Genome downsizing, physiological novelty, and the global dominance of flowering plants

During the Cretaceous (145-66 Ma), early angiosperms rapidly diversified, eventually outcompeting the ferns and gymnosperms previously dominating most ecosystems. Heightened competitive abilities of angiosperms are often attributed to higher rates of transpiration facilitating faster growth. This hypothesis does not explain how angiosperms were able to develop leaves with smaller, but densely packed stomata and highly branched venation networks needed to support increased gas exchange rates. Although genome duplication and reorganization have likely facilitated angiosperm diversification, here we show that genome downsizing facilitated reductions in cell size necessary to construct leaves with a high density stomata and veins. Rapid genome downsizing during the early Cretaceous allowed angiosperms to push the frontiers of anatomical trait space. In contrast, during the same time period ferns and gymnosperms exhibited no such changes in genome size, stomatal size, or vein density. Further reinforcing the effect of genome downsizing on increased gas exchange rates, we found that species employing water-loss limiting crassulacean acid metabolism (CAM) photosynthesis, have significantly larger genomes than C3 and C4 species. By directly affecting cell size and gas exchange capacity, genome downsizing brought actual primary productivity closer to its maximum potential. These results suggest species with small genomes, exhibiting a larger range of final cell size, can more finely tune their leaf physiology to environmental conditions and inhabit a broader range of habitats.

• Publication year

  2017

• Venue

  bioRxiv

• Publication date

  2017-08-10

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1371/journal.pbio.2003706PMID 29324757PMCID 5764239
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A 4000-species dataset provides new insight into the evolution of ferns.

  2016cited by this paper
• Optimal allocation of leaf epidermal area for gas exchange

  2016cited by this paper
• Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade.

  2016cited by this paper
• The Developmental Basis of Stomatal Density and Flux1[OPEN]

  2016cited by this paper
• Genome sizes for 71 species of Zamia (Cycadales: Zamiaceae) correspond with three different biogeographic regions

  2016cited by this paper
• Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution

  2015cited by this paper
• Weak coordination among petiole, leaf, vein, and gas‐exchange traits across Australian angiosperm species and its possible implications

  2015cited by this paper
• mvmorph: an r package for fitting multivariate evolutionary models to morphometric data

  2015cited by this paper
• Coordination of stomatal physiological behavior and morphology with carbon dioxide determines stomatal control.

  2015cited by this paper
• How Does Leaf Anatomy Influence Water Transport outside the Xylem?1[OPEN]

  2015cited by this paper
• A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity.

  2015cited by this paper
• Environmental adaptation in stomatal size independent of the effects of genome size

  2014cited by this paper
• Inferring climate from angiosperm leaf venation networks.

  2014cited by this paper
• Elevation-Related Variation in Leaf Stomatal Traits as a Function of Plant Functional Type: Evidence from Changbai Mountain, China

  2014cited by this paper
• Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology

  2014cited by this paper
• The enigma of the rise of angiosperms: can we untie the knot?

  2014cited by this paper
• Phylogeny and Divergence Times of Gymnosperms Inferred from Single-Copy Nuclear Genes

  2014cited by this paper
• Genome size evolution in Ontario ferns (Polypodiidae): evolutionary correlations with cell size, spore size, and habitat type and an absence of genome downsizing.

  2014cited by this paper
• Reconstructing relative genome size of vascular plants through geological time.

  2014cited by this paper
• Morphology and Leaflet Anatomy of the Ceratozamia norstogii (Zamiaceae, Cycadales) Species Complex in Mexico with Comments on Relationships and Speciation

  2013cited by this paper
• The Fossil Record of Plant-Insect Dynamics

  2013cited by this paper
• Comparative morphological, epidermal, and anatomical studies of Pinus roxburghii needles at different altitudes in the North-West Indian Himalayas

  2013cited by this paper
• Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates.

  2013cited by this paper
• Unified changes in cell size permit coordinated leaf evolution.

  2013cited by this paper
• Polyploidy enhances the occupation of heterogeneous environments through hydraulic related trade-offs in Atriplex canescens (Chenopodiaceae).

  2013cited by this paper
• Climate drives vein anatomy in Proteaceae.

  2013cited by this paper
• Allometry of cells and tissues within leaves.

  2013cited by this paper
• Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks.

