Advertisement

Planta

, 251:24 | Cite as

Biotechnological strategies for improved photosynthesis in a future of elevated atmospheric CO2

  • Stacy D. SingerEmail author
  • Raju Y. Soolanayakanahally
  • Nora A. Foroud
  • Roland Kroebel
Review

Abstract

Main conclusion

The improvement of photosynthesis using biotechnological approaches has been the focus of much research. It is now vital that these strategies be assessed under future atmospheric conditions.

Abstract

The demand for crop products is expanding at an alarming rate due to population growth, enhanced affluence, increased per capita calorie consumption, and an escalating need for plant-based bioproducts. While solving this issue will undoubtedly involve a multifaceted approach, improving crop productivity will almost certainly provide one piece of the puzzle. The improvement of photosynthetic efficiency has been a long-standing goal of plant biotechnologists as possibly one of the last remaining means of achieving higher yielding crops. However, the vast majority of these studies have not taken into consideration possible outcomes when these plants are grown long-term under the elevated CO2 concentrations (e[CO2]) that will be evident in the not too distant future. Due to the considerable effect that CO2 levels have on the photosynthetic process, these assessments should become commonplace as a means of ensuring that research in this field focuses on the most effective approaches for our future climate scenarios. In this review, we discuss the main biotechnological research strategies that are currently underway with the aim of improving photosynthetic efficiency and biomass production/yields in the context of a future of e[CO2], as well as alternative approaches that may provide further photosynthetic benefits under these conditions.

Keywords

Biotechnology Climate change Yield Root growth Sink strength Nitrogen assimilation 

