Background Suboptimal water and nutrient availability are primary constraints in global agriculture. Root anatomy plays key roles in soil resource acquisition. In this article we summarize evidence that root anatomical phenotypes present opportunities for crop breeding. Scope Root anatomical phenotypes influence soil resource acquisition by regulating the metabolic cost of soil exploration, exploitation of the rhizosphere, the penetration of hard soil domains, the axial and radial transport of water, and interactions with soil biota including mycorrhizal fungi, pathogens, insects, and the rhizosphere microbiome. For each of these topics we provide examples of anatomical phenotypes which merit attention as selection targets for crop improvement. Several cross-cutting issues are addressed including the importance of phenotypic plasticity, integrated phenotypes, C sequestration, in silico modeling, and novel methods to phenotype root anatomy including image analysis tools. Conclusions An array of anatomical phenes have substantial importance for the acquisition of water and nutrients. Substantial phenotypic variation exists in crop germplasm. New tools and methods are making it easier to phenotype root anatomy, determine its genetic control, and understand its utility for plant fitness. Root anatomical phenotypes are underutilized yet attractive breeding targets for the development of the efficient, resilient crops urgently needed in global agriculture.

HighlightComprehensive analysis of maize root phenotypes over the past century indicates that they have evolved to be more efficient in acquiring nitrogen.

Root phenes and phene states that reduce the metabolic cost of soil exploration may improve plant growth under low phosphorus availability. We tested the hypothesis that under low phosphorus, reduced living cortical area (LCA) would increase soil exploration, phosphorus capture, biomass, and grain yield. Maize genotypes contrasting in LCA were grown in the field and in greenhouse mesocosms under optimal and suboptimal phosphorus regimes. Percent LCA in nodal roots ranged from 25% to 67%. Plants with 0.2 mm less LCA under low phosphorus had 75% less root segment respiration, 54% less root phosphorus content, rooted 20 cm deeper, allocated up to four times more roots between 60 and 120 cm depth, had between 20% and 150% more biomass, 35-40% greater leaf phosphorus content, and 60% greater grain yield compared with plants with high LCA. Low-LCA plants had up to 55% less arbuscular mycorrhizal colonization in axial roots, but this decrease was not correlated with biomass or phosphorus content. The LCA components cortical cell file number and cortical cell size were important for biomass and phosphorus content under low phosphorus. These results are consistent with the hypothesis that root phenes that decrease the metabolic cost of soil exploration are adaptive under phosphorus stress.

Soil biota have important effects on crop productivity, but can be difficult to study in situ. Laser ablation tomography (LAT) is a novel method that allows for rapid, three-dimensional quantitative and qualitative analysis of root anatomy, providing new opportunities to investigate interactions between roots and edaphic organisms. LAT was used for analysis of maize roots colonized by arbuscular mycorrhizal fungi, maize roots herbivorized by western corn rootworm, barley roots parasitized by cereal cyst nematode, and common bean roots damaged by Fusarium. UV excitation of root tissues affected by edaphic organisms resulted in differential autofluorescence emission, facilitating the classification of tissues and anatomical features. Samples were spatially resolved in three dimensions, enabling quantification of the volume and distribution of fungal colonization, western corn rootworm damage, nematode feeding sites, tissue compromised by Fusarium, and as well as root anatomical phenotypes. Owing to its capability for high-throughput sample imaging, LAT serves as an excellent tool to conduct large, quantitative screens to characterize genetic control of root anatomy and interactions with edaphic organisms. Additionally, this technology improves interpretation of root–organism interactions in relatively large, opaque root segments, providing opportunities for novel research investigating the effects of root anatomical phenes on associations with edaphic organisms.

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