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, 16 (1), e2003706
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Genome Downsizing, Physiological Novelty, and the Global Dominance of Flowering Plants

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Genome Downsizing, Physiological Novelty, and the Global Dominance of Flowering Plants

Kevin A Simonin et al. PLoS Biol.

Abstract

The abrupt origin and rapid diversification of the flowering plants during the Cretaceous has long been considered an "abominable mystery." While the cause of their high diversity has been attributed largely to coevolution with pollinators and herbivores, their ability to outcompete the previously dominant ferns and gymnosperms has been the subject of many hypotheses. Common among these is that the angiosperms alone developed leaves with smaller, more numerous stomata and more highly branching venation networks that enable higher rates of transpiration, photosynthesis, and growth. Yet, how angiosperms pack their leaves with smaller, more abundant stomata and more veins is unknown but linked-we show-to simple biophysical constraints on cell size. Only angiosperm lineages underwent rapid genome downsizing during the early Cretaceous period, which facilitated the reductions in cell size necessary to pack more veins and stomata into their leaves, effectively bringing actual primary productivity closer to its maximum potential. Thus, the angiosperms' heightened competitive abilities are due in no small part to genome downsizing.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. The distribution of genome size among 393 land plant species.
Branch lengths are colored according to clade (ferns, gymnosperms, angiosperms). Orange bars at the tips are scaled proportional to genome size for each terminal species. Data can be found in S1 Data.
Fig 2
Fig 2
Relationships between genome size and anatomical traits: (a) lg, (b) Ds, and (c) Dv. In all panels, insets show log-log relationships and R2 values are from standard major axis regressions (lg n = 242; Ds n = 247; Dv n = 198). Phylogenetically corrected major axis regressions have similar slopes, R2, and p-values, and are shown in Table 1. Data can be found in S1 Data. Ds, stomatal density; Dv, leaf vein density; lg, guard cell length.
Fig 3
Fig 3. The major axis regressions between genome size and gs, max (solid line; R2 = 0.24, n = 184) and gs, op, operational stomatal conductance (dashed lines; n = 198), plotted on a log-log scale. gs, op was calculated using a hydraulic model based on vein spacing under assumptions of three leaf thicknesses (70 μm, R2 = 0.47; 100 μm, R2 = 0.45; 130 μm, R2 = 0.44; see Eqs 2–6 for details) and an assumed vapor pressure deficit of 2 kPa.
Variation in vapor pressure deficit will affect the intercept of gs, op but not the slope. Points are omitted for clarity. Phylogenetically corrected major axis regressions are similarly significant and are reported in Table 1. gs, max, maximum stomatal conductance; gs, op, operational stomatal conductance.
Fig 4
Fig 4. Ancestral state reconstructions of genome size, Dv, lg, and Ds through time for angiosperms (A; blue circles), gymnosperms (G; pink triangles), and ferns (F; grey squares).
Error bars around reconstructed values represent error due to phylogenetic uncertainty. The shaded timespan indicates the Cretaceous period, during which most major lineages of angiosperms diversified. Lines represent the best-fit models through the lower (genome size and lg) and upper (Dv and Ds) 10% of reconstructed values. For all traits, extreme trait values of angiosperms rapidly changed during the Cretaceous period, whereas fern and gymnosperm lineages underwent no such changes. (a) Genome size of ferns (genome size = 10.24; n = 51, df = 11, p < 0.001), gymnosperms (genome size = 19.46; n = 53, df = 13, p < 0.001), and angiosperms (genome size = 1.08 + 2.53/(1 + e^(−(time − 119.28) / 9.52; n = 289, df = 20, p < 0.001). (b) Leaf Dv of ferns (Dv = 1.70; n = 10, df = 1, p < 0.01), gymnosperms (Dv = 1.74; n = 23, df = 9, p < 0.001), and angiosperms (Dv = 4.39 + 4.42 / (1 + e^(−[time − 125.32] / [−8.22]), n = 165, df = 17, p < 0.001). (c) lg of ferns (lg = 43.04; n = 38, df = 12, p < 0.001), gymnosperms (lg = 55.48; n = 20, df = 8, p < 0.001), and angiosperms (lg = 26.93 + 10.58 / (1 + e^(−[time − 119.73] / 6.12); n = 184, df = 16, p < 0.001. (d) Ds of ferns (Ds = 1.80; n = 26, df = 2, p < 0.001), gymnosperms (Ds = 1.94; n = 37, df = 11, p < 0.001), and angiosperms (Ds = 2.33 − 0.364 / (1 + e^(−[time − 121.65] / 17.39); n = 184, df = 15, p < 0.001). Marginal plots on the outside of each panel represent the median (points), interquartile ranges (solid lines), and ranges (dotted lines) of trait values for extant species. A, angiosperms; Ds, stomatal density; Dv, vein density; F, ferns; G, gymnosperms; lg, guard cell length.

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Grant support

The authors received no specific funding for this work.
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