  2013cited by this paper
• Spatial coordination between veins and stomata links water supply with water loss in leaves

  2013cited by this paper
• Megacycles of atmospheric carbon dioxide concentration correlate with fossil plant genome size

  2012cited by this paper
• Evolutionary Association of Stomatal Traits with Leaf Vein Density in Paphiopedilum, Orchidaceae

  2012cited by this paper
• Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations

  2012cited by this paper
• Geometrical constraints in the scaling relationships between genome size, cell size and cell cycle length in herbaceous plants

  2012cited by this paper
• Developmentally based scaling of leaf venation architecture explains global ecological patterns

  2012cited by this paper
• Differential leaf expansion can enable hydraulic acclimation to sun and shade.

  2012cited by this paper
• A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution

  2012cited by this paper
• Hydraulic conductance of leaves correlates with leaf lifespan: implications for lifetime carbon gain.

  2012cited by this paper
• Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.

  2012cited by this paper
• phytools: an R package for phylogenetic comparative biology (and other things)

  2012cited by this paper
• Leaf micromorphology of Aesculus hippocastanum L. and damage caused by leaf-mining larvae of Cameraria ohridella Deschka and Dimić

  2012cited by this paper
• smatr 3– an R package for estimation and inference about allometric lines

  2012cited by this paper
• Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution

  2012cited by this paper
• Angiosperm leaf vein patterns are linked to leaf functions in a global-scale data set.

  2011cited by this paper
• Cycads show no stomatal-density and index response to elevated carbon dioxide and subambient oxygen

  2011cited by this paper
• Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves

  2011cited by this paper
• MicroRNA122 is a key regulator of α-fetoprotein expression and influences the aggressiveness of hepatocellular carcinoma.

  2011cited by this paper
• Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture1[W][OA]

  2011cited by this paper
• Nuclear DNA amounts in angiosperms: targets, trends and tomorrow.

  2011cited by this paper
• Venation networks and the origin of the leaf economics spectrum.

  2011cited by this paper
• Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution

  2011cited by this paper
• Density and length of stomatal and epidermal cells in

  2011cited by this paper
• Ancestral polyploidy in seed plants and angiosperms

  2011cited by this paper
• Could Land Plant Evolution Have Fed the Marine Revolution?

  2011cited by this paper
• Picante: R tools for integrating phylogenies and ecology

  2010cited by this paper
• Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification.

  2010cited by this paper
• Impact of the hydraulic capacity of plants on water and carbon fluxes in tropical South America

  2010cited by this paper
• Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers.

  2010cited by this paper
• Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog?

  2010cited by this paper
• The value of leaf cuticle characteristics in the identification and classification of Iberian Mediterranean members of the genus Pinus

  2009cited by this paper
• Taxonomic diversity of stomata in dicot flora of a district tank (N.W.F.P.) in Pakistan

  2009cited by this paper
• The angiosperm radiation revisited, an ecological explanation for Darwin’s ‘abominable mystery’

  2009cited by this paper
• CO2‐forced evolution of plant gas exchange capacity and water‐use efficiency over the Phanerozoic

  2009cited by this paper
• Genome size as a predictor of guard cell length in Arabidopsis thaliana is independent of environmental conditions.

  2009cited by this paper
• Darwin's second 'abominable mystery': Why are there so many angiosperm species?

  2009cited by this paper
• Genome size and morphology of the Dryopteris affinis group in Central Europe

  2009cited by this paper
• Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time

  2009cited by this paper
• The meaning of Darwin's 'abominable mystery'.

  2009cited by this paper
• Angiosperm leaf vein evolution was physiologically and environmentally transformative

  2009cited by this paper
• Genome size is a strong predictor of cell size and stomatal density in angiosperms.

  2008cited by this paper
• VARIATION IN GENOMIC FORM IN PLANTS AND ITS ECOLOGICAL IMPLICATIONS

  2008cited by this paper
• Taxon sampling and the accuracy of phylogenetic analyses

  2008cited by this paper
• Scaling of xylem vessels and veins within the leaves of oak species

  2008cited by this paper
• The Biology of Invasive Alien Plants in Canada. 10. Nymphoides peltata (S. G. Gmel.) Kuntze

  2008cited by this paper
• Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange.

  2008cited by this paper
• Phylocom: software for the analysis of phylogenetic community structure and trait evolution

  2008cited by this paper
• Phylogenetics Phylocom : software for the analysis of phylogenetic community structure and trait evolution

  2008cited by this paper
• Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics1[W][OA]

  2007cited by this paper
• Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees.

  2006cited by this paper
• Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution

  2006cited by this paper
• The Mechanical Diversity of Stomata and Its Significance in Gas-Exchange Control[OA]

  2006cited by this paper
• Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species.

  2005cited by this paper
• Evolution of DNA amounts across land plants (embryophyta).

