REVIEW

Recent progress in the single-cell C4 photosynthesis in terrestrial plants

  • Shiu-Cheung LUNG 1 ,
  • Makoto YANAGISAWA 2 ,
  • Simon D. X. CHUONG , 1
Expand
  • 1. Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada
  • 2. Agronomy Department, Purdue University, West Lafayette, IN 47907-2054, USA

Received date: 31 Aug 2012

Accepted date: 09 Oct 2012

Published date: 01 Dec 2012

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

Abstract

Currently, single-cell C4 photosynthesis has been reported in four terrestrial plant species, Bienertia cycloptera, B. sinuspersici, B. kavirense and Suaeda aralocaspica, of family Chenopodiaceae. These species possess novel mechanisms of C4 photosynthesis through spatial partitioning of organelles and key enzymes in distinct cytoplasmic domains within single chlorenchyma cells. Anatomical and biochemical studies have shown that the three Bienertia species and S. aralocaspica utilize biochemical and organellar compartmentation to achieve the equivalent spatial separation of Kranz anatomy but within a single photosynthetic cell. These discoveries have challenged the paradigm for C4 photosynthesis in terrestrial plants which had suggested for more than 40 years that the Kranz feature was indispensably required for its C4 function. In this review, we focus on the recent progress in understanding the cellular and molecular mechanisms that control the spatial relationship of organelles in these unique single-cell C4 systems. The demonstrated interaction of dimorphic chloroplasts with microtubules and actin filaments has shed light on the importance of these cytoskeleton components in the intracellular partitioning of organelles. Future perspectives on the potential function of the cytoskeleton in targeting gene products to specific subcellular compartments are discussed.

Cite this article

Shiu-Cheung LUNG , Makoto YANAGISAWA , Simon D. X. CHUONG . Recent progress in the single-cell C4 photosynthesis in terrestrial plants[J]. Frontiers in Biology, 2012 , 7(6) : 539 -547 . DOI: 10.1007/s11515-012-9248-z

Acknowledgments

This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and the University of Waterloo Start-Up Fund.
1
Akhani H, Barroca J, Koteeva N K, Voznesenskaya E V, Franceschi V, Edwards G, Ghaffari S, Ziegler H (2005). Bienertia sinuspersici (Chenopodiaceae): A new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Syst Bot, 30(2): 290–301

DOI

2
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 Biosys,

DOI

3
Bashirullah A, Cooperstock R L, Lipshitz H D (1998). RNA localization in development. Annu Rev Biochem, 67(1): 335–394

DOI PMID

4
Chen X, Schnell D J (1999). Protein import into chloroplasts. Trends Cell Biol, 9(6): 222–227

DOI PMID

5
Chuong S D X, Franceschi V R, Edwards G E (2006). The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell, 18(9): 2207–2223

DOI PMID

6
Chuong S D X, Park N I, Freeman M C, Mullen R T, Muench D G (2005). The peroxisomal multifunctional protein interacts with cortical microtubules in plant cells. BMC Cell Biol, 6(1): 40

DOI PMID

7
Collings D A, Lill A W, Himmelspach R, Wasteneys G O (2006). Drug sensitisation studies show actin microfilaments and microtubules interact during root elongation in Arabidopsis thaliana. New Phytol, 170: 275–290

DOI PMID

8
Crofts A J, Washida H, Okita T W, Satoh M, Ogawa M, Kumamaru T, Satoh H (2005). The role of mRNA and protein sorting in seed storage protein synthesis, transport, and deposition. Biochem Cell Biol, 83(6): 728–737

DOI PMID

9
Edwards G E, Franceschi V R, Voznesenskaya E V (2004). Single cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu Rev Plant Physiol Plant Mol Biol, 55: 173–196

10
Edwards G E, Huber S C (1981). The C4 pathway. In The biochemistry of plants, a comprehensive treatise. Vol.8. Photosynthesis, M.D. Hatch and N.K. Boardman, eds (N.Y., London, Toronto, Sydney, San Francisco: Acad. Press), pp. 237–281.

11
Edwards G E, Voznesenskaya V E, Smith M, Koteyeva N K, Park Y I, Park J H, Kiirats O, Okita T W, Chuong S D X (2008). Breaking the paradigm in C4 photosynthesis: Does it hold promise for C4 rice? In: Charting New Pathways to C4Rice. Eds Sheehy JE, Mitchell PL and Hardy B. World Scientific Publishing Co. pp. 249–273.

12
Edwards G E, Walker D A (1983). C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis. Oxford: Blackwell Scientific Publications

13
Freitag H, Stichler W (2000). A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodeaceae. Plant Biol, 2(2): 154–160

DOI

14
Hatch M D, Slack C R (1970). Photosynthetic CO2-fixation pathways. Annu Rev Plant Physiol, 21: 141–163. In: Hatch M D, Osmond C B, Slatyer R O, eds (1971). Mechanism and function of C4 photosynthesis. In: Photosynthesis and Photorespiration. New York: Wiley-Interscience, pp. 139–152.

