Single-cell C4 Photosynthesis

Öz

Single-cell C4 photosynthesis is a set of molecular biochemical, molecular, anatomical features. Single C4 photosynthesis is estimated to have occurred in the Oligocene about 25-30 million ago due to decreased CO2 levels. In higher plants, the efficiency of photosynthesis at high temperatures is limited by the oxygenase activity of the Rubisco (Ribulose 1,5 bisphosphate carboxylase/oxygenase) enzyme. Some terrestrial plants have developed enhancing mechanisms for Rubisco's CO2 retention to minimize the amount of carbon lost by photorespiration, and single-cell C4 photosynthesis has evolved in two different cell types called mesophyll and bundle sheath cells. C4 photosynthesis dimorphic chloroplast structure varies in Kranz anatomy and biochemistry of the C4 pathway. Single-cell C4 photosynthesis in terrestrial plants in the mid-1960s in four species belonging to the family Cheponodiaceae (Bienertia aralospica, Bienertia cycloptera, Bienertia sinuspersici, Bienertia kavirense) was also discovered. Single-cell C4 photosynthesis in Hydrilla verticillata, an aquatic and facultative (living in both an oxygenated and oxygen-free environment) monocot plant, has been discovered. In recent years, many studies have continued to be carried out to determine the properties of C4 plants. In this review, it is aimed to examine the subjects such as Single-cell C4 photosynthesis in terrestrial and aquatic plants, mechanism and chemistry of C4 photosynthesis.

Anahtar Kelimeler

• Single-cell C4 photosynthesis
• Rubisco
• C4 plants

Tek Hücre C4 Fotosentezi

Öz

Tek hücre C4 fotosentezi moleküler, biyokimyasal, anatomik özelliklerin bir bütünüdür. C4 fotosentezinin yaklaşık 25-30 milyon önce Oligosen’de CO2 seviyesindeki azalmaya bağlı olarak ortaya çıktığı tahmin edilmektedir. Yüksek yapılı bitkilerde, yüksek sıcaklıklarda fotosentezin verimliliği, Rubisco (Ribuloz 1,5 bisfosfat karboksilaz/oksijenaz) enziminin oksijenaz aktivitesi ile sınırlanmaktadır. Karasal bitkilerin bazıları fotorespirasyon ile kaybedilen karbon miktarını en aza indirmek için Rubisco’nun CO2 tutması için arttırıcı mekanizmalar geliştirmiştir ve tek hücre C4 fotosentezi Kranz anatomi olarak isimlendirilen mezofil ve demet kını adı verilen iki farklı hücre tipinde evrimleşmiştir. C4 fotosentezi dimorfik kloroplast yapısı, Kranz anatomi ve C4 yolunun biyokimyası olarak çeşitlilik göstermektedir. Karasal bitkilerde tek hücre C4 fotosentezi 1960’ların ortalarında Chenopodiaceae familyasına ait dört türde (Bienertia aralospica, Bienertia cycloptera, Bienertia sinuspersici, Bienertia kavirense), sucul ve fakültatif (hem oksijenli hem de oksijensiz ortamda yaşayan) tek çenekli bir bitki olan Hydrilla verticillata’ da keşfedilmiştir. Son yıllarda C4 bitkilerinin özelliklerinin ortaya konması için birçok çalışma yapılmaya devam edilmektedir. Bu derlemede, karasal ve sucul bitkilerde tek hücre C4 fotosentezi, C4 fotosentezinin mekanizması, kimyası gibi konuların incelenmesi amaçlanmıştır.

