMs operate by concentrating bicarbonate and converting it into CO in a compartment that houses Rubisco (in contrast with other CCMs that concentrate CO via an organic intermediate, such as malate in the case of C CCMs). This activity provides Rubisco with a high concentration of its substrate, thereby increasing its reaction rate. The genetic engineering of a biophysical CCM into land plants is being pursued as a strategy to increase crop yields. This review focuses on the progress toward understanding the molecular components of cyanobacterial and algal CCMs, as well as recent advances toward engineering these components into land plants.

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2020-04-29
2024-05-02
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Literature Cited

  1. 1. 
    Ainsworth EA, Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–71
    [Google Scholar]
  2. 2. 
    Antal TK, Kovalenko IB, Rubin AB, Tyystjarvi E 2013. Photosynthesis-related quantities for education and modeling. Photosynth. Res. 117:1–30
    [Google Scholar]
  3. 3. 
    Atkinson N, Feike D, Mackinder LCM, Meyer MT, Griffiths H et al. 2016. Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol. J. 14:1302–15Several algal CCM components could localize to their corresponding subcellular compartments in tobacco and Arabidopsis.
    [Google Scholar]
  4. 4. 
    Atkinson N, Leitão N, Orr DJ, Meyer MT, Carmo-Silva E et al. 2017. Rubisco small subunits from the unicellular green alga Chlamydomonas complement Rubisco-deficient mutants of Arabidopsis. New Phytol 214:2655–67
    [Google Scholar]
  5. 5. 
    Atkinson N, Velanis CN, Wunder T, Clarke DJ, Mueller-Cajar O, McCormick AJ 2019. The pyrenoidal linker protein EPYC1 phase separates with hybrid Arabidopsis–Chlamydomonas Rubisco through interactions with the algal Rubisco small subunit. J. Exp. Bot. 70:5271–85
    [Google Scholar]
  6. 6. 
    Aubry S, Brown NJ, Hibberd JM 2011. The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J. Exp. Bot. 62:3049–59
    [Google Scholar]
  7. 7. 
    Badger MR, Price GD. 2003. CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J. Exp. Bot. 54:609–22
    [Google Scholar]
  8. 8. 
    Badger MR, Price GD, Long BM, Woodger FJ 2006. The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J. Exp. Bot. 57:2249–65
    [Google Scholar]
  9. 9. 
    Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D et al. 2011. The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50:4402–10
    [Google Scholar]
  10. 10. 
    Battchikova N, Eisenhut M, Aro E-M 2011. Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim. Biophys. Acta Bioenerget. 1807:935–44
    [Google Scholar]
  11. 11. 
    Bonacci W, Teng PK, Afonso B, Niederholtmeyer H, Grob P et al. 2012. Modularity of a carbon-fixing protein organelle. PNAS 109:478–83
    [Google Scholar]
  12. 12. 
    Borkhsenious ON, Mason CB, Moroney JV 1998. The intracellular localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. Plant Physiol 116:1585–91
    [Google Scholar]
  13. 13. 
    Cai F, Bernstein SL, Wilson SC, Kerfeld CA 2016. Production and characterization of synthetic carboxysome shells with incorporated luminal proteins. Plant Physiol 170:1868–77
    [Google Scholar]
  14. 14. 
    Cai F, Dou Z, Bernstein SL, Leverenz R, Williams EB et al. 2015. Advances in understanding carboxysome assembly in Prochlorococcus and Synechococcus implicate CsoS2 as a critical component. Life 5:1141–71
    [Google Scholar]
  15. 15. 
    Cameron JC, Wilson SC, Bernstein SL, Kerfeld CA 2013. Biogenesis of a bacterial organelle: the carboxysome assembly pathway. Cell 155:1131–40Observing β-carboxysome formation in Δccm cells expressing truncated ccm operons provided key insights into the order of assembly of β-carboxysomes.
    [Google Scholar]
  16. 16. 
    Caspari OD, Meyer MT, Tolleter D, Wittkopp TM, Cunniffe NJ et al. 2017. Pyrenoid loss in Chlamydomonas reinhardtii causes limitations in CO2 supply, but not thylakoid operating efficiency. J. Exp. Bot. 68:3903–13
    [Google Scholar]
  17. 17. 
    Chaijarasphong T, Nichols RJ, Kortright KE, Nixon CF, Teng PK et al. 2016. Programmed ribosomal frameshifting mediates expression of the α-carboxysome. J. Mol. Biol. 428:153–64
    [Google Scholar]
  18. 18. 
