Root plasticity versus elasticity - when are responses acclimative?

Spatiotemporal soil heterogeneity and the resulting edaphic stress cycles can be decisive for crop growth. However, our understanding of the acclimative value of root responses to heterogeneous soil conditions remains limited. We outline a framework to evaluate the acclimative value of root responses that distinguishes between stress responses that are persistent and reversible upon stress release, termed 'plasticity' and 'elasticity', respectively. Using energy balances, we provide theoretical evidence that the advantage of plasticity over elasticity increases with the number of edaphic stress cycles and if responses lead to comparatively high energy gains. Our framework provides a conceptual basis for assessing the acclimative value of root responses to soil heterogeneity and can catalyse research on crop adaptations to heterogeneous belowground environments.

Genotypic differences in systemic root responses to mechanical obstacles.

As roots grow through the soil to forage for water and nutrients, they encounter mechanical obstacles such as patches of dense soil and stones that locally impede root growth. Here, we investigated hitherto poorly understood systemic responses of roots to localised root impedance. Seedlings of two wheat genotypes were grown in hydroponics and exposed to impenetrable obstacles constraining the vertical growth of the primary or a single seminal root. We deployed high-resolution in vivo imaging to quantify temporal dynamics of root elongation rate, helical root movement, and root growth direction. The two genotypes exhibited distinctly different patterns of systemic responses to localised root impedance, suggesting different strategies to cope with obstacles, namely stress avoidance and stress tolerance. Shallower growth of unconstrained seminal roots and more pronounced helical movement of unconstrained primary and seminal roots upon localised root impedance characterised the avoidance strategy shown by one genotype. Stress tolerance to localised root impedance, as exhibited by the other genotype, was indicated by relatively fast elongation of primary roots and steeper seminal root growth. These different strategies highlight that the effects of mechanical obstacles on spatiotemporal root growth patterns can differ within species, which may have major implications for resource acquisition and whole-plant growth.

Effects of soil compaction on grain yield of wheat depend on weather conditions.

The use of heavy farm machinery has resulted in widespread soil compaction in many regions of the world. Compacted soil limits the access of crops to soil water and nutrients and is expected to reduce crop productivity, but the influence of weather conditions on the interactions between compacted soil and crop productivity is unclear. Furthermore, early vigor has been regarded as a promising trait for improving the yield of crops grown under edaphic stress such as soil compaction. We aimed to assess the combined effects of soil compaction and contrasting weather conditions on growth and grain yield of spring wheat, and to evaluate the association between early vigor and grain yield under temporal variations of the soil physical conditions. Nine spring wheat genotypes were grown on compacted and non-compacted soils during two cropping seasons with contrasting weather conditions in Central Sweden. Compared to the non-compacted treatment, soil compaction increased the relative growth rate of shoot biomass from sowing to stem elongation, and from stem elongation to flowering in the drier year (2018), but decreased the same traits in the wetter year (2019). The contrasting effects of soil compaction on shoot growth in the two years could be explained by soil moisture and penetration resistance associated with the interactive effects of soil compaction and weather condition. Higher early vigor, here indicated by higher relative growth rate from sowing to stem elongation, was associated with reduced grain yield under the progressively drying and hardening soil conditions during the entire cropping season of both years. We conclude that the interactive effects of soil physical and weather conditions need to be considered when evaluating the impact of soil compaction on crop growth and productivity. The potential of early vigor to increase grain yield is strongly influenced by the temporal dynamics of soil physical conditions.

Evidence for magnesium-phosphorus synergism and co-limitation of grain yield in wheat agriculture.

Modern crop production is characterized by high nitrogen (N) application rates, which can influence the co-limitation of harvested yield by other nutrients. Using a multidimensional niche volume concept and scaling exponents frequently applied in plant ecological research, we report that increased N and phosphorus (P) uptake in a growing wheat crop along with enhanced grain biomass is associated with more than proportional increase of other nutrients. Furthermore, N conversion efficiency and grain yield are strongly affected by the magnesium (Mg) to P ratio in the growing crop. We analyzed a field trial in Central Sweden including nine wheat varieties grown during two years with contrasting weather, and found evidence for Mg co-limitation at lower grain yields and P co-limitation at higher yields. We argue that critical concentrations of single nutrients, which are often applied in agronomy, should be replaced by nutrient ratios. In addition, links between plant P and Mg contents and root traits were found; high root number enhanced the P:N ratio, whilst steep root angle, indicating deep roots, increased the Mg:N ratio. The results have significant implications on the management and breeding targets of agriculturally grown wheat, which is one of the most important food crops worldwide.

