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Evolutionary Patterns and Biogeochemical Significance of Angiosperm Root Traits

On the basis of 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. On the basis of phylogenetic analyses of root traits among extant plant species, we suggest that 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 fourfold 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.