    DiMario RJ, Clayton H, Mukherjee A, Ludwig M, Moroney JV 2017. Plant carbonic anhydrases: structures, locations, evolution, and physiological roles. Mol. Plant 10:30–46
    [Google Scholar]
  19. 19. 
    Du J, Förster B, Rourke L, Howitt SM, Price GD 2014. Characterisation of cyanobacterial bicarbonate transporters in E. coli shows that SbtA homologs are functional in this heterologous expression system. PLOS ONE 9:e115905
    [Google Scholar]
  20. 20. 
    Duanmu D, Miller AR, Horken KM, Weeks DP, Spalding MH 2009. Knockdown of limiting-CO2–induced gene HLA3 decreases HCO3 transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii. PNAS 106:5990–95
    [Google Scholar]
  21. 21. 
    Edwards GE, Franceschi VR, Voznesenskaya EV 2004. Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu. Rev. Plant Biol. 55:173–96
    [Google Scholar]
  22. 22. 
    Engel BD, Schaffer M, Kuhn Cuellar L, Villa E, Plitzko JM, Baumeister W 2015. Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. eLife 4:e04889
    [Google Scholar]
  23. 23. 
    Fang Y, Huang F, Faulkner M, Jiang Q, Dykes GF et al. 2018. Engineering and modulating functional cyanobacterial CO2-fixing organelles. Front. Plant Sci. 9:739A synthetic β-carboxysome with functional Rubisco was assembled in E. coli using 12 genes from the β-cyanobacterium Synechococcuselongatus PCC7942.
    [Google Scholar]
  24. 24. 
    Fett JP, Coleman JR. 1994. Regulation of periplasmic carbonic anhydrase expression in Chlamydomonas reinhardtii by acetate and pH. Plant Physiol 106:1103–8
    [Google Scholar]
  25. 25. 
    Field CB, Behrenfeld MJ, Randerson JT, Falkowski P 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–40
    [Google Scholar]
  26. 26. 
    Findinier J, Laurent S, Duchêne T, Roussel X, Lancelon-Pin C et al. 2019. Deletion of BSG1 in Chlamydomonas reinhardtii leads to abnormal starch granule size and morphology. Sci. Rep. 9:1990
    [Google Scholar]
  27. 27. 
    Flamholz AI, Prywes N, Moran U, Davidi D, Bar-On YM et al. 2019. Revisiting trade-offs between Rubisco kinetic parameters. Biochemistry 58:3365–76
    [Google Scholar]
  28. 28. 
    Freeman Rosenzweig ES, Xu B, Kuhn Cuellar L, Martinez-Sanchez A, Schaffer M et al. 2017. The eukaryotic CO2-concentrating organelle is liquid-like and exhibits dynamic reorganization. Cell 171:148–62.e19The Chlamydomonas pyrenoid matrix has liquid-like properties, and a portion disperses at the end of each cell cycle.
    [Google Scholar]
  29. 29. 
    Furbank RT. 2016. Walking the C4 pathway: past, present, and future. J. Exp. Bot. 67:4057–66
    [Google Scholar]
  30. 30. 
    García MA, Martino MN, Zaritzky NE 1999. Edible starch films and coatings characterization: scanning electron microscopy, water vapor, and gas permeabilities. Scanning 21:348–53
    [Google Scholar]
  31. 31. 
    Ghannoum O, Evans JR, von Caemmerer S 2010. Nitrogen and water use efficiency of C4 plants. C4 Photosynthesis and Related CO2 Concentrating Mechanisms 32 A Raghavendra, R Sage 129–146 Dordrecht, Neth: Springer
    [Google Scholar]
  32. 32. 
    Guzmán-Zapata D, Sandoval-Vargas JM, Macedo-Osorio KS, Salgado-Manjarrez E, Castrejón-Flores JL et al. 2019. Efficient editing of the nuclear APT reporter gene in Chlamydomonas reinhardtii via expression of a CRISPR-Cas9 module. Int. J. Mol. Sci. 20:1247
    [Google Scholar]
  33. 33. 
    Hanson MR, Gray BN, Ahner BA 2013. Chloroplast transformation for engineering of photosynthesis. J. Exp. Bot. 64:731–42
    [Google Scholar]
  34. 34. 
    Herdean A, Teardo E, Nilsson AK, Pfeil BE, Johansson ON et al. 2016. A voltage-dependent chloride channel fine-tunes photosynthesis in plants. Nat. Commun. 7:11654
    [Google Scholar]
  35. 35. 
