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

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.

Keywords

C₄ plants / single-cell C₄ photosynthesis / Chenopodiaceae / dimorphic chloroplasts / organelle compartmentation / photosynthetic enzymes / cytoskeleton / protein targeting

References

[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

[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,

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

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

[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

[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

[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

[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

[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

[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

[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

[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

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

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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

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

[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

[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

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

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

[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

[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

[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

[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

[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

[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

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

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

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

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.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg