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A Critical Review on the Improvement of Photosynthetic Carbon Assimilation in C3 Plants Using Genetic Engineering

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A Critical Review on the Improvement of Photosynthetic Carbon Assimilation in C3 Plants Using Genetic Engineering Critical Reviews in Biotechnology ISSN: 0738-8551 (Print) 1549-7801 (Online) Journal homepage: http://www.tandfonline.com/loi/ibty20 A critical review on the improvement of photosynthetic carbon assimilation in C3 plants using genetic engineering Cheng-Jiang Ruan, Hong-Bo Shao & Jaime A. Teixeira da Silva To cite this article: Cheng-Jiang Ruan, Hong-Bo Shao & Jaime A. Teixeira da Silva (2012) A critical review on the improvement of photosynthetic carbon assimilation in C3 plants using genetic engineering, Critical Reviews in Biotechnology, 32:1, 1-21, DOI: 10.3109/07388551.2010.533119 To link to this article: https://doi.org/10.3109/07388551.2010.533119 Published online: 24 Jun 2011. Submit your article to this journal Article views: 1003 View related articles Citing articles: 23 View citing articles Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ibty20 Critical Reviews in Biotechnology Critical Reviews in Biotechnology, 2012; 32(1): 1–21 2012 © 2012 Informa Healthcare USA, Inc. ISSN 0738-8551 print/ISSN 1549-7801 online 32 DOI: 10.3109/07388551.2010.533119 1 1 REVIEW ARTICLE 21 04 June 2010 A critical review on the improvement of photosynthetic 14 October 2010 carbon assimilation in C3 plants using genetic engineering 14 October 2010 Cheng-Jiang Ruan1, Hong-Bo Shao2, and Jaime A. Teixeira da Silva3 0738-8551 1Key Laboratory of Biotechnology & Bio-Resources Utilization, Dalian Nationalities University, Dalian City, Liaoning, China, 2Yantai Institute of Costal Zone Research , Chinese Academy of Sciences, Yantai, China, and 3Faculty of 1549-7801 Agriculture and Graduate School of Agriculture, Kagawa University, Miki-cho, Kagawa, Japan © 2012 Informa Healthcare USA, Inc. Abstract 10.3109/07388551.2010.533119 Global warming is one of the most serious challenges facing us today. It may be linked to the increase in atmospheric CO and other greenhouse gases (GHGs), leading to a rise in sea level, notable shifts in ecosystems, and in the BBTN 2 frequency and intensity of wild fires. There is a strong interest in stabilizing the atmospheric concentration of CO2 533119 and other GHGs by decreasing carbon emission and/or increasing carbon sequestration. Biotic sequestration is an important and effective strategy to mitigate the effects of rising atmospheric CO2 concentrations by increasing carbon sequestration and storage capacity of ecosystems using plant photosynthesis and by decreasing carbon emission using biofuel rather than fossil fuel. Improvement of photosynthetic carbon assimilation, using transgenic engineering, potentially provides a set of available and effective tools for enhancing plant carbon sequestration. In this review, firstly different biological methods of CO2 assimilation in C3, C4 and CAM plants are introduced and three types of C4 pathways which have high photosynthetic performance and have evolved as CO2 pumps are briefly summarized. Then (i) the improvement of photosynthetic carbon assimilation of C3 plants by transgenic engineering using non-C4 genes, and (ii) the overexpression of individual or multiple C4 cycle photosynthetic genes (PEPC, PPDK, PCK, NADP–ME and NADP-MDH) in transgenic C3 plants (e.g. tobacco, potato, rice and Arabidopsis) are highlighted. Some transgenic C3 plants (e.g. tobacco, rice and Arabidopsis) overexpressing the FBP/SBPase, ictB and cytochrome c6 genes showed positive effects on photosynthetic efficiency and growth characteristics. However, over the last 28 years, efforts to overexpress individual, double or multiple 4C enzymes in C3 plants like tobacco, potato, rice, and Arabidopsis have produced mixed results that do not confirm or eliminate the possibility of improving photosynthesis of C3 plants by this approach. Finally, a prospect is provided on the challenges of enhancing carbon assimilation of C3 plants using transgenic engineering in the face of global warming, and the trends of the most promising approaches to improving the photosynthetic performance of C3 plants. Keywords: Global warming, increase in CO2 concentration, biotic carbon sequestration, C3 plants, C4 plants, CAM plants, overexpression of C4 enzymes, transgenic C3 plants, improvement of photosynthesis Introduction st The concentration of carbon dioxide (CO2) in the Earth’s to increase by 1.5–5.88°C during the 21 century (IPCC, atmosphere has increased by 31% from 280 parts per mil- 2001). In addition to a rise in sea level by 15–23 cm during lion (ppm) in 1850 to 380 ppm in 2005 (IPCC, 2007). It is the 20th century (IPCC, 2007), there have been notable presently increasing at 1.7 ppm yr−1 or 0.46% yr−1, which shifts in