15
Hiltbrunner A, Bauer J, Vidi P A, Infanger S, Weibel P, Hohwy M, Kessler F (2001). Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane. J Cell Biol, 154(2): 309–316

DOI PMID

16
Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J (1994). A receptor component of the chloroplast protein translocation machinery. Science, 266(5193): 1989–1992

DOI PMID

17
Ivanova Y, Smith M D, Chen K, Schnell D J (2004). Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell, 15(7): 3379–3392

DOI PMID

18
Jansen R P (2001). mRNA localization: message on the move. Nat Rev Mol Cell Biol, 2(4): 247–256

DOI PMID

19
Jouhet J, Gray J C (2009). Interaction of actin and the chloroplast protein import apparatus. J Biol Chem, 284(28): 19132–19141

DOI PMID

20
Kandasamy M K, Meagher R B (1999). Actin-organelle interaction: association with chloroplast in Arabidopsis leaf mesophyll cells. Cell Motil Cytoskeleton, 44(2): 110–118

DOI PMID

21
Kubis S, Patel R, Combe J, Bédard J, Kovacheva S, Lilley K, Biehl A, Leister D, Ríos G, Koncz C, Jarvis P (2004). Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell, 16(8): 2059–2077

DOI PMID

22
Kwok E Y, Hanson M R (2003). Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J, 35(1): 16–26

DOI PMID

23
Lara M V, Offermann S, Smith M, Okita T W, Andreo C S, Edwards G E (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(1): 593–610

DOI PMID

24
Logan D C, Scott I, Tobin A K (2003). The genetic control of plant mitochondrial morphology and dynamics. Plant J, 36(4): 500–509

DOI PMID

25
Lung S C, Chuong S D X (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(4): 1560–1578

DOI PMID

26
Lung S C, Yanagisawa M, Chuong S D X (2011). Protoplast isolation and transient gene expression in the single-cell C4 species, Bienertia sinuspersici. Plant Cell Rep, 30(4): 473–484

DOI PMID

27
Lung S C, Yanagisawa M, Chuong S D X (2012). Isolation of dimorphic chloroplasts from the single-cell C4 species Bienertia sinuspersici. Plant Methods, 8(1): 8

DOI PMID

28
Offermann S, Okita T W, Edwards G E (2011). Resolving the compartmentation and function of C4 photosynthesis in the single-cell C4 species Bienertia sinuspersici. Plant Physiol, 155(4): 1612–1628

DOI PMID

29
Park J H, Knoblauch M, Okita T W, Edwards G E (2009). Structural changes in the vacuole and cytoskeleton are key to development of the two cytoplasmic domains supporting single-cell C(4) photosynthesis in Bienertia sinuspersici. Planta, 229(2): 369–382

DOI PMID

30
Park J H, Okita T W, Edwards G E (2010). Expression profiling and proteomic analysis of isolated photosynthetic cells of the non-Kranz C4 species Bienertia sinuspersici. Funct Plant Biol, 37(1): 1–13

DOI

31
Petrásek J, Schwarzerová K (2009). Actin and microtubule cytoskeleton interactions. Curr Opin Plant Biol, 12(6): 728–734

DOI PMID

32
Sage R F (1999). Why C4 photosynthesis? In C4 Plant Biology. Physiological Ecology series, Sage R F and Monson R K, eds (San Diego: Academic Press), pp. 3–16.

33
Sage R F (2003). Atmospheric CO2, environmental stress and the evolution of C4 photosynthesis. In: Ehleringer J R, Cerling T E, Dearing D, eds. A History of Atmospheric CO2 and its Effects on Plants, Animals and Ecosystems., Berlin: Springer-Verlag

34
Sampathkumar A, Lindeboom J J, Debolt S, Gutierrez R, Ehrhardt D W, Ketelaar T, Persson S (2011). Live cell imaging reveals structural associations between the actin and microtubule cytoskeleton in Arabidopsis. Plant Cell, 23(6): 2302–2313

DOI PMID

35
Sato Y, Wada M, Kadota A (2001). Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. J Cell Sci, 114(Pt 2): 269–279

PMID

36
Schnell D J, Kessler F, Blobel G (1994). Isolation of components of the chloroplast protein import machinery. Science, 266(5187): 1007–1012

DOI PMID

37
Smith M D (2006). Protein import into chloroplasts: an ever-evolving story. Can J Bot, 84(4): 531–542

DOI

38
Smith M D, Rounds C M, Wang F, Chen K, Afitlhile M, Schnell D J (2004). atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J Cell Biol, 165(3): 323–334

DOI PMID

39
Van Gestel K, Köhler R H, Verbelen J P (2002). Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. J Exp Bot, 53(369): 659–667

DOI PMID

40
Voznesenskaya E V, Edwards G E, Kiirats O, Artyusheva E G, Franceschi V R (2003). Development of biochemical specialization and organelle partitioning in the single-cell C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). Am J Bot, 90(12): 1669–1680

DOI PMID

41
Voznesenskaya E V, Franceschi V R, Kiirats O, Artyusheva E G, Freitag H, Edwards G E (2002). Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). Plant J, 31(5): 649–662

DOI PMID

42
Voznesenskaya E V, Franceschi V R, Kiirats O, Freitag H, Edwards G E (2001). Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. Nature, 414(6863): 543–546

DOI PMID

43
Voznesenskaya E V, Koteyeva N K, Chuong S D X, Akhani H, Edwards G E, Franceschi V R (2005). Differentiation of cellular and biochemical features of the single-cell C4 syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae). Am J Bot, 92(11): 1784–1795

DOI PMID

44
Wada M, Kagawa T, Sato Y (2003). Chloroplast movement. Annu Rev Plant Biol, 54(1): 455–468

DOI PMID

45
Wada M, Suetsugu N (2004). Plant organelle positioning. Curr Opin Plant Biol, 7(6): 626–631

DOI PMID

46
Winter K, Smith J A C (1996). Crassulacean Acid Metabolism. New York: Spring

Outlines

/