Nature's green revolution: the remarkable evolutionary rise of C4 plants

Abstract

Plants with the C4 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 CO2-concentrating pump, which leads to high photosynthetic efficiency in warm climates and low atmospheric CO2 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 CO2 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 C4 success in North America. CO2-starvation is implicated in the origins of C4 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 C4 mechanism at this time, although possible ancestral components of the C4 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.

Figure 1

Simple schematic diagram of the C₄ photosynthetic pathway showing compartmentalization of the different enzyme systems involved, and the connection between CO₂-pumping by the C₄ cycle and CO₂-fixation by the C₃ cycle. Abbreviations: CA, carbonic anhydrase; HCO₃, bicarbonate; PEPc, phosphoenolpyruvate carboxylase; DC, decarboxylase enzyme(s); Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase.

Figure 2

Modelled interaction between temperature and CO₂ on the photosynthetic quantum yields (maximum light-use efficiencies) of C₃ and C₄ plants. Notice that the temperature at which C₃ and C₄ quantum yields cross over declines with falling atmospheric CO₂ concentration.

Figure 3

Increase in δ¹³C from palaeosols and tooth enamel showing apparent synchronicity in the transition to C₄-dominated terrestrial ecosystems across continents. Data for (a) from Cerling et al. (1997), (b) from Quade & Cerling (1995) and (c) from Passey et al. (2002).

Figure 4

Atmospheric CO₂ trends over the past 35 Myr, as reconstructed from three different proxies (data from Pagani et al. 1999; Pearson & Palmer 2000; Royer et al. 2001).

Figure 5

Geological evidence from the Indian subcontinent of ecosystem dynamics and climate change through the Late Miocene and Pliocene: (a) δ¹³C of palaeosol carbonates (data from Quade & Cerling 1995) and inferred C₄ plant productivity (following Fox & Koch 2003), (b) δ¹³C of tooth enamel from Equids (horses) and Proboscideans (elephant-like mammals) (data from Quade & Cerling 1995) and the inferred proportion of diet comprised of C₄ plant biomass (following Passey et al. 2002), (c) δ¹⁸O of palaeosol carbonates (data source as (a)), (d) abundance of Globigerinoides bulloides in the Arabian Sea (data from Zhisheng et al. 2001), (e) vegetation type inferred from pollen abundance (data from Hoorn et al. 2000), and (f) charcoal flux to North Pacific sediments (data from Keeley & Rundel 2003).

Figure 6

Geological evidence from the Great Plains of North America of ecosystem dynamics and climate change through the Late Miocene and Pliocene. Data sources are: (a) and (b) Janis et al. (2000); (c) Cerling et al. (1997), Latorre et al. (1997) and Passey et al. (2002), (d) Cerling et al. (1997) and Passey et al. (2002), (e) Fox & Koch (2003), and (f) MacFadden et al. (1999) and Passey et al. (2002).

Figure 7

Variations in: (a) the partial pressure of atmospheric CO₂ and O₂ over the past 500 Myr of the Phanerozoic, (b) calculated changes in global mean surface temperature, and (c) calculated changes in the tropics. Also shown in (c) are estimates of tropical temperatures from oxygen isotope ratios of fossil foraminifera shells (Pearson et al. 2001) and calculations from marine calcium carbonate fossils (Veizer et al. 2000) corrected for the CO₂-effects on ocean pH (Royer et al. 2004).

Figure 8

Calculated changes in: (a) quantum yield of C₃ and C₄ plants through the past 500 Myr of the Phanerozoic, (b) the effects of CO₂ in combination with either tropical climate (filled squares) or global mean climate (open squares) on quantum yield, and (c) the calculated crossover temperature for C₄ and C₄ plants in comparison with the tropical climate (with and without the effects of solar forcing) shown in figure 7.

Figure 9

Simulated global distribution of C₄ plants using a generalized dynamic global vegetation model (Beerling & Woodward 2001) and either the land surface climatology from the UGAMP (lower left map) or NCAR (lower right map) GCMs. Central picture shows the palaeogeography of the Late Carboniferous (Westphalian; Scotese & McKerrow 1990) and the main regions/localities from which fossil plants were sampled for stable carbon isotope analysis (see appendix A for details). The frequency histograms depict the calculated values of carbon isotope discrimination and, for comparison, the values expected if plants operated with the C₄ photosynthetic pathway.

Figure 10

Photographic evidence showing the incorporation of ¹⁴C-labelled malate into insoluble compounds in leaves of (a) Osmunda regalis and (b) Ginkgo biloba (Palmer & Quick, unpublished data). Note the ¹⁴C activity concentrated around vascular tissues.