Cortical parenchyma wall width (CPW) regulates root metabolic cost and maize performance under suboptimal water availability

Abstract

We describe how increased root cortical parenchyma wall width (CPW) can improve tolerance to drought stress in maize by reducing the metabolic costs of soil exploration. Significant variation (1.0 to 5.0 {micro}m) for CPW was observed within maize germplasm. The functional-structural model RootSlice predicts that increasing CPW from 2 to 4 {micro}m is associated with ca. 15% reduction in root cortical cytoplasmic volume, respiration rate, and nitrogen content. Analysis of genotypes with contrasting CPW grown with and without water stress in the field confirms that increased CPW is correlated with ca. 32 to 42% decrease in root respiration. Under water stress in the field, increased CPW is correlated with 125% increased stomatal conductance, 325% increased leaf CO2 assimilation rate, 73 to 78% increased shoot biomass, and 92 to 108% increased grain yield. CPW was correlated with leaf mesophyll midrib parenchyma wall width, indicating pleiotropy. GWAS analysis identified candidate genes underlying CPW. OpenSimRoot modeling predicts that a reduction in root respiration due to increased CPW would also benefit maize growth under suboptimal nitrogen, which requires empirical testing. We propose CPW as a new phene that has utility under edaphic stress meriting further investigation. Significance StatementSuboptimal water availability is a primary constraint for global crop production that is intensifying due to climate change. The metabolic cost of soil exploration is a critical factor in plant performance under suboptimal water availability. This study highlights how increased root cortical parenchyma wall width (CPW) reduces root metabolic cost and improves crop adaptation to water deficit. Modeling results also indicate that increased CPW would be beneficial under suboptimal nitrogen availability. Therefore, CPW is a promising target for breeding crops with improved water and nitrogen use efficiency.