On the cover

The root is an organ that is easily forgotten in the process of breeding because it is hidden underground. Beneath the ground, however, even the same crop species can have diversified root system architecture adapted to different soil environments (each image of soil monolith shows different abiotic stress such as flooding, drought, and phosphorus deficit). It will be necessary to better understand the interaction between genes involved in the root functions and the soil environment when we consider how to best utilize the root functions in the breeding of climate-resilient crops (This issue, p. 3–12).

(Y. Uga: National Agriculture and Food Research Organization)

Roots are essential organs for capturing water and nutrients from the soil. In particular, root system architecture (RSA) determines the extent of the region of the soil where water and nutrients can be gathered. As global climate change accelerates, it will be important to improve belowground plant parts, as well as aboveground ones, because roots are front-line organs in the response to abiotic stresses such as drought, flooding, and salinity stress. However, using conventional breeding based on phenotypic selection, it is difficult to select breeding lines possessing promising RSAs to adapted to abiotic stress because roots remain hidden underground. Therefore, new breeding strategies that do not require phenotypic selection are necessary. Recent advances in molecular biology and biotechnology can be applied to the design-oriented breeding of RSA without phenotypic selection. Here I summarize recent progress in RSA ideotypes as “design” and RSA-related gene resources as “materials” that will be needed in leveraging these technologies for the RSA breeding. I also highlight the future challenges to design-oriented breeding of RSA and explore solutions to these challenges.

Resource acquisition, one of the major functions of roots, can contribute to crop growth and mitigating environmental impacts. The spatio-temporal distribution of roots in the soil in relation to the dynamics of the soil resources is critical in resource acquisition. Root distribution is determined by root system development. The root system consists of many individual roots of different types and ages. Each individual root has specific development, resource acquisition, and transport traits, which change with root growth. The integration of individual root traits in the root system could exhibit crop performance in the various environments via root distribution in the soil. However, the relationship between individual root traits and the pattern of root distribution is complicated. To understand this complicated relationship, we need to evaluate enormous numbers of individual root traits and understand the relationship between individual root development and root distribution as well as the integrated functions of individual root traits along with dynamics of resources in the soil.

Different types of water stress severely affect crop production, and the plant root system plays a critical role in stress avoidance. In the case of rice, a cereal crop cultivated under the widest range of soil hydrologic conditions, from irrigated anaerobic conditions to rainfed conditions, phenotypic root plasticity is of particular relevance. Recently, important plastic root traits under different water stress conditions, and their physiological and molecular mechanisms have been gradually understood. In this review, we summarize these plastic root traits and their contributions to dry matter production through enhancement of water uptake under different water stress conditions. We also discuss the physiological and molecular mechanisms regulating the phenotypic plasticity of root systems.

Flooding stress caused by excessive precipitation and poor drainage threatens upland crop production and food sustainability, so new upland crop cultivars are needed with greater tolerance to soil flooding (waterlogging). So far, however, there have been no reports of highly flooding-tolerant upland crop cultivars, including maize, because of the lack of flooding-tolerant germplasm and the presence of a large number of traits affecting flooding tolerance. To achieve the goal of breeding flooding-tolerant maize cultivars by overcoming these difficulties, we chose highly flooding-tolerant teosinte germplasm. These flooding-tolerance-related traits were separately assessed by establishing a method for the accurate evaluation of each one, followed by performing quantitative trait locus (QTL) analyses for each trait using maize × teosinte mapping populations, developing introgression lines (ILs) or near-isogenic lines (NILs) containing QTLs and pyramiding useful traits. We have identified QTLs for flooding-tolerance-related root traits, including the capacity to form aerenchyma, formation of radial oxygen loss barriers, tolerance to flooded reducing soil conditions, flooding-induced adventitious root formation and shallow root angle. In addition, we have developed several ILs and NILs with flooding-tolerance-related QTLs and are currently developing pyramided lines. These lines should be valuable for practical maize breeding programs focused on flooding tolerance.

Internal aeration is crucial for root growth under waterlogged conditions. Many wetland plants have a structural barrier that impedes oxygen leakage from the basal part of roots called a radial oxygen loss (ROL) barrier. ROL barriers reduce the loss of oxygen transported via the aerenchyma to the root tips, enabling long-distance oxygen transport for cell respiration at the root tip. Because the root tip does not have an ROL barrier, some of the transferred oxygen is released into the waterlogged soil, where it oxidizes and detoxifies toxic substances (e.g., sulfate and Fe²⁺) around the root tip. ROL barriers are located at the outer part of roots (OPRs). Their main component is thought to be suberin. Suberin deposits may block the entry of potentially toxic compounds in highly reduced soils. The amount of ROL from the roots depends on the strength of the ROL barrier, the length of the roots, and environmental conditions, which causes spatiotemporal changes in the root system’s oxidization pattern. We summarize recent achievements in understanding how ROL barrier formation is regulated and discuss opportunities for breeding waterlogging-tolerant crops.

