Nature's green revolution: the remarkable evolutionary rise of C₄plants

Abstract

Plants with the C 4 photosynthetic pathway dominate today's tropical savannahs and grasslands, and account for some 30% of global terrestrial carbon fixation. Their success stems from a physiological CO 2 -concentrating pump, which leads to high photosynthetic efficiency in warm climates and low atmospheric CO 2 concentrations. Remarkably, their dominance of tropical environments was achieved in only the past 10 million years (Myr), less than 3% of the time that terrestrial plants have existed on Earth. We critically review the proposal that declining atmospheric CO 2 triggered this tropical revolution via its effects on the photosynthetic efficiency of leaves. Our synthesis of the latest geological evidence from South Asia and North America suggests that this emphasis is misplaced. Instead, we find important roles for regional climate change and fire in South Asia, but no obvious environmental trigger for C 4 success in North America. CO 2 -starvation is implicated in the origins of C 4 plants 25-32 Myr ago, raising the possibility that the pathway evolved under more extreme atmospheric conditions experienced 10 times earlier. However, our geochemical analyses provide no evidence of the C 4 mechanism at this time, although possible ancestral components of the C 4 pathway are identified in ancient plant lineages. We suggest that future research must redress the substantial imbalance between experimental investigations and analyses of the geological record.

The evolution of inorganic carbon concentrating mechanisms in photosynthesis

“…Inorganic carbon availability in submerged palustrine habitats is not, as Keeley & Rundel (2003) point out, closely coupled to the atmospheric CO 2 level. There are very few carbon isotope data consistent with terrestrial CCMs during the low CO 2 episode (Royer et al 2007) in the Carboniferous some 300 Myr ago (Keeley & Rundel 2003;Osborne & Beerling 2006). Badger et al (2002), following Raven (1997b), suggest that CCMs in cyanobacteria and algae evolved in the low CO 2 (and high O 2 ) environment of the Carboniferous.…”

“…However, it must be remembered that not all photosynthetic O 2 evolvers have CCMs (Raven et al 2005a,b); optimality criteria that compare the costs and benefits of the trait should be employed to investigate the distribution of CCMs (Rosen 1967;Raven et al 2008). As will be seen under consideration of when CCMs evolved, a low CO 2 concentration, either globally or locally, is frequently considered as a selective factor in the evolution of CCMs (Keeley & Rundel 2003;Giordano et al 2005;Osborne & Beerling 2006), if not always in their spread (Keeley & Rundel 2005). The role of O 2 in the evolution of CCMs is not clear (Giordano et al 2005;Riding 2006).…”

Bulk organic geochemistry of sediments from Puyehue Lake and its watershed (Chile, 40°S): Implications for paleoenvironmental reconstructions

“…It is noteworthy that the δ 13 C signal does not follow the changes in ƒ T , and therefore probably reflects changes in lake productivity instead of changes in the origin of the sedimentary organic matter. In addition, minor increases in δ 13 C might be due to the development of C4 plants in the lake watershed, which was however relatively limited since plants using the C4 pathway are characteristic for dry and warm environments, such as tropical grasslands and savannah (Osborne and Beerling, 2006). …”

Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change

“…While there is now a realisation that CCMs are among the confounding factors in using the δ 13 C of organic matter in marine sediments to estimate past atmospheric CO 2 levels (Laws et al 2002), these δ 13 C measurements are not of use in dating the time of origin of CCMs or their subsequent degree of expression. By contrast, there is anatomical, molecular clock and natural abundance stable isotope data for the timing of the polyphyletic origin of C 4 photosynthesis in flowering plants on land (Cerling et al 1989(Cerling et al , 1998Osborne and Beerling 2006).…”