Cortical cell size regulates root metabolic cost

Abstract It has been hypothesized that vacuolar occupancy in mature root cortical parenchyma cells regulates root metabolic cost and thereby plant fitness under conditions of drought, suboptimal nutrient availability, and soil mechanical impedance. However, the mechanistic role of vacuoles in reducing root metabolic cost was unproven. Here we provide evidence to support this hypothesis. We first show that root cortical cell size is determined by both cortical cell diameter (CCD) and cell length (CCL). Significant genotypic variation for both CCD (∼1.1 to 1.5- fold) and CCL (∼ 1.3 to 7-fold) was observed in maize and wheat. GWAS and QTL analyses indicate CCD and CCL are heritable and under independent genetic control. We identify candidate genes for both phenes. Empirical results from isophenic lines contrasting for CCD and CCL show that increased cell size, due to either CCD or CCL, is associated with reduced root respiration, root nitrogen content, and root phosphorus content. RootSlice , a functional-structural model of root anatomy, predicts that an increased ratio of vacuolar to cytoplasmic volume causes reduced root respiration and tissue nutrient content. Ultrastructural imaging of cortical parenchyma cells with varying CCD and CCL confirms the in-silico predictions and shows that an increase in cell size is correlated with increased vacuolar volume and reduced cytoplasmic volume. Phylogenetic analysis of terrestrial plants reveals that CCD has not significantly changed throughout plant evolution. Vacuolar occupancy and its relationship with CCD/CCL merits further investigation as a phene for improving crop adaptation to edaphic stress. Significance Statement Cortical cell size is an important phene determining root metabolic cost, but the underlying physiological mechanism is unclear. Here, using in silico and empirical approaches, we provide evidence that supports the hypothesis that vacuolar occupancy in cortical parenchyma cells regulates root metabolic cost. We also show that vacuolar occupancy is associated with cortical cell diameter and cell length, phenes that are under distinct genetic control and hold the potential for improving crop yields under edaphic stress.