    Ho C, Sturtevant JM. 1963. The kinetics of the hydration of carbon dioxide at 25°. J. Biol. Chem. 238:3499–501
    [Google Scholar]
  36. 36. 
    Iancu CV, Morris DM, Dou Z, Heinhorst S, Cannon GC, Jensen GJ 2010. Organization, structure, and assembly of α-carboxysomes determined by electron cryotomography of intact cells. J. Mol. Biol. 396:105–17
    [Google Scholar]
  37. 37. 
    Itakura AK, Chan KX, Atkinson N, Pallesen L, Wang L et al. 2019. A Rubisco-binding protein is required for normal pyrenoid number and starch sheath morphology in Chlamydomonas reinhardtii. PNAS 116:18445–54
    [Google Scholar]
  38. 38. 
    Jablonski LM, Wang X, Curtis PS 2002. Plant reproduction under elevated CO2 conditions: a meta‐analysis of reports on 79 crop and wild species. New Phytol 156:9–26
    [Google Scholar]
  39. 39. 
    Jin S, Sun J, Wunder T, Tang D, Cousins AB et al. 2016. Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases. PNAS 113:14716–21
    [Google Scholar]
  40. 40. 
    Kerfeld CA, Melnicki M. 2016. Assembly, function and evolution of cyanobacterial carboxysomes. Curr. Opin. Plant Biol. 31:66–75
    [Google Scholar]
  41. 41. 
    Khalifah RG. 1971. The carbon dioxide hydration activity of carbonic anhydrase. I. Stop-flow kinetic studies on the native human isoenzymes B and C. J. Biol. Chem. 246:2561–73
    [Google Scholar]
  42. 42. 
    Kim E-J, Cerutti H. 2009. Targeted gene silencing by RNA interference in Chlamydomonas. Methods Cell Biol 93:99–110
    [Google Scholar]
  43. 43. 
    Kinney JN, Axen SD, Kerfeld CA 2011. Comparative analysis of carboxysome shell proteins. Photosynth. Res. 109:21–32
    [Google Scholar]
  44. 44. 
    Kinney JN, Salmeen A, Cai F, Kerfeld CA 2012. Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J. Biol. Chem. 287:17729–36
    [Google Scholar]
  45. 45. 
    Larsson AM, Hasse D, Valegård K, Andersson I 2017. Crystal structures of β-carboxysome shell protein CcmP: Ligand binding correlates with the closed or open central pore. J. Exp. Bot. 68:3857–67
    [Google Scholar]
  46. 46. 
    Li X, Patena W, Fauser F, Jinkerson RE, Saroussi S et al. 2019. A genome-wide algal mutant library and functional screen identifies genes required for eukaryotic photosynthesis. Nat. Genet. 51:627–35
    [Google Scholar]
  47. 47. 
    Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR 2014. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513:547–50
    [Google Scholar]
  48. 48. 
    Liu Y, He X, Lim W, Mueller J, Lawrie J et al. 2018. Deciphering molecular details in the assembly of alpha-type carboxysome. Sci. Rep. 8:15062
    [Google Scholar]
  49. 49. 
    Long BM, Badger MR, Whitney SM, Price GD 2007. Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J. Biol. Chem. 282:29323–35
    [Google Scholar]
  50. 50. 
    Long BM, Hee WY, Sharwood RE, Rae BD, Kaines S et al. 2018. Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nat. Commun. 9:3570α-Carboxysome-like structures were formed in tobacco chloroplasts through transformation of a minimal gene set.
    [Google Scholar]
  51. 51. 
    Long BM, Rae BD, Badger MR, Price GD 2011. Over-expression of the β-carboxysomal CcmM protein in Synechococcus PCC7942 reveals a tight co-regulation of carboxysomal carbonic anhydrase (CcaA) and M58 content. Photosynth. Res. 109:33–45
    [Google Scholar]
  52. 52. 
    Long BM, Tucker L, Badger MR, Price GD 2010. Functional cyanobacterial β-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein. Plant Physiol 153:285–93
    [Google Scholar]
  53. 53. 
    Long SP, Marshall-Colon A, Zhu X-G 2015. Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell 161:56–66
    [Google Scholar]
  54. 54. 
    Machingura MC, Bajsa-Hirschel J, Laborde SM, Schwartzenburg JB, Mukherjee B et al. 2017. Identification and characterization of a solute carrier, CIA8, involved in inorganic carbon acclimation in Chlamydomonas reinhardtii. J. Exp. Bot 68:3879–90
    [Google Scholar]
  55. 55. 
