Evolutionary patterns and biogeochemical significance of angiosperm root traits

Authors: Comas, Louise; MUELLER, K - University Of Minnesota; TAYLOR, L - University Of Sheffield; MIFORD, P - Duke University; CALLAHAN, H - Columbia University - New York; BEERLING, D - University Of Sheffield

Submitted to: International Journal of Plant Science
Publication Type: Review Article
Publication Acceptance Date: 2/14/2012
Publication Date: 7/31/2012
Citation: Comas, L.H., Mueller, K.E., Taylor, L.L., Miford, P.E., Callahan, H., Beerling, D.J. 2012. Evolutionary patterns and biogeochemical significance of angiosperm root traits. International Journal of Plant Science. pp. 584-595.

Interpretive Summary: Plant roots traits and their associations with fungi are intimately tied to soil development and chemistry. We examined root trait patterns and fungal associations among modern plants that evolved between 65-145 million years ago. Our analyses showed that during this period, plants evolved thinner roots with greater length per invested biomass. The evolution of root traits corresponded to a decline in atmospheric CO2 concentration, water, and readily-available soil nutrients. Root morphology of thinner diameter and greater length per biomass allows plants to produce a larger root system and acquire more water and nutrients. Plants during this period also evolved new associations with different types of fungi to acquire nutrients. Our modeling of soil processes indicated that both the density of roots in soil, and the amount and type of root colonization by fungi stimulates mineral weathering, which also increases plant-available nutrients. Thus, our results suggest that plant water and nutrient requirements together have shaped the evolution of plant growth strategies with important consequences for the functioning of ecosystems.

Technical Abstract: Based on a synthesis of recent progress in belowground ecology, we advance and discuss a hypothesis that relates root trait evolution to the increased dominance of angiosperms into dry upland habitats and the decline of atmospheric CO2 concentration that began in the Cretaceous. Our hypothesis is built from examining patterns of fine root adaptations during the Cretaceous, when angiosperms dramatically diversified in association with arbuscular and ectomycorrhizal root-fungal symbionts. We then explore the potential effects of root adaptations and mycorrhizas on the geochemical carbon cycle. Based on phylogenetic analyses of root traits among extant plant species, we suggest angiosperm taxa, which diversified since the early Cretaceous, evolved thinner roots with greater root length per unit of biomass invested (i.e. specific root length, SRL) than earlier diverging taxa. We suggest that these changes in root morphology were facilitated by a decline in atmospheric CO2, which likely caused water to become more limiting and nutrients more bound to organic matter. Under these conditions, we suggest that thin roots with long SRL would have allowed plants to more efficiently forage for soil water and nutrients. This assertion is supported by the observation that SRL correlates with greater root length density in soil and increased root capacity to take up water. Simulations indicate that the evolution of angiosperm root systems with greater SRL and ectomycorrhizas during the Cretaceous and Cenozoic substantially increased mineral weathering rates with a four-fold increase in SRL equivalent to a quadrupling of atmospheric CO2 concentration. The hypothesis presented here raises the possibility that plant hydraulic status and nutrient balance together shaped whole plant growth strategies with important consequences for the evolution of the biosphere.