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.

    • "The effect of increased growth of C 4 plants may be further increased because these highly productive plants would provide more fuel for fire during dry seasons. Fire would promote the expansion of C 4 plants by destroying and replacing C 3 with C 4 plants (Beerling and Osborne, 2006; Bond et al., 2005; Daniau et al., 2010; Osborne and Beerling, 2006). Thus, fire effects may explain why C 4 plants spread during times of enhanced insolation. "
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    ABSTRACT: Global and local climatic forcing, e.g. concentration of atmospheric CO2 or insolation, influence the distribution of C3 and C4 plants in southwest Africa. C4 plants dominate in more arid and warmer areas and are favoured by lower pCO2 levels. Several studies have assessed past and present continental vegetation by the analysis of terrestrial n-alkanes in near-coastal deep sea sediments using single samples or a small number of samples from a given climatic stage. The objectives of this study were to evaluate vegetation changes in southwest Africa with regard to climatic changes during the Late Pleistocene and the Holocene and to elucidate the potential of single sample simplifications. We analysed two sediment cores at high resolution, altogether ca. 240 samples, from the Southeast Atlantic Ocean (20°S and 12°S) covering the time spans of 18 to 1 ka and 56 to 2 ka, respectively. Our results for 20°S showed marginally decreasing C4 plant domination (of ca. 5%) during deglaciation based on average chain length (ACL27–33 values) and carbon isotopic composition of the C31 and C33n-alkanes. Values for single samples from 18 ka and the Holocene overlap and, thus, are not significantly representative of the climatic stages they derive from. In contrast, at 12°S the n-alkane parameters show a clear difference of plant type for the Late Pleistocene (C4 plant domination, 66% C4 on average) and the Holocene (C3 plant domination, 40% C4 on average). During deglaciation vegetation change highly correlates with the increase in pCO2 (r² = 0.91). Short-term climatic events such as Heinrich Stadials or Antarctic warming periods are not reflected by vegetation changes in the catchment area. Instead, smaller vegetation fluctuations during the Late Pleistocene occur in accordance with local variations of insolation.
    Quaternary Science Reviews 10/2015; 125:160-171. DOI:10.1016/j.quascirev.2015.08.004 · 4.57 Impact Factor
    • "Dated phylogenies suggest that the diversification in Neotropical savannas occurred no later than 10–4 Ma (Pennington et al., 2006; Simon et al., 2009). Fossil records show evidence of early diversification of C 4 grasses in the late Pliocene , c. 4 Ma, also supporting the hypothesis that savannas originated in the past 10 Myr (Osborne & Beerling, 2006). "
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    ABSTRACT: AimWe investigated the phylogenetic structure of woody Caesalpinioideae species to address whether in situ diversification or habitat shifts from other biomes explain the species diversity in the Cerrado.LocationAmazon and Atlantic rain forests, Cerrado and Caatinga in Brazil.Methods We obtained occurrence data and generated a phylogenetic hypothesis for all woody Caesalpinioideae species occurring in Brazil. We calculated the net relatedness index (NRI) to measure the phylogenetic structure and performed a nodesig analysis to identify which clades contributed to phylogenetic clustering or overdispersion. We also calculated phylogenetic and taxonomic indices of beta diversity to investigate species turnover between Cerrado habitats and neighbouring biomes.ResultsSpecies occurring in savannas and forested savannas were more related than expected by chance, i.e. phylogenetic clustering. Clades that were overabundant in savannas and forested savannas, such as Bauhinia, were poorly represented in neighbouring biomes, providing evidence of in situ diversification in some lineages. Savannas shared clades and showed lower phylogenetic than taxonomic dissimilarity from Caatinga, consistent with habitat shifts, mainly in the Cassia and Caesalpinia clades.Main conclusionsDry, open habitats (savannas, forested savannas and Caatinga) have lineages that diversified more recently than those in forest habitats. Caesalpinioideae lineages from savannas and Caatinga are closely related, and this dissimilarity was due to both turnover (55.5%) and nestedness (44.5%). Hence, species inhabiting Caatinga and savannas are often resolved as pairs of sister species, indicating habitat shifts (especially in the Cassia and Caesalpinia clades). The higher phylogenetic diversity of species in the Caatinga than in savanna and forested savanna may indicate that lineage shifts may have occurred, mainly from the Caatinga into the savanna habitats. Phylogenetic and taxonomic dissimilarity of savannas with Amazon and Atlantic rain forests was mainly due to the turnover of lineages, with evidence of in situ diversification in some clades, especially Bauhinia.
    Journal of Biogeography 01/2015; DOI:10.1111/jbi.12634 · 4.59 Impact Factor
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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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