Anahtar Kelimeler

• Tek hücre C4 fotosentezi
• Rubisco
• C4 bitkileri

Kaynakça

1. Akhani H, Chatrenoor T, Dehghani M, Khoshravesh R, Mahdavi P, Matinzadeh Z. 2012. A new species of Bienertia (Chenopodiaceae) from Iranian salt deserts: a third species of the genus and discovery of a fourth terrestrial C4 plant without Kranz anatomy. Plant Biosystems-An International J Dealing with all Aspects of Plant Biology, 146(3): 550-559.
2. Andersson I, Backlund A. 2008. Structure and function of Rubisco. Plant Physiology and Biochemistry, 46(3): 275-291.
3. Badger MR, Spalding MH, Leegood RC, Sharkey TD, von Caemmerer S. 2000. Photosynthesis: physiology and metabolism. Switzerland: Springer, 369-397.
4. Bar-On YM, Milo R. 2019. The global mass and average rate of Rubisco. Proceedings of the National Academy of Sci, 116(10): 4738-4743.
5. Benedict CR, Beevers H. 1961. Formation of sucrose from malate in germinating castor beans. I. Conversion of malate to phosphoenol-pyruvate. Plant Physiology, 36(5): 540.
6. Bowes G, Salvucci ME. 1989. Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquatic Botany, 34(1-3): 233-266.
7. Bowes G, Rao SK, Reiskind JB. 2003. Photosynthetic acclimation of rice to global climate change: Will a same-cell C4 system help? In Rice Sci: Innovations and impact for livelihood. Proceedings of the International Rice Research Conference, 16-19 September, Beijing, China, pp. 659-671.
8. Bowes G, Rao SK, Estavillo GM, Reiskind JB. 2002. C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Functional Plant Biology, 29(3): 379-392.