Notes

Acknowledgements

The authors are grateful for the support provided by Agriculture and Agri-Food Canada.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aharon R, Shahak Y, Wininger S, Bendov R, Kapulnik Y, Galili G (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. Plant Cell 15:439–447PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ainsworth EA, Lemonnier P (2018) Phloem function: a key to understanding and manipulating plant responses to rising atmospheric [CO2]? Curr Opin Plant Biol 43:50–56PubMedCrossRefPubMedCentralGoogle Scholar
  3. 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 165:351–372PubMedCrossRefPubMedCentralGoogle Scholar
  4. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ainsworth EA, Rogers A, Leakey ADB (2008) Targets for crop biotechnology in a future high-CO2 and high-O3 world. Plant Physiol 147:13–19PubMedPubMedCentralCrossRefGoogle Scholar
  6. Alexandratos N, Bruinsma J (2012) World agriculture towards 2030/2050: the 2012 revision. ESA Working paper No. 12-03. Rome, FAOGoogle Scholar
  7. Anderson JM, Price GD, Chow WS, Hope AB, Badger MR (1997) Reduced levels of cytochrome bf complex in transgenic tobacco leads to marked photochemical reduction of the plastoquinone pool, without significant change in acclimation irradiance. Photosynth Res 53:215–227CrossRefGoogle Scholar
  8. Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568PubMedCrossRefPubMedCentralGoogle Scholar
  9. Aranjuelo I, Erice G, Nogués S, Morales F, Irigoyen JJ, Sánchez-Díaz M (2008) The mechanism(s) involved in the photoprotection of PSII at elevated CO2 in nodulated alfalfa plants. Environ Exp Bot 64:295–306CrossRefGoogle Scholar
  10. Assmann SM (1999) The cellular basis of guard cell sensing of rising CO2. Plant Cell Environ 22:629–637CrossRefGoogle Scholar
  11. Atkinson N, Feike D, Mackinder LCM, Meyer MT, Griffiths H, Jonikas MC, Smith AM, McCormick AJ (2016) Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol J 14:1302–1315PubMedCrossRefPubMedCentralGoogle Scholar
  12. Azam A, Hameed A, Khan I (2017) Impact of elevated atmospheric carbon dioxide on yield, vitamin C, proximate, fatty acid and amino acid composition of capsicum (Capsicum annuum). Environ Pollut Prot 2:153–167Google Scholar
  13. Badger MR, Price GD (2003) CO2 concentrating mechanism in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622PubMedCrossRefPubMedCentralGoogle Scholar
  14. Badiani M, D’Annibale A, Paolacci AR, Miglietta F, Raschi A (1993) The antioxidant status of soybean (Glycine max Merrill) leaves grown under natural CO2-enrichment in the field. Austral J Plant Physiol 20:275–284Google Scholar
  15. Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ, Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Exp Bot 46:1269–1276CrossRefGoogle Scholar
  16. Bao A, ZhaoZ Ding G, Shi L, Xu F, Cai H (2014) Accumulated expression level of cytosolic glutamine synthetase 1 gene (OsGS1;1 or OsGS1;2) alter plant development and the carbon-nitrogen metabolic status in rice. PLoS One 9:e95581PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15:269–275PubMedCrossRefPubMedCentralGoogle Scholar
  19. Baxter CJ, Foyer CH, Turner J, Rolfe SA, Quick WP (2003) Elevated sucrose-phosphate synthase activity in transgenic tobacco sustains photosynthesis in older leaves and alters development. J Exp Bot 54:1813–1820PubMedCrossRefPubMedCentralGoogle Scholar
  20. Beleggia R, Fragasso M, Miglietta F, Cattivelli L, Menga V, Nigro F, Pecchioni N, Fares C (2018) Mineral composition of durum wheat grain and pasta under increasing atmospheric CO2 concentrations. Food Chem 242:53–61PubMedCrossRefPubMedCentralGoogle Scholar
  21. Berners-Lee M, Kennelly C, Watson R, Hewitt CN (2018) Current global food production is sufficient to meet human nutritional needs in 2050 provided there is radical societal adaptation. Elem Sci Anth 6:52CrossRefGoogle Scholar
  22. Betti M, Bauwe H, Busch FA, Fernie AR, Keech O, Levey M, Ort DR, Parry MAJ, Sage R, Timm S, Walker B, Weber APM (2016) Manipulating photorespiration to increase plant productivity: recent advances and perspectives for crop improvement. J Exp Bot 67:2977–2988PubMedCrossRefPubMedCentralGoogle Scholar
  23. Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97PubMedCrossRefPubMedCentralGoogle Scholar
  24. Blankenship RE, Tiede DM, Barber J et al (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809PubMedCrossRefPubMedCentralGoogle Scholar
  25. Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166PubMedCrossRefPubMedCentralGoogle Scholar
  26. Broberg M, Högy P, Pleijel H (2017) CO2-induced changes in wheat grain composition: meta-analysis and response functions. Agronomy 7:32CrossRefGoogle Scholar
  27. Cardona T, Shao S, Nixon PJ (2018) Enhancing photosynthesis in plants: the light reaction. Essay Biochem 62:85–94CrossRefGoogle Scholar
  28. Carmo-Silva E, Scales JC, Madgwick PJ, Parry MA (2015) Optimizing Rubisco and its regulation for greater resource use efficiency. Plant Cell Environ 38:1817–1832PubMedCrossRefPubMedCentralGoogle Scholar
  29. Carriquí M, Douthe C, Molins A, Flexas J (2019) Leaf anatomy does not explain apparent short-term responses of mesophyll conductance to light and CO2 in tobacco. Physiol Plant 165:604–618PubMedCrossRefPubMedCentralGoogle Scholar
  30. Carvalho JFC, Madgwick PJ, Powers SJ, Keys AJ, Lea PJ, Parry MAJ (2011) An engineered pathway for glyoxylate metabolism in tobacco plants aimed to avoid the release of ammonia in photorespiration. BMC Biotechnol 11:111PubMedCentralCrossRefGoogle Scholar
  31. Chen XM, Alm DM, Hesketh JD (1995) Effects of atmospheric CO2 concentration on photosynthetic performance of C3 and C4 plants. Biotronics 24:65–72Google Scholar
  32. Chen D, Richardson T, Chai S, McIntyre CL, Rae AL, Xue GP (2016) Drought-up-regualated TaNAC69-1 is a transcriptional repressor of TaSHY2 and TaIAA7, and enhances root length and biomass in wheat. Plant Cell Physiol 57:2076–2090PubMedCrossRefPubMedCentralGoogle Scholar
  33. Chen D, Chai S, McIntyre CL, Xue G-P (2018) Overexpression of a predominantly root-expressed NAC transcription factor in wheat roots enhances root length, biomass and drought tolerance. Plant Cell Rep 37:225–237PubMedCrossRefPubMedCentralGoogle Scholar
  34. Chida H, Nakazawa A, Akazaki H et al (2007) Expression of the algal cytochrome c6 gene in Arabidopsis enhances photosynthesis and growth. Plant Cell Physiol 48:948–957PubMedCrossRefPubMedCentralGoogle Scholar
  35. Comas LH, Becker SR, Cruz VM, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442PubMedPubMedCentralCrossRefGoogle Scholar
  36. Conley AJ, Zhu H, Le LC, Jevnikar AM, Lee BH, Brandle JE, Menassa R (2011) Recombinant protein production in a variety of Nicotiana hosts: a comparative analysis. Plant Biotechnol J 9:434–444PubMedCrossRefPubMedCentralGoogle Scholar
  37. Cramer WA, Zhang H (2006) Consequences of the structure of the cytochrome b6f complex for its charge transfer pathways. Biochim Biophys Acta 1757:339–345PubMedCrossRefPubMedCentralGoogle Scholar
  38. Dalal J, Lopez H, Vasani NB, Hu Z, Swift JE, Yalamanchili R, Dvora M, Lin X, Xie D, Qu R, Sederoff HW (2015) A photorespiratory bypass increases plant growth and seed yield in biofuel crop Camelina sativa. Biotechnol Biofuels 8:175PubMedPubMedCentralCrossRefGoogle Scholar
