What Does It Take to Be C4? Lessons from the Evolution of C4 Photosynthesis

Abstract

Twenty-five years ago research had already established a firm biochemical and physiological understanding of the CO 2 -concentrating mechanism that creates a high CO 2 environment (1,000-3,000 bar) in bundle-sheath cells in leaves of C 4 plants and accounts for most of their distinctive photosynthetic properties (5). It was then clear that the minimum requirements for this CO 2 concentrating mechanism included: (a) cell-specific amplification of enzymes of C 4 photosynthesis (i.e. phosphoenolpyruvate carboxylase [PEPC] in mesophyll, and C 4 acid decarboxylases and Rubisco in bundle-sheath cells), with complementary adjustments of photosystem and electron transport activities; (b) novel cell-specific organelle metabolite translocators; (c) symplastic connections of the spatially separated sources and sinks of 4C-dicarboxylic acid transport metabolites; and (d) barriers to CO 2 diffusion between the site of CO 2 fixation by PEPCase in mesophyll cells and sites of CO 2 release and refixation by Rubisco in bundle-sheath cells.These requirements have been met in a great variety of ways during the evolution of C 4 plants, through diverse cooperative pathways of carbon metabolism and integrated photoreactions in adjacent, differentiated photosynthetic cells. Perhaps the most simple, highly evolved system is that in Sorghum (detailed in the legend of Fig. 1), but it is in the diversity of other systems that we can expect to discover clues as to what it takes to be C 4 .

Differential use of two cyclic electron flows around photosystem I for driving CO 2 -concentration mechanism in C 4 photosynthesis

“…In fact, when we observed chlorophyll fluorescence in cross sections of P. grandiflora leaves by using a MicroFluorCam (Photon Systems Instruments, Bruno, Czech Republic), the level of fluorescence emitted from the mesophyll cells was much higher than that from the bundlesheath cells (data not shown). This observation has also been reported in S. bicolor in confocal microscopy (30).…”

Pyruvate,Orthophosphate Dikinase in Leaves and Chloroplasts of C3 Plants Undergoes Light-/Dark-Induced Reversible Phosphorylation

“…The independent emergence of C 4 photosynthesis in diverse angiosperm families implies a more or less common evolutionary pathway. Supporting this notion is the fact that all of the C 4 cycle enzymes occur in C 3 plants, albeit functioning as non-photosynthetic isoforms (Edwards et al, 2001). Less obvious for this hypothesis has been the C 3 origins of proteins that up-/down-regulate certain "target" enzymes in the C 4 pathway.…”

“…Whatever the function(s) of PPDK is in C 3 plants, its conversion from a non-photosynthetic role to a photosynthetic one in mesophyll chloroplasts of C 4 leaves was a transition repeated independently in a diverse range of angiosperm families during the evolution of C 4 photosynthesis. This implies a more or less common evolutionary pathway for C 4 photosynthesis facilitated by the preexistence of homologs of the C 4 cycle enzymes in C 3 plants (Edwards et al, 2001). Potentially more problematic for understanding how the C 4 pathway emerged independently are the origins of certain regulatory "converter" enzymes that fulfill the crucial role of controlling carbon flux through the C 4 pathway.…”

Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity

“…Taken together, these results suggest that this regulatory threonyl phosphorylation of the PPDK is a very ancient mechanism. This notion implies a common evolutionary pathway for C 4 photosynthesis facilitated by the preexistence of homologs of C 4 enzymes in C 3 plants (Edwards et al, 2001;Hibberd and Quick, 2002;Wang et al, 2009). The most significant adaptation for the enzyme to be utilized in C 4 photosynthesis may have already occurred well before the emergence of the pathway in modern angiosperms .…”