Temperature responses of root carbon use efficiency are linked to cortical cell expansion

Plant roots are essential for water and nutrient acquisition and constitute a major source of organic matter input to soil, underscoring their significance in global change adaptation and mitigation. Thereby, the partitioning of carbon between biomass formation and respiration in growing roots plays a decisive role for root foraging efficiency and carbon retention in the plant-soil system. Here, we elucidated structural-functional relationships between root growth physiology and root anatomy in rice (Oryza sativa L.) to uncover the hitherto unknown mechanisms regulating root carbon partitioning in response to warming. High-resolution X-ray computed tomography (1.8 μm) revealed nonlinear temperature responses in cortical cell volume of primary roots, which peaked at ∼28 °C and decreased at lower and higher temperatures. Similar nonlinearities occurred for root carbon partitioning during the first 4 d of growth following primary root emergence. At low and high temperatures, carbon allocation shifted from root biomass formation toward respiration. Compared with an ABA biosynthesis mutant (Osaba2-1), the wild type showed >40% greater temperature sensitivity in both cortical cell volume and carbon partitioning. Genotypic dose-response curves and structural-functional relationships between root cortical cell volume and carbon partitioning (R2 = 0.50) provided evidence that the ability to maintain cortical cell expansion under temperature stress increases carbon allocation to biomass formation over respiration. Thus, our study highlights the pivotal importance of fundamental root physiological processes in shaping the impacts of global warming on carbon fluxes in plant-soil systems that underpin plant growth, productivity, and terrestrial carbon cycling.