  2005cited by this paper
• Torus-Margo Pits Help Conifers Compete with Angiosperms

  2005cited by this paper
• Stomatal architecture and evolution in basal angiosperms.

  2005cited by this paper
• Pollination Syndromes and Floral Specialization

  2004cited by this paper
• Genome downsizing in polyploid plants

  2004cited by this paper
• APE: Analyses of Phylogenetics and Evolution in R language

  2004cited by this paper
• Stochastic mapping of morphological characters.

  2003cited by this paper
• Variation in nuclear DNA content across environmental gradients: a quantile regression analysis

  2002cited by this paper
• CAM‐cycling in the cycad Dioon edule Lindl. in its natural tropical deciduous forest habitat in central Veracruz, Mexico

  2002cited by this paper
• Molecular Phylogenetics and Evolution

  2001cited by this paper
• Ancestral state estimation and taxon sampling density.

  2001cited by this paper
• The effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana.

  2001cited by this paper
• Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record

  1997cited by this paper
• Crassulacean acid metabolism: Biochemistry, ecophysiology and evolution

  1996cited by this paper
• Crassulacean acid metabolism : biochemistry, ecophysiology, and evolution

  1996cited by this paper
• Taxonomic distribution of crassulacean acid metabolism

  1996cited by this paper
• Shifts in Diversification Rate with the Origin of Angiosperms

  1994cited by this paper
• Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution.

  1994cited by this paper
• Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation

  1993cited by this paper

• Gapless pangenome analyses reveal fast Brassica rapa subspeciation.

  2026cites this paper
• The evolutionary success of angiosperms: a foundation of bioenergetic surplus.

  2026cites this paper
• A comprehensive review of cytogenetic data of Epidendroideae (Orchidaceae): the OrchidCounts, a new database as a tool for evolution studies

  2026cites this paper
• Plastid and nuclear phylogenomics of Cyphostemma (Vitaceae) provide new insights into genome size evolution across sub-Saharan Africa.

  2026cites this paper
• Xylem Hydraulic Conductance and Stomatal Aperture Ratio Are Key Factors in Enhancing Drought Tolerance in Cotton

  2026cites this paper
• Leaf epidermal cell size in trees: developmental possibilities stay wide with height growth in two angiosperm tree species.

  2025cites this paper
• Towards Understanding the Factors Shaping the Composition and Function of the Noccaea Microbiome in Metal-Contaminated Environments

  2025cites this paper
• Elucidation of the adaptability of Cinnamomum camphora seedlings from different provenances via analyzing photosynthetic characteristics and anatomical structure

  2025cites this paper
• Interactive effects of life cycle and monocot-dicot lineage on genome size–trait relationships in angiosperms: a phylogenetically informed analysis

  2025cites this paper
• Plant Genome Size Mediates Species and Community Responses to Precipitation Change and Nitrogen Enrichment in Grasslands

  2025cites this paper
• Small Genome Size Ensures Adaptive Flexibility for an Alpine Ginger

  2025influential citation
• Large Genomes Are Associated With Greater Cell Size and Ecological Shift Towards More Nitrogen‐Rich and Higher‐Latitude Environments in Microalgae of the Genus Synura

  2025cites this paper
• Diploidization in a wild rice allopolyploid is both episodic and gradual

  2025cites this paper
• Heterogeneous trait responses of Páramo plant species and community to experimental warming

  2025cites this paper
• Which morphological traits can be used to reconstruct genome size in fossil plants? Assessing sporomorph size and stomatal guard cell length as paleo-genome size proxies

  2025influential citation
• Rampant transitions between dispersal syndromes during angiosperm evolution

  2025cites this paper
• Reductional dysploidy and genome size diversity in Pooideae, the largest subfamily of grasses (Poaceae)

  2025cites this paper
• Persistent Habitat Instability and Patchiness, Sexual Attraction, Founder Events, Drift and Selection: A Recipe for Rapid Diversification of Orchids

  2025cites this paper
• Mosses Reveal a Universal Genome-Cell Size Relationship Across Land Plants Shaped by Shared Evolutionary Pressures.

  2025cites this paper
• Polyploidy drives changes in tissue allocation modifying whole-plant water relations

  2025cites this paper
• Distinct patterns of genome size evolution in each bryophyte lineage are not correlated with whole genome duplication.

  2025cites this paper
• Cell size has pervasive effects on the functional composition and morphology of leaves: a case study in Rhododendron (Ericaceae)

  2025cites this paper
• Genome size variation and whole-genome duplications in the monocot order Poales

  2025cites this paper
• Convergent evolution of cell size enables adaptation to the mangrove habitat.

