Recent progress in the single-cell C<sub>4</sub> photosynthesis in terrestrial plants

doi:10.1007/s11515-012-9248-z

Front Biol

2012, Vol. 7

Issue (6) : 539-547 https://doi.org/10.1007/s11515-012-9248-z

REVIEW

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

Shiu-Cheung LUNG¹, Makoto YANAGISAWA², Simon D. X. CHUONG¹(

)

1. Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada; 2. Agronomy Department, Purdue University, West Lafayette, IN 47907-2054, USA

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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

Corresponding Author(s): CHUONG Simon D. X.,Email:schuong@uwaterloo.ca

Issue Date: 01 December 2012

Cite this article:

Shiu-Cheung LUNG,Makoto YANAGISAWA,Simon D. X. CHUONG. Recent progress in the single-cell C₄ photosynthesis in terrestrial plants[J]. Front Biol, 2012, 7(6): 539-547.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-9248-z
https://academic.hep.com.cn/fib/EN/Y2012/V7/I6/539

Fig.1 Simplified schematic diagrams of the C, C and CAM photosynthetic pathways. A: In the C or Calvin-Benson pathway, Rubisco catalyzes the carboxylation of CO to RuBP to generate C acids. Most of the C acids are used for the regeneration of RuBP whereas the remainder is used in sucrose or starch synthesis. B: In the C pathway, CO fixation involves two cell types- the mesophyll (M) and bundle sheath (BS) cells. In the M cell, CO is hydrated to by carbonic anhydrase (CA) which is used to react with phosphoenolpyruvate (PEP) catalyzes by PEP carboxylase (PEPC) producing a C acid. The C acid is transported to the BS cell where it is decarboxylated by NAD-/NADP-malic enzyme (ME) or PEP carboxykinase (PEP-CK) yielding CO and a C acid (pyruvate). The CO is refixed by Rubisco of the Calvin-Benson cycle while the C product moves back to the M cell for the regeneration of PEP by pyruvate phosphate dikinase (PPDK). C: In the CAM pathway, CO is taken up at night when stomata are open and it is hydrated by CA to . PEPC catalyzes the reaction between and PEP to generate a C acid which is stored in the vacuole. During the day when stomata are closed, the stored C acid is released from the vacuole for the decarboxylation reaction and the resulting CO is converted to sucrose or starch by the Calvin-Benson cycle.

Fig.2 General leaf anatomy of (A-C) and (D-F). A: under controlled growth conditions. B: leaf cross section with two layers of chlorenchyma cells (ch) surrounding water storage cells (ws) and vascular tissues (vt). C: A close-up view of chlorenchyma cells showing the nucleus (n) and the central (ccc) and peripheral (pcc) cytoplasmic compartments connected by transvacuolar cytoplasmic strands (tvs; arrows). D: under controlled growth conditions. E: leaf cross section showing a single layer of elongated chlorenchyma cells sandwiched between water storage cells (ws) beneath the epidermis (e). F: A close-up view of chlorenchyma cells depicting the distal (d) and proximal (p) cytoplasmic compartments respectively. Scale bars (A, D) = 1 cm, (B, E) = 150 μm, (C, F) = 50 μm.

Fig.3 Proposed models for the C pathway in the single-cell systems. Confocal microscopy of live (A) and (B) chlorenchyma cells stained with rhodamine 123 showing the partitioning of chloroplasts (red fluorescence) and mitochondria (yellow fluorescence) in distinct cytoplasmic compartments. A: In , the initial fixation of atmospheric CO into C acids occurs in the peripheral compartment, C acids diffuse via cytoplasmic channel to the central compartment for decarboxylation, and the released CO are recaptured by Rubisco. B: In , atmospheric CO enters the distal compartment of the cell where it is fixed in the C cycle, the C acids diffuse to the proximal compartment where they are decarboxylated, and the released CO are refixed by Rubisco.

Fig.4 Transient expression of fluorescent fusion proteins in protoplasts of . Transfected protoplasts were observed under a confocal laser scanning microscope. Merged images showing green fluorescent protein signals (green) and chlorophyll autofluorescence (red) in protoplasts transfected with constructs of protein fusions to: A, talin, an actin binding protein; B, MAP4, a microtubule binding protein; C, Rubisco small-subunit; D, the transit peptide of NAD-malic enzyme; E, a peroxisomal targeting signal, or; F, a nuclear localization signal. Scale bars= 5 μm.

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