Plants require water, but a deficit or excess of water can negatively impact their growth and functioning. Soil flooding, in which root-zone is filled with excess water, restricts oxygen diffusion into the soil. Global climate change is increasing the risk of crop yield loss caused by flooding, and the development of flooding tolerant crops is urgently needed. Root anatomical traits are essential for plants to adapt to drought and flooding, as they determine the balance between the rates of water and oxygen transport. The stele contains xylem and the cortex contains aerenchyma (gas spaces), which respectively contribute to water uptake from the soil and oxygen supply to the roots; this implies that there is a trade-off between the ratio of cortex and stele sizes with respect to adaptation to drought or flooding. In this review, we analyze recent advances in the understanding of root anatomical traits that confer drought and/or flooding tolerance to plants and illustrate the trade-off between cortex and stele sizes. Moreover, we introduce the progress that has been made in modelling and fully automated analyses of root anatomical traits and discuss how key root anatomical traits can be used to improve crop tolerance to soil flooding.

As sessile organisms, plants rely on their roots for anchorage and uptake of water and nutrients. Plant root is an organ showing extensive morphological and metabolic plasticity in response to diverse environmental stimuli including nitrogen (N) and phosphorus (P) nutrition/stresses. N and P are two essential macronutrients serving as not only cell structural components but also local and systemic signals triggering root acclimatory responses. Here, we mainly focused on the current advances on root responses to N and P nutrition/stresses regarding transporters as well as long-distance mobile proteins and peptides, which largely represent local and systemic regulators, respectively. Moreover, we exemplified some of the potential pitfalls in experimental design, which has been routinely adopted for decades. These commonly accepted methods may help researchers gain fundamental mechanistic insights into plant intrinsic responses, yet the output might lack strong relevance to the real situation in the context of natural and agricultural ecosystems. On this basis, we further discuss the established—and yet to be validated—improvements in experimental design, aiming at interpreting the data obtained under laboratory conditions in a more practical view.

Genome-wide transcriptome profiling is a powerful tool for identifying key genes and pathways involved in plant development and physiological processes. This review summarizes studies that have used transcriptome profiling mainly in rice to focus on responses to macronutrients such as nitrogen, phosphorus and potassium, and spatio-temporal root profiling in relation to the regulation of root system architecture as well as nutrient uptake and transport. We also discuss strategies based on meta- and co-expression analyses with different attributed transcriptome data, which can be used for investigating the regulatory mechanisms and dynamics of nutritional responses and adaptation, and speculate on further advances in transcriptome profiling that could have potential application to crop breeding and cultivation.

Soil salinity is an increasing threat to the productivity of glycophytic crops worldwide. The root plays vital roles under various stress conditions, including salinity, as well as has diverse functions in non-stress soil environments. In this review, we focus on the essential functions of roots such as in ion homeostasis mediated by several different membrane transporters and signaling molecules under salinity stress and describe recent advances in the impacts of quantitative trait loci (QTLs) or genetic loci (and their causal genes, if applicable) on salinity tolerance. Furthermore, we introduce important literature for the development of barriers against the apoplastic flow of ions, including Na⁺, as well as for understanding the functions and components of the barrier structure under salinity stress.

As plants cannot relocate, they require effective root systems for water and nutrient uptake. Root development plasticity enables plants to adapt to different environmental conditions. Research on improvements in crop root systems is limited in comparison with that in shoots as the former are difficult to image. Breeding more effective root systems is proposed as the “second green revolution”. There are several recent publications on root system architecture (RSA), but the methods used to analyze the RSA have not been standardized. Here, we introduce traditional and current root-imaging methods and discuss root structure phenotyping. Some important root structures have not been standardized as roots are easily affected by rhizosphere conditions and exhibit greater plasticity than shoots; moreover, root morphology significantly varies even in the same genotype. For these reasons, it is difficult to define the ideal root systems for breeding. In this review, we introduce several types of software to analyze roots and identify important root parameters by modeling to simplify the root system characterization. These parameters can be extracted from photographs captured in the field. This modeling approach is applicable to various legacy root data stored in old or unpublished formats. Standardization of RSA data could help estimate root ideotypes.