  39. Davin EL, Seneviratne SI, Ciais P, Olioso A, Wang T (2014) Preferential cooling of hot extremes from cropland albedo management. Proc Nat Acad Sci 111:9757–9761PubMedCrossRefPubMedCentralGoogle Scholar
  40. Den Herder G, Isterdael GV, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607CrossRefGoogle Scholar
  41. Ding F, Wang M, Zhang S, Ai X (2016) Changes in SBPase activity influence photosynthetic capacity, growth, and tolerance to chilling stress in transgenic tomato plants. Sci Rep 6:32741PubMedPubMedCentralCrossRefGoogle Scholar
  42. Drake BG, Gonzalez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639PubMedCrossRefPubMedCentralGoogle Scholar
  43. Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ, Sparks CA, Jones HD, Lawson T, Parry MAJ, Raines CA (2017) Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Phil Trans Royal Soc B Biol Sci 372:20160384CrossRefGoogle Scholar
  44. Ehlers I, Augusti A, Betson TR, Nilsson MB, Schleucher J (2015) Detecting long-term metabolic shifts using isotopomers: CO2-driven suppression of photorespiration in C3 plants over the 20th century. Proc Natl Acad Sci USA 112:15585PubMedPubMedCentralGoogle Scholar
  45. Erice G, Sanz-Sáez A, Aranjuelo I, Irigoyen JJ, Aguirreolea J, Avice J-C, Sánchez-Díaz M (2011) Photosynthesis, N2 fixation and taproot reserves during the cutting regrowth cycle of alfalfa under elevated CO2 and temperature. J Plant Physiol 168:2007–2014PubMedCrossRefPubMedCentralGoogle Scholar
  46. Feng L, Wang K, Li Y, Tan Y, Kong J, Li H, Li Y, Zhu Y (2007a) Overexpression of SBPase enhances photosynthesis against high temperature stress in transgenic rice plants. Plant Cell Rep 26:1635–1646PubMedCrossRefPubMedCentralGoogle Scholar
  47. Feng L, Han Y, Liu G, An B, Yang J, Yang G, Li Y, Zhu Y (2007b) Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants. Funct Plant Biol 34:822–834CrossRefGoogle Scholar
  48. Fernando N, Panozzo J, Tausz M, Norton R, Fitzgerald G, Khan A, Seneweera S (2015) Rising CO2 concentration altered wheat grain proteome and flour rheological characteristics. Food Chem 170:448–454PubMedCrossRefPubMedCentralGoogle Scholar
  49. Fernie AR, Bauwe H, Eisenhut M et al (2013) Perspectives on plant photorespiratory metabolism. Plant Biol 15:748–753PubMedCrossRefPubMedCentralGoogle Scholar
  50. Flexas J, Ribas-Carbó M, Hanson DT, Bota J, Otto B, Cifre J, McDowell N, Medrano H, Kaldenhoff R (2006) Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2in vivo. Plant J 48:427–439PubMedCrossRefPubMedCentralGoogle Scholar
  51. Flexas J, Niinemets Ü, Gallé A et al (2013) Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynth Res 117:45–59PubMedCrossRefPubMedCentralGoogle Scholar
  52. Foyer CH, Bloom AJ, Queval G, Noctor G (2009) Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60:455–484PubMedCrossRefPubMedCentralGoogle Scholar
  53. Fuentes SI, Allen DJ, Ortiz-Lopez A, Hernández G (2001) Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. J Exp Bot 52:1071–1081PubMedCrossRefPubMedCentralGoogle Scholar
  54. Fukayama H, Kobara T, Shiomi K, Morita R, Sasayama D, Hatanaka T, Azuma T (2018) Rubisco small subunits of C4 plants, Napier grass and guinea grass confer C4-like catalytic properties on Rubisco in rice. Plant Prod Sci.  https://doi.org/10.1080/1343943X.2018.1540279 CrossRefGoogle Scholar
  55. Gao J, Han X, Seneweera S, Li P, Zong Y-Z, Dong Q, Lin E-D, Hao X-Y (2015) Leaf photosynthesis and yield components of mung bean under fully open-air elevated [CO2]. J Integr Agric 14:977–983CrossRefGoogle Scholar
  56. Gao Y, de Bang TC, Schjoerring JK (2018) Cisgenic overexpression of cytosolic glutamine synthetase improves nitrogen utilization efficiency in barley and prevents grain protein decline under elevated CO2. Plant Biotechnol J.  https://doi.org/10.1111/pbi.13046 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Geiger M, Haake V, Ludewig F, Sonnewald U, Stitt M (1999) The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco. Plant Cell Environ 22:1177–1199CrossRefGoogle Scholar
  58. Gillespie KM, Rogers A, Ainsworth EA (2011) Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max). J Exp Bot 62:2667–2678PubMedCrossRefPubMedCentralGoogle Scholar
  59. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131PubMedCrossRefPubMedCentralGoogle Scholar
  60. Gong HY, Li Y, Fang G, Hu DH, Jin WB, Wang ZH, Li YS (2015) Transgenic rice expressing Ictb and FBP/Sbpase derived from cyanobacteria exhibits enhanced photosynthesis and mesophyll conductance to CO2. PLoS One 10:e0140928PubMedPubMedCentralCrossRefGoogle Scholar
  61. Gonzalez N, Beemster GT, Inzé D (2009) David and Goliath: what can the tiny weed Arabidopsis teach us to improve biomass production in crops? Curr Opin Plant Biol 12:157–164PubMedCrossRefPubMedCentralGoogle Scholar
  62. Gowik U, Westhoff P (2011) The path from C3 to C4 photosynthesis. Plant Physiol 155:56–63PubMedCrossRefPubMedCentralGoogle Scholar
  63. Grombone-Guaratini MT, Gaspar M, Oliveira VF, Torres MAMG, do Nascimento A, Aidar MPM (2013) Atmospheric CO2 enrichment markedly increases photosynthesis and growth in a woody tropical bamboo from the Brazilian Atlantic Forest. NZ J Bot 51:275–285CrossRefGoogle Scholar
  64. Gu J, Zhou Z, Li Z, Chen Y, Wang Z, Zhang H (2017a) Rice (Oryza sativa L.) with reduced chlorophyll content exhibit higher photosynthetic rate and efficiency, improved canopy light distribution, and greater yields than normally pigmented plants. Field Crops Res 200:58–70CrossRefGoogle Scholar
  65. Gu J, Zhou Z, Li Z, Chen Y, Wang Z, Zhang H, Yang J (2017b) Photosynthetic properties and potentials for improvement of photosynthesis in pale green leaf rice under high light conditions. Front Plant Sci 8:1082PubMedPubMedCentralCrossRefGoogle Scholar
  66. Haimovich-Dayan M, Lieman-Hurwitz J, Orf I, Hagemann M, Kaplan A (2015) Does 2-phosphoglycolate serve as an internal signal molecule of inorganic carbon deprivation in the cyanobacterium Synechocystis sp. PCC 6803? Environ Microbiol 17:1794–1804PubMedCrossRefPubMedCentralGoogle Scholar
  67. Hanba YT, Shibasaka M, Hayashi Y, Hayakawa T, Kasamo K, Terashima I, Katsuhara M (2004) Overexpression of the barley aquaporin HvPIP2;1 increases internal CO2 conductance and CO2 assimilation in the leaves of transgenic rice plants. Plant Cell Physiol 45:521–529PubMedCrossRefPubMedCentralGoogle Scholar
  68. Hanson MR, Lin MT, Carmo-Silva AE, Parry MAJ (2016) Towards engineering carboxysomes into C3 plants. Plant J 87:38–50PubMedPubMedCentralCrossRefGoogle Scholar
  69. Hay WT, Bihmidine S, Mutlu N, Hoang KL, Awada T, Weeks DP, Clemente TE, Long SP (2017) Enhancing soybean photosynthetic CO2 assimilation using a cyanobacterial membrane protein, ictB. J Plant Physiol 212:58–68PubMedCrossRefPubMedCentralGoogle Scholar
  70. Ho MY, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353:aaf9178PubMedCrossRefPubMedCentralGoogle Scholar
  71. Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. J Cereal Sci 48:580–591CrossRefGoogle Scholar
  72. Hu M, Zhao X, Liu Q, Hong X, Zhang W, Zhang Y, Sun L, Li H, Tong Y (2018) Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol J 16:1858–1867PubMedPubMedCentralCrossRefGoogle Scholar
  73. Hunter P (2016) The potential of molecular biology and biotechnology for dealing with global warming. EMBO Rep 17:946–948PubMedPubMedCentralCrossRefGoogle Scholar
