Large root cortical cells and reduced cortical cell files improve growth under suboptimal nitrogen in silico

Abstract

Suboptimal nitrogen availability is a primary constraint to plant growth. We used OpenSimRoot, a functional-structural plant/soil model, to test the hypothesis that larger root cortical cell size (CCS), reduced cortical cell file number (CCFN), and their interactions with root cortical aerenchyma (RCA) and lateral root branching density (LRBD) are useful adaptations to suboptimal soil nitrogen availability in maize (Zea mays). Reduced CCFN increased shoot dry weight over 80%. Reduced respiration, reduced nitrogen content, and reduced root diameter accounted for 23%, 20%, and 33% of increased shoot biomass, respectively. Large CCS increased shoot biomass by 24% compared with small CCS. When simulated independently, reduced respiration and reduced nutrient content increased the shoot biomass by 14% and 3%, respectively. However, increased root diameter resulting from large CCS decreased shoot biomass by 4% due to an increase in root metabolic cost. Under moderate N stress, integrated phenotypes with reduced CCFN, large CCS, and high RCA improved shoot biomass in silt loam and loamy sand soils. In contrast, integrated phenotypes composed of reduced CCFN, large CCS, and reduced LRBD had the greatest growth in silt loam, while phenotypes with reduced CCFN, large CCS, and high LRBD were the best performers in loamy sands. Our results support the hypothesis that larger CCS, reduced CCFN, and their interactions with RCA and LRBD could increase nitrogen acquisition by reducing root respiration and root nutrient demand. Phene synergisms may exist between CCS, CCFN, and LRBD. CCS and CCFN merit consideration for breeding cereal crops with improved nitrogen acquisition, which is critical for global food security.

Figure 1.

Interaction of root anatomical phenotypes, root growth, and soil nitrogen availability. The visualized output of the simulated root architecture of A) reduced CCFN, increased CCFN, B) Large CCS, and small CCS under moderate N stress. The continuous gradient in the simulated soil represents nitrogen depletion by root uptake and leaching.

Figure 2.

Relative benefit of respiration, nitrogen content, and root diameter of reduced CCFN and large CCS phenotypes. The x axis shows the performance of the simulated plants under varying levels of nitrogen stress, where 100% is the absence of stress. The y axis shows the benefit in shoot dry weight and root length relative to the reference phenotypes (increased CCFN and small CCS, respectively). “Total” represents the combined effect of respiration, nutrient content, and root diameter. “Transphenic” represents the large CCS phenotype using the root diameter of small CCS.

Figure 3.

Sensitivity analysis of phenotypic variation for cortical cell file number and cortical cell size under low-, medium-, and high-nitrogen stress and the effect on shoot dry weight (SDW). Low, medium, and high stress corresponds to an average of 25%, 50%, and 75% shoot biomass reduction compared with a nonstressed plant, respectively.

Figure 4.

Effect of the interaction between CCFN, CCS, and RCA on shoot dry weight (SDW) under suboptimal nitrogen availability in silt loam and loamy sand soils. The scale bar shows different values for shoot dry weight. Aerenchyma levels correspond to 10%, 20%, and 30% for low, medium, and high, respectively).

Figure 5.

Effect of the interaction between LRBD, CCFN, and CCS on shoot dry weight (SDW) under suboptimal nitrogen availability in silt loam and loamy soils.