One decade after the discovery of single-cell C4 species in terrestrial plants: What did we learn about the minimal requirements of C 4 photosynthesis?

Photosynthesis Research

Volumn 119, Issue 1-2, 2014, Pages 169-180

  Sharpe, Richard M ^a   Offermann, Sascha ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Bundle sheath; Chloroplast differentiation; Kranz; Mesophyll; Photorespiration; Single cell C4 photosynthesis

Indexed keywords

BIENERTIA; SUAEDA;

CARBON DIOXIDE; ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE;

AMARANTHACEAE; CHLOROPLAST; CYTOLOGY; HISTOLOGY; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; REVIEW;

CARBON DIOXIDE; CHENOPODIACEAE; CHLOROPLASTS; ENZYMES; LIGHT; NAD; PHOTOSYNTHESIS; PLANT LEAVES;

EID: 84891628924     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-013-9810-9     Document Type: Review

References (74)

1. Akhani H, Barroca J, Koteeva N et al (2005) Bienertia sinuspersici (Chenopodiaceae): a new species from southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. System Bot 30:290-301
2. Akhani H, Lara MV, Ghasemkhani M et al (2008) Does Bienertia cycloptera with the single-cell system of C4 photosynthesis exhibit a seasonal pattern of δ13C values in nature similar to co-existing C4 Chenopodiaceae having the dual-cell (Kranz) system? Photosynth Res 99:23-36. doi: 10.1007/s11120-008-9376- 0
3. Akhani H, Chatrenoor T, Dehghani M, et al. (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 Biosys: Intl J Deal Aspect Plant Biol 1-10. doi: 10.1080/11263504.2012. 662921
4. Berry JO, McCormac DJ, Long JJ et al (1997) Photosynthetic gene expression in Amaranth, an NAD-ME type C4 dicot. Funct Plant Biol 24:423-428
5. Bowes G, Salvucci ME (1989) Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat Bot 34:233-266. doi: 10.1016/0304-3770(89)90058-2
6. Bowes G, Rao S, Estavillo GM, Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29:379-392
7. Buchmann N, Brooks JR, Rapp KD, Ehleringer JR (1996) Carbon isotope composition of C4 grasses is influenced by light and water supply. Plant, Cell Environ 19:392-402. doi: 10.1111/j.1365-3040.1996.tb00331.x
8. Carnal NW, Agostino A, Hatch MD (1993) Photosynthesis in phosphoenolpyruvate carboxykinase-type C-4 plants: mechanism and regulation of C-4 acid decarboxylation in bundle-sheath cells. Arch Biochem Biophys 306:360-367
9. Christin PA, Osborne CP, Sage RF et al (2011) C4 eudicots are not younger than C4 monocots. J Exp Bot 62:3171-3181. doi: 10.1093/jxb/err041
10. Chuong SDX, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell 18:2207-2223. doi: 10.1105/tpc.105.036186
11. Davis PA, Caylor S, Whippo CW, Hangarter RP (2011) Changes in leaf optical properties associated with light-dependent chloroplast movements. Plant, Cell Environ 34:2047-2059. doi: 10.1111/j.1365-3040.2011.02402.x
12. Doroshenk KA, Crofts AJ, Washida H et al (2010) Characterization of the rice glup4 mutant suggests a role for the small GTPase Rab5 in the biosynthesis of carbon and nitrogen storage reserves in developing endosperm. Breeding Sci 60:556-567
13. 2 concentrating mechanisms. Advances in photosynthesis and respiration, vol 32. Springer, Dordrecht, pp 29-61
14. Edwards GE, Voznesenskaya E, Smith M et al (2007) Breaking the Kranz paradigm in terrestrial C4 plants: does it hold promise for C4 rice? In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting new pathways to C4 rice. International Rice Research Institute, World Scientific, Los Banos
15. Farquhar G (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205. doi: 10.1071/PP9830205
16. Freitag H, Stichler W (2000) A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiaceae. Plant Biol 2:154-160. doi: 10.1055/s-2000-9462
17. Freitag H, Stichler W (2002) Bienertia cycloptera Bunge ex Boiss., Chenopodiaceae, another C4 plant without Kranz tissues. Plant Biol 4:121-132. doi: 10.1055/s-2002-20444
18. Furbank RT (2011) Evolution of the C4 photosynthetic mechanism: are there really three C4 acid decarboxylation types? J Exp Bot 62:3103-3108. doi: 10.1093/jxb/err080
19. Furumoto T, Yamaguchi T, Ohshima-Ichie Y et al (2011) A plastidial sodium-dependent pyruvate transporter. Nature 478:274. doi: 10.1038/nature10518
20. Hatch MD (1987) C-4 photosynthesis - a unique blend of modified biochemistry, anatomy and ultrastructure. Biochem Biophys Acta 895:81-106
21. 4 species. Funct Plant Biol 19:263-285
22. Inoue H, Rounds C, Schnell DJ (2010) The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22:1947-1960