Shoot and Root Traits Underlying Genotypic Variation in Early Vigor and Nutrient Accumulation in Spring Wheat Grown in High-Latitude Light Conditions.

Plants with improved nutrient use efficiency are needed to maintain and enhance future crop plant production. The aim of this study was to explore candidate traits for pre-breeding to improve nutrient accumulation and early vigor of spring wheat grown at high latitudes. We quantified shoot and root traits together with nutrient accumulation in nine contrasting spring wheat genotypes grown in rhizoboxes for 20 days in a greenhouse. Whole-plant relative growth rate was here correlated with leaf area productivity and plant nitrogen productivity, but not leaf area ratio. Furthermore, the total leaf area was correlated with the accumulation of six macronutrients, and could be suggested as a candidate trait for the pre-breeding towards improved nutrient accumulation and early vigor in wheat to be grown in high-latitude environments. Depending on the nutrient of interest, different root system traits were identified as relevant for their accumulation. Accumulation of nitrogen, potassium, sulfur and calcium was correlated with lateral root length, whilst accumulation of phosphorus and magnesium was correlated with main root length. Therefore, special attention needs to be paid to specific root system traits in the breeding of wheat towards improved nutrient accumulation to counteract the suboptimal uptake of some nutrient elements.

Limited resilience of the soil microbiome to mechanical compaction within four growing seasons of agricultural management.

Soil compaction affects many soil functions, but we have little information on the resistance and resilience of soil microorganisms to this disturbance. Here, we present data on the response of soil microbial diversity to a single compaction event and its temporal evolution under different agricultural management systems during four growing seasons. Crop yield was reduced (up to -90%) in the first two seasons after compaction, but mostly recovered in subsequent seasons. Soil compaction increased soil bulk density (+15%), and decreased air permeability (-94%) and gas diffusion (-59%), and those properties did not fully recover within four growing seasons. Soil compaction induced cropping system-dependent shifts in microbial community structures with little resilience over the four growing seasons. Microbial taxa sensitive to soil compaction were detected in all major phyla. Overall, anaerobic prokaryotes and saprotrophic fungi increased in compacted soils, whereas aerobic prokaryotes and plant-associated fungi were mostly negatively affected. Most measured properties showed large spatial variability across the replicated blocks, demonstrating the dependence of compaction effects on initial conditions. This study demonstrates that soil compaction is a disturbance that can have long-lasting effects on soil properties and soil microorganisms, but those effects are not necessarily aligned with changes in crop yield.

Enhanced root carbon allocation through organic farming is restricted to topsoils.

Soils store significant amounts of carbon (C) and thus can play a critical role for mitigating climate change. Crop roots represent the main C source in agricultural soils and are particularly important for long-term C storage in agroecosystems. To evaluate the potential of different farming systems to contribute to soil C sequestration and thus climate change mitigation, it is of great importance to gain a better understanding of the factors influencing root C allocation and distribution. So far, it is still unclear how root C allocation varies among farming systems and whether the choice of management practices can help to enhance root C inputs. In this study, we compared root C allocation in three main arable farming systems, namely organic, no-till, and conventional farming. We assessed root biomass, vertical root distribution to 0.75 m soil depth, and root-shoot ratios in 24 winter wheat fields. We further evaluated the relative importance of the farming system compared to site conditions and quantified the contribution of individual management practices and pedoclimatic drivers. Farming system explained one third of the variation in topsoil root biomass and root-shoot ratios, both being strongly positively related to weed biomass and soil organic C content and negatively to mineral nitrogen fertilization intensity. Root C allocation was significantly higher in organic farming as illustrated by an increase in root biomass (+40%) and root-shoot ratios (+60%) compared to conventional farming. By contrast, the overall impact of no-till was low. The importance of pedoclimatic conditions increased substantially with soil depth and deep root biomass was largely controlled by precipitation and soil texture, while the impact of management was close to zero. Our findings highlight the potential of organic farming in promoting root C inputs to topsoils and thereby contributing to soil organic matter build-up and improved soil quality in agroecosystems.

