Single cell C4 photosynthesis

A.T. WickramageBS/2008/220

Contents01 •Photosynthesis

02 •Calvin cycle

03 •Four Carbon (C4) pathway

04 •Kranz anatomy

05 •Single cell C4 photosynthesis

06 •Terrestrial single cell C4 photosynthesis

07 •Cell compartmentalization

08 •Aquatic single cell C4 photosynthesis

09 •Discussion

10 •References

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• The transduction of the energy of sunlight to chemical energy by green plants is called as photosynthesis.6CO2 + 6H2O C6H12O6 + 6O2

Two types of reactions in photosynthesis• Light dependent reactions• Light independent reactions

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Photosynthesis

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Schematic diagram of the overall organization of the membranes in the chloroplast

The light dependent reactions• Occur in the thylakoid membrane• Converts light energy to chemical energy• Chlorophyll and several other accessory pigments are

involved• Final products– NADPH– ATP– O2

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Light independent reactions – The fixation of CO2

• Take place in the stroma within the chloroplast• Converts CO2 to sugar• Involves the Calvin cycle• Two basic types of photosynthetic mechanisms – C3

– C4

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Calvin cycle

• Chemical energy harvested by the light dependent reactions, used to reduce carbon (CO2)

• The Calvin cycle consists of three main parts– Carboxylation – Reduction– Regeneration

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A summary of the Calvin cycle

3 ATP

6 NADPH

6 ATP

Four Carbon (C4) pathway• In some plants, the first product of CO2 fixation is not the

three-carbon molecule 3-PGA, but four-carbon molecule oxaloacetate (OAA).

• The C4 photosynthetic carbon cycle is an elaborated addition to the C3 photosynthetic pathway.

• It evolved as an adaptation to – high light intensities– high temperatures– suppress photorespiration– increase carbon gain (Edwards et al., 2010)

• Associates with the Kranz anatomy

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Kranz anatomy

• Thereby, – Oxygenase reaction and the following photorespiration are repressed – Rubisco accumulates in BSCs chloroplasts– phosphoenolpyruvate carboxylase (PEPC) accumulate in the cytoplasm and

chloroplasts of MCs– MCs and BSCs show differences in the biochemistry of carbon fixation. – Division of labor achieved (Hatch, 1987)

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Diagram of C4 leaf cross section

• Wrapping of vascular bundles by two specialized cell types, the mesophyll cells (MCs) and bundle sheath cells (BSCs)

• To concentrate CO2 around Rubisco

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Leaf cross section of Panicum miliaceum, which exhibits Kranz anatomy

Mesophyll cell

Bundle sheath cell

(Source: http://sydney.edu.au/science/biology/learning/plantform_function/revisionmodules/2003A_ Pmodules/module1/1C9.shtml)

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An electron micrograph of grana- deficient chloroplasts in bundle sheath cells and granal chloroplasts in mesophyll cells.

(Source: http://teosinte.uoregon.edu/cp_biogenesis/)

Mesophyll cell chloroplast(Granal chloroplast)

Bundle sheath cell chloroplast(Grana deficient Chloroplast) Starch granule

Grana

The C4 pathway consists of three key steps

1. Initial fixation of CO2 by phosphoenolpyruvate carboxylase (PEPC) to form a C4 acid

2. Decarboxylation of a C4 acid to release CO2 near the site of the Calvin cycle

3. Regeneration of the primary CO2 acceptor phosphoenolpyruvate (PEP)

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A diagram showing a summary of metabolic division of labor in mesophyll cells and bundle sheath cells of C4 plants

Mesophyll cell Bundle sheath cell

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Single cell C4 photosynthesis

• Kranz type leaf anatomy was synonymous with C4 photosynthesis.

• Single cell C4 photosynthesis lacks Kranz anatomy.