  2025cites this paper
• Geographically proximate rare species exhibit strong population divergence while maintaining intraspecific genetic diversity in Homoranthus (Myrtaceae).

  2025cites this paper
• Hidden in Plain Sight. How Ks histogram dynamics can reveal and obscure ancient whole genome duplications

  2025cites this paper
• Causes of delayed angiosperm diversification: The photosynthetic revolution, increased opportunity costs of anti‐herbivore defenses, selection for qualitative toxins, and acceleration of plant–herbivore coevolution

  2025cites this paper
• Ancient hybridization and repetitive element proliferation in the evolutionary history of the monocot genus Amomum (Zingiberaceae)

  2024cites this paper
• Mechanistic insights into plant community responses to environmental variables: genome size, cellular nutrient investments, and metabolic tradeoffs

  2024influential citation
• Genomic correlates of vascular plant reproductive complexity and the uniqueness of angiosperms

  2024cites this paper
• Exploring the complexity of genome size reduction in angiosperms

  2024cites this paper
• Intraspecific genome size variation in Rorippa indica reveals a tropical adaptation by genomic enlargement

  2024cites this paper
• Bigger genomes provide environment‐dependent growth benefits in grasses

  2024cites this paper
• First insight into the genomes of the Pulmonaria officinalis group (Boraginaceae) provided by repeatome analysis and comparative karyotyping

  2024cites this paper
• Stomatal behaviour and water relations in ferns and lycophytes across habits and habitats

  2024cites this paper
• Climate and genome size shape the intraspecific variation in ecological adaptive strategies of a cosmopolitan grass species

  2024cites this paper
• Limited effects of xylem anatomy on embolism resistance in cycad leaves.

  2024cites this paper
• Evolutionary patterns of variations in chromosome counts and genome sizes show positive correlations with taxonomic diversity in tropical gingers.

  2024cites this paper
• Genome size, ploidy estimates, and leaf morphology of temperate Lindera (Lauraceae) cultivated in North America

  2024cites this paper
• Polyploidy – A tool in adapting trees to future climate changes? A review of polyploidy in trees

  2024cites this paper
• Genomic and transcriptomic studies on flavonoid biosynthesis in Lagerstroemia indica

  2024cites this paper
• Competition for epidermal area, instead of coordination, between stomata and vein patterns in Ficus (Moraceae) with different growth forms

  2024cites this paper
• Plant invasion and naturalization are influenced by genome size, ecology and economic use globally

  2024cites this paper
• Plant microphenotype: from innovative imaging to computational analysis

  2024cites this paper
• The dual role of the angiosperm radiation on insect diversification

  2023cites this paper
• Traits-based approach: leveraging genome size in plant-microbe interactions.

  2023cites this paper
• Karyotype and genome size variation in Delphinium subg. Anthriscifolium (Ranunculaceae)

  2023cites this paper
• Does the evolution of micromorphology accompany chromosomal changes on dysploid and polyploid levels in the Barnardia japonica complex (Hyacinthaceae)?

  2023cites this paper
• Neopolyploidy increases stress tolerance and reduces fitness plasticity across multiple urban pollutants: support for the “general-purpose” genotype hypothesis

  2023cites this paper
• Genome size is positively correlated with extinction risk in herbaceous angiosperms

  2023cites this paper
• The Plant DNA C-Values Database: A One-Stop Shop for Plant Genome Size Data.

  2023cites this paper
• Comparative triple-color FISH mapping and genome size advances understanding of the cytogenetic diversity in wild Solanum species

  2023cites this paper
• From genome size to trait evolution during angiosperm radiation.

  2023cites this paper
• Genome material costs and functional tradeoffs in the autopolyploid Solidago gigantea (Giant Goldenrod) series.

  2023cites this paper
• Cytological Pattern Reveals Genome Downsizing in Cynodon dactylon (L.) Pers along the Longitudinal Gradient

  2023cites this paper
• Endoreplication—Why Are We Not Using Its Full Application Potential?

  2023cites this paper
• Creating a virtual leaf

  2023cites this paper
• Stomatal dynamics are regulated by leaf hydraulic traits and guard cell anatomy in nine true mangrove species

  2023cites this paper
• Hydraulic differences between flowers and leaves are driven primarily by pressure-volume traits and water loss

  2023cites this paper
• Coordination of inter-tracheid pit traits and climate effects among cycads.

