Phosphoenolpyruvate carboxylase reduces photorespiration in Panicum milioides, a C 3C 4 intermediate species

Abstract

Panicum milioides represents the first well-documented example of a higher plant species with reduced photorespiration and O 2 inhibition of photosynthesis. We have investigated the biochemical mechanism(s) involved in reducing O 2 sensitivity of photosynthesis in this species by parallel enzyme inhibitor experiments with thin leaf slices of P. milioides and C 3 and C 4 Panicum species. The reduced O 2 sensitivity of net photosynthesis in P. milioides gradually increased with increasing concentrations of the phosphoenolpyruvate carboxylase (EC 4.1.1.31) inhibitors, maleate and malonate. At saturating levels of inhibitor, photosynthesis in 2% O 2 was decreased by about 18%, and the inhibitory effects of both 21% O 2 and 49% O 2 were identical to those observed with a C 3 Panicum species in the absence or presence of inhibitor. A significant potential for C 4 photosynthesis in P. milioides, compared to its complete absence in a C 3 Panicum species, was demonstrated on the basis of: (a) a coupling of leaf slice CO 2 fixation by phosphoenolpyruvate carboxylase with the C 3 cycle; (b) NAD-malic enzyme (EC 1.1.1.39)-dependent aspartate and malate decarboxylation in leaf slices; (c) a full complement of C 4 cycle enzymes in leaf extracts, including pyruvate, P i dikinase (EC 2.7.9.1) and NAD-malic enzyme; and (d) Kranz-like leaf anatomy with numerous plasmodesmata traversing the mesophyll-bundle sheath interfacial cell wall. These data indicate that the reduced photorespiration and O 2 inhibition of photosynthesis in P. milioides is due to phosphoenolpyruvate carboxylase participation, possibly by creating a limited C 4-like CO 2 pump, rather than an altered ribulose 1,5-bisphosphate carboxylase-oxygenase (EC 4.1.1.39).