  74. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate change 2007: the physical science basis. In: Solomon S et al (eds) Contribution of working group I to the fourth annual assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 996Google Scholar
  75. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF et al (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 1535Google Scholar
  76. Ishikawa C, Hatanaka T, Misoo S, Miyake C, Fukayama H (2011) Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiol 156:1603–1611PubMedPubMedCentralCrossRefGoogle Scholar
  77. Jansson C, Wullschleger SD, Kalluri UC, Tuskan GA (2010) Phytosequestration: carbon biosequestration by plants and the prospects of genetic engineering. BioSci 60:685–696CrossRefGoogle Scholar
  78. Jansson C, Vogel J, Hazen S, Brutnell T, Mockler T (2018) Climate-smart crops with enhanced photosynthesis. J Exp Bot 69:3801–3809PubMedCrossRefPubMedCentralGoogle Scholar
  79. Jez JM, Lee SG, Sherp AM (2016) The next green movement: plant biology for the environment and sustainability. Science 353:1241–1244PubMedCrossRefPubMedCentralGoogle Scholar
  80. Julkowska M (2018) Releasing the cytokinin brakes on root growth. Plant Physiol 177:865–866PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kanevski I, Maliga P, Rhoades DF, Gutteridge S (1999) Plastome engineering of ribulose-1,5-bisphosphate carboxylase/oxygenase in tobacco to form a sunflower large subunit and tobacco small subunit hybrid. Plant Physiol 119:133–142PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kanno K, Suzuki Y, Makino A (2017) A small decrease in Rubisco content by individual suppression of RBCS genes leads to improvement of photosynthesis and greater biomass production in rice under conditions of elevated CO2. Plant Cell Physiol 58:635–642PubMedCrossRefPubMedCentralGoogle Scholar
  83. Kaur H, Peel A, Acosta K, Gebril S, Ortega JL, Sengupta-Gopalan C (2019) Comparison of alfalfa plants overexpressing glutamine synthetase with those overexpressing sucrose phosphate synthase demonstrates a signaling mechanism integrating carbon and nitrogen metabolism between the leaves and nodules. Plant Dir 3:e00115CrossRefGoogle Scholar
  84. Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch H-J, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599PubMedCrossRefPubMedCentralGoogle Scholar
  85. Kell DB (2011) Breeding crop plants with deep roots: their role in sustainable carbon, nutrient and water sequestration. Annals Bot 108:407–418CrossRefGoogle Scholar
  86. Khadilkar AS, Yadav UP, Salazar C, Shulaev V, Paez-Valencia J, Pizzio GA, Gaxiola RA, Ayre BG (2016) Constitutive and companion-cell specific over-expression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport. Plant Physiol 170:401–414PubMedCrossRefPubMedCentralGoogle Scholar
  87. Khumsupan P, Donovan S, McCormick AJ (2019) CRISPR/Cas in Arabidopsis: overcoming challenges to accelerate improvements in crop photosynthetic efficiencies. Physiol Plant.  https://doi.org/10.1111/ppl.12937 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Kirst H, Gabilly ST, Niyogi KK, Lemaux PG, Melis A (2017) Photosynthetic antenna engineering to improve crop yields. Planta 245:1009–1020PubMedCrossRefPubMedCentralGoogle Scholar
  89. Kirst H, Shen Y, Vamvaka E, Betterle N, Xu D, Warek U, Strickland JA, Melis A (2018) Downregulation of the CpSRP43 gene expression confers a truncated light-harvesting antenna (TLA) and enhances biomass and leaf-to-stem ratio in Nicotiana tabacum canopies. Planta 248:139–154PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kitao M, Koike T, Tobita H, Maruyama Y (2005) Elevated CO2 and limited nitrogen nutrition can restrict excitation energy dissipation in photosystem II of Japanese white birch (Betula platyphylla var. japonica) leaves. Physiol Plant 125:64–73CrossRefGoogle Scholar
  91. Köhler IH, Ruiz-Vera UM, VanLoocke A, Thomey ML, Clemente T, Long SP, Ort DR, Bernacchi CJ (2017) Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions. J Exp Bot 68:715–726PubMedPubMedCentralGoogle Scholar
  92. Kromdijk J, Long SP (2016) One crop breeding cycle from starvation? How engineering crop photosynthesis for rising CO2 and temperature could be one important route to alleviation. Proc Biol Sci 283:20152578PubMedPubMedCentralCrossRefGoogle Scholar
  93. Kromdijk J, Glowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861PubMedCrossRefPubMedCentralGoogle Scholar
  94. Kurasova I, Kalina J, Štroch M, Urban O, Špunda V (2003) Response of photosynthetic apparatus of spring barley (Hordeum vulgare L.) to combined effect of elevated CO2 concentration and different growth irradiance. Photosynthetica 41:209–219CrossRefGoogle Scholar
  95. Lanoue J, Leonardos ED, Khosla S, Hao X, Grodzinski B (2018) Effect of elevated CO2 and spectral quality on whole plant gas exchange patterns in tomatoes. PLoS One 13:e0205861PubMedPubMedCentralCrossRefGoogle Scholar
  96. Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19:3889–3900PubMedPubMedCentralCrossRefGoogle Scholar
  97. Laporte MM, Galagan JA, Shapiro JA, Boersig MR, Shewmaker CK, Sharkey TD (1997) Sucrose-phosphate synthase activity and yield analysis of tomato plants transformed with maize sucrose-phosphate synthase. Planta 203:253–259CrossRefGoogle Scholar
  98. Laporte MM, Galagan JA, Prasch AL, Vanderveer PJ, Hanson DT, Shewmaker CK, Sharkey TD (2001) Promoter strength and tissue specificity effects on growth of tomato plants transformed with maize sucrose-phosphate synthase. Planta 212:817–822PubMedCrossRefPubMedCentralGoogle Scholar
  99. Lawson T, Bryant B, Lefebvre S, Lloyd JC, Raines CA (2006) Decreased SBPase activity alters growth and development in transgenic tobacco plants. Plant Cell Environ 29:48–58PubMedCrossRefPubMedCentralGoogle Scholar
  100. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876PubMedCrossRefPubMedCentralGoogle Scholar
  101. Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138:451–460PubMedPubMedCentralCrossRefGoogle Scholar
  102. Leggewie G, Kolbe A, Lemoine R, Roessner U, Lytovchenko A, Zuther E, Kehr J, Frommer WB, Riesmeier JW, Willmitzer L, Fernie AR (2003) Overexpression of the sucrose transporter SoSUT1 in potato results in alterations in leaf carbon partitioning and in tuber metabolism but has little impact on tuber morphology. Planta 217:158–167PubMedPubMedCentralGoogle Scholar
  103. Lehmeier C, Pajor R, Lundgren MR et al (2017) Cell density and air-space patterning in the leaf can be manipulated to increase leaf photosynthetic capacity. Plant J 92:981–994PubMedPubMedCentralCrossRefGoogle Scholar
  104. Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272PubMedPubMedCentralCrossRefGoogle Scholar
  105. Lewis JD, Wang XZ, Griffin KL, Tissue DT (2002) Effects of age and ontogeny on photosynthetic responses of a determinate annual plant to elevated CO2 concentrations. Plant Cell Environ 25:359–368CrossRefGoogle Scholar
  106. Li T, Li H, Zhang YX, Liu JY (2011) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833PubMedCrossRefPubMedCentralGoogle Scholar
  107. Lieman-Hurwitz J, Rachmilevitch S, Mittler R, Marcus Y, Kaplan A (2003) Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3 accumulation in cyanobacteria. Plant Biotechnol J 1:43–50PubMedCrossRefPubMedCentralGoogle Scholar