    Mackinder LCM, Chen C, Leib RD, Patena W, Blum SR et al. 2017. A spatial interactome reveals the protein organization of the algal CO2-concentrating mechanism. Cell 171:133–47.e14This protein–protein interactome study in Chlamydomonas has illuminated multiple novel interactions in the algal CCM.
    [Google Scholar]
  56. 56. 
    Mackinder LCM, Meyer MT, Mettler-Altmann T, Chen VK, Mitchell MC et al. 2016. A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle. PNAS 113:5958–63
    [Google Scholar]
  57. 57. 
    Mahinthichaichan P, Morris DM, Wang Y, Jensen GJ, Tajkhorshid E 2018. Selective permeability of carboxysome shell pores to anionic molecules. J. Phys. Chem. B 122:9110–18
    [Google Scholar]
  58. 58. 
    Mangan NM, Flamholz A, Hood RD, Milo R, Savage DF 2016. pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism. PNAS 113:E5354–62
    [Google Scholar]
  59. 59. 
    Mariscal V, Moulin P, Orsel M, Miller AJ, Fernández E, Galván A 2006. Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. Protist 157:421–33
    [Google Scholar]
  60. 60. 
    McCloskey MA, Duanmu D, Benge N, Spalding MH 2017. The HLA3 protein of C. reinhardtii enhances HCO3-transport activity of mammalian cells. Biophys. J. 112:571A
    [Google Scholar]
  61. 61. 
    McGrath JM, Long SP. 2014. Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164:2247–61
    [Google Scholar]
  62. 62. 
    McGurn LD, Moazami-Goudarzi M, White SA, Suwal T, Brar B et al. 2016. The structure, kinetics and interactions of the β-carboxysomal β-carbonic anhydrase, CcaA. Biochem. J. 473:4559–72
    [Google Scholar]
  63. 63. 
    Meyer MT, Genkov T, Skepper JN, Jouhet J, Mitchell MC et al. 2012. Rubisco small-subunit α-helices control pyrenoid formation in Chlamydomonas. PNAS 109:19474–79
    [Google Scholar]
  64. 64. 
    Meyer MT, Whittaker C, Griffiths H 2017. The algal pyrenoid: key unanswered questions. J. Exp. Bot. 68:3739–49
    [Google Scholar]
  65. 65. 
    Moroney JV, Ma Y, Frey WD, Fusilier KA, Pham TT et al. 2011. The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosynth. Res. 109:133–49
    [Google Scholar]
  66. 66. 
    Moroney JV, Ynalvez RA. 2007. Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii.Eukaryot. Cell 6:1251–59
    [Google Scholar]
  67. 67. 
    Mukherjee A, Lau CS, Walker CE, Rai AK, Prejean CI et al. 2019. Thylakoid localized bestrophin-like proteins are essential for the CO2 concentrating mechanism of Chlamydomonas reinhardtii. PNAS 116:16915–20
    [Google Scholar]
  68. 68. 
    Ohnishi N, Mukherjee B, Tsujikawa T, Yanase M, Nakano H et al. 2010. Expression of a low CO2-inducible protein, LCI1, increases inorganic carbon uptake in the green alga Chlamydomonas reinhardtii. Plant Cell 22:3105–17
    [Google Scholar]
  69. 69. 
    Pengelly JJL, Förster B, von Caemmerer S, Badger MR, Price GD, Whitney SM 2014. Transplastomic integration of a cyanobacterial bicarbonate transporter into tobacco chloroplasts. J. Exp. Bot. 65:3071–80
    [Google Scholar]
  70. 70. 
    Peterhansel C, Horst I, Niessen M, Blume C, Kebeish R et al. 2010. Photorespiration. Arabidopsis Book 8:e0130
    [Google Scholar]
  71. 71. 
    Price GD. 2011. Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism. Photosynth. Res. 109:47–57
    [Google Scholar]
  72. 72. 
    Price GD, Badger MR. 1989. Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-requiring phenotype: evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91:505–13Expressing a carbonic anhydrase in the cyanobacterial cytosol impairs the CCM, demonstrating that HCO3 is maintained at high concentrations in the cytosol.
    [Google Scholar]
  73. 73. 
    Price GD, Badger MR, von Caemmerer S 2011. The prospect of using cyanobacterial bicarbonate transporters to improve leaf photosynthesis in C3 crop plants. Plant Physiol 155:20–26
    [Google Scholar]
  74. 74. 
