Advertisement

Photosynthesis Research

, Volume 119, Issue 1–2, pp 169–180 | Cite as

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

  • Richard M. Sharpe
  • Sascha OffermannEmail author
Review

Abstract

Until about 10 years ago the general accepted textbook knowledge was that terrestrial C4 photosynthesis requires separation of photosynthetic functions into two specialized cell types, the mesophyll and bundle sheath cells forming the distinctive Kranz anatomy typical for C4 plants. This paradigm has been broken with the discovery of Suaeda aralocaspica, a chenopod from central Asia, performing C4 photosynthesis within individual chlorenchyma cells. Since then, three more single-cell C4 (SCC4) species have been discovered in the genus Bienertia. They are interesting not only because of their unusual mode of photosynthesis but also present a puzzle for cell biologists. In these species, two morphological and biochemical specialized types of chloroplasts develop within individual chlorenchyma cells, a situation that has never been observed in plants before. Here we review recent literature concerning the biochemistry, physiology, and molecular biology of SCC4 photosynthesis. Particularly, we focus on what has been learned in relation to the following questions: How does the specialized morphology required for the operation of SCC4 develop and is there a C3 intermediate type of photosynthesis during development? What is the degree of specialization between the two chloroplast types and how does this compare to the chloroplasts of Kranz C4 species? How do nucleus-encoded proteins that are targeted to chloroplasts accumulate differentially in the two chloroplast types and how efficient is the CO2 concentrating mechanism in SCC4 species compared to the Kranz C4 forms?

Keywords

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

Notes

Acknowledgments

We are grateful to Gerald E. Edwards and Christoph Peterhaensel for critical reading of the manuscript. This study was supported by grants from the National Science Foundation, Grants IOS 0641232 and MCB 1146928 and by the Civilian Research and Development Foundation Grant RUB1-2982-ST-10 in support of RMS and from the Deutsche Forschungsgemeinschaft (OF106/1-1) to SO.

References

  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 30:290–301CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 24:423–428Google Scholar
  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 CrossRefGoogle Scholar
  6. Bowes G, Rao S, Estavillo GM, Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29:379–392CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 306:360–367PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 60:556–567CrossRefGoogle Scholar
  13. Edwards GE, Voznesenskaya EV (2011) C4 photosynthesis: Kranz forms and single-cell C4 in terrestrial plants. In: Raghavendra AS, Sage RF (eds) C4 photosynthesis and related CO2 concentrating mechanisms. Advances in photosynthesis and respiration, vol 32. Springer, Dordrecht, pp 29–61Google Scholar
  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 BanosGoogle Scholar
  15. Farquhar G (1983) On the nature of carbon isotope discrimination in C4 species. Aust J Plant Physiol 10:205. doi: 10.1071/PP9830205 CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  19. Furumoto T, Yamaguchi T, Ohshima-Ichie Y et al (2011) A plastidial sodium-dependent pyruvate transporter. Nature 478:274. doi: 10.1038/nature10518 CrossRefGoogle Scholar
  20. Hatch MD (1987) C-4 photosynthesis—a unique blend of modified biochemistry, anatomy and ultrastructure. Biochem Biophys Acta 895:81–106CrossRefGoogle Scholar
  21. Henderson S, Caemmerer S, Farquhar G (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Funct Plant Biol 19:263–285Google Scholar
  22. Inoue H, Rounds C, Schnell DJ (2010) The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22:1947–1960PubMedCentralPubMedCrossRefGoogle Scholar
  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 15:3379–3392PubMedCentralPubMedCrossRefGoogle Scholar
  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 164:959–986CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  28. Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int Rev Cel Mol Bio 280:185–218CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  30. King JL, Edwards GE, Cousins AB (2012) The efficiency of the CO2-concentrating mechanism during single-cell C4 photosynthesis. Plant, Cell Environ 35:513–523. doi: 10.1111/j.1365-3040.2011.02431.x CrossRefGoogle Scholar
  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 91:47–58PubMedCrossRefGoogle Scholar
  32. Kubis S, Patel R, Combe J et al (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16:2059–2077PubMedCentralPubMedCrossRefGoogle Scholar
  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 PubMedGoogle Scholar
  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 7:3643–3651PubMedGoogle Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar
  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 106:201–214PubMedCrossRefGoogle Scholar
  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 PubMedCentralPubMedGoogle Scholar
  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 24:1560–1578PubMedCentralPubMedCrossRefGoogle Scholar
  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 30:473–484PubMedCrossRefGoogle Scholar
  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 73:697–704PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 108:101–109CrossRefGoogle Scholar
  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 141:1078–1088PubMedCentralPubMedCrossRefGoogle Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  47. Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35:415–442. doi: 10.1146/annurev.pp.35.060184.002215 CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar
  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 30:1541–1553PubMedCrossRefGoogle Scholar
  54. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 57:89–102PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 262:11726–11730PubMedGoogle Scholar
  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 165:323–334PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  64. von Caemmerer S (2000) Biochemical models of leaf photosynthesis. Techniques in plant science. CSIRO Publishing, Collingwood, VICGoogle Scholar
  65. von Caemmerer S (2003) C4 photosynthesis in a single C3 cell is theoretically inefficient but may ameliorate internal CO2 diffusion limitations of C3 leaves. Plant, Cell Environ 26:1191–1197CrossRefGoogle Scholar
  66. von Caemmerer S, Furbank R (2003) The C4 pathway: an efficient CO2 pump. Photosynth Res 77:191–207CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 CrossRefGoogle Scholar
  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 PubMedCrossRefGoogle Scholar
  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 PubMedCentralPubMedGoogle Scholar
  73. Warburg O (1920) Über die Geschwindigkeit der photochemischen Kohlensäurezersetzung in lebenden Zellen. II. Biochem. Z. 103:188–217Google Scholar
  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 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.School of Biological ScienceWashington State UniversityPullmanUSA
  2. 2.Molecular Plant Sciences Graduate ProgramWashington State UniversityPullmanUSA
  3. 3.Institute of BotanyLeibniz UniversityHannoverGermany

Personalised recommendations