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

SummaryDuring 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.

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A stomatal model of anatomical tradeoffs between gas exchange and pathogen colonization

10.1101/871228 ◽

2019 ◽

Author(s):

Christopher D. Muir

Keyword(s):

Gas Exchange ◽

Leaf Surface ◽

Stomatal Density ◽

Leaf Gas Exchange ◽

Stomatal Closure ◽

Exchange Capacity ◽

Pathogen Defense ◽

Stomatal Size ◽

Scaling Relationships ◽

Pathogen Colonization

ABSTRACTStomatal pores control both leaf gas exchange and are one route for infection of internal plant tissues by many foliar pathogens, setting up the potential for tradeoffs between photosynthesis and defense. Anatomical shifts to lower stomatal density and/or size may also limit pathogen colonization, but such developmental changes could permanently reduce the gas exchange capacity for the life of the leaf. I developed and analyzed a spatially explicit model of pathogen colonization on the leaf as a function of stomatal size and density, anatomical traits which partially determine maximum rates of gas exchange. The model predicts greater stomatal size or density increases the probability of colonization, but the effect is most pronounced when the fraction of leaf surface covered by stomata is low. I also derived scaling relationships between stomatal size and density that preserves a given probability of colonization. These scaling relationships set up a potential anatomical conflict between limiting pathogen colonization and minimizing the fraction of leaf surface covered by stomata. Although a connection between gas exchange and pathogen defense has been suggested empirically, this is the first mathematical model connecting gas exchange and pathogen defense via stomatal anatomy. A limitation of the model is that it does not include variation in innate immunity and stomatal closure in response to pathogens. Nevertheless, the model makes predictions that can be tested with experiments and may explain variation in stomatal anatomy among plants. The model is generalizable to many types of pathogens, but lacks significant biological realism that may be needed for precise predictions.

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Fossil evidence for low gas exchange capacities for Early Cretaceous angiosperm leaves

Paleobiology ◽

10.1666/10015.1 ◽

2011 ◽

Vol 37 (2) ◽

pp. 195-213 ◽

Cited By ~ 32

Author(s):

Taylor S. Feild ◽

Garland R. Upchurch ◽

David S. Chatelet ◽

Timothy J. Brodribb ◽

Kunsiri C. Grubbs ◽

...

Keyword(s):

Gas Exchange ◽

Early Cretaceous ◽

Leaf Gas Exchange ◽

Exchange Capacity ◽

Basal Angiosperm ◽

Photosynthetic Gas Exchange ◽

Angiosperm Evolution ◽

Early Angiosperm ◽

Fossil Evidence ◽

Functional Analyses

The photosynthetic gas exchange capacities of early angiosperms remain enigmatic. Nevertheless, many hypotheses about the causes of early angiosperm success and how angiosperms influenced Mesozoic ecosystem function hinge on understanding the maximum capacity for early angiosperm metabolism. We applied structure-functional analyses of leaf veins and stomatal pore geometry to determine the hydraulic and diffusive gas exchange capacities of Early Cretaceous fossil leaves. All of the late Aptian—early Albian angiosperms measured possessed low vein density and low maximal stomatal pore area, indicating low leaf gas exchange capacities in comparison to modern ecologically dominant angiosperms. Gas exchange capacities for Early Cretaceous angiosperms were equivalent or lower than ferns and gymnosperms. Fossil leaf taxa from Aptian to Paleocene sediments previously identified as putative stem-lineages to Austrobaileyales and Chloranthales had the same gas exchange capacities and possibly leaf water relations of their living relatives. Our results provide fossil evidence for the hypothesis that high leaf gas exchange capacity is a derived feature of later angiosperm evolution. In addition, the leaf gas exchange functions of austrobaileyoid and chloranthoid fossils support the hypothesis that comparative research on the biology of living basal angiosperm lineages reveals genuine signals of Early Cretaceous angiosperm ecophysiology.

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Flooding tolerance of Carex species. II. Root gas-exchange capacity

Planta ◽

10.1007/s004250050473 ◽

1998 ◽

Vol 207 (2) ◽

pp. 199-206 ◽

Cited By ~ 16

Author(s):

Petra R. Moog ◽

Wolfgang Brüggemann

Keyword(s):

Gas Exchange ◽

Exchange Capacity ◽

Flooding Tolerance

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Gas-Exchange Rates in a Small Lake as Determined by the Radon Method

Journal of the Fisheries Research Board of Canada ◽

10.1139/f73-237 ◽

1973 ◽

Vol 30 (10) ◽

pp. 1475-1484 ◽

Cited By ~ 36

Author(s):

Steve Emerson ◽

Wallace Broecker ◽

D. W. Schindler

Keyword(s):

Exchange Rate ◽

Gas Exchange ◽

Exchange Rates ◽

Partial Pressure ◽

Lake Water ◽

Radon Concentration ◽

Natural Waters ◽

Carbon Dioxide Partial Pressure ◽

Nitrogen And Phosphorus ◽

Gas Exchange Rate

The radon method, used previously in ocean-atmosphere systems, is used here to determine the gas-exchange rate between the atmosphere and lake 227 of the Experimental Lakes Area. Fertilization of the lake with nitrogen and phosphorus caused the carbon dioxide partial pressure in the lake water to drop well below atmospheric levels; hence, in order to better understand the carbon budget of the lake, an estimate of the CO2 gas-exchange rate was necessary.To determine gas-exchange rates by measuring radon evasion to the atmosphere the source of radon in the lake water must be dissolved radium. Since the radon concentration in lakes derives not only from the decay of dissolved radium but also from the inflow of radon-rich groundwaters, radium was added to the lake to increase the radon concentration well above this fluctuating background level. Although this procedure was complicated by algal uptake of the radium in the lake (Emerson and Hesslein 1973), we were able to place limits on the gas-exchange rate.Our results indicate that the "stagnant boundary layer" thickness is approximately 300 μ. This value is among the largest observed in natural waters. Using this value and the partial pressure of CO2 in the lake water we have calculated an invasion rate of 17 ± 8 mmoles CO2/m2 day.

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