    Price GD, Coleman JR, Badger MR 1992. Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100:784–93
    [Google Scholar]
  75. 75. 
    Price GD, Howitt SM, Harrison K, Badger MR 1993. Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. J. Bacteriol. 175:2871–79
    [Google Scholar]
  76. 76. 
    Qu Z, Hartzell HC. 2008. Bestrophin Cl channels are highly permeable to HCO3. Am. J. Physiol. Cell Physiol. 294:C1371–77
    [Google Scholar]
  77. 77. 
    Rae BD, Long BM, Badger MR, Price GD 2012. Structural determinants of the outer shell of β-carboxysomes in Synechococcus elongatus PCC 7942: roles for CcmK2, K3-K4, CcmO, and CcmL. PLOS ONE 7:e43871
    [Google Scholar]
  78. 78. 
    Rae BD, Long BM, Badger MR, Price GD 2013. Functions, compositions, and evolution of the two types of carboxysomes: polyhedral microcompartments that facilitate CO2 fixation in cyanobacteria and some proteobacteria. Microbiol. Mol. Biol. Rev. 77:357–79
    [Google Scholar]
  79. 79. 
    Ramazanov Z, Rawat M, Henk MC, Mason CB, Matthews SW, Moroney JV 1994. The induction of the CO2-concentrating mechanism is correlated with the formation of the starch sheath around the pyrenoid of Chlamydomonas reinhardtii. Planta 195:210–16
    [Google Scholar]
  80. 80. 
    Raven JA. 1997. CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification. Plant Cell Environ 20:147–54
    [Google Scholar]
  81. 81. 
    Raven JA. 2013. Rubisco: still the most abundant protein of Earth. New Phytol 198:1–3
    [Google Scholar]
  82. 82. 
    Reinfelder JR, Milligan AJ, Morel FMM 2004. The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135:2106–11
    [Google Scholar]
  83. 83. 
    Rolland V, Badger MR, Price GD 2016. Redirecting the cyanobacterial bicarbonate transporters BicA and SbtA to the chloroplast envelope: Soluble and membrane cargos need different chloroplast targeting signals in plants. Front. Plant Sci. 7:185With a chloroplast transit peptide from Arabidopsis, cyanobacterial HCO3 transporters could be targeted to the Nicotianabenthamiana chloroplast envelope.
    [Google Scholar]
  84. 84. 
    Ryan P, Forrester TJB, Wroblewski C, Kenney TMG, Kitova EN et al. 2019. The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit. J. Biol. Chem. 294:2593–603
    [Google Scholar]
  85. 85. 
    Savir Y, Noor E, Milo R, Tlusty T 2010. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. PNAS 107:3475–80
    [Google Scholar]
  86. 86. 
    Schlüter U, Weber APM. 2020. Regulation and evolution of C4 photosynthesis. Annu. Rev. Plant Biol. 71:183–215
    [Google Scholar]
  87. 87. 
    Schuler ML, Mantegazza O, Weber APM 2016. Engineering C4 photosynthesis into C3 chassis in the synthetic biology age. Plant J 87:51–65
    [Google Scholar]
  88. 88. 
    Schuller JM, Saura P, Thiemann J, Schuller SK, Gamiz-Hernandez AP et al. 2020. Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I. Nat. Commun. 11:494
    [Google Scholar]
  89. 89. 
    Sharpe RM, Offermann S. 2014. One decade after the discovery of single-cell C4 species in terrestrial plants: What did we learn about the minimal requirements of C4 photosynthesis. Photosynth. Res. 119:169–80
    [Google Scholar]
  90. 90. 
    Sommer M, Cai F, Melnicki M, Kerfeld CA 2017. β-Carboxysome bioinformatics: identification and evolution of new bacterial microcompartment protein gene classes and core locus constraints. J. Exp. Bot. 68:3841–55
    [Google Scholar]
  91. 91. 
    Sommer M, Sutter M, Gupta S, Kirst H, Turmo A et al. 2019. Heterohexamers formed by CcmK3 and CcmK4 increase the complexity of beta carboxysome shells. Plant Physiol 179:156–67
    [Google Scholar]
  92. 92. 
    South PF, Cavanagh AP, Liu HW, Ort DR 2019. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:eaat9077
    [Google Scholar]
  93. 93. 
    Spalding MH, Spreitzer RJ, Ogren WL 1983. Carbonic anhydrase-deficient mutant of Chlamydomonas reinhardtii requires elevated carbon dioxide concentration for photoautotrophic growth. Plant Physiol 73:268–72
    [Google Scholar]
  94. 94. 