  108. Lin MT, Occhialini A, Andralojc JP, Devonshire J, Hines KM, Parry MAJ, Hanson MR (2014a) β-carboxysomal proteins assemble into highly organized structures in Nicotiana chloroplasts. Plant J 79:1–12PubMedPubMedCentralCrossRefGoogle Scholar
  109. Lin MT, Occhialini A, Andralojc J, Parry MAJ, Hanson MR (2014b) A faster Rubisco with potential to increase photosynthesis in crops. Nature 513:547–550PubMedPubMedCentralCrossRefGoogle Scholar
  110. Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ 14:729–739CrossRefGoogle Scholar
  111. Long S (1993) The significance of light-limiting photosynthesis to crop canopy carbon gain and productivity—a theoretical analysis. In: Abrol Y et al (eds) Photosynthesis: photoreactions to plant productivity. Springer, Dordrecht, pp 547–560CrossRefGoogle Scholar
  112. Long SP, Spence AK (2013) Toward cool C(4) crops. Annu Rev Plant Biol 64:701–722PubMedCrossRefPubMedCentralGoogle Scholar
  113. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662CrossRefGoogle Scholar
  114. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefPubMedCentralGoogle Scholar
  115. 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 161:56–66PubMedCrossRefPubMedCentralGoogle Scholar
  116. Long BM, Hee WY, Sharwood RE, Rae BD, Kaines S, Lim Y-L, Nguyen ND, Massey B, Bala S, von Caemmerer S, Badger MR, Price GD (2018) Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nat Comm 9:3570CrossRefGoogle Scholar
  117. López-Calcagno P, 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 field-grown transgenic tobacco plants. Plant Biotechnol J 17:141–151PubMedCrossRefPubMedCentralGoogle Scholar
  118. Ludewig F, Sonnewald U (2016) Demand for food as driver for plant sink development. J Plant Physiol 203:110–115PubMedCrossRefPubMedCentralGoogle Scholar
  119. Mahinthichaichan P, Morris DM, Wang Y, Jensen GJ, Tajkhorshid E (2018) Selective permeability of carboxysome shell pores to anionic molecules. J Phys Chem B 122:9110–9118PubMedPubMedCentralCrossRefGoogle Scholar
  120. Maier A, Fahnenstich H, von Caemmerer S, Engqvist MKM, Weber APM, Flügge U-I, Maurin VG (2012) Transgenic introduction of a glycolate oxidative cycle into A. thaliana chloroplasts leads to growth improvement. Front Plant Sci 3:38PubMedPubMedCentralCrossRefGoogle Scholar
  121. Maliga P, Bock R (2011) Plastid biotechnology: food, fuel, and medicine for the 21st century. Plant Physiol 155:1501–1510PubMedPubMedCentralCrossRefGoogle Scholar
  122. Maugarny-Calès A, Gonçalves B, Jouannic S, Melkonian M, Wong GKS, Laufs P (2016) Apparition of the NAC transcription factors predates the emergence of land plants. Mol Plant 9:1345–1348PubMedCrossRefPubMedCentralGoogle Scholar
  123. Maurino VG, Peterhänsel C (2010) Photorespiration: current status and approaches for metabolic engineering. Curr Opin Plant Biol 13:249–256PubMedCrossRefPubMedCentralGoogle Scholar
  124. McGrath JM, Long SP (2014) Can the cyanobacterial carbon-concentrating mechanism increase photosynthesis in crop species? A theoretical analysis. Plant Physiol 164:2247–2261PubMedPubMedCentralCrossRefGoogle Scholar
  125. Meinshausen M, Smith SJ, Calvin K, Daniel JS, Kainuma MLT, Lamarque J-F, Matsumoto K, Montzka SA, Raper SCB, Riahi K, Thomson A, Velders GJM, van Vuuren DPP (2011) The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim Chang 109:213CrossRefGoogle Scholar
  126. Meng Q, Runkle ES (2019) Far-red radiation interacts with relative and absolute blue and red photon flux densities to regulate growth, morphology, and pigmentation of lettuce and basil seedlings. Sci Hortic 255:269–280CrossRefGoogle Scholar
  127. Meyer M, Griffiths H (2013) Origins and diversity of eukaryotic CO2- concentrating mechanisms: lessons for the future. J Exp Bot 64:769–786PubMedCrossRefPubMedCentralGoogle Scholar
  128. Meyer FD, Talbert LE, Martin JM, Lanning SP, Greene TW, Giroux MJ (2007) Field evaluation of transgenic wheat expressing a modified ADP-glucose pyrophosphorylase large subunit. Crop Sci 47:336–342CrossRefGoogle Scholar
  129. Meyer MT, Genkov T, Skepper JN, Jouhet J, Mitchell MC, Spreitzer RJ, Griffiths H (2012) Rubisco small-subunit alpha-helices control pyrenoid formation in Chlamydomonas. Proc Natl Acad Sci USA 109:19474–19479PubMedCrossRefPubMedCentralGoogle Scholar
  130. Micallef BJ, Haskins KA, Vanderveer PJ, Roh K-S, Shewmaker CK, Sharkey TD (1995) Altered photosynthesis, flowering, and fruiting in transgenic tomato plants that have an increased capacity for sucrose synthesis. Planta 196:327–334CrossRefGoogle Scholar
  131. Miyagawa Y, Tamoi M, Shigeoka S (2001) Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nat Biotechnol 19:965–969PubMedCrossRefPubMedCentralGoogle Scholar
  132. Moore BD, Cheng SH, Sims D, Seemann JR (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated atmospheric CO2. Plant Cell Environ 22:567–582CrossRefGoogle Scholar
  133. Myers SS, Zanobetti A, Kloog I et al (2014) Increasing CO2 threatens human nutrition. Nature 510:139–142PubMedPubMedCentralCrossRefGoogle Scholar
  134. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565PubMedCrossRefPubMedCentralGoogle Scholar
  135. Nölke G, Houdelet M, Kreuzaler F, Peterhänsel C, Schillberg S (2014) The expression of a recombinant glycolate dehydrogenase polyproteins in potato (Solanum tuberosum) plastids strongly enhances photosynthesis and tuber yield. Plant Biotechnol J 12:734–742PubMedCrossRefPubMedCentralGoogle Scholar
  136. Nölke G, Barsoum M, Houdelet M, Arcalís E, Kreuzaler F, Fischer R, Schillberg S (2018) The integration of algal carbon concentration mechanism components into tobacco chloroplasts increases photosynthetic efficiency and biomass. Biotechnol J 14:e1800170CrossRefGoogle Scholar
  137. Occhialini A, Lin MT, Andralojc PJ, Hanson MR, Parry MAJ (2016) Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO2. Plant J 85:148–160PubMedPubMedCentralCrossRefGoogle Scholar
  138. Oiestad AJ, Martin JM, Giroux MJ (2016) Overexpression of ADP-glucose pyrophosphorylase in both leaf and seed tissue synergistically increase biomass and seed number in rice (Oryza sativa ssp. japonica). Funct Plant Biol 43:1194–1204CrossRefGoogle Scholar
  139. Oliveira IC, Brears T, Knight TJ, Clark A, Coruzzi GM (2002) Overexpression of cytosolic glutamine synthetase. Relation to nitrogen, light and photorespiration. Plant Physiol 129:1170–1180PubMedPubMedCentralCrossRefGoogle Scholar
  140. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87PubMedCrossRefPubMedCentralGoogle Scholar
  141. Onoda Y, Hikosaka K, Hirose T (2005) Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum. J Exp Bot 56:755–763PubMedCrossRefPubMedCentralGoogle Scholar
  142. Orr DJ, Pereira AM, da Fonseca Pereira P, Pereira-Lima ÍA, Zsögön A, Araújo WL (2017) Engineering photosynthesis: progress and perspectives. F1000 Res 6:1891CrossRefGoogle Scholar
  143. Ort DR, Zhu XG, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85PubMedCrossRefPubMedCentralGoogle Scholar
  144. Ort DR, Merchant SS, Alric J et al (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Nat Acad Sci 112:8529–8536PubMedCrossRefPubMedCentralGoogle Scholar
