Nature's green revolution: The remarkable evolutionary rise of C 4 plants

Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Philosophical Transactions of The Royal Society B Biological Sciences (Impact Factor: 7.06). 02/2006; 361(1465):173-94. DOI: 10.1098/rstb.2005.1737
Source: PubMed


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.

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    • "We find this idea compelling to explain at least some of the historical contingency that may account for more recent instances of exceptional angiosperm diversification. The reasons for this interpretation are that (1) CCMs confer increased photosynthetic capacity and water-use efficiency (WUE) in arid environments (Cushman 2001; Osborne and Beerling 2006; Kadereit et al. 2012; Osborne and Sack 2012; Pau et al. 2013), (2) CCMs have numerous , independent origins within angiosperms (Smith and Winter 1996; Silvera et al. 2010; Sage et al. 2011a; Edwards and Ogburn 2012), and (3) CCM plants exhibit a high degree of dominance in contemporary dryland ecosystems (Lüttge 2004; Sage 2004; Edwards and Smith 2010; Alvarado-Cárdenas et al. 2013). Furthermore , divergence time estimates of major angiosperm clades in which CCMs are present suggest that the timing of diversification rate increases in these clades is consistent with the hypothesis that Miocene/Pliocene aridification was an important extrinsic driver of these events (Klak et al. 2004; Good-Avila et al. 2006; Arakaki et al. 2011; Hernández-Hernández et al. 2014; Spriggs et al. 2014). "
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    ABSTRACT: The mid-Cenozoic decline of atmospheric CO2 levels that promoted global climate change was critical to shaping contemporary arid ecosystems. Within angiosperms, two CO2 -concentrating mechanisms (CCMs)-CAM and C4 -evolved from the C3 photosynthetic pathway, enabling more efficient whole-plant function in such environments. Many angiosperm clades with CCMs are thought to have diversified rapidly due to Miocene aridification, but links between this climate change, CCM evolution, and increased net diversification rates (r) remain to be further understood. Euphorbia (∼2000 species) includes a diversity of CAM-utilizing stem succulents, plus a single species-rich C4 subclade. We used ancestral state reconstructions with a dated molecular phylogeny to reveal that CCMs independently evolved 17-22 times in Euphorbia, principally from the Miocene onwards. Analyses assessing among-lineage variation in r identified eight Euphorbia subclades with significantly increased r, six of which have a close temporal relationship with a lineage-corresponding CCM origin. Our trait-dependent diversification analysis indicated that r of Euphorbia CCM lineages is approximately three-fold greater than C3 lineages. Overall, these results suggest that CCM evolution in Euphorbia was likely an adaptive strategy that enabled the occupation of increased arid niche space accompanying Miocene expansion of arid ecosystems. These opportunities evidently facilitated recent, replicated bursts of diversification in Euphorbia. This article is protected by copyright. All rights reserved.
    Evolution 12/2014; 68(12):3485-3504. DOI:10.1111/evo.12534 · 4.61 Impact Factor
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    • "Ehleringer et al., 1997; Huang et al., 2001; Osborne and Beerling, 2006; Edwards et al., 2010; Bremond et al., 2012; Campo-Bescos et al., 2013). [CO 2 ] affects the water use efficiency of C 3 plants disproportionally compared to C 4 plants, which, in seasonally wet tropical savannas, leads to C 4 plants being more competitive at low [CO 2 ] (Ehleringer et al., 1997; Osborne and Beerling, 2006). Hence, C 4 plants are more productive than C 3 plants at very high air temperatures because the CO 2 concentrating mechanism of C 4 photosynthesis alleviates the biochemical disadvantage of the temperature dependence of the CO 2 versus O 2 uptake by the primary photosynthetic enzyme Rubisco (e.g. "
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    ABSTRACT: The savanna vegetation of southern tropical Africa is characterized by co-dominance of C4 grasslands and C3 woodlands. Long-term variations in the tropical savanna vegetation in arid and semi-arid climates are commonly considered to be primarily sensitive to precipitation and atmospheric CO2 concentrations. The sensitivity of tropical vegetation to temperature, however, is often considered as secondary or negligible, particularly in paleostudies due to difficulties of reconstructing terrestrial temperature in the tropics. In this study, we use the terrestrial vegetation model BIOME4, which was forced by climate simulations from the Kiel Climate Model (KCM) for the Holocene and by climate reconstructions for the most recent glacial period to understand reconstructed vegetation changes in southern tropical Africa of the past 37,000 yr. We focus on these two periods because vegetation reconstructions from a marine sediment core near the Zambezi River mouth cannot be explained by precipitation changes and changes of atmospheric CO2 alone. For the Holocene, we force BIOME4 simulations with reconstructed atmospheric CO2 concentrations, and spatial and seasonal climate patterns from the early- and mid-Holocene (9.5 and 6 ka BP) simulations with the KCM. For the glacial period, we analyze idealized experiments based upon reconstructed temperature, precipitation and CO2 at 31, 28 and 21 ka BP. Our study shows that both Holocene and glacial simulations of vegetation cover exhibit good agreement with reconstructed C4:C3C4:C3 ratios when temperature changes are taken into account. While both precipitation and temperature control the C4:C3C4:C3 ratio during the Holocene atmospheric CO2 and temperature variations are major factors controlling vegetation changes during the glacial period. In our simulations, variations in temperature along with precipitation and atmospheric CO2 reconcile the evolution of vegetation observed in the Zambezi catchment during the last 37,000 yr. In consequence, the effect of temperature variations on tropical savanna vegetation should be taken into account with respect to modeling past or future climates.
    Earth and Planetary Science Letters 10/2014; 403:407–417. DOI:10.1016/j.epsl.2014.06.043 · 4.73 Impact Factor
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    • "2010 ) . This event probably started from North America ( Osborne and Beerling 2006 ) . "
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    ABSTRACT: Xerinae is the most species-rich subfamily of the Sciuridae (Rodentia). This group of animals has a long complex evolutionary history, which witnessed severe environmental changes. In this paper, a comprehensive approach integrating information from fossil records, morphological, molecular and geographical data of extant species, and events of paleoclimate and paleogeography, were used to explore the evolutionary processes in the Xerinae. Xerinae probably originated in Eurasia around the early Oligocene, and dispersed to Africa via the Africa-Eurasia Land Bridge on two occasions during the Miocene, and subsequently evolved into the Protoxerini and African Xerini. The tribe Marmotini derived from a Eurasian ancestor and thrived in North America. Tamias re-occupied Eurasia in the early Miocene, while the distributions of Marmota and ‘Spermophilus’ genus-groups were restricted to North America at least until the late Miocene. Global cooling and the emergence of grass-dominated ecosystems from 15 Ma are likely to be the main causes for the radiation of Marmotini. The body form of Xerinae displays an allometric mode of evolution, with ground-living taxa, such as Marmota, Cynomys and Xerus notably enlarged, while Tamias has remained slim in body form. To cope with the global environmental changes, particularly the global cooling induced forest degradation and grassland expansion in the late Miocene, most Marmotini developed into true ground squirrels with short tails. The slim body adaptation in Tamias may be related to competition from tree squirrels, or their hoarding behavior, the latter helping them to cope with cold winter.
    Evolutionary Biology 03/2014; 41(1):99-114. DOI:10.1007/s11692-013-9250-7 · 2.61 Impact Factor
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