Walking the C4 pathway: Past, present, and future

Journal of Experimental Botany

Volumn 67, Issue 14, 2016, Pages 4057-4066

  Furbank, Robert T ^a,b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b CSIRO   (Australia)

Author keywords

Bundle sheath; C4 decarboxylation; C4 photosynthesis; Kranz anatomy; PEP carboxylase; Rubisco

Indexed keywords

CARBON DIOXIDE;

ANATOMY AND HISTOLOGY; BOTANY; EVOLUTION; FORECASTING; GENETIC ENGINEERING; HISTORY; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; TRANSGENIC PLANT; TRENDS;

BIOLOGICAL EVOLUTION; BOTANY; CARBON DIOXIDE; FORECASTING; GENETIC ENGINEERING; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; METABOLIC NETWORKS AND PATHWAYS; PHOTOSYNTHESIS; PLANTS; PLANTS, GENETICALLY MODIFIED;

EID: 84977499151     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw161     Document Type: Review

References (78)

1. Ashton AR, Burnell JN, Furbank RT, Jenkins CLD, Hatch MD. 1990. Enzymes of C4 photosynthesis. In: Lea PJ, ed. Methods in plant biochemistry, vol. 7. London: Academic Press, 39-72
2. Aubry S, Kelly S, Kumpers BMC, Smith-una RD, Hibberd JM. 2014. Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of C4 photosynthesis. PLoS Genetics 10, e1004365
3. Bassham JA. 2003. Mapping the carbon reduction cycle, a personal retrospective. Photosynthesis Reseach 76, 35-52
4. Berry JA. 2012. There ought to be an equation for that. Annual Review of Plant Biology 63, 1-17
5. Berry JA, Downton WJS, Tregunna EB. 1970. The photosynthetic carbon metabolism of Zea mays and Gomphrena globosa, the location of the CO2 fixation and carboxyl transfer reactions. Canadian Jouranl of Botany 48, 777-786
6. Bjorkman O, Gauhl E. 1969. Carboxydismutase activity in plants with and without β-carboxylation photosynthesis. Planta 88, 197-203
7. Black CC, Chen TM, Brown RH. 1969. Biochemical basis for plant competition. Weed Science 17, 338-344
8. Bräutigam A, Gowik U. 2016. Photorespiration connects C3 and C4 photosynthesis. Journal of Experimental Botany 67, 2953-2962
9. Bräutigam A, Schliesky S, Külahoglu C, Osborne CP, Weber APM. 2014. Towards an integrative model of C4 photosynthetic subtypes, insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species. Journal of Experimental Botany 65, 3579-3593
10. Brutnell TP, Wang L, Swartwood K, Goldschmidt A, Jackson D, Zhu XG, Kellogg E, Van Eck J. 2010. Setaria viridis, a model for C4 photosynthesis. The Plant Cell 22, 2537-2544
11. Chitty JA, Furbank RT, Marshall J, Chen Z, TaylorWC. 1994. Genetic transformation of the C4 plant, Flaveria bidentis. The Plant Journal 6, 949-956
12. Ding Z, Weissmann S, Wang M, Du B, Huang L, Tu X, Zhong S, Myers C, Brutnell TP, Sun Q, Li P. 2015. Identification of photosynthesis-associated C4 candidate genes through comparative leaf gradient transcriptome in multiple lineages of C3 and C4 species. PLoS One 10, e0140629
13. Downton WJS, Tregunna EB. 1968. Carbon dioxide compensation-its relation to photosynthetic carboxylation reactions, systematics of the Gramineae and leaf anatomy. Canadian Journal of Botany 46, 207-215
14. Edwards GE, Kanai R, Black CC. 1971. Phosphoenolpyruvate carboxykinase in leaves of certain plants which fix CO2 by the C4 dicarboxylic cycle of photosynthesis. Biochemical and Biophysical Research Communications 45, 278-285
15. Edwards GE, Lee S, Chen TM, Black CC. 1970. Carboxylation reactions and photosynthesis of carbon compounds in isolated mesophyll and bundle sheath cells of Digitaria sanguinalis (L) Scop. Biochemical and Biophysical Research Communications 39, 389-395
16. Egan A, Schlueter J, Spooner DM. 2012. Applications of next generation sequencing in plant biology. American Jornal of Botany 99, 175-185
17. El-Sharkaway MA, Hesketh JD. 1964 Effect of temperature and water deficit on leaf photosynthetic rates of different species. Crop Science 4, 514-518
18. Engelmann S, Zogel C, Koczor M, Schlue U, Streubel M, Westhoff P. 2008. Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 species Flaveria trinervia, the role of the proximal promoter region. BMC Plant Biology 8, 4
19. Farquhar GD. 1983. On the nature of carbon isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, 205-206
20. Furbank RT. 2011. Evolution of the C4 photosynthetic mechanism, are there really three C4 acid decarboxylation types? Journal of Experimental Botany 62, 3103-3108
21. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S, Ashton AR. 1997. Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Australian Journal of Plant Physiology 24, 477-485