  145. Pan J, Huang D, Guo Z, Kuang Z, Zhang H, Xie X, Ma Z, Gao S, Lerdau MT, Chu C, Li L (2018a) Overexpression of microRNA408 enhances photosynthesis, growth, and seed yield in diverse plants. J Integ Plant Biol 60:323–340CrossRefGoogle Scholar
  146. Pan X, Ma J, Su X, Cao P, Chang W, Liu Z, Zhang X, Li M et al (2018b) Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II. Science 360:1109–1113PubMedCrossRefPubMedCentralGoogle Scholar
  147. Park J-Y, Canam T, Kang K-Y, Ellis DD, Mansfield SD (2008) Over-expression of an Arabidopsis family A sucrose phosphate synthase (SPS) gene alters plant growth and fibre development. Transgenic Res 17:181–192PubMedCrossRefPubMedCentralGoogle Scholar
  148. Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ (2003) Manipulation of Rubisco: the amount, activity, function and regulation. J Exp Bot 54:1321–1333PubMedCrossRefPubMedCentralGoogle Scholar
  149. Parry MAJ, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE, Alonso H, Whitney SM (2013) Rubisco activity and regulation as targets for crop improvement. J Exp Bot 64:717–730PubMedCrossRefPubMedCentralGoogle Scholar
  150. Peet MM, Huber SC, Patterson DT (1986) Acclimation to high CO2 in monoecious cucumbers II. Carbon exchange rates, enzyme activities, and starch and nutrient concentrations. Plant Phyiol 80:63–67CrossRefGoogle Scholar
  151. Pérez-López U, Robredo A, Lacuesta M, Sgherri C, Mena-Petite A, Navari-Izzo F, Muñoz-Rueda A (2010) Lipoic acid and redox status in barley plants subjected to salinity and elevated CO2. Physiol Plant 139:256–268PubMedPubMedCentralGoogle Scholar
  152. Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Phyisol 155:49–55CrossRefGoogle Scholar
  153. Peterhänsel C, Horst I, Niessen M, Blume C, Kebeish R, Kürkcüoglu S, Kreuzaler F (2010) Photorespiration. Arabidopsis Book 8:e0130PubMedPubMedCentralCrossRefGoogle Scholar
  154. Pinter PJ, Idso SB, Hendrix DL, Rokey RR, Raschkolb RS, Mauney JR, Kimball BA, Hendrey GR, Lewin KF, Nagy J (1994) Effect of free-air CO2 enrichment on the chlorophyll content of cotton leaves. Agric Forest Meteorol 70:163–169CrossRefGoogle Scholar
  155. Pizzio GA, Paez-Valencia J, Khadilkar AS et al (2015) Arabidopsis type I proton-pumping pyrophosphatase expresses strongly in phloem, where it is required for pyrophosphate metabolism and photosynthate partitioning. Plant Physiol 167:1541–1553PubMedPubMedCentralCrossRefGoogle Scholar
  156. Poovaiah CR, Mazarei M, Decker SR, Turner GB, Sykes RW, Davis MF, Stewart CN (2015) Transgenic switchgrass (Panicum virgatum L.) biomass is increased by overexpression of switchgrass sucrose synthase (PvSUS1). Biotechnol J 10:552–563PubMedCrossRefPubMedCentralGoogle Scholar
  157. Preiss J (1997) Modulation of starch synthesis. In: Foyer CH, Quick W (eds) A molecular approach to primary metabolism in higher plants. Taylor and Francis, London, pp 81–104Google Scholar
  158. Price GD, Howitt SM (2014) Towards turbocharged photosynthesis. Nature 513:497–498PubMedCrossRefPubMedCentralGoogle Scholar
  159. Ramireddy E, Hosseini SA, Eggert K, Gillandt S, Gnad H, von Wirén N, Scmülling T (2018) Root engineering in barley: increasing cytokinin degradation produces a larger root system, mineral enrichment in the shoot and improved drought tolerance. Plant Physiol 177:1078–1095PubMedPubMedCentralCrossRefGoogle Scholar
  160. Redillas MCFR, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, Ha S-H, Reuzeau C, Kim J-K (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10:792–805PubMedCrossRefPubMedCentralGoogle Scholar
  161. Reed S, Atkinson T, Gorecki C, Espinosa K, Przybylski S, Goggi AS, Palmer RG, Sandhu D (2014) Candidate gene identification for a lethal chlorophyll-deficient mutant in soybean. Agronomy 4:462–469CrossRefGoogle Scholar
  162. Ren T, Weraduwage SM, Sharkey TD (2019) Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology. J Exp Bot 70:1153–1165PubMedCrossRefPubMedCentralGoogle Scholar
  163. Robredo A, Pérez-López U, Lacuesta M, Mena-Petite A, Muñoz-Rueda A (2010) Influence of water stress on photosynthetic characteristics in barley plants under ambient and elevated CO2 concentrations. Biol Plant 54:285–292CrossRefGoogle Scholar
  164. Robson TM, Klem K, Urban O, Jansen MAK (2015) Re-interpreting plant morphological responses to UV-B radiation. Plant Cell Environ 38:856–866PubMedCrossRefPubMedCentralGoogle Scholar
  165. Rochaix J-D (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta Bioenerg 1807:375–383CrossRefGoogle Scholar
  166. Rogers A, Ainsworth EA (2006) The response of foliar carbohydrates to elevated [CO2]. In: Nösberger J et al (eds) Managed Ecosystems and CO2. Case studies, processes and perspectives. Springer-Verlag, Berlin, pp 293–310CrossRefGoogle Scholar
  167. Rogers A, Ellsworth DS (2002) Photosynthetic acclimation of Pinus taeda (loblolly pine) to long-term growth in elevated pCO2 (FACE). Plant Cell Environ 25:851–858CrossRefGoogle Scholar
  168. Rogers A, Humphries SW (2000) A mechanistic evaluation of photosynthetic acclimation at elevated CO2. Glob Chang Biol 6:1005–1011CrossRefGoogle Scholar
  169. Rogers A, Fischer BU, Bryant J, Frehner M, Blum H, Raines CA, Long SP (1998) Acclimation of photosynthesis to elevated CO2 under low N nutrition is effected by the capacity for assimilated utilization. Perennial ryegrass under free-air CO2 enrichment. Plant Physiol 118:683–692PubMedPubMedCentralCrossRefGoogle Scholar
  170. Rosenthal DM, Locke AM, Khozaei M, Raines CA, Long SP, Ort DR (2011) Over-expressing the C3 photosynthesis cycle enzyme Sedoheptulose-1,7 bisphosphatase improves photosynthetic carbon gain and yield under fully open air CO2 fumigation (FACE). BMC Plant Biol 11:123PubMedPubMedCentralCrossRefGoogle Scholar
  171. Ruan CJ, Shao HB, Teixeira da Silva JA (2012) A critical review on the improvement of photosynthetic carbon assimilation in C3 plants using genetic engineering. Crit Rev Biotechnol 32:1–21PubMedCrossRefPubMedCentralGoogle Scholar
  172. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916PubMedPubMedCentralCrossRefGoogle Scholar
  173. Rutherford A, Faller P (2003) Photosystem II: evolutionary perspectives. Phil Trans R Soc Lond B 358:245–253CrossRefGoogle Scholar
  174. Rutherford AW, Osyczka A, Rappaport F (2012) Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett 586:603–616PubMedCrossRefPubMedCentralGoogle Scholar
  175. Ruuska SA, Andrews TJ, Badger MR, Price GD, von Caemmerer S (2000) The role of chloroplast electron transport and metabolites in modulating rubisco activity in tobacco. Insights from transgenic plants with reduced amounts of cytochrome b/f complex or glyceraldehyde 3-phosphate dehydrogenase. Plant Physiol 122:491–504PubMedPubMedCentralCrossRefGoogle Scholar
  176. Saalbach I, Mora-Ramírez I, Weichert N et al (2014) Increased grain yield and micronutrient concentration in transgenic winter wheat by ectopic expression of a barley sucrose transporter. J Cereal Sci 60:75–81CrossRefGoogle Scholar
  177. Sage RF, Sharkey TD, Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89:590–596PubMedPubMedCentralCrossRefGoogle Scholar
  178. Sage RF, Kocacinar F, Kubien DS (2010) C4 photosynthesis and temperature. In: Raghavendra A, Sage R (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Advances in photosynthesis and respiration, vol 32. Springer, Dordrecht, pp 161–195CrossRefGoogle Scholar
