Abstract
Proliferation of plasmodesmata (PD) connections between bundle sheath (BS) and mesophyll (M) cells has been proposed as a key step in the evolution of two-cell C4 photosynthesis; However, a lack of quantitative data has hampered further exploration and validation of this hypothesis. In this study, we quantified leaf anatomical traits associated with metabolite transport in 18 species of BEP and PACMAD grasses encompassing four origins of C4 photosynthesis and all three C4 subtypes (NADP-ME, NAD-ME, and PCK). We demonstrate that C4 leaves have greater PD density between M and BS cells than C3 leaves. We show that this greater PD density is achieved by increasing either the pit field (cluster of PD) area or the number of PD per pit field area. NAD-ME species had greater pit field area per M-BS interface than NADP-ME or PCK species. In contrast, NADP-ME and PCK species had lower pit field area with increased number of PD per pit field area than NAD-ME species. Overall, PD density per M-BS cell interface was greatest in NAD-ME species while PD density in PCK species exhibited the largest variability. Finally, the only other anatomical characteristic that clearly distinguished C4 from C3 species was their greater Sb value, the BS surface area to subtending leaf area ratio. In contrast, BS cell volume was comparable between the C3 and C4 grass species examined.
Highlights
Most plants obtain sugars by fixing atmospheric CO2 using the enzyme Rubisco
NAD malic enzyme (NAD-ME) species had fewer PD per pit field area on the M– bundle sheath (BS) cell interface compared to NADP malic enzyme (NADP-ME) and most phosphoenolpyruvate carboxykinase (PCK) species (Fig. 4A, Supplementary Table S1)
This was offset by the greater percent pit field area per M–BS cell interface area in NAD-ME species compared to NADP-ME and PCK species (Fig. 4B, Supplementary Table S1)
Summary
Most plants obtain sugars by fixing atmospheric CO2 using the enzyme Rubisco (ribulose bis-phosphate carboxylase oxygenase). This process is inherently inefficient as O2 competes with CO2 at the enzyme’s active site, resulting in formation of compounds that cost energy to recycle in a process known as photorespiration. CO2 is first captured in mesophyll (M) cells as C4 acids, which diffuse into bundle sheath (BS) cells, where Rubisco is located, and decarboxylated, resulting in greatly elevated local CO2 concentrations (Furbank and Hatch, 1987) This CO2-concentrating mechanism reduces photorespiration and enables Rubisco to operate close to its catalytic maximum (von Caemmerer and Furbank, 2003; Sage et al, 2012). It is thought that a reduction in atmospheric CO2 concentration ~35 million years ago may have driven the evolution of this CO2-concentrating mechanism (Sage, 2004)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