  2023cites this paper
• Genome size variation within Crithmum maritimum: Clues on the colonization of insular environments

  2023cites this paper
• Stomatal distribution pattern for 90 species in Loess Plateau – Based on replicated spatial analysis

  2023cites this paper
• Fewer chromosomes, more co-occurring species within plant lineages - a likely effect of local survival and colonization.

  2023cites this paper
• Contextualizing Stomata

  2022cites this paper
• New Insights Into the Evolution of C4 Photosynthesis Offered by the Tarenaya Cluster of Cleomaceae

  2022cites this paper
• Structural organization of the spongy mesophyll

  2022cites this paper
• Are chromosome number and genome size associated with habit and environmental niche variables? Insights from the Neotropical orchids.

  2022cites this paper
• Genomic regions associate with major axes of variation driven by gas exchange and leaf construction traits in cultivated sunflower (Helianthus annuus L.)

  2022cites this paper
• Priming Seeds with Indole and (Z)-3-Hexenyl Acetate Enhances Resistance Against Herbivores and Stimulates Growth

  2022cites this paper
• Scaling relationships of leaf vein and areole traits versus leaf size for nine Magnoliaceae species differing in venation density

  2022cites this paper
• Correlated evolution of seed mass and genome size varies among life forms in flowering plants

  2022cites this paper
• S0960258522000071jra 46..52

  2022cites this paper
• Uncovering the influence of genomic traits in shaping land plant diversity. A commentary on 'Are chromosome number and genome size associated with habit and environmental niche variables? Insights from the Neotropical orchids'.

  2022cites this paper
• Do water and soil nutrient scarcities differentially impact the performance of diploid and tetraploid Solidago gigantea (Giant Goldenrod, Asteraceae)?

  2022cites this paper
• Packing limits and developmental integration are not sufficient to explain stomatal anatomical evolution in flowering plants

  2022influential citation
• Cell types as species: Exploring a metaphor

  2022cites this paper
• Impact of polyploidy on plant tolerance to abiotic and biotic stresses

  2022cites this paper
• Plant genome size modulates grassland community responses to multi-nutrient additions.

  2022cites this paper
• How Important Are Functional and Developmental Constraints on Phenotypic Evolution? An Empirical Test with the Stomatal Anatomy of Flowering Plants

  2022cites this paper
• Diverse mangroves deviate from other angiosperms in their genome size, leaf cell size, and cell packing density relationships.

  2022cites this paper
• Egg cell-secreted aspartic proteases ECS1/2 promote gamete attachment to prioritize the fertilization of egg cells over central cells in Arabidopsis.

  2022cites this paper
• Phylogenomics and genome size evolution in Amomum s. s. (Zingiberaceae): comparison of traditional and modern sequencing methods.

  2022cites this paper
• Linkages between stomatal density and minor leaf vein density across different altitudes and growth forms

  2022cites this paper
• The limiting effect of genome size on xylem vessel diameter is shifted by environmental pressures in seed plants

  2022influential citation
• The functional significance of the stomatal size to density relationship: Interaction with atmospheric [CO2] and role in plant physiological behaviour.

  2022cites this paper
• The ecological adaptation of the unparalleled plastome character evolution in slipper orchids

  2022cites this paper
• Gigantic Genomes Provide Empirical Tests of Transposable Element Dynamics Models

  2021cites this paper
• Genome Size and Labellum Epidermal Cell Size Are Evolutionarily Correlated With Floral Longevity in Paphiopedilum Species

  2021influential citation
• Putting vascular epiphytes on the traits map

  2021cites this paper
• The ecology of palm genomes: repeat‐associated genome size expansion is constrained by aridity

  2021cites this paper
• Spatiotemporal limitations in plant biology research.

  2021cites this paper
• The Angiosperm Terrestrial Revolution and the origins of modern biodiversity.

  2021influential citation
• Application‐based guidelines for best practices in plant flow cytometry

  2021cites this paper
• Contrasting Water Use, Stomatal Regulation, Embolism Resistance, and Drought Responses of Two Co-Occurring Mangroves

  2021cites this paper
• Reproductive innovations and pulsed rise in plant complexity

  2021cites this paper
• Changes in ploidy affect vascular allometry and hydraulic function in Mangifera indica trees.

  2021cites this paper
• Reintegrating Biology Through the Nexus of Energy, Information, and Matter.

  2021cites this paper
• The nature of intraspecific and interspecific genome size variation in taxonomically complex eyebrights

  2021cites this paper
• β-diversity in temperate grasslands is driven by stronger environmental filtering of plant species with large genomes.

  2021cites this paper
• Exploring environmental selection on genome size in angiosperms.

  2021cites this paper