• Two types

1. Terrestrial single cell C4 photosynthesis

2. Aquatic single cell C4 photosynthesis

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Terrestrial single cell C4 photosynthesis

1. Bienertia cycloptera 2. Bienertia sinuspersici 3. Suaeda aralocaspica

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The family Chenopodiaceae

• A family of flowering plants, also called the Goosefoot Family.

• Contains approximately 1300 species worldwide and range from annual herbs to trees.

• Majority are weeds and many are salt and drought tolerant.

• Many chenopod species have C4 photosynthesis.

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Bienertia cycloptera• Widespread in Central Asia• Grows in salty depressions• Plant is usually shorter, precise measurements are not

available.• Flowering time is from July to August and fruiting period

is in September

A photograph of Bienertia cycloptera

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Bienertia sinuspersici

• Distribution is restricted to Persian Gulf areas and Baluchistan• Plant height is up to 130-160 cm• Flowering time is October and fruiting period is from

November to December

A photograph of Bienertia sinuspersici

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Suaeda aralocaspica• Restricted to the deserts of central Asia • It is a monoecious, annual, halophyte.• Grows to a height of between 20- 50 cm

A photograph of Suaeda aralocaspica

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• Lacks Kranz anatomy• Compartmentalization of organelles and photosynthetic

enzymes into two distinct regions within a single cell• Cytoskeleton associates with the positioning of chloroplasts

and other organelles• Lack of night time CO2 fixation

• Function with a unique C4 mechanism

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Features of single cell C4 photosynthesis

Cell compartmentalization (1)• In Suaeda aralocaspica

– Two chloroplast types are arranged in cylindrical chlorenchyma cells. – Spatially separated to opposite ends of the cell

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Proximal compartment

Distal compartment

Microscopy image of the distal and proximal compartments in S. aralocaspica

Nucleus

• Distal compartment– Lack grana– Pyruvate, Pi dikinase (PPDK) is present– No starch– C4 carbon fixation

• Proximal compartment– Rubisco is concentrated– NAD-malic enzyme is present– C3 carbon fixation

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Microscopy image of immunolocalization of photosynthetic enzymes S.aralocaspica

Rubisco

PPDK

• In Bienertia Species– One chloroplast type in the periphery [peripheral chloroplast (P-CP)]– Other chloroplast type (central compartment chloroplast [C-CP]) in central– Compartments are spatially separated by a vacuole– Cytoplasmic compartments are interconnected by cytoplasmic channels

(Voznesenskaya et al., 2002; Edwards et al., 2004)

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Peripheral compartment

Central compartment

Nucleus

Microscopy image of the peripheral and central compartments in B. sinuspersici

Cell compartmentalization (2)

• Peripheral cytoplasmic compartment (PCC) – Less number of mitochondria – Has grana-deficient chloroplasts– Contain pyruvate, Phosphate dikinase,

Phosphoenolpyruvate carboxylase – C4 carbon fixation

• Central cytoplasmic compartment (CCC) – Filled with mitochondria and granal chloroplasts– Rubisco is abundant– C3 carbon fixation

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The actin cytoskeleton in chlorenchyma cells of B. sinuspersici (left) and S. aralocaspica (right)

Actin cytoskeleton

( Source: Chuong et al., 2006)

CO2 concentration mechanism in Bienertia species

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Aquatic single cell C4 photosynthesis

• CO2 HCO3- in water

• The availability of inorganic carbon for photosynthesis in water is limited by diffusion and pH.

• Some eukaryotic phytoplankton/ angiosperm species have evolved energy dependent mechanisms for concentrating CO2.

1. Thalassiosira weissflogii2. Hydrilla verticillata

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Thalassiosira weissflogii

• Centric, unicellular diatom • Found in marine environments and also in inland waters in many

parts of the world• Initial incorporation of CO2 into four carbon acids and the

subsequent transfer of carbon to 3-phosphoglycerate and sugars

Image of Thalassiosira weissflogii

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Hydrilla verticillata

• Found in fresh water environments• C4 photosynthesis is accomplished without any

compartmentation and chloroplast differentiation.• A facultative C4 plant

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A photograph of Hydrilla verticillata

Discussion• Many important crops are C3 plants.