    Suss KH, Prokhorenko I, Adler K 1995. In situ association of Calvin cycle enzymes, ribulose-1,5-bisphosphate carboxylase/oxygenase activase, ferredoxin-NADP+ reductase, and nitrite reductase with thylakoid and pyrenoid membranes of Chlamydomonas reinhardtii chloroplasts as revealed by immunoelectron microscopy. Plant Physiol 107:1387–97
    [Google Scholar]
  95. 95. 
    Tanaka S, Kerfeld CA, Sawaya MR, Cai F, Heinhorst S et al. 2008. Atomic-level models of the bacterial carboxysome shell. Science 319:1083–86
    [Google Scholar]
  96. 96. 
    Tcherkez GGB, Farquhar GD, Andrews TJ 2006. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. PNAS 103:7246–51
    [Google Scholar]
  97. 97. 
    Tilman D, Balzer C, Hill J, Befort BL 2011. Global food demand and the sustainable intensification of agriculture. PNAS 108:20260–64
    [Google Scholar]
  98. 98. 
    Uehara S, Adachi F, Ito-Inaba Y, Inaba T 2016. Specific and efficient targeting of cyanobacterial bicarbonate transporters to the inner envelope membrane of chloroplasts in Arabidopsis.Front. Plant Sci 7:16The cyanobacterial HCO3 transporters BicA and SbtA were targeted to the Arabidopsis chloroplast envelope inner membrane.
    [Google Scholar]
  99. 99. 
    van Lun M, Hub JS, van der Spoel D, Andersson I 2014. CO2 and O2 distribution in Rubisco suggests the small subunit functions as a CO2 reservoir. J. Am. Chem. Soc. 136:3165–71
    [Google Scholar]
  100. 100. 
    Villarejo A, Martinez F, del Pino Plumed M, Ramazanov Z 1996. The induction of the CO2 concentrating mechanism in a starch-less mutant of Chlamydomonas reinhardtii.Physiol. Plant 98:798–802
    [Google Scholar]
  101. 101. 
    Volokita M, Zenvirth D, Kaplan A, Reinhold L 1984. Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76:599–602
    [Google Scholar]
  102. 102. 
    Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR 2016. The costs of photorespiration to food production now and in the future. Annu. Rev. Plant Biol. 67:107–29
    [Google Scholar]
  103. 103. 
    Wang H, Yan X, Aigner H, Bracher A, Nguyen ND et al. 2019. Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature 566:131–35
    [Google Scholar]
  104. 104. 
    Wang L, Yamano T, Kajikawa M, Hirono M, Fukuzawa H 2014. Isolation and characterization of novel high-CO2-requiring mutants of Chlamydomonas reinhardtii.Photosynth. Res 121:175–84
    [Google Scholar]
  105. 105. 
    Wang Y, Spalding MH. 2014. Acclimation to very low CO2: contribution of limiting CO2 inducible proteins, LCIB and LCIA, to inorganic carbon uptake in Chlamydomonas reinhardtii. Plant Physiol 166:2040–50
    [Google Scholar]
  106. 106. 
    Wunder T, Cheng SLH, Lai S-K, Li H-Y, Mueller-Cajar O 2018. The phase separation underlying the pyrenoid-based microalgal Rubisco supercharger. Nat. Commun. 9:5076Rubisco and its linker EPYC1 were sufficient to form pyrenoid matrix-like droplets in vitro.
    [Google Scholar]
  107. 107. 
    Yamano T, Sato E, Iguchi H, Fukuda Y, Fukuzawa H 2015. Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii. PNAS 112:7315–20
    [Google Scholar]
  108. 108. 
    Yamano T, Tsujikawa T, Hatano K, Ozawa S-I, Takahashi Y, Fukuzawa H 2010. Light and low-CO2-dependent LCIB-LCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Cell Physiol 51:1453–68
    [Google Scholar]
  109. 109. 
    Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM 2008. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat. Rev. Microbiol. 6:681–91
    [Google Scholar]
  110. 110. 
    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. J. Exp. Bot. 68:2345–60
    [Google Scholar]
  111. 111. 
    Zeeman SC, Kossmann J, Smith AM 2010. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61:209–34
    [Google Scholar]
  112. 112. 
    Zhan Y, Marchand CH, Maes A, Mauries A, Sun Y et al. 2018. Pyrenoid functions revealed by proteomics in Chlamydomonas reinhardtii. PLOS ONE 13:e0185039
    [Google Scholar]
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