23. Ivanova Y, Smith MD, Chen K et al (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 15:3379-3392
24. Kadereit G, Borsch T, Weising K et al (2003) Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis. Int J Plant Sci 164:959-986
25. Kadereit G, Ackerly D, Pirie MD (2012) A broader model for C4 photosynthesis evolution in plants inferred from the goosefoot family (Chenopodiaceae s.s.). Proc Royal Soc B: Biol Sci 279(1741):3304-3311. doi: 10.1098/rspb.2012.0440
26. Kagawa T (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138-2141. doi: 10.1126/science.291.5511.2138
27. Kapralov MV, Akhani H, Voznesenskaya EV et al (2006) Phylogenetic relationships in the Salicornioideae/Suaedoideae/Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets. System Bot 31:571-585. doi: 10.1043/06-01.1
28. Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int Rev Cel Mol Bio 280:185-218
29. Kerstetter RA, Poethig RS (1998) The specification of leaf identity during shoot development. Annu Rev Cell Dev Biol 14:373-398. doi: 10.1146/annurev.cellbio.14.1.373
30. 2-concentrating mechanism during single-cell C4 photosynthesis. Plant, Cell Environ 35:513-523. doi: 10.1111/j.1365-3040.2011.02431.x
31. Kubasek J, Setlik J, Dwyer S et al (2007) Light and growth temperature alter carbon isotope discrimination and estimated bundle sheath leakiness in C4 grasses and dicots. Photosynth Res 91:47-58
32. Kubis S, Patel R, Combe J et al (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16:2059-2077
33. Langdale J, Nelson T (1991) Spatial regulation of photosynthetic development in C4 plants. Trends Genet 7:191-196. doi: 10.1016/0168-9525(91) 90124-9
34. Langdale JA, Zelitch I, Miller E, Nelson T (1988) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J 7:3643-3651
35. Lara MV, Chuong SDX, Akhani H et al (2006) Species having C4 single-cell-type photosynthesis in the Chenopodiaceae family evolved a photosynthetic phosphoenolpyruvate carboxylase like that of Kranz-type C4 species. Plant Physiol 142:673-684. doi: 10.1104/pp.106.085829
36. Lara MV, Offermann S, Smith M et al (2008) Leaf Development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to Chlorenchyma structure under different light conditions. Plant Physiol 148:593-610. doi: 10.1104/pp.108.124008
37. Leisner CP, Cousins AB, Offermann S et al (2010) The effects of salinity on photosynthesis and growth of the single-cell C4 species Bienertia sinuspersici (Chenopodiaceae). Photosynth Res 106:201-214
38. Long JJ, Berry JO (1996) Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of Amaranth mitochondria. Plant Physiol 112:473-482. doi: 10.1104/pp.112.2.473
39. Lung SC, Chuong SD (2012) A transit peptide-like sorting signal at the C terminus directs the Bienertia sinuspersici preprotein receptor Toc159 to the chloroplast outer membrane. Plant Cell 24:1560-1578
40. Lung SC, Yanagisawa M, Chuong SD (2011) Protoplast isolation and transient gene expression in the single-cell C4 species Bienertia sinuspersici. Plant Cell Rep 30:473-484
41. Michaud M, Marechal-Drouard L, Duchene AM (2010) RNA trafficking in plant cells: targeting of cytosolic mRNAs to the mitochondrial surface. Plant Mol Biol 73:697-704
42. Mullen JL, Weinig C, Hangarter RP (2006) Shade avoidance and the regulation of leaf inclination in Arabidopsis. Plant, Cell Environ 29:1099-1106. doi: 10.1111/j.1365-3040.2005.01484.x
43. Northmore J, Zhou V, Chuong S (2012) Multiple shoot induction and plant regeneration of the single-cell C4 species Bienertia sinuspersici. Plant Cell Tiss Organ Cult 108:101-109
44. Offermann S, Danker T, Dreymüller D et al (2006) Illumination is necessary and sufficient to induce histone acetylation independent of transcriptional activity at the C4-specific phosphoenolpyruvate carboxylase promoter in maize. Plant Physiol 141:1078-1088
45. Offermann S, Okita TW, Edwards GE (2011a) Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiol 155:1612-1628. doi: 10.1104/pp.110.170381
46. Offermann S, Okita TW, Edwards GE (2011b) How do single cell C4 species form dimorphic chloroplasts? Plant Sig Behav 6:762-765. doi: 10.4161/psb.6.5.15426
47. Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35:415-442. doi: 10.1146/annurev.pp.35.060184.002215
48. Oswald A, Streubel M, Ljungberg U et al (1990) Differential biogenesis of photosystem-II in mesophyll and bundle-sheath cells of 'malic' enzyme NADP(+)-type C4 plants. A comparative protein and RNA analysis. Eur J Biochem 190:185-194. doi: 10.1111/j.1432-1033.1990.tb15563.x
