Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era

Beerling, David J.; Osborne, Colin P.; Chaloner, W. G.

doi:10.1038/35066546

Cited by 246 publications

(160 citation statements)

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“…Previously hypothesized modifications of the water transport system and associated plant features driven by low CO 2 include the evolution of xylem vessels and stomata [108], and the planate leaf [109,110] with high vein density [78]. These innovations permitted more rapid growth and diversification, leading to the succession of dominance from pteridophytes to gymnosperms to angiosperms [78,80,111,112].…”

Section: Discussionmentioning

confidence: 99%

Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics

Osborne

Sack²

2012

Phil. Trans. R. Soc. B

183

193

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C 4 photosynthesis has evolved more than 60 times as a carbon-concentrating mechanism to augment the ancestral C 3 photosynthetic pathway. The rate and the efficiency of photosynthesis are greater in the C 4 than C 3 type under atmospheric CO 2 depletion, high light and temperature, suggesting these factors as important selective agents. This hypothesis is consistent with comparative analyses of grasses, which indicate repeated evolutionary transitions from shaded forest to open habitats. However, such environmental transitions also impact strongly on plant -water relations. We hypothesize that excessive demand for water transport associated with low CO 2 , high light and temperature would have selected for C 4 photosynthesis not only to increase the efficiency and rate of photosynthesis, but also as a water-conserving mechanism. Our proposal is supported by evidence from the literature and physiological models. The C 4 pathway allows high rates of photosynthesis at low stomatal conductance, even given low atmospheric CO 2 . The resultant decrease in transpiration protects the hydraulic system, allowing stomata to remain open and photosynthesis to be sustained for longer under drying atmospheric and soil conditions. The evolution of C 4 photosynthesis therefore simultaneously improved plant carbon and water relations, conferring strong benefits as atmospheric CO 2 declined and ecological demand for water rose.

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Section: Discussionmentioning

confidence: 99%

Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics

Osborne

Sack²

2012

Phil. Trans. R. Soc. B

183

193

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“…8. The maximum viable leaf size was calculated by adjusting the modeled path length for air flow over the leaf until a leaf temperature of 45°C was reached.…”

Section: Methodsmentioning

confidence: 99%

“…Fossil evidence therefore demonstrates that the genes required for laminate structures had already evolved in independent groups, and that no intrinsic genetic or developmental barriers delayed the widespread appearance of leaves. Theory suggests an environmental barrier to leaf evolution, involving evaporative and convective cooling, leaf size, and CO 2 -mediated stomatal evolution (8). This mechanism draws attention to the fact that low stomatal frequencies of early land plants (9,10) in the high CO 2 atmosphere of the middle Paleozoic (Fig.…”

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confidence: 99%

“…This mechanism draws attention to the fact that low stomatal frequencies of early land plants (9,10) in the high CO 2 atmosphere of the middle Paleozoic (Fig. 1A) placed a tight physical limit on evaporative energy loss (8). Large leaves developing in these plants would therefore have been prone to lethal overheating because of greater interception of solar energy and lower convective heat dissipation than a leafless stem (8).…”

mentioning

confidence: 99%

“…1A) placed a tight physical limit on evaporative energy loss (8). Large leaves developing in these plants would therefore have been prone to lethal overheating because of greater interception of solar energy and lower convective heat dissipation than a leafless stem (8). As atmospheric CO 2 levels subsequently declined (11) (Fig.…”

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confidence: 99%

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Biophysical constraints on the origin of leaves inferred from the fossil record

Osborne

Beerling

Lomax

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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The molecular tool kit for producing flat-bladed photosynthetic structures evolved in marine and terrestrial plants during the middle Paleozoic, but it took a further 20 million years before leaves suddenly spread throughout land floras. This delay has long been difficult to explain, given the apparent advantage of leaves for photosynthetic primary production. Theory and experiments predict that exceptionally high atmospheric CO 2 levels in the middle Paleozoic delayed the origin of leaves by restricting stomatal development. This would have limited evaporative cooling, leading to lethal overheating of leaves absorbing large quantities of solar energy. Here we test the central prediction of this argument with a morphometric analysis of 300 plant fossils from major European collections. We show a 25-fold enlargement of leaf blades in two phylogenetically independent clades as atmospheric CO 2 levels fell during the late Paleozoic. Furthermore, preliminary data suggest that the first abrupt increase in leaf size was accompanied by an 8-fold rise in stomatal density. These evolutionary patterns support the relaxation of biophysical constraints on leaf area predicted by theory and point to a significant role for CO 2 in plant evolution.

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On the Evolution of the Carbon Cycle

Falkowski¹

2002

Phytoplankton Productivity

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Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era

Cited by 246 publications

References 29 publications

Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics

Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics

Biophysical constraints on the origin of leaves inferred from the fossil record

On the Evolution of the Carbon Cycle

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Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic era

Cited by 246 publications

References 29 publications

Evolution of C 4 plants: a new hypothesis for an interaction of CO 2 and water relations mediated by plant hydraulics

Evolution of C 4 plants: a new hypothesis for an interaction of CO 2 and water relations mediated by plant hydraulics

Biophysical constraints on the origin of leaves inferred from the fossil record

On the Evolution of the Carbon Cycle

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Product

Resources

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Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics

Evolution of C ₄ plants: a new hypothesis for an interaction of CO ₂ and water relations mediated by plant hydraulics