22. Furbank RT, Hatch MD. 1987. Mechanism of C4 Photosynthesis. The Size and Composition of the Inorganic Carbon Pool in Bundle Sheath Cells. Plant Physiology 85, 958-964
23. Furbank RT, Jenkins CLD, Hatch MD. 1990. C4 photosynthesis, quantum requirement, C4 acid overcycling and Q-cycle involvement. Australian Journal of Plant Physiology 17, 1-7
24. Furbank RT, Quick WP, Sirault XRR. 2015. Improving photosynthesis and yield potential in cereal crops by targeted genetic manipulation. Prospects, progress and challenges. Field Crops Research 182, 19-29
25. Furbank RT, von Caemmerer S, John Sheehy J, Edwards G. 2009. C4 rice, a challenge for plant Phenomics. Functional Plant Biology 36, 845-856
26. Grass Phylogeny Working Group II. 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytologist 193, 304-312
27. Haberlandt G. 1904. Physiologische Pflanzenanatomie. Leipzig: Wilhelm Engelman
28. Hatch MD. 1971. The C4-pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C4-dicarboxylic acid. Biochemical Journal 125, 425-432
29. Hatch MD. 1987. C4 photosynthesis, a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81-106
30. Hatch MD. 1992a. The making of the C4 pathway. In: Murata N, ed. Research in photosynthesis. Vol. 3, Dordrecht, The Netherlands: KIuwer Academic Publishers, 747-756
31. Hatch MD. 1992b. I can't believe my luck, personal perspective. Photosynthesis Research 33, 1-14
32. Hatch MD. 1997. Resolving C4 photosynthesis, trials, tribulations and other unpublished stories. Australian Journal of Plant Physiology 24, 413-422
33. Hatch MD, Agostino A, Burnell JN. 1988. Photosynthesis in phosphoenolpyruvate carboxykinase-type C-4 plants-activity and role of mitochondria in bundle sheath-cells. Archives Of Biochemistry And Biophysics 261, 357-367
34. Hatch MD, Kagawa T. 1976. Photosynthetic activities of isolated bundle sheath cells in relation to differing mechanisms of C4 pathway photosynthesis. Archives of Biochemistry and Biophysics 175, 39-53
35. Hatch MD, Kagawa T, Craig S. 1975. Subdivision of C4 pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Australian Journal of Plant Physiology 2, 111-128
36. Hatch MD, Osmond CB. 1976. Compartmentation and transport in C4 photosynthesis. In: Stocking CR, Heber U, eds. Transport in plants III, Vol. 3. Berlin: Springer, 144-184
37. Hatch MD, Osmond CB, Slatyer RO, eds. 1971. Photosynthesis and photorespiration. New York: Wiley-Interscience
38. Hatch MD, Slack CR. 1966. Photosynthesis by sugar cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochemical Journal 101, 103-111
39. Hatch MD, Slack CR. 1998 C4 photosynthesis, discovery, resolution, recognition and significance. In: Kung S, Yang S, eds. Discoveries in plant biology, Vol 1. Singapore: World Scientific Publishing, 175-196
40. Hatch MD, Slack CR, Johnson HS. 1967. Further studies on a new pathway of photosynthetic CO2 fixation in sugar cane and its occurrence in other plant species. Biochemical Journal 102, 417-422
41. Hesketh JD. 1963. Limitations to photosynthesis responsible for differences among species. Crop Science 3, 493-496
42. Hibberd JM, Covshoff S. 2010. The regulation of gene expression required for C4 photosynthesis. Annual Review of Plant Biology 61, 181-207
43. Hodge AJ, McLean JD, Mercer FV. 1955. Ultrastructure of the lamellae and grana in the chloroplasts of Zea mays L. Journal of Biophysics, Biochemistry and Cytology 25, 605-614
44. Hudson GS, Evans JR, von Caemmerer S, Arvidsson YBC, Andrews TJ. 1992. Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. Plant Physiology 98, 294-302
45. Johnson H, Hatch MD. 1968. Distribution of the C4 dicarboxylic acid pathway and its occurrence in dicotyledonous plants. Phytochemistry 7, 375-380
46. Karpilov YS. 1960. The distribution of radioactive carbon 14 amongst the products of photosynthesis of maize. Trudy Kazansk Sel'shokoz Institute 41, 15-24
47. Kortschak HP, Hartt CE, Burr GO. 1965. Carbon dioxide fixation in sugarcane leaves. Plant Physiology 40, 209-213
48. Koteyeva NK, Voznesenskaya EV, Edwards GE. 2015. An assessment of the capacity for phosphoenolpyruvate carboxykinase to contribute to C4 photosynthesis. Plant Science 235, 70-80
49. Krysan PJ, Young JC, Sussman MR. 1999 T-DNA as an insertional mutagen in Arabidopsis. The Plant Cell 11, 2283-2290
50. Külahoglu C, Denton AK, Sommer M, et al. 2014. Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C3 and C4 plant species. The Plant Cell 26, 3243-3260