ecosystems (Greene and Pershing, 2007) and in will lead to 50% higher levels in 2050 than today (Sun the frequency and intensity of occurrence of wild fires et al., 2009). Global surface temperature has increased (Running, 2006; Westerling et al., 2006). The increase in th by 0.88°C since the late 19 century, and 11 out of the 12 atmospheric CO2 and other greenhouse gases (GHGs) warmest years on record have occurred during 1995–2006 e.g. methane (CH4) and nitrous oxide (N2O), may be the (IPCC, 2007). The Earth’s mean temperature is projected major reasons for climate change (Nowak et al., 2004); Address for Correspondence: Cheng-Jiang Ruan, Key Laboratory of Biotechnology & Bio-Resources Utilization, Dalian Nationalities University, Dalian City, Liaoning, China. Tel.: +86 411 87656015; Fax: +86 411 87618179; E-mail: [email protected] (Received 04 June 2010; revised 14 October 2010; accepted 14 October 2010) 1 2 Cheng-Jiang Ruan et al. Abbreviations ATP adenosine 5′-triphosphate PEP phosphoenolpyruvate CAM crassulacean acid metabolism PEPC phosphoenolpyruvate carboxylase CH4 methane PGA phosphoglycerate CO2 carbon dioxide PGAL phosphoglyceraldehyde DHAP dihydroxy acetone phosphate PPDK pyruvate orthophosphate dikinase FBPase fructose-1, 6-bisphosphatase ppm parts per million Fru-6P fructose 6-phosphate rca regulation carboxylation activity or the Rubisco G3P/GA-3P glyceraldehyde 3-phosphate activase gene GHGs greenhouse gases RCA Rubisco activase GP glycerate 3-phosphate Ru-5P ribulose 5-phosphate N2O nitrous oxide Rubisco ribulose 1,5-bisphosphate carboxylase/oxygenase NADP nicotinamide adenine dinucleotide phosphate RuBP ribulose-1,5-bisphosphate NADP-MDH NADP-malate dehydrogenase SBPase sedoheptulose-1,7-bisphosphatase NADP-ME NADP-malic enzyme Sed-7P sedoheptulose 7-phosphate OAA oxaloacetic acid SPS sucrose phosphate synthase PCK phosphoenolpyruvate carboxykinase WT wild type hence, there is a strong interest in stabilizing the atmo- photosynthetic pathway. The majority of terrestrial plants, spheric abundance of CO2 and other GHGs to mitigate including many important crops such as rice (Oryza the risks of global warming (Kerr, 2007; Kintisch, 2007; sativa L.), wheat (Triticum aestivum), soybean (Glycine Kluger, 2007; Mikkelsen et al., 2010). CO2 is the most max), and potato (Solanum tuberosum), are C3 plants prominent GHG in the Earth’s atmosphere. Among the (Matsuoka et al., 2001); (ii) C4 plants e.g. maize (Zea different ways to reduce CO2 emission and increase car- mays) and sugarcane (Saccharum officinarum), which bon capture and storage (e.g. chemical transformations, evolved the C4 photosynthetic pathway (Sage and Pearcy, biological conversions, reforming and inorganic transfor- 1987); and (iii) CAM (crassulacean acid metabolism) mations, and manipulations of the soil carbon pool) (Lal, plants, in which the stomata are closed during the day 2004; 2008; 2009), biotic carbon sequestration (Figure 1) and open only at night when the temperature decreases is recommended by the Kyoto Protocol as one of the and humidity rises; at night, CO2 is stored as malate in the important and effective strategies to mitigate the effects of large vacuoles and is released for photosynthesis during rising atmospheric CO2 concentrations by enhanced car- the day. While C3 plants grow well in temperate climates, bon sequestration (Hill et al., 2007). The Kyoto Protocol CAM plants such as stonecrops (Lithops spp.) and cactus is the first international environmental agreement to adapt to extreme arid conditions, but their photosyn- require binding greenhouse gas emission reductions by thetic capacity is very low (Black, 1973). In contrast, C4 industrialized nations (http://en.wikipedia.org/wiki/ plants such as maize and sugarcane adapt to high light, Kyoto_Protocol). Compared to different techniques of arid, and warm environments and achieve higher pho- carbon sequestration, biotic techniques are immediately tosynthetic capacity and higher water- and nitrogen-use applicable, natural, and cost-effective processes, with efficiencies compared to3 C plants (Black, 1973). Both C4 numerous ancillary benefits but a finite sink capacity and CAM plants evolved from an ancestral C3 species in (Lal, 2008). The increase in atmospheric CO2 concentra- response to changes in environmental conditions that tion is mainly from burning fossil fuel, thus, in the future caused a decrease in CO2 availability. C4 plants evolved in CO2 mitigation schemes have to match the scale of man- response to low atmospheric CO2 concentrations, while made CO2 in the atmosphere. For example, if fossil fuel CAM plants evolved either in response to the selection emissions from 1990 to 2100 are limited to 600 PgC, biotic of increased water-use efficiency or for increased carbon carbon stocks must increase by 120 PgC to stabilize CO2 gain (Ehleringer and Monson, 1993).
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