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

Abstract

The evolution of C 4 photosynthesis in many taxa involves the establishment of a two-celled photorespiratory CO 2 pump, termed C 2 photosynthesis. How C 3 species evolved C 2 metabolism is critical to understanding the initial phases of C 4 plant evolution. To evaluate early events in C 4 evolution, we compared leaf anatomy, ultrastructure, and gas-exchange responses of closely related C 3 and C 2 species of Flaveria, a model genus for C 4 evolution. We hypothesized that Flaveria pringlei and Flaveria robusta, two C 3 species that are most closely related to the C 2 Flaveria species, would show rudimentary characteristics of C 2 physiology. Compared with less-related C 3 species, bundle sheath (BS) cells of F. pringlei and F. robusta had more mitochondria and chloroplasts, larger mitochondria, and proportionally more of these organelles located along the inner cell periphery. These patterns were similar, although generally less in magnitude, than those observed in the C 2 species Flaveria angustifolia and Flaveria sonorensis. In F. pringlei and F. robusta, the CO 2 compensation point of photosynthesis was slightly lower than in the less-related C 3 species, indicating an increase in photosynthetic efficiency. This could occur because of enhanced refixation of photorespired CO 2 by the centripetally positioned organelles in the BS cells. If the phylogenetic positions of F. pringlei and F. robusta reflect ancestral states, these results support a hypothesis that increased numbers of centripetally located organelles initiated a metabolic scavenging of photorespired CO 2 within the BS. This could have facilitated the formation of a glycine shuttle between mesophyll and BS cells that characterizes C 2 photosynthesis.

Comparative studies of C3 and C4Atriplex hybrids in the genomics era: physiological assessments

“…Mitochondria still occur between chloroplasts, but to less of a degree than seen in A. rosea . Many of the mitochondria in the hybrids also appear between the inner BS wall and the chloroplasts, resembling a pattern apparent in C 3 -C 4 intermediate plants using the C 2 -type of CCM (Monson and Rawsthorne, 2000; Sage et al , 2011; 2013). These observations further indicate that the BS cells of the F 2 hybrids use the C 2 mode of photosynthesis, although this will depend upon whether enough GDC is present in the BS mitochondria to create a strong sink for glycine produced in the M tissue.…”

Improved method for measuring the apparent CO2 photocompensation point resolves the impact of multiple internal conductances to CO2 to net gas exchange

“…Significant ( p < 0.05) interaction of C i * with measuring range according to ANOVA analysis is indicated by different letters above each plot. Data was obtained from a variety of reports ( L aisk, ; K irschbaum and Farquhar, ; B rooks and Farquhar, ; J acob and Lawlor, ; B erry et al ., ; V illar et al ., ; von C aemmerer et al ., ; B alaguer et al ., ; Häusler et al ., 1996; B unce, ; E vans and L oreto, ; B ernacchi et al ., ; P eisker and Apel, ; I gamberdiev et al ., ; P ons and Westbeek, ; G uo et al ., ; G almés et al ., ; S chneidereit et al ., ; W arren and Dreyer, ; F lexas et al ., ; K ebeish et al ., ; W eston et al ., ; L i et al ., ; T omaz et al ., ; C ano et al ., ; C ousins et al ., ; T holen and Z hu, ; D outhe et al ., ; G ilbert et al ., ; T holen et al ., ; B usch et al ., ; G iuliani et al ., ; S age et al ., ; W alker et al ., ,; W alker and Cousins, ; W alker et al ., ; W eise et al ., ).…”

The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria

“…The evolution of C 4 photosynthesis occurred at least 62 times in 19 different families of the angiosperms (Sage et al, 2011), implying a low evolutionary barrier towards expression of this trait. The analysis of recent intermediate species (Bauwe and Kolukisaoglu, 2003; Sage, 2004; Bauwe, 2011; Sage et al, 2012, 2013; Schulze et al, 2013) indicates that establishing a photorespiratory CO 2 pump was an early and important step in the evolution towards C 4 photosynthesis (Figure 1C). Since the two-carbon compound glycine serves as a transport metabolite, this photorespiratory CO 2 concentrating mechanism is also termed C 2 photosynthesis.…”