9. Bowes, G, Rao, S. K, Reiskind, J. B, Estavillo, G. M, Rao, V. S. 2008. Hydrilla: retrofitting a C3 leaf with a single-cell C4 NADP-Malik enzym system. In Charting new pathways to C4 rice (pp. 275-296).
10. Brown JMA, Dromgoole FI, Towsey MW. 1974. Photosynthesis and photorespiration in aquatic macrophytes. Bull R Soc NZ.
11. Burnell JN, Hatch MD. 1988. Photosynthesis in phosphoenolpyruvate carboxykinase-type C4 plants: pathways of C4 acid decarboxylation in bundle sheath cells of Urochloa panicoides. Archives of Biochemistry and Biophysics, 260(1): 187-199.
12. Burnell JN. 2011. Hurdles to engineering greater photosynthetic rates in crop plants: C4 rice. In: Raghavendra, A.S, Sage, R.B. (Eds.): C4Photosynthesis and Related CO2 Concentrating Mechanisms. Springer, Dordrecht, The Netherlands,pp. 361–378.
13. Busch FA. 2020. Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism. The Plant J, 101(4): 919-939.
14. Casati P, Lara MV, Andreo CS. 2000. Induction of a C4-Like Mechanism of CO2 Fixation in Egeria densa, a Submersed Aquatic Species. Plant Physiology, 123(4): 1611-1622.
15. Chapman KS, Hatch MD. 1983. Intracellular location of phosphoenolpyruvate carboxykinase and other C4 photosynthetic enzymes in mesophyll and bundle sheath protoplasts of Panicum maximum. Plant Sci Letters, 29(2-3): 145-154.
16. Chuong SD, Franceschi VR, Edwards GE. 2006. The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. The Plant Cell, 18(9): 2207-2223.
17. Dengler NG, Nelson T. 1999. Leaf structure and development in C4 plants.
18. Dittrich P, Campbell, W. H, Black Jr, C. C. 1973. Phosphoenolpyruvate carboxykinase in plants exhibiting crassulacean acid metabolism. Plant Physiology, 52(4): 357-361.
19. Drozak A, Wasilewska W, Buczyńska A, Romanowska E. 2012. C4 type photosynthesis. Postepy Biochemii, 58(1): 44-53.
20. Edwards, G. E, Franceschi, V. R, Voznesenskaya, E. V. 2004. Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu. Rev. Plant Biol, 55, 173-196.
21. Falkowski PG, Raven JA. 2013. Aquatic photosynthesis. In Aquatic Photosynthesis. Princeton University Press.
22. Fan Y, Asao S, Furbank RT, von Caemmerer S, Day DA, Tcherkez G, Atkin OK. 2022. The crucial roles of mitochondria in supporting C4 photosynthesis. New Phytologist, 233(3): 1083-1096.
23. Freitag H, Stichler W. 2000. A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiaceae. Plant Biology, 2(2): 154-160.
24. Furbank RT. 2011. Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? J Experiment Botany, 62(9): 3103-3108.
25. Furbank RT. 2016. Walking the C4 pathway: past, present, and future. J Experimental Botany, 67(14): 4057-4066.
26. Garner DM, Mure CM, Yerramsetty P, Berry JO. 2016. Kranz anatomy and the C4 pathway. eLS. Chichester: John Wiley & Sons Ltd. URL: http://www. els. net [doi: 10.1002/9780470015902. a0001295. pub3].
27. Grass Phylogeny Working Group II. 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist, 193(2): 304-312.
28. Gutierrez M, Gracen VE, Edwards GE. 1974. Biochemical and cytological relationships in C4 plants. Planta, 119(4): 279-300.
29. Hatch MD. 1987. C4 Photosynthesis: a Unique Elend of Modified Biochemistry, Anatomy and Ultrastructure. Biochimica et Biophysica Acta (BBA)-Reviews on Bioenergetics, 895:2, 81-106.
30. Hatch MD. 1992. C4 photosynthesis: an unlikely process full of surprises. Plant and Cell Physiology, 33.4: 333-342.
31. Hatch MD. 2005. C4 photosynthesis: discovery and resolution. Discoveries in Photosynthesis, 875-880.
32. Hattersley, PW, Watson, L. 1976. C4 grasses: an anatomical criterion for distinguishing between NADP-malic enzyme species and PCK or NAD-malic enzyme species. Australian J Botany, 24(2): 297-308.
33. Hayes JM. 1994. Global methanotrophy at the Archean-Proterozoic transition. Early life on Earth, 220-236.
34. Heckmann D, Schulze S, Denton A, Gowik U, Westhoff P, Weber AP, Lercher MJ. 2013. Predicting C4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell, 153(7): 1579-1588.
35. Holaday AS, Bowes G. 1980. C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata). Plant Physiology, 65(2): 331-335.
36. Hopkinson BM, Dupont CL, Allen AE, Morel FM. 2011. Efficiency of the CO2-concentrating mechanism of diatoms. Proceedings of the National Academy of Sci, 108(10): 3830-3837.
37. Karki S, Rizal G, Quick WP. 2013. Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C4 pathway. Rice, 6(1): 1-8.
38. Ku MS, Spalding MH, Edwards GE. 1980. Intracellular localization of phosphoenolpyruvate carboxykinase in leaves of C4 and CAM plants. Plant Sci Letters, 19(1): 1-8.
39. Leegood RC, Ap Rees T. 1978. Phosphoenolpyruvate carboxykinase and gluconeogenesis in cotyledons of Cucurbita pepo. Biochimica et Biophysica Acta, 524(1): 207-218.
40. Leegood RC, Walker RP. 1999. Regulation of the C4 pathway. In C4 Plant Biology (Sage, R.F. and Monson, R.K, eds): pp. 89–131, Academic Press
41. Lundgren MR, Osborne CP, Christin PA. 2014. Deconstructing Kranz anatomy to understand C4 evolution. J Experimental Botany, 65(13): 3357-3369.
42. Lung SC, Yanagisawa M, Chuong SD. 2012. Recent progress in the single-cell C4 photosynthesis in terrestrial plants. Frontiers in biology, 7(6): 539-547.
