Location: root architecture structures rhizosphere microbial associations.

Root architectural phenotypes are promising targets for crop breeding, but root architectural effects on microbial associations in agricultural fields are not well understood. Architecture determines the location of microbial associations within root systems, which, when integrated with soil vertical gradients, determines the functions and the metabolic capability of rhizosphere microbial communities. We argue that variation in root architecture in crops has important implications for root exudation, microbial recruitment and function, and the decomposition and fate of root tissues and exudates. Recent research has shown that the root microbiome changes along root axes and among root classes, that root tips have a unique microbiome, and that root exudates change within the root system depending on soil physicochemical conditions. Although fresh exudates are produced in larger amounts in root tips, the rhizosphere of mature root segments also plays a role in influencing soil vertical gradients. We argue that more research is needed to understand specific root phenotypes that structure microbial associations and discuss candidate root phenotypes that may determine the location of microbial hotspots within root systems with relevance to agricultural systems.

Root cortical anatomy is associated with differential pathogenic and symbiotic fungal colonization in maize.

Root anatomical phenotypes vary among maize (Zea mays) cultivars and may have adaptive value by modifying the metabolic cost of soil exploration. However, the microbial trade-offs of these phenotypes are unknown. We hypothesized that nodal roots of maize with contrasting cortical anatomy have different patterns of mutualistic and pathogenic fungal colonization. Arbuscular mycorrhizal colonization in the field and mesocosms, root rots in the field, and Fusarium verticillioides colonization in mesocosms were evaluated in maize genotypes with contrasting root cortical anatomy. Increased aerenchyma and decreased living cortical area were associated with decreased mycorrhizal colonization in mesocosm and field experiments with inbred genotypes. In contrast, mycorrhizal colonization of hybrids increased with larger aerenchyma lacunae; this increase coincided with larger root diameters of hybrid roots. F. verticillioides colonization was inversely correlated with living cortical area in mesocosm-grown inbreds, and no relation was found between root rots and living cortical area or aerenchyma in field-grown hybrids. Root rots were positively correlated with cortical cell file number and inversely correlated with cortical cell size. Mycorrhizae and root rots were inversely correlated in field-grown hybrids. We conclude that root anatomy is associated with differential effects on pathogens and mycorrhizal colonization of nodal roots in maize.

Laser ablation tomography for visualization of root colonization by edaphic organisms.

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.

Reduced root cortical burden improves growth and grain yield under low phosphorus availability in maize.

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 mm2 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.

Evolution of US maize (Zea mays L.) root architectural and anatomical phenes over the past 100 years corresponds to increased tolerance of nitrogen stress.

Increasing the nitrogen use efficiency of maize is an important goal for food security and agricultural sustainability. In the past 100 years, maize breeding has focused on yield and above-ground phenes. Over this period, maize cultivation has changed from low fertilizer inputs and low population densities to intensive fertilization and dense populations. The authors hypothesized that through indirect selection the maize root system has evolved phenotypes suited to more intense competition for nitrogen. Sixteen maize varieties representing commercially successful lines over the past century were planted at two nitrogen levels and three planting densities. Root systems of the most recent material were 7 º more shallow, had one less nodal root per whorl, had double the distance from nodal root emergence to lateral branching, and had 14% more metaxylem vessels, but total mextaxylem vessel area remained unchanged because individual metaxylem vessels had 12% less area. Plasticity was also observed in cortical phenes such as aerenchyma, which increased at greater population densities. Simulation modelling with SimRoot demonstrated that even these relatively small changes in root architecture and anatomy could increase maize shoot growth by 16% in a high density and high nitrogen environment. The authors concluded that evolution of maize root phenotypes over the past century is consistent with increasing nitrogen use efficiency. Introgression of more contrasting root phene states into the germplasm of elite maize and determination of the functional utility of these phene states in multiple agronomic conditions could contribute to future yield gains.

Microbial Community-Level Physiological Profiles and Genetic Prokaryotic Structure of Burned Soils Under Mediterranean Sclerophyll Forests in Central Chile.

Forest fires alter soil microbial communities that are essential to support ecosystem recovery following land burning. These alterations have different responses according to soil abiotic pre- and post-fire conditions and fire severity, among others, and tend to decrease along vegetation recovery over time. Thus, understanding the effects of fires on microbial soil communities is critical to evaluate ecosystem resilience and restoration strategies in fire-prone ecosystems. We studied the state of community-level physiological profiles (CLPPs) and the prokaryotic community structure of rhizosphere and bulk soils from two fire-affected sclerophyll forests (one surveyed 17 months and the other 33 months after fire occurrence) in the Mediterranean climate zone of central Chile. Increases in catabolic activity (by average well color development of CLPPs), especially in the rhizosphere as compared with the bulk soil, were observed in the most recently affected site only. Legacy of land burning was still clearly shaping soil prokaryote community structure, as shown by quantitative PCR (qPCR) and Illumina MiSeq sequencing of the V4 region of the 16S rRNA gene, particularly in the most recent fire-affected site. The qPCR copy numbers and alpha diversity indexes (Shannon and Pielou's evenness) of sequencing data decreased in burned soils at both locations. Beta diversity analyses showed dissimilarity of prokaryote communities at both study sites according to fire occurrence, and NO3 - was the common variable explaining community changes for both of them. Acidobacteria and Rokubacteria phyla significantly decreased in burned soils at both locations, while Firmicutes and Actinobacteria increased. These findings provide a better understanding of the resilience of soil prokaryote communities and their physiological conditions in Mediterranean forests of central Chile following different time periods after fire, conditions that likely influence the ecological processes taking place during recovery of fire-affected ecosystems.

Improving Soil Resource Uptake by Plants Through Capitalizing on Synergies Between Root Architecture and Anatomy and Root-Associated Microorganisms.

Root architectural and anatomical phenotypes are highly diverse. Specific root phenotypes can be associated with better plant growth under low nutrient and water availability. Therefore, root ideotypes have been proposed as breeding targets for more stress-resilient and resource-efficient crops. For example, root phenotypes that correspond to the Topsoil Foraging ideotype are associated with better plant growth under suboptimal phosphorus availability, and root phenotypes that correspond to the Steep, Cheap and Deep ideotype are linked to better performance under suboptimal availability of nitrogen and water. We propose that natural variation in root phenotypes translates into a diversity of different niches for microbial associations in the rhizosphere, rhizoplane and root cortex, and that microbial traits could have synergistic effects with the beneficial effect of specific root phenotypes. Oxygen and water content, carbon rhizodeposition, nutrient availability, and root surface area are all factors that are modified by root anatomy and architecture and determine the structure and function of the associated microbial communities. Recent research results indicate that root characteristics that may modify microbial communities associated with maize include aerenchyma, rooting angle, root hairs, and lateral root branching density. Therefore, the selection of root phenotypes linked to better plant growth under specific edaphic conditions should be accompanied by investigating and selecting microbial partners better adapted to each set of conditions created by the corresponding root phenotype. Microbial traits such as nitrogen transformation, phosphorus solubilization, and water retention could have synergistic effects when correctly matched with promising plant root ideotypes for improved nutrient and water capture. We propose that elucidation of the interactive effects of root phenotypes and microbial functions on plant nutrient and water uptake offers new opportunities to increase crop yields and agroecosystem sustainability.