Physiological, anatomical and biochemical characterisation of photosynthetic types in genus Cleome (Cleomaceae)

Abstract

C4 photosynthesis has evolved many times in 18 different families of land plants with great variation in leaf anatomy, ranging from various forms of Kranz anatomy to C4 photosynthesis occurring within a single type of photosynthetic cell. There has been little research on photosynthetic typing in the family Cleomaceae, in which only one C4 species has been identified, Cleome gynandra L. There is recent interest in selecting and developing a C4 species from the family Cleomaceae as a model C4 system, since it is the most closely related to Arabidopsis, a C3 model system (Brown et al. 2005). From screening more than 230 samples of Cleomaceae species, based on a measure of the carbon isotope composition (δ13C) in leaves, we have identified two additional C4 species, C. angustifolia Forssk. (Africa) and C. oxalidea F.Muell. (Australia). Several other species have δ13C values around –17‰ to –19‰, suggesting they are C4-like or intermediate species. Eight species of Cleome were selected for physiological, anatomical and biochemical analyses. These included C. gynandra, a NAD–malic enzyme (NAD–ME) type C4 species, C. paradoxa R.Br., a C3–C4 intermediate species, and 6 others which were characterised as C3 species. Cleome gynandra has C4 features based on low CO2 compensation point (Γ), C4 type δ13C values, Kranz-type leaf anatomy and bundle sheath (BS) ultrastructure, presence of C4 pathway enzymes, and selective immunolocalisation of Rubisco and phosphoenolpyruvate carboxylase. Cleome paradoxa was identified as a C3–C4 intermediate based on its intermediate Γ (27.5 μmol mol–1), ultrastructural features and selective localisation of glycine decarboxylase of the photorespiratory pathway in mitochondria of BS cells. The other six species are C3 plants based on Γ, δ13C values, non-Kranz leaf anatomy, and levels of C4 pathway enzymes (very low or absent) typical of C3 plants. The results indicate that this is an interesting family for studying the genetic basis for C4 photosynthesis and its evolution from C3 species.

Initial Events during the Evolution of C4 Photosynthesis in C3 Species of Flaveria

“…GDC is thought to be absent in the M cells of well-developed C 2 species, perhaps as a result of a knockout mutation early in C 2 evolution (Rawsthorne, 1992;Sage et al, 2012). Consistently, GDCp is not observed in the M cells of many well-developed C 2 species, for example, in the genera Cleome (Marshall et al, 2007;Voznesenskaya et al, 2007), Euphorbia (Sage et al, 2011b), Brassica (Ueno, 2011), and Heliotropium (Muhaidat et al, 2011). In Flaveria spp., Hylton et al (1988) observed no significant immunogold labeling for GDCp in M cell mitochondria of the C 2 species Flaveria linearis and F. floridana.…”

An mRNA Blueprint for C4 Photosynthesis Derived from Comparative Transcriptomics of Closely Related C3 and C4 Species

“…Chloroplasts in the BS of C. gynandra are larger than those in the BS of C 3 species and, as in many other C 4 plants, are positioned in a strictly centripetal pattern (Marshall et al, 2007;Voznesenskaya et al, 2007). Transcripts derived from the GIANT CHLOROPLAST1 (GC1) gene were more abundant in C. gynandra than in C. spinosa (Table IV).…”

Evolutionary transition from C3 to C4 photosynthesis and the route to C4 rice

“…As a consequence, the Kranz anatomy was formed in which enlarged BS cells surrounded each vein and the BS cells were in turn surrounded by M cells. Within BS cells, organelle numbers were further increased (Muhaidat et al 2011;Marshall et al 2007;Sage et al 2011b;Voznesenskaya et al 2007). To re-utilize the photorespiratory CO 2 escaping from BS into M cells, the expression level of PEPC in the cytosol of the M cells were greatly enhanced.…”