Energy use efficiency of root growth - a theoretical bioenergetics framework.

Metabolic efficiency of root growth is a crucial physiological parameter, contributing to the amount of photosynthate that plants need to invest into soil exploration. Common measurements of metabolic efficiency usually rely on CO2 respiration measurements with the underlying assumption that all metabolic processes are taking place under aerobic conditions. In this conceptual paper, we introduce energy use efficiency based on the quantification of heat dissipation and energy fluxes as an alternative metric to quantify the metabolic efficiency of root growth. In a theoretical framework, we adopted recently published heat dissipation data from wheat seedlings and show that energy use efficiency decreases in response to (i) soil hypoxia and (ii) increased soil penetration resistance. In contrast to traditional CO2 respiration measurements, heat dissipation measurements account for both aerobic as well as anaerobic respiration in growing roots. Hence, we advocate that the quantification of heat dissipation provides a more complete picture of the metabolic efficiency of root growth than CO2 respiration measurements alone. We therefore propose that energy use efficiency should be included in future studies assessing the metabolic efficiency of root growth.

Cortical Cell Diameter Is Key To Energy Costs of Root Growth in Wheat.

Root growth requires substantial amounts of energy and thus carbohydrates. The energy costs of root growth are particularly high in both dry and compacted soil, due to high soil penetration resistance. Consequently, more carbon must be allocated from aboveground plant tissue to roots, which limits crop productivity. In this study, we tested the utility of root cortical cell diameter as a potential selection target to reduce the energy costs of root growth. Isothermal calorimetry was adopted for in situ quantification of the energy costs of root growth of 16 wheat (Triticum aestivum) genotypes under three levels of penetration resistance. We show that cortical cell diameter is a pivotal and heritable trait, which is strongly related to the energy costs of root growth. Genotypic diversity was found for cortical cell diameter and the energy costs of root growth. A large root cortical cell diameter correlated with reduced energy costs of root growth, particularly under high soil penetration resistance. Moreover, significant correlations were found between the ability to radially enlarge cortical cells upon greater penetration resistance (i.e. phenotypic plasticity) and the responsiveness in the energy costs of root growth. A higher degree of phenotypic plasticity in cortical cell diameter was associated with reduced energy costs of root growth as soil penetration resistance increased. We therefore suggest that genotypic diversity and phenotypic plasticity in cortical cell diameter should be harnessed to adapt crops to dry and compacted soils.

Feedbacks between soil penetration resistance, root architecture and water uptake limit water accessibility and crop growth - A vicious circle.

Water is the most limiting resource for global crop production. The projected increase of dry spells due to climate change will further increase the problem of water limited crop yields. Besides low water abundance and availability, water limitations also occur due to restricted water accessibility. Soil penetration resistance, which is largely influenced by soil moisture, is the major soil property regulating root elongation and water accessibility. Until now the interactions between soil penetration resistance, root system properties, water uptake and crop productivity are rarely investigated. In the current study we quantified how interactive effects between soil penetration resistance, root architecture and water uptake affect water accessibility and crop productivity in the field. Maize was grown on compacted and uncompacted soil that was either tilled or remained untilled after compaction, which resulted in four treatments with different topsoil penetration resistance. Higher topsoil penetration resistance caused root systems to be shallower. This resulted in increased water uptake from the topsoil and hence topsoil drying, which further increased the penetration resistance in the uppermost soil layer. As a consequence of this feedback, root growth into deeper soil layers, where water would have been available, was reduced and plant growth decreased. Our results demonstrate that soil penetration resistance, root architecture and water uptake are closely interrelated and thereby determine the potential of plants to access soil water pools. Hence, these interactions and their feedbacks on water accessibility and crop productivity have to be accounted for when developing strategies to alleviate water limitations in cropping systems.

Root Tip Shape Governs Root Elongation Rate under Increased