Predominant localization of mitochondria enriched with glycine‐decarboxylating enzymes in bundle sheath cells of Alternanthera tenella, a C₃–C₄ intermediate species

Abstract

Mesophyll protoplasts and bundle sheath cells were prepared by enzymatic digestion of leaves of Alternanthera tenella, a C3‐C4 intermediate species. The intercellular distribution of selected photosynthetic, photorespiratory and respiratory (mitochondrial) enzymes in these meso‐phyll and bundle sheath cells was studied. The activity levels of photosynthetic enzymes such as PEP carboxylase (EC 4.1.1.31) or NAD‐malic enzyme (EC 1.1.1.39) and photorespiratory enzymes such as glycolate oxidase (EC 1.1.3.1) or NADH‐hydroxypyruvate reductase (EC 1.1.1.29) were similar in the two cell types. The activity levels of mitochondrial TCA cycle enzymes such as citrate synthase (EC 4.1.3.7) or fumarase (EC 4.2.1.2) were 2‐ to 3‐fold higher in bundle sheath cells. On the other hand, the activity levels of mitochondrial photorespiratory enzymes, namely glycine decarboxylase (EC 2.1.2.10) and serine hydroxymethyltransferase (EC 2.1.2.1), were 6‐9‐fold higher in bundle sheath cells than in mesophyll protoplasts. Such preferential localization of mitochondria enriched with the glycine‐decarboxylating system in the inner bundle sheath cells would result in efficient refixa‐tion of CO2 from not only photorespiration but also dark respiration before its exit from the leaf. We propose that predominant localization of mitochondria specialized in glycine decarboxylation in bundle sheath cells may form the basis of reduced photorespiration in this C3‐C4 intermediate species.

Phenotypic landscape inference reveals multiple evolutionary paths to C4 photosynthesis

“…These results were consistent with previous work on subsets of C 4 lineages that proposed the BS-specificity of GDC occurs prior to the evolution of C 4 metabolism (Hylton et al, 1988; Rawsthorne et al, 1988; Devi et al, 1995; Sage et al, 2012), and loss of RuBisCO from M cells occurs late (Cheng et al, 1988; Khoshravesh et al, 2012), but also provided higher resolution insight into the order of events generating C 4 metabolism. Alterations to leaf anatomy as well as cell-specificity and increased abundance of multiple C 4 cycle enzymes were predicted to evolve prior to any alteration to the primary C 3 and C 4 photosynthetic enzymes RuBisCO and phospho enol pyruvate carboxylase (PEPC) (Figure 3).…”

Effects of low atmospheric CO2 and elevated temperature during growth on the gas exchange responses of C3, C3–C4 intermediate, and C4 species from three evolutionary lineages of C4 photosynthesis

“…Increasing the measurement temperature from 30 to 40°C increased in C 3 species by an average of 25 mol mol ¡1 , while in C 3 -C 4 intermediates, the increase was 16 mol mol ¡1 . Flaveria ramosissima, a C 3 -C 4 species with some C 4 -cycle activity, exhibited lower than Alternanthera tenella and Heliotropium convolvulaceum which lack signiWcant C 4 -cycle activity (Table 1; Monson et al 1986;Devi et al 1995;Vogan et al 2007). These species' gas exchange results did not otherwise diVer.…”

Evolution of C4 phosphoenolpyruvate carboxylase in the genus Alternanthera: gene families and the enzymatic characteristics of the C4 isozyme and its orthologues in C3 and C3/C4 Alternantheras

“…This lowered apparent photorespiration in A. tenella is due to the compartmentation of the photorespiratory enzymes, i.e. glycine decarboxylase, in the bundle-sheath cells (Devi et al 1995). Together with Moricandia arvensis and Parthenium argentatum, A. tenella belongs to that group of C 3 /C 4 intermediate plant species whose intermediate properties are predominantly caused by a photorespiratory CO 2 pump due to the restriction of glycine decarboxylase to the bundle-sheath compartment and not by the establishment of an at least rudimentary C 4 cycle (Sage 2004).…”