  179. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47PubMedCrossRefPubMedCentralGoogle Scholar
  180. Sakowska K, Alberti G, Genesio L et al (2018) Leaf and canopy photosynthesis of a chlorophyll deficient soybean mutant. Plant Cell Environ 41:1427–1437PubMedCrossRefPubMedCentralGoogle Scholar
  181. Seger M, Ortega JL, Bagga S, Gopalan CS (2009) Repercussion of mesophyll-specific overexpression of a soybean cytosolic glutamine synthetase gene in alfalfa (Medicago sativa L.) and tobacco (Nicotiana tabacum L.). Plant Sci 176:119–129PubMedPubMedCentralCrossRefGoogle Scholar
  182. Seger M, Gebril S, Tabilona J, Peel A, Sengupta-Gopalan C (2015) Impact of concurrent overexpression of cytosolic glutamine synthetase (GS1) and sucrose phosphate synthase (SPS) on growth and development in transgenic tobacco. Planta 241:69–81PubMedCrossRefPubMedCentralGoogle Scholar
  183. Seneweera S (2011) Effects of elevated CO2 on plant growth and nutrient partitioning of rice (Oryza sativa L.) at rapid tillering and physiological maturity. J Plant Interact 6:35–42CrossRefGoogle Scholar
  184. 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 requirement of C4 photosynthesis? Photosynth Res 119:169–180PubMedCrossRefPubMedCentralGoogle Scholar
  185. Sharwood RE (2017) Engineering chloroplasts to improve Rubisco catalysis: prospects for translating improvements into food and fiber crops. New Phytol 213:494–510PubMedCrossRefPubMedCentralGoogle Scholar
  186. Sheen J (1994) Feedback control of gene expression. Photosynth Res 39:427–438PubMedCrossRefPubMedCentralGoogle Scholar
  187. Shen B-R, Wang L-M, Lin X-L, Yao Z, Xu H-W, Zhu C-H, Teng H-Y, Cui L-L, Liu E-E, Zhang J-J, He Z-H, Peng X-X (2019) Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice. Mol Plant 12:199–214PubMedCrossRefPubMedCentralGoogle Scholar
  188. Signora L, Galtier N, Skøt L, Lucas H, Foyer CH (1998) Over-expression of sucrose phosphate synthase in Arabidopsis thaliana results in increased foliar sucrose/starch ratios and favours decreased foliar carbohydrate accumulation in plants after prolonged growth with CO2 enrichment. J Exp Bot 49:669–680Google Scholar
  189. Simkin AJ, McAusland L, Headland LR, Lawson T, Raines CA (2015) Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield. J Exp Bot 66:4075–4090PubMedPubMedCentralCrossRefGoogle Scholar
  190. Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T, Timm S, Bauwe H, Raines CA (2017a) Simultaneous stimulation of sedoheptulose 1,7-bisphosphatase, fructose 1,6-bisphosphate aldolase and the photorespiratory glycine decarboxylase-H protein increases CO2 assimilation, vegetative biomass and seed yield in Arabidopsis. Plant Biotechnol J 15:805–816PubMedPubMedCentralCrossRefGoogle Scholar
  191. Simkin AJ, McAusland L, Lawson T, Raines CA (2017b) Over-expression of the RieskeFeS protein increases electron transport rates and yield in Arabidopsis. Plant Physiol 175:134–145PubMedPubMedCentralCrossRefGoogle Scholar
  192. Simkin AJ, López-Calcagno PE, Raines CA (2019) Feeding the world: improving photosynthetic efficiency for sustainable crop production. J Exp Bot 70:1119–1140PubMedPubMedCentralCrossRefGoogle Scholar
  193. Slattery RA, Ort DR (2015) Photosynthetic energy conversion efficiency: setting a baseline for gauging future improvements in important food and biofuel crops. Plant Physiol 168:383–392PubMedPubMedCentralCrossRefGoogle Scholar
  194. Slattery RA, VanLoocke A, Bernacchi CJ, Zhu X-G, Ort DR (2017) Photosynthesis, light use efficiency, and yield of reduced-chlorophyll soybean mutants in field conditions. Front Plant Sci 8:549PubMedPubMedCentralCrossRefGoogle Scholar
  195. Smidansky ED, Meyer FD, Blakeslee B, Weglarz TE, Greene TW, Giroux MJ (2007) Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism. Planta 225:965–976PubMedCrossRefPubMedCentralGoogle Scholar
  196. Song Z, Zhang L, Wang Y, Li H, Li S, Zhao H, Zhang H (2018) Constitutive expression of miR408 improves biomass and seed yield in Arabidopsis. Front Plant Sci 8:2114PubMedPubMedCentralCrossRefGoogle Scholar
  197. Sonnewald U, Fernie AR (2018) Next-generation strategies for understanding and influencing source-sink relations in crop plants. Curr Opin Plant Biol 43:63–70PubMedCrossRefPubMedCentralGoogle Scholar
  198. South PF, Cavanagh AP, Liu HW, Ort DR (2019) Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:eaat9077PubMedCrossRefPubMedCentralGoogle Scholar
  199. Srinivasan V, Kumar P, Long SP (2017) Decreasing, not increasing, leaf area will raise crop yields under global atmospheric change. Glob Chang Biol 23:1626–1635PubMedCrossRefPubMedCentralGoogle Scholar
  200. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  201. Su XD, Ma J, Wei XP et al (2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357:816–820CrossRefGoogle Scholar
  202. Sun A, Dai Y, Zhang X, Li C, Meng K, Xu H, Wei X, Xiao G, Ouwerkerk PBF, Wang M, Zhu Z (2011) A transgenic study on affecting potato tuber yield by expressing the rice sucrose transporter genes OsSUT5Z and OsSUT2M. J Integ Plant Biol 53:586–595CrossRefGoogle Scholar
  203. Suzuki Y, Miyamoto T, Yoshizawa R, Mae T, Makino A (2009) Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant Cell Environ 32:417–427PubMedCrossRefPubMedCentralGoogle Scholar
  204. Taler D, Galperin M, Benjamin I, Cohen Y, Kenigsbuch D (2004) Plant eR genes that encode photorespiratory enzymes confer resistance against disease. Plant Cell 16:172–184PubMedPubMedCentralCrossRefGoogle Scholar
  205. Tang W, Su T, Han M et al (2016) Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean (Glycine max). J Exp Bot 68:469–482PubMedCentralGoogle Scholar
  206. Tausz M, Tausz-Posch S, Norton RM, Fitzgerald GJ, Nicolas ME, Seneweera S (2013) Understanding crop physiology to select breeding targets and improve crop management under increasing atmospheric CO2 concentrations. Environ Exper Bot 88:71–80CrossRefGoogle Scholar
  207. Tcherkez GG, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA 103:7246–7251PubMedCrossRefPubMedCentralGoogle Scholar
  208. Thompson M, Gamage D, Hirotsu N, Martin A, Seneweera S (2017) Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk. Front Physiol 8:578PubMedPubMedCentralCrossRefGoogle Scholar
  209. Tilman D, Clark M (2015) Food, agriculture and the environment: can we feed the world and save the Earth? Daedalus 144:8–23CrossRefGoogle Scholar
  210. Timm S, Florian A, Arrivault S, Stitt M, Fernie AR, Bauwe H (2012a) Glycine decarboxylase controls photosynthesis and plant growth. FEBS Lett 586:3692–3697PubMedCrossRefPubMedCentralGoogle Scholar
  211. Timm S, Mielewczik M, Florian A, Frankenbach S, Dreissen A, Hocken N, Fernie AR, Walter A, Bauwe H (2012b) High-to-low CO2 acclimation reveals plasticity of the photorespiratory pathway and indicates regulatory links to cellular metabolism of Arabidopsis. PLoS One 7:e42809PubMedPubMedCentralCrossRefGoogle Scholar
  212. Timm S, Wittmiß M, Gamlien S, Ewald R, Florian A, Frank M, Wirtz M, Hell R, Fernie AR, Bauwe H (2015) Mitochondrial dihydrolipoyl dehydrogenase activity shapes photosynthesis and photorespiration of Arabidopsis thaliana. Plant Cell 27:1968–1984PubMedPubMedCentralCrossRefGoogle Scholar
  213. Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716PubMedCrossRefPubMedCentralGoogle Scholar