51. Li P, Ponnala L, Gandotra N, et al. 2010. The developmental dynamics of the maize leaf transcriptome. Nature Genetics 42, 1060-1067
52. Loomis RS, Williams WA. 1963. Maximum crop productivity-an estimate. Crop Science 3, 67-72
53. Lunn JE, Furbank RT, Hatch MD. 1997. ATP-mediated activation of sucrose-phosphate synthase in bundle sheath cells of C4 plants. Planta 202, 249-256
54. Meister M, Agostino A, Hatch MD. 1996. The roles of malate and aspartate in C4 photosynthetic metabolism of Flaveria bidentis (L.). Planta 199, 262-269
55. Moss DN. 1962. The limiting carbon dioxide concentration for photosynthesis. Nature 193, 587
56. Osmond CB. 1967. P-Carboxylation during photosynthesis in Atriplex. Biochimica et Biophysica Acta 141, 197-199
57. Rhoades MM, Carvalho A. 1944. The function and structure of the parenchyma sheath plastids of maize leaf. Bulletin if the Torrey Botanical Club 7, 335-346
58. Sage RF, Sage T, Kocacinar F. 2012. Photorespiration and the evolution of C4 photosynthesis. Annual Review of Plant Biology 63, 19-47
59. Settles MA, Holding DR, Tan BC, et al. 2007. Sequence-indexed mutations in maize using the UniformMu transposon-tagging population. BMC Genomics 8, 116
60. Shantz HL, Piemeisel LN. 1927. The water requirement of plants at Akron Colorado. Journal of Agricultural Research 34, 1093-1189
61. Sheehy JE, Ferrer AB, Mitchell PL, Elmino-Mabilangan A, Pablico P, Dionora MJA. 2007. How the rice crop works and why it needs a new engine. In: Sheehy JE, Mitchell PL, Hardy B, eds. Charting new pathways to C4 rice. Los Baños, Philippines: International Rice Institute, 3-26
62. Slack CR, Hatch MD. 1967. Comparative studies on the activities of carboxylases and other enzymes in relation to the new pathway of photosynthetic CO, fixation in tropical grasses. Biochemical Journal 103, 660-665
63. Slack CR, Hatch MD, Goodchild D. 1969. Distribution of enzymes in mesophyll and parenchyma sheath chloroplasts of maize leaves in relation to the C4 dicarboxylic add pathway of photosynthesis. Biochemical Journal 114, 489-498
64. Slewinski TL. 2013. Using evolution as a guide to engineer Kranz-type C4 photosynthesis. Frontiers in Plant Science 4, 212
65. Sonnewald U, Brauer M, von Schaewen A, Stitt M, Willmitzer L. 1991. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. The Plant Journal 1, 95-106
66. Stockhaus J, Schlue U, Koczor M, Chitty JA, Taylor WC, Westhoff P. 1997. The promoter of the gene encoding the C4 form of phosphoenolpyruvate carboxylase directs mesophyll-specific expression in transgenic C4 Flaveria spp. The Plant Cell 9, 479-489
67. von Caemmerer S, Furbank RT. 2003. The C4 pathway, an efficient CO2 pump. Photosynthesis Research 77, 191-207
68. von Caemmerer S, Furbank RT. 2016. Strategies for improving C4 photosynthesis. Current Opinion in Plant Biology (in press)
69. von Caemmerer S, Ghannoum O, Pengelly JJL, Cousins AB. 2014. Carbon isotope discrimination as a tool to explore C4 photosynthesis. Journal of Experimental Botany 65, 3459-3470
70. von Caemmerer S, Quick WP, Furbank RT. 2012. The development of C4 rice. Progress and future challenges. Science 336, 1671-1672
71. Voznesenskay EV, Franceschi VR, Kiirats O, Freitag H, Edwards GE. 2001. Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414, 543-546
72. Wang P, Kelly S, Fouracre JP, Langdale JA. 2013. Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 Kranz anatomy. The Plant Journal 75, 656-670
73. Wang Y, Bräutigam A, Weber APM, Zhu X-G. 2014. Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. Journal of Experimental Botany 65, 3567-3578
74. Wang L, Czedik-Eysenberg A, Mertz R, et al. 2014. Comparative analysis of C4 and C3 photosynthesis in developing leaves of maize and rice. Nature Biotechnology 32, 1158-1165
75. Weber APM, von Caemmerer S. 2010. Plastid transport and metabolism of C3 and C4 plants-comparative analysis and possible biotechnological exploitation. Current Opinion in Plant Biology 13, 257-265
76. Weiner H, Burnell J, Woodrow IE, Heldt H, Hatch MD. 1988. Metabolite diffusion into bundle sheath cells from C4 plants. Plant Physiology 88, 815-822
77. Williams BP, Burgess SJ, Reyna-Llorens I, Knerova J, Aubry S, Stanley S, Julian M, Hibberd JM. 2016. An untranslated cis-element regulates the accumulation of multiple C4 enzymes in Gynandropsis gynandra mesophyll cells. The Plant Cell 28, 454-465
78. Willmitzer L. 1988. The use of transgenic plants to study plant geneexpression. Trends in Genetics 4, 13-18