On the mechanism of C4 photosynthesis intermediate exchange between Kranz mesophyll and bundle sheath cells in grasses

Abstract

C(4) photosynthesis involves cell-to-cell exchange of photosynthetic intermediates between the Kranz mesophyll (KMS) and bundle sheath (BS) cells. This was believed to occur by simple diffusion through plentiful plasmodesmatal (PD) connections between these cell types. The model of C(4) intermediates' transport was elaborated over 30 years ago and was based on experimental data derived from measurements at the time. The model assumed that plasmodesmata occupied about 3% of the interface between the KMS and BS cells and that the plasmodesmata structure did not restrict metabolite movement. Recent advances in the knowledge of plasmodesmatal structure put these assumptions into doubt, so a new model is presented here taking the new anatomical details into account. If one assumes simple diffusion as the sole driving force, then calculations based on the experimental data obtained for C(4) grasses show that the gradients expected of C(4) intermediates between KMS and BS cells are about three orders of magnitude higher than experimentally estimated. In addition, if one takes into account that the plasmodesmata microchannel diameter might constrict the movement of C(4) intermediates of comparable Stokes' radii, the differences in concentration of photosynthetic intermediates between KMS and BS cells should be further increased. We believe that simple diffusion-driven transport of C(4) intermediates between KMS and BS cells through the plasmodesmatal microchannels is not adequate to explain the C(4) metabolite exchange during C(4) photosynthesis. Alternative mechanisms are proposed, involving the participation of desmotubule and/or active mechanisms as either apoplasmic or vesicular transport.

Integrating Phylogeny into Studies of C4 Variation in the Grasses

“…In addition to the C 4 enzymes, C 4 photosynthesis evolution necessitated rearrangements of chloroplast envelope proteins (Bräutigam et al, 2008). Furthermore, transport of C 4 intermediates between M and BS cells is probably not performed through simple diffusion, which suggests that other, unidentified, mechanisms exist (Sowinski et al, 2008), which may be yet another C 4 -specific adaptation.…”

Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis

“…This indicates that a rapid diffusion between BSCs and MCs can potentially be supported. However, a recent theoretical analysis based on plasmodesmatal structure and its diffusional properties showed that the required metabolite gradient between BSCs and MCs to support observed rate of C4 photosynthetic CO 2 uptake should be at least three orders of magnitude higher than experimentally measured (Sowinski et al, 2008). Recent and historical measurement indicated that unidirectional transport of fluorescent protein through plasmodesmata exists in unique surfaces (Arisz, 1969;Christensen et al, 2009), which suggested that active transport or accelerated diffusion of small molecules of certain size may occur through plasmodesmata.…”

“…S2). In the simulation, the same permeability was assumed for both T3P and PGA (C3P [compounds containing three carbons and a phosphate group]), because they have the same diffusion properties (Sowinski et al, 2008). At a given permeability to C3P transport, increasing the permeability of plasmodesmata to CO 2 first increases and then decreases A (Fig.…”

“…Different metabolites have different diffusion coefficients in the cytosol (D cyt ), according to molecular sizes. In this model, the D cyt of C3P is assumed to be 5.25 3 10 210 m 2 s 21 (Sowinski et al, 2008). CO 2 leakage is described also as a diffusion process with a diffusion coefficient in the cytosol of 1.7 3 10 29 m 2 s 21 (Evans et al, 2009).…”

Understanding metabolite transport and metabolism in C4 plants through RNA-seq

“…Their localization necessitates the presence of transport proteins which connect the reactions of the C 4 cycle to the cytosol [16]. In turn, the cytosols of the PEPC containing mesophyll tissue and the RubisCO containing bundle sheath tissue share a symplastic connection [17][18][19][20]. Molecular identification of the transport proteins lags behind identification of the enzymes.…”