  214. 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. J Exp Bot 63:3001–3009PubMedCrossRefPubMedCentralGoogle Scholar
  215. United Nations Department of Economic and Social Affairs (2017) World population prospects. The 2017 revision. Key findings and advance tables. ESA/P/WP/248Google Scholar
  216. Van der Kooi CJ, Reich M, Löw M, De Kok LJ, Tausz M (2016) Growth and yield stimulation under elevated CO2 and drought: a meta-analysis on crops. Environ Exp Bot 122:150–157CrossRefGoogle Scholar
  217. Vercruyssen L, Gonzalez N, Werner T, Schmülling T, Inzé D (2011) Combining enhanced root and shoot growth reveals cross talk between pathways that control plant organ size in Arabidopsis. Plant Physiol 155:1339–1352PubMedPubMedCentralCrossRefGoogle Scholar
  218. Vicentini A, Barber JC, Aliscioni SS, Giussani LM, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Chang Biol 14:2963–2977CrossRefGoogle Scholar
  219. Von Caemmerer S, Furbank RT (2003) The C(4) pathway: an efficient CO(2) pump. Photosynth Res 77:191–207CrossRefGoogle Scholar
  220. Von Caemmerer S, Quick WP (2000) Rubisco: physiology in vivo. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis. Advances in photosynthesis and respiration, vol 9. Springer, Dordrecht, pp 85–113Google Scholar
  221. Von Schweinichen C, Büttner M (2005) Expression of a plant cell wall invertase in roots of Arabidopsis leads to early flowering and an increase in whole plant biomass. Plant Biol (Stuttg) 7:469–475CrossRefGoogle Scholar
  222. Voss I, Sunil B, Scheibe R, Raghavendra AS (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol 15:713–722PubMedCrossRefPubMedCentralGoogle Scholar
  223. 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 67:107PubMedCrossRefPubMedCentralGoogle Scholar
  224. Walker BJ, Drewry DT, Slattery RA, VanLoocke A, Cho YB, Ort DR (2017) Chlorophyll can be reduced in crop canopies with little penalty to photosynthesis. Plant Physiol 176:1215–1232PubMedPubMedCentralCrossRefGoogle Scholar
  225. Wang D, Heckathorn SA, Wang X, Philpott SM (2012) A meta-analysis of plant physiological and growth responses to temperature and elevated CO2. Oecologia 169:1–13PubMedCrossRefPubMedCentralGoogle Scholar
  226. Wang L, Feng Z, Schjoerring JK (2013) Effects of elevated atmospheric CO2 on physiology and yield of wheat (Triticum aestivum L.): a meta-analytic test of current hypotheses. Agric Ecosyst Environ 178:57–63CrossRefGoogle Scholar
  227. Wang L, Lu Q, Wen X, Lu C (2015) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862PubMedPubMedCentralGoogle Scholar
  228. Wang L-F, Qi X-X, Huang X-S, Xu L-L, Jin C, Wu J, Zhang S-L (2016) Overexpression of sucrose transporter gene PbSUT2 from Pyrus bretschneideri, enhances sucrose content in Solanum lycopersicum fruit. Plant Physiol Biochem 105:150–161PubMedCrossRefPubMedCentralGoogle Scholar
  229. Warren JM, Jensen AM, Medlyn BE, Norby RJ, Tissue DT (2015) Carbon dioxide stimulation of photosynthesis in Liquidambar styraciflua is not sustained during a 12-year field experiment. AoB Plants 7:plu074CrossRefGoogle Scholar
  230. Werner T, Nehnefajova E, Köllmer I, Novák O, Stmad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920PubMedPubMedCentralCrossRefGoogle Scholar
  231. West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PE (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530PubMedCrossRefPubMedCentralGoogle Scholar
  232. Whitney SM, Baldet P, Hudson GS, Andrews TJ, Form I (2001) Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26:535–547PubMedCrossRefPubMedCentralGoogle Scholar
  233. Whitney S, Birch R, Kelso C, Beck JL, Kapralov MV (2015) Improving recombinant Rubisco biogenesis, plant photosynthesis and growth by coexpressing its ancillary RAF1 chaperone. Proc Natl Acad Sci USA 112:3564–3569PubMedCrossRefPubMedCentralGoogle Scholar
  234. Wingler A, Lea PJ, Quick P, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Phil Trans R Soc Lond B Biol Sci 355:1517–1529CrossRefGoogle Scholar
  235. Woodward FI, Bardgett RD, Raven JA, Hetherington AM (2009) Biological approaches to global environment change mitigation and remediation. Curr Biol 19:R615–R623PubMedCrossRefPubMedCentralGoogle Scholar
  236. Xhu C, Kobayashi K, Loladze I, Zhu J, Jiang Q, Xu X, Liu G, Seneweera S, Ebi KL, Drewnowski A, Fukagawa NK, Ziska LH (2018) Carbon dioxide (CO2) levels this century will alter the protein, micronutrients, and vitamin content of rice grains with potential health consequences for the poorest rice-dependent countries. Sci Adv 4:eaaq1012CrossRefGoogle Scholar
  237. Xu F, Wang K, Yuan W, Xu W, Shuang L, Kronzucker HJ, Chen G, Miao R, Zhang M, Ding M, Xiao L, Kai L, Zhang J, Zhu Y (2019) Overexpression of rice aquaporin OsPIP1;2 improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport. J Exp Bot 70:671–681PubMedCrossRefPubMedCentralGoogle Scholar
  238. Yadav SK, Khatri K, Rathore MS, Jha B (2018) Introgression of UfCyt c6, a thylakoid lumen protein from a green seaweed Ulva fasciata Delile enhanced photosynthesis and growth in tobacco. Mol Biol Rep 45:1745–1758PubMedCrossRefPubMedCentralGoogle Scholar
  239. Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S (2011) The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol 155:956–962PubMedCrossRefPubMedCentralGoogle Scholar
  240. Yeates TO, Kerfeld CA, Heinhorst S, Cannon GC, Shively JM (2008) Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat Rev 6:681–691Google Scholar
  241. Zamft BM, Conrado RJ (2015) Engineering plants to reflect light: strategies for engineering water-efficient plants to adapt to a changing climate. Plant Biotechnol J 13:867–874PubMedCrossRefPubMedCentralGoogle Scholar
  242. Zhang H, Zhao X, Li J, Cai H, Deng XW, Li L (2014) MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper. Plant Cell 26:4933–4953PubMedPubMedCentralCrossRefGoogle Scholar
  243. Zhang J-P, Yu Y, Feng Y-Z, Zhou Y-F, Zhang F, Yang Y-W, Lei M-Q, Zhang Y-C, Chen Y-Q (2017) MiR408 regulates grain yield and photosynthesis via a phytocyanin protein. Plant Physiol 175:1175–1185PubMedPubMedCentralCrossRefGoogle Scholar
  244. Zheng Y, Li F, Hao L, Shedayi AA, Guo L, Ma C, Huang B, Xu M (2018) The optimal CO2 concentrations for the growth of three perennial grass species. BMC Plant Biol 18:27PubMedPubMedCentralCrossRefGoogle Scholar
  245. Zhu XG, Ort DR, Whitmarsh J, Long SP (2004a) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. J Exp Bot 55:1167–1175PubMedCrossRefPubMedCentralGoogle Scholar
  246. Zhu X-G, Portis AR Jr, Long SP (2004b) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165CrossRefGoogle Scholar
  247. Zhu X-G, 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 Physiol 145:513–526PubMedPubMedCentralCrossRefGoogle Scholar
  248. Zhu XG, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Curr Opin Biotechnol 19:153–159PubMedCrossRefPubMedCentralGoogle Scholar
  249. Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Crown 2019

Authors and Affiliations

  • Stacy D. Singer
    • 1
    Email author
  • Raju Y. Soolanayakanahally
    • 2
  • Nora A. Foroud
    • 1
  • Roland Kroebel
    • 1
  1. 1.Lethbridge Research and Development CentreAgriculture and Agri-Food CanadaLethbridgeCanada
  2. 2.Saskatoon Research and Development CentreAgriculture and Agri-Food CanadaSaskatoonCanada

Personalised recommendations