Cost-Benefit Analysis of the Upland-Rice Root Architecture in Relation to Phosphate: 3D Simulations Highlight the Importance of S-Type Lateral Roots for Reducing the Pay-Off Time

Abstract

The rice root system develops a large number of nodal roots from which two types of lateral roots branch out, large L-types and fine S-types, the latter being unique to the species. All roots including S-types are covered by root hairs. To what extent these fine structures contribute to phosphate (P) uptake under P deficiency was investigated using a novel 3-D root growth model that treats root hairs as individual structures with their own Michaelis-Menten uptake kinetics. Model simulations indicated that nodal roots contribute most to P uptake followed by L-type lateral roots and S-type laterals and root hairs. This is due to the much larger root surface area of thicker nodal roots. This thickness, however, also meant that the investment in terms of P needed for producing nodal roots was very large. Simulations relating P costs and time needed to recover that cost through P uptake suggest that producing nodal roots represents a considerable burden to a P-starved plant, with more than 20 times longer pay-off time compared to S-type laterals and root hairs. We estimated that the P cost of these fine root structures is low enough to be recovered within a day of their formation. These results expose a dilemma in terms of optimizing root system architecture to overcome P deficiency: P uptake could be maximized by developing more nodal root tissue, but when P is growth-limiting, adding more nodal root tissue represents an inefficient use of the limiting factor P. In order to improve adaption to P deficiency in rice breeding two complementary strategies seem to exist: (1) decreasing the cost or pay-off time of nodal roots and (2) increase the biomass allocation to S-type roots and root hairs. To what extent genotypic variation exists within the rice gene pool for either strategy should be investigated.

TopoRoot: a method for computing hierarchy and fine-grained traits of maize roots from 3D imaging

“…To validate other fine-grained traits produced by our method, we supplement the CT data set with a large benchmark of synthetically generated root images. We adopt OpenSimRoot [ 19 ], a highly customizable 3D root growth simulation software that has been widely used in modeling and visualizing root growth [ 27 , 28 ]. We used OpenSimRoot to create 55 maize root systems ranging in days of growth from 30 to 40 days, numbers of nodal roots ranging from 31 to 69, number of whorls from 5 to 6, and lateral root branching frequency from 0.3 to 0.7 cm / branch.…”

Rice increases phosphorus uptake in strongly sorbing soils by intra‐root facilitation

“…Treating S-type laterals independent of parent roots reduced their contribution to total P-uptake from 30% to 11% (Figure S3). Likewise, using a model that did not explicitly allow for solubilization, Gonzalez et al (2021) found that S-types contributed little to total P-uptake by the root system. Nonetheless, they showed that the low P cost of forming S-type laterals can be recovered by their P uptake within a day, much faster than other root types.…”

“…The crown and lateral roots, including the fine S‐types, produce hairs. Recent 3D modelling, allowing for soil transport, uptake limitations, S‐type lateral roots, and hairs, shows that the P cost of those fine laterals is recovered within a day of their formation (Gonzalez et al, 2021). They are therefore efficient in the use of P.…”

“…The sink strength is modelled as a function of P concentration in solution at the root surface and the activity of P uptake transporters in the root membrane. Such models greatly under‐predict P uptake by upland rice grown in strongly P‐sorbing soils, both when root architecture is (De Bauw et al, 2020; Gonzalez et al, 2021) and is not considered (Kirk et al, 1999). In strongly sorbing soils, P concentrations in the soil solution can be so low that even high‐affinity transporters may still be slow in taking it up.…”

TopoRoot: A method for computing hierarchy and fine-grained traits of maize roots from X-ray CT images

“…To validate other fine-grained traits produced by our method, we supplement the real data set with a systematically created set of simulated root images. We adopt OpenSimRoot [24], a highly customizable 3D root growth simulation software that has been widely used in modeling and visualizing root growth [11,31,7]. We used OpenSimRoot to create 55 maize roots ranging in days of growth from 30 to 40 days, numbers of nodal roots ranging from 31 to 69, number of whorls from 5 to 6, and lateral root branching frequency from 0.3 to 0.7 cm / branch.…”