• The solar energy conversion efficiency to biomass is lower in C3

photosynthesis than that of C4 photosynthesis.

• C4 plants were evolved from C3 plants, acquiring the C4 photosynthetic

pathway in addition to the C3 pathway.

• Transfer of C4 traits to C3 plants has been one strategy for improving the

photosynthetic performance of C3 plants.

• This was initially attempted by means of conventional hybridization between C3 and C4 plants and more recently using transgenic techniques.

– e.g. C4 rice project

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• Akhani, H., Barroca, J., Koteeva, N., Voznesenskaya, E., Franceschi, V., Edwards, G., Ghaffari, M., and Ziegler, H. (2005). Bienertia sinuspersici (Chenopodiaceae): a new species from Southwest Asia and discovery of a third terrestrial C4 plant without Kranz anatomy. Systematic Botany 30(2): 290–301.

• Bowes, G., Rao, S.K., Estavillo, G.M., Reiskind, J.B. (2002). C4 mechanisms in aquatic angiosperms:

comparisons with terrestrial C4 systems. Functional Plant Biology 29: 379–392.

• Brown, R.H., Bouton, J.H. (1993). Physiology and genetics of inter specific hybrids between photosynthetic

types. Annual Review of Plant Physiology and Plant Molecular Biology 44: 435–456. • Chuong, S.D.X., Franceschi, V.R., and Edwards, G.E. (2006). The cytoskeleton maintains organelle partitioning

required for single-cell C4 photosynthesis in Chenopodiaceae Species. The Plant Cell 18: 2207–2223.

• Edwards, G.E., Franceschi, V.R., Voznesenskaya, E.V. (2004). Single cell C4 photosynthesis versus the dual-cell

(Kranz) paradigm. Annual Review of Plant Biology 55, 173–196. • Fukayama, H., Tsuchida, H., Agarie, S. (2001). Significant accumulation of C4-specific pyruvate, orthophosphate

dikinase in a C3 plant, rice. Plant Physiology 127, 1136–1146.

• Hatch, M.D. (1987). C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.

Biochimica et Biophysica Acta 895, 81–106. • Hausler, R.E., Hirsch, H.J., Peterhansel, K.F. (2002). Overexpression of C4-cycle enzymes in transgenic C3 plants:

a biotechnological approach to improve C3-photosynthesis. Journal of Experimental Botany 53, 591–607.

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References

• Lara, M.V., Chuong, S.D.X., Akhani, H., Andreo, C.S., and Edwards, G.E. (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 Physiology 142: 673–684.

• Miyao, M., Masumoto, C., Miyazawa, S., and Fukayama, H. (2011). Lessons from engineering a single-cell C4 photosynthetic pathway into rice. Journal of Experimental Botany 62(9): 3021–3029.

• Offermann, S., Okita, T.W., and Edwards, G.E. (2011). Resolving the Compartmentation and Function of C4 Photosynthesis in the Single-Cell C4 Species Bienertia sinuspersici. Plant Physiology 155: 1612–1628.

• Voznesenskaya, E.V., Edwards, G.E., Kiirats, O., Artyusheva, E.G., and Franceschi, V.R. (2003). Development

of biochemical specialization and organelle partitioning in the single celled C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). American Journal of Botany 90, 1669–1680.

• Voznesenskaya, E.V., Franceschi, V.R., and Edwards, G.E. (2004). Light-dependent development of single cell

C4 photosynthesis in cotyledons of Borszczowia aralocaspica (chenopodiaceae) during transformation from a storage to a photosynthetic organ. Annals of Botany 93: 177-187.

• Voznesenskaya, E.V., Franceschi, V.R., Kiirats, O., Artyusheva, E.G., Freitag, H., and Edwards, G.E. (2002).

Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). The Plant Journal 31: 649–662.

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

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Thank you

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