Oligocene CO2 Decline Promoted C4 Photosynthesis in Grasses

Abstract

C4 photosynthesis is an adaptation derived from the more common C3 photosynthetic pathway that confers a higher productivity under warm temperature and low atmospheric CO2 concentration [1, 2]. C4 evolution has been seen as a consequence of past atmospheric CO2 decline, such as the abrupt CO2 fall 32-25 million years ago (Mya) [3-6]. This relationship has never been tested rigorously, mainly because of a lack of accurate estimates of divergence times for the different C4 lineages [3]. In this study, we inferred a large phylogenetic tree for the grass family and estimated, through Bayesian molecular dating, the ages of the 17 to 18 independent grass C4 lineages. The first transition from C3 to C4 photosynthesis occurred in the Chloridoideae subfamily, 32.0-25.0 Mya. The link between CO2 decrease and transition to C4 photosynthesis was tested by a novel maximum likelihood approach. We showed that the model incorporating the atmospheric CO2 levels was significantly better than the null model, supporting the importance of CO2 decline on C4 photosynthesis evolvability. This finding is relevant for understanding the origin of C4 photosynthesis in grasses, which is one of the most successful ecological and evolutionary innovations in plant history.

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…Although there is some dominance in the use of individual C 4 acid decarboxylases, apparently associated with different C 4 lineages, most species use a mixture of the three decarboxylases, the make-up of which varies depending on environmental conditions [19 -21]. Most estimates suggest that in both monocots and eudicots, the earliest origins of C 4 photosynthesis occurred approximately 25 -30 Ma during the mid-Oligocene [22,23]. An abrupt reduction in the concentration of atmospheric CO 2 during this period is thought to have favoured natural selection for the C 4 pathway [2,23].…”

Setaria viridis: A Model for C4 Photosynthesis

“…The C 4 photosynthetic pathway has originated multiple times within the grasses (Kellogg, 1999;Christin et al, 2008;Vicentini et al, 2008), having evolved, apparently independently, in subfamilies Aristidoideae, Chloridoideae, Micrairoideae, and Panicoideae (Sinha and Kellogg, 1996;Grass Phylogeny Working Group, 2001). The number of origins has been estimated to be as high as 17, although the precise number depends on whether reversal to C 3 is considered a possibility (Vicentini et al, 2008).…”

“…A summary of the origins and diversity of C 4 subtypes in the grasses is shown in Figure 1. This is a pruned tree based on relationships described by Vicentini et al (2008) and Christin et al (2008).…”

Loss of the Transit Peptide and an Increase in Gene Expression of an Ancestral Chloroplastic Carbonic Anhydrase Were Instrumental in the Evolution of the Cytosolic C4 Carbonic Anhydrase in Flaveria

“…The primary driver for the evolution of the pathway is believed to be the reduction in atmospheric CO 2 concentrations to near present-day levels, which were reached at the Oligocene/Miocene boundary about 24 million years ago, with other environmental factors such as heat, aridity, and salinity also playing important roles in the development and expansion of the C 4 syndrome (Sage, 2004;Osborne and Beerling, 2006;Tipple and Pagani, 2007;Christin et al, 2008;Vicentini et al, 2008). The plants that evolved as a result of these selective pressures were able to concentrate CO 2 in their leaves because of an exquisite blend of anatomy and biochemistry (Hatch, 1987).…”