C4 and C3 Photosynthesis in Terrestrial Plants may Take Place within the Same Cell. C4 Does Not Require Kranz Anatomy

A number of species, including maize and sugarcane, operate the C4 photosynthetic pathway. Unlike C3 photosynthesis, in which the carboxylating reactions take place only in the mesophyll, C4 photosynthesis makes use of both the mesophyll and the bundle sheath cells. The bundle sheath cells form a layer of tissue surrounding the vascular bundle (phloem and xylem). Thus this type of wreath-like anatomy is referred to as ‘Kranz anatomy’ (‘Kranz’ is the German word for wreath). In C4 plants, CO2 enters through the stomata and diffuses into the mesophyll tissue. CO2 is fixed by phosphoenolpyruvate carboxylase (PEPC) to form oxaloacetate. Oxaloacetate is then converted into a 4-carbon acid such as malate or aspartate, which moves through plasmodesmata into the bundle sheath cells. In the bundle sheath cells, the C4 acid is decarboxylated. The released CO2 is refixed by Rubisco and assimilated through the enzymes of the photosynthetic carbon reduction (PCR) cycle to form sucrose and starch.

C4 photosynthesis is thought to provide an evolutionary advantage in environments where CO2 concentrations are low, and enables enhanced water-use efficiency. In addition, due to high concentrations of CO2 in bundle sheath cells, Rubisco in C4 plants does not catalyze the oxygenation of PGA, thereby preventing photorespiration in C4 plants. As a result, temperatures above 30 degrees C do not pose photorespiratory stress to C4 plants as they do in C3 plants.

In the July issue of Trends in Plant Science (vol.7: 283-285), Rowan F. Sage (University of Toronto, Canada) describes recent analyses of two chenopods, Borszczowia aralocaspica and Bienertia cycloptera, which have the ability to perform C4 photosynthesis in absence of Kranz anatomy. These plants represent the first known exceptions to the Kranz anatomy feature in terrestrial C4 plant species. B. aralocaspica and Bi. cyclopteracarry out C4 photosynthesis via spatial compartmentation of photosynthetic enzymes. These observations belie the traditional notion that the presence of thick-walled bundle sheath cells bordering the mesophyll cells is required to prevent CO2 leakage in C4 plants.

The author points out that C4 plants resort to carbon-concentrating mechanism to compensate for low CO2 in the atmosphere. Some aquatic angiosperms such as Hydrilla verticillata and Egeria densa and some diatoms such as Thalassiosira weissflogii carry out C4 photosynthesis in individual photosynthetic cells. Since land plants are not surrounded by water, it was thought that Kranz leaf anatomy is essential to separate PCA (photosynthetic carbon assimilation) regions from PCR (photosynthetic carbon reduction) regions in order to prevent CO2 loss while allowing rapid diffusion of metabolites between PCA and PCR sites via plasmodesmata. The identification of C4 terrestrial plants without Kranz leaf anatomy was therefore a breakthrough discovery.

Single-cell C4 photosynthesis was first reported by Elena Voznesenskaya and her colleagues in the semi-succulent halophyte Borszczowia aralocaspica of the family Chenopodiaceae. The researchers observed that the C4pathway operates in single photosynthetic cells of this species in spite of the absence of any periclinal walls separating the PCA region from the PCR region. The author points out that PCA and PCR reactions occur at opposite ends of the same elongated cell. Furthermore, it was found that the enzyme PEPC is not localized differentially but rather distributed throughout the cytoplasm, indicating that PCA and PCR metabolism are carried out by the differential localization of Rubisco, the decarboxylase enzymes and PPDK (pyruvate phosphate dikinase). Bienertia cycloptera, another halophytic species of the same tribe, exhibits the isotopic signature characteristic of a C4 plant, although it was initially classified as a C3 species based on biochemical studies. However, the spatial distribution of the PCA and PCR regions is distinct from that observed in B. aralocaspica. The cytoplasm of photosynthetic cells of Bi. cycloptera is divided into a region at the cell periphery containing the PCA region and a central area containing the PCR region. The vacuole plays an important role in minimizing CO2 efflux while cytoplasmic strands serve as the channels for metabolic change.

Five distinct C4 origins are suspected within the Suaedeae tribe, and the author suggests that the extreme saline soils of Central Asia provide strong selective pressure characteristics that increase water-use efficiency. Lack of competition between the species that grow in that highly saline area may have accelerated the speed of their evolution.

The author concludes that these discoveries may usher in a new chapter in the field of genetic engineering, because anatomical barriers had been thought to impede genetic manipulation to convert a C3 crop into a C4 variety. Such an undertaking, which could allow development of crops with improved water-use efficiency, may prove to be more plausible than previously thought.

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