Genotypic variation and nitrogen stress effects on root anatomy in maize are node specific

Abstract

Root phenotypes that improve nitrogen acquisition are avenues for crop improvement. Root anatomy affects resource capture, metabolic cost, hydraulic conductance, anchorage, and soil penetration. Cereal root phenotyping has centered on primary, seminal, and early nodal roots, yet critical nitrogen uptake occurs when the nodal root system is well developed. This study examined root anatomy across nodes in field-grown maize (Zea mays L.) hybrid and inbred lines under high and low nitrogen regimes. Genotypes with high nitrogen use efficiency (NUE) had larger root diameter and less cortical aerenchyma across nodes under stress than genotypes with lower NUE. Anatomical phenes displayed slightly hyperallometric relationships to shoot biomass. Anatomical plasticity varied across genotypes; most genotypes decreased root diameter under stress when averaged across nodes. Cortex, stele, total metaxylem vessel areas, and cortical cell file and metaxylem vessel numbers scaled strongly with root diameter across nodes. Within nodes, metaxylem vessel size and cortical cell size were correlated, and root anatomical phenotypes in the first and second nodes were not representative of subsequent nodes. Node, genotype, and nitrogen treatment affect root anatomy. Understanding nodal variation in root phenes will enable the development of plants that are adapted to low nitrogen conditions.

Keywords: Axial root anatomy; genotypic variation; maize (Zea mays L.); nitrogen use efficiency; node; phenotyping; plasticity.

Fig. 1.

Nodal variation in maize root anatomy. Nodal root cross-section images from high N field-grown maize hybrids, sampled from older to younger nodes (left to right, numbered) from two genotypes (row A, B). Scale applies to all images.

Fig. 2.

Principal component analysis of root anatomy phenes. Biplot of the first two principal components (PC 1, 2) of a principal component analysis on 11 root anatomy phenes. Points indicate scores of individual roots on these two components, from nodes 1 to 5 (by color, and outlined by convex hull) of field-grown maize inbred lines and hybrids (PA14, PA15, PA16, total n=1171) in high and low nitrogen treatments (by shape). Arrows represent loadings of root anatomy phenes (labeled) on these two components. See Table 1 for phene abbreviations. PC1 and PC2 explained 66.7% and 9.7% of total variance, respectively.

Fig. 3.

Root anatomy variation by node in field-grown maize hybrids. Boxplots of nodal root anatomy phenes evaluated in nodes 1 (oldest) through 5 (left to right in each plot) from 44 field-grown maize hybrid genotypes, including high and low nitrogen treatments (PA16). Horizontal box lines indicate the 25th, 50th, and 75th percentile; whiskers indicate range, excluding outliers (points). Total n=469 per plot. See Table 1 for phene abbreviations.

Fig. 4.

Maize root anatomy phene relationships across nodes. Correlation matrix of root anatomy phenes evaluated in nodes 2, 3, and 4 (numbered) in n=69 mean phene values per node from low nitrogen field-grown maize hybrids (PA16). Color scale indicates Spearman’s ranked correlation coefficient. Larger circle size reflects smaller P-value; blank cells indicate that correlation was not significant at P<0.05. Most strongly related phenes are ordered and grouped in black boxes according to hierarchical clustering. See Table 1 for phene abbreviations.

Fig. 5.

Genotypic variation in plasticity of total metaxylem vessel area (mm²) under low nitrogen. Mean ±SE metaxylem vessel area (mm²) across nodes 2, 3, and 4 under high or low nitrogen (HN, blue; LN, red) for select maize hybrid genotypes (see Supplementary Table S1 for genotype codes). Asterisks represent genotypes with significant differences (P<0.05) between nitrogen treatments according to a pairwise comparison of phene values matched by node.

Fig. 6.

Anatomical differences among HNUE and LNUE genotypes. Genotypes were matched based on high N yield and then grouped according to high or low N use efficiency (HNUE, black; LNUE, gray) based on low N yield. For PA16, 22 hybrid genotypes were included in each group; for PA15, four inbred genotypes were in each group. Genotypes with variable performance were excluded. Means ±SE of yield and select anatomical phenes under high and low N (HN, LN) conditions are plotted; phenes are averaged across nodes 2, 3, and 4 for PA16, and nodes 1, 2, and 3 for PA15. See Table 1 for phene abbreviations and units.

Fig. 7.

Node-specific root anatomy responses to nitrogen stress. Root phene means ±SE by node (x-axis) and nitrogen treatment (blue, HN; red, LN) in field-grown maize genotypes (PA16). Total n=469 roots per plot. See Table 1 for phene abbreviations and units. Percentage changes under LN by node are given in Supplementary Table S5.