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. 2016 Jul;87(1):38-50.
doi: 10.1111/tpj.13139. Epub 2016 Jun 20.

Towards engineering carboxysomes into C3 plants

Maureen R Hanson  1 , Myat T Lin  1 , A Elizabete Carmo-Silva  2 , Martin A J Parry  2
Affiliations

Towards engineering carboxysomes into C3 plants

Maureen R Hanson et al. Plant J. 2016 Jul.

Abstract

Photosynthesis in C3 plants is limited by features of the carbon-fixing enzyme Rubisco, which exhibits a low turnover rate and can react with O2 instead of CO2 , leading to photorespiration. In cyanobacteria, bacterial microcompartments, known as carboxysomes, improve the efficiency of photosynthesis by concentrating CO2 near the enzyme Rubisco. Cyanobacterial Rubisco enzymes are faster than those of C3 plants, though they have lower specificity toward CO2 than the land plant enzyme. Replacement of land plant Rubisco by faster bacterial variants with lower CO2 specificity will improve photosynthesis only if a microcompartment capable of concentrating CO2 can also be installed into the chloroplast. We review current information about cyanobacterial microcompartments and carbon-concentrating mechanisms, plant transformation strategies, replacement of Rubisco in a model C3 plant with cyanobacterial Rubisco and progress toward synthesizing a carboxysome in chloroplasts.

Keywords: Nicotiana; Rubisco; Synechococcus elongatus; carbon-concentrating mechanism; carboxysome; chloroplast; chloroplast transformation; photosynthesis; transgenic; transplastomic.

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Figures

Figure 1
Figure 1
The carboxylation and oxygenation reactions of Rubisco. (a) Diagram of Rubisco-catalyzed reactions in C3 plants. Carboxylation of RuBP initiates the Calvin Cycle and leads to production of carbohydrates. Oxygenation of RuBP initiates photorespiration and results in the net loss of fixed CO2 and NH3, and consumption of energy. The carboxylation of RuBP by Rubisco and subsequent reactions in the Calvin Cycle are shown in green arrows. The oxygenation of RuBP by Rubisco and the subsequent photorespiration process are shown in red arrows. RuBP = Ribulose-1,5-bisphosphate; 3PGA = 3-phosphoglycerate; 2PG = 2-phosphoglycolate; G3P = glyceraldehyde 3-phosphate. (b) Rubisco specificity (SC/O) and maximum carboxylation rate (VC) in tobacco (C3 model species), wheat (C3 crop), limonium (L. gibertii, C3 with high specificity), maize and sorghum (C4 crops), S. elongatus (cyanobacteria, β-carboxysome species) and Rhodospirilum rubrum (purple bacteria, α-carboxysome species). Data are averages of values reported by: (Jordan and Ogren 1981, Jordan and Ogren 1983, Jordan and Ogren 1984, Makino et al. 1985, Parry et al. 1987, Parry et al. 1989, Sage and Seemann 1993, Kane et al. 1994, Delgado, et al. 1995, Uemura et al. 1996, Whitney et al. 1999, Whitney et al. 2001, Pearce 2006, Mueller-Cajar et al. 2007, Parry et al. 2007, Kubien et al. 2008, Mueller-Cajar and Whitney 2008, Sharwood et al. 2008, Carmo-Silva et al. 2010, Genkov et al. 2010, Whitney et al. 2011b, Occhialini et al. 2016, Prins et al. 2016).
Figure 2
Figure 2
The components of β-carboxysomes. (a) Structural model of β-carboxysome in S. elongatus PCC7942. Data on protein location and assembly as described by Cameron et al. (2013). Please note that the role of CcmO remains unclear although it is represented as pseudohexamers here. Carboxysome model courtesy of Kevin Hines. (b) Operons present in S. elongatus PCC7942 (Heinhorst et al. 2014).
Figure 3
Figure 3
Transient expression of cyanobacterial shell proteins in Nicotiana benthamiana. (a) Diffuse localization of CcmO-YFP within chloroplasts when CcmK2 and CcmL are absent. (b) Formation of YFP fluorescent punctate loci (green) within the chloroplasts (red) of N. benthamiana transiently expressing CcmK2, CcmL and CcmO-YFP. (c) and (d) Spherical structures formed in plants transiently expression CcmK2-YFP, CcmL, and CcmO-YFP. Microscopic images from Lin et al. (2014a), with permission.
Figure 4
Figure 4
Schematics of gene arrangements in synthetic operons to express cyanobacterial Rubisco from chloroplasts. (a) Replacement of the tobacco rbcL gene with cyanobacterial transgenes and a selectable marker by homologous recombination. (b) A typical gene arrangement in a synthetic operon with two generic cyanobacterial genes, ccm1 and ccm2. Each gene is followed by a different terminator sequence denoted as T1 or T2. In the intergenic region between ccm1 and ccm2, an intercistronic expression element (IEE) and a ribosome binding site (RBS) are inserted immediately upstream of ccm2 for processing of the dicistronic transcript into monocristronic ones for more efficient translation of the downstream gene, ccm2. (c) Schematics of synthetic operons in four different constructs to express cyanobacterial transgenes from the tobacco rbcL locus (Occhialini, et al. 2016). Se LS, Se SS, RbcX, and M35 represent rbcL, rbcS, rbcX, and ccmM35 genes from S. elongatus PCC7942 respectively. RBS: ribosome binding site. Single (SD) or triple (SD18) Shine-Dalgarno sequences from T7 gene 10 (Drechsel and Bock 2011).
Figure 5
Figure 5
Characterization of transgenic tobacco plants engineered with cyanobacterial Rubisco. (a) Relative size of wild-type (wt) and SeLS, SeLSX, SeLSM35 and SeLSYM35 tobacco plants when grown for 42 days in 3% CO2. (b) Rubisco content per leaf area in wt tobacco growing in air vs. wt and transgenic lines growing in 3% CO2. (c–d) Localization of cyanobacterial Rubisco in the chloroplast stroma of the SeLS (c) and SeLSYM35 (d) tobacco transplastomic lines probed with anti-Se Rubisco antibody and a secondary antibody conjugated with 10 nm gold particles (black circles or dots). Scale bars = 500 nm. Modified from Occhialini et al. 2016, with permission.
Figure 6
Figure 6
Rubisco specificity (SC/O) and maximum carboxylation rate (VC) in wild-type and SeLS, SeLSX, SeLSM35 and SeLSYM35 transplastomic tobacco plants. Data from Occhialini et al. (2016).
Figure 7
Figure 7
Diagram of carboxysomes in cyanobacteria and hypothetically in a chloroplast. Diagram visualizes approximate relative size of S. elongatus cell and typical tobacco chloroplast. A typical S. elongatus cell contains an average of 4 carboxysomes (Savage et al. 2010). However, modeling indicates more will be needed for adequate Rubisco to be present (McGrath and Long 2014).
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