49. Park J, Knoblauch M, Okita TW, Edwards GE (2008) Structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single-cell C4 photosynthesis in Bienertia sinuspersici. Planta 229:369-382. doi: 10.1007/s00425-008-0836-8
50. Park J, Okita TW, Edwards GE (2009) Salt tolerant mechanisms in single-cell C4 species Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae). Plant Sci 176:616-626. doi: 10.1016/j.plantsci.2009.01.014
51. Park J, Okita TW, Edwards GE (2010) Expression profiling and proteomic analysis of isolated photosynthetic cells of the non-Kranz C4 species Bienertia sinuspersici. Funct Plant Biol 37:1. doi: 10.1071/FP09074
52. Pick TR, Brautigam A, Schluter U et al (2011) Systems analysis of a maize leaf developmental gradient redefines the current C4 model and provides candidates for regulation. Plant Cell 23:4208-4220. doi: 10.1105/tpc.111.090324
53. Rosnow J, Offermann S, Park J et al (2011) In vitro cultures and regeneration of Bienertia sinuspersici (Chenopodiaceae) under increasing concentrations of sodium chloride and carbon dioxide. Plant Cell Rep 30:1541-1553
54. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341-370
55. Sage RF, Christin P-A, Edwards EJ (2011) The C4 plant lineages of planet earth. J Exp Bot 62:3155-3169. doi: 10.1093/jxb/err048
56. Sakurai N, Domoto K, Takagi S (2004) Blue-light-induced reorganization of the actin cytoskeleton and the avoidance response of chloroplasts in epidermal cells of Vallisneria gigantea. Planta 221:66-74. doi: 10.1007/s00425-004-1416-1
57. Schütze P, Freitag H, Weising K (2003) An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr. (Chenopodiaceae). Plant Sys Evo 239:257-286. doi: 10.1007/s00606-003-0013-2
58. Sharpe RM, Mahajan A, Takacs E et al (2011) Developmental and cell type characterization of bundle sheath and mesophyll chloroplast transcript abundance in maize. Curr Genet 57:89-102
59. Sheen J (1999) C4 gene expression. Annu Rev Plant Physiol Plant Mol Biol 50:187-217. doi: 10.1146/annurev.arplant.50.1.187
60. Sheen JY, Bogorad L (1987) Differential expression of C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 262:11726-11730
61. Smith MD, Rounds CM, Wang F et al (2004) AtToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J Cell Biol 165:323-334
62. Smith ME, Koteyeva NK, Voznesenskaya EV et al (2009) Photosynthetic features of non-Kranz type C4 versus Kranz type C4 and C3 species in subfamily Suaedoideae (Chenopodiaceae). Funct Plant Biol 36:770. doi: 10.1071/FP09120
63. Sommer M, Bräutigam A, Weber APM (2012) The dicotyledonous NAD malic enzyme C4 plant Cleome gynandra displays age-dependent plasticity of C4 decarboxylation biochemistry. Plant Biol 14:621-629. doi: 10.1111/j.1438-8677. 2011.00539.x
64. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. Techniques in plant science. CSIRO Publishing, Collingwood, VIC
65. 2 diffusion limitations of C3 leaves. Plant, Cell Environ 26:1191-1197
66. 2 pump. Photosynth Res 77:191-207
67. Voznesenskaya EV, Franceschi VR, Kiirats O et al (2001) Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature 414:543-546. doi: 10.1038/35107073
68. Voznesenskaya EV, Franceschi VR, Kiirats O et al (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J 31:649-662. doi: 10.1046/j.1365-313X.2002.01385.x
69. Voznesenskaya EV, Edwards GE, Kiirats O et al (2003) Development of biochemical specialization and organelle partitioning in the single-cell C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). Am J Bot 90:1669-1680. doi: 10.3732/ajb.90.12.1669
70. Voznesenskaya EV, Franceschi VR, Edwards GE (2004) Light-dependent development of single cell C4 photosynthesis in cotyledons of Borszczowia aralocaspica (Chenopodiaceae) during transformation from a storage to a photosynthetic organ. Annal Bot 93:177-187. doi: 10.1093/aob/mch026
71. Voznesenskaya EV, Koteyeva NK, Chuong SDX et al (2005) Differentiation of cellular and biochemical features of the single-cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). Am J Bot 92:1784-1795. doi: 10.3732/ajb.92.11.1784
72. Wang JL, Long JJ, Hotchkiss T, Berry JO (1993) C4 photosynthetic gene expression in light- and dark-grown Amaranth cotyledons. Plant Physiol 102:1085-1093. doi: 10.1104/pp.102.4.1085
73. Warburg O (1920) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen. II. Biochem. Z. 103:188-217
74. Weiner H, Burnell JN, Woodrow IE et al (1988) Metabolite diffusion into bundle sheath cells from C4 Plants. Plant Physiol 88:815-822. doi: 10.1104/pp.88.3.815