43. Maberly SC, Gontero B. 2017. Ecological imperatives for aquatic CO2-concentrating mechanisms. J Experimental Botany, 68(14): 3797-3814.
44. Magnin NC, Cooley BA, Reiskind JB, Bowes G. 1997. Regulation and localization of key enzymes during the induction of Kranz-less, C4-type photosynthesis in Hydrilla verticillata. Plant Physiology, 115(4): 1681-1689.
45. Matsuoka, M, Furbank, R. T, Fukayama, H, Miyao, M. 2001. Molecular engineering of C4 photosynthesis. Annual Review of Plant Biology, 52(1): 297-314.
46. McKown AD, Dengler NG. 2007. Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). American J Botany, 94(3): 382-399.
47. Prendergast, H. D. V, Hattersley, P. W, Stone, N. E. 1987. New structural/biochemical associations in leaf blades of C4 grasses (Poaceae). Functional Plant Biology, 14(4): 403-420.
48. Rao S, Reiskind J, Bowes G. 2006. Light Regulation of the Photosynthetic Phosphoenol pyruvate Carboxylase (PEPC) in Hydrilla verticillata. Plant and Cell Physiology, 47(9): 1206-1216.
49. Rao, X, Dixon, R. A. 2016. The differences between NAD-ME and NADP-ME subtypes of C4 photosynthesis: more than decarboxylating enzymes. Frontiers Plant Sci, 7, 1525..
50. Reinfelder JR, Kraepiel AM, Morel FM. 2000. Unicellular C4 photosynthesis in a marine diatom. Nature, 407(6807): 996-999.
51. Reinfelder JR, Milligan AJ, Morel FM. 2004. The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology, 135(4): 2106-2111.
52. Reiskind JB, Bowes G. 1991. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proceedings of the National Academy of Sci, 88(7): 2883-2887.
53. Roberts K, Granum E, Leegood RC, Raven JA. 2007. C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology, 145(1): 230-235.
54. Roell MS, von Borzyskowski LS, Westhoff P, Plett A, Paczia N, Claus P, Weber AP. 2021. A synthetic C4 shuttle via the β-hydroxyaspartate cycle in C3 plants. Proceedings of the National Academy of Sci, 118(21).
55. Sage RF, Li M, Monson RK. 1999. The taxonomic distribution of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 173–211. Academic Press, San Diego, California
56. Sage RF. 1999. Why C4 photosynthesis. C4plant biology, 3-16.
57. Sage RF. 2004. The evolution of C4 photosynthesis. New phytologist, 161(2): 341-370.
58. Sage RF, Christin, P. A, Edwards, E. J. 2011. The C4 plant lineages of planet Earth. J Experimental Botany, 62(9): 3155-3169.
59. Sage RF, Sage TL, Kocacinar F. 2012. Photorespiration and the evolution of C4 photosynthesis. Annual review of plant biology, 63, 19-47.
60. Sage TL, Sage RF. 2009. The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant and Cell Physiology, 50(4): 756-772.
61. Salvucci ME, Bowes G. 1981. Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. Plant Physiology, 67(2): 335-340.
62. Salvucci ME, Bowes, G. 1983. Ethoxyzolamide repression of the low photorespiration state in two submersed angiosperms. Planta, 158(1): 27-34.
63. Soros CL, Dengler, N. G. 2001. Ontogenetic derivation and cell differentiation in photosynthetic tissues of C3 and C4 Cyperaceae. American J Botany, 88(6): 992-1005.
64. Van Ginkel, L. C, Bowes, G, Reiskind, J. B, Prins, H. B. 2001. A CO2-flux mechanism operating via pH-polarity in Hydrilla verticillata leaves with C3 and C4 photosynthesis. Photosynthesis Research, 68(1): 81-88.
65. Van TK, Haller WT, Bowes G. 1976. Comparison of the photosynthetic characteristics of three submersed aquatic plants. Plant Physiology, 58(6): 761-768.
66. Von Caemmerer, S. 2013. Steady‐state models of photosynthesis. Plant, Cell, Environ, 36(9): 1617-1630.
67. Von Caemmerer, S. Ghannoum, O. Furbank R. T. 2017. C4 photosynthesis: 50 years of discovery and innovation. J Experiment Botany, 68: 97-102.
68. Von Caemmerer, S, Furbank, R. T. 2016. Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology, 31, 125-134.
69. Von Caemmerer, S, Edwards, G. E, Koteyeva, N, Cousins, A. B. 2014. Single cell C4 photosynthesis in aquatic and terrestrial plants: a gas exchange perspective. Aquatic Botany, 118, 71-80.
70. Von Caemmerer S, Quick WP, Furbank RT. 2012. The development of C4 rice: current progress and future challenges. Sci, 336(6089): 1671-1672.
71. Voznesenskaya EV, Edwards GE, Kiirats O, Artyusheva EG, Franceschi VR. 2003. Development of biochemical specialization and organelle partitioning in the single‐cell C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). American J Botany, 90(12): 1669-1680.
72. Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H, Edwards GE. 2002. Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J, 31(5): 649-662.
73. Voznesenskaya EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE. 2001. Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature, 414(6863): 543-546.
74. Voznesenskaya EV, Koteyeva NK, Chuong SD, Akhani H, Edwards GE, Franceschi VR. 2005. Differentiation of cellular and biochemical features of the single‐cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). American J Botany, 92(11): 1784-1795.
75. Wang S, Tholen D, Zhu X. G. 2017. C4 photosynthesis in C3 rice: a theoretical analysis of biochemical and anatomical factors. Plant, Cell, Environ, 40(1): 80-94.
76. Yoshimura Y, Kubota F, Ueno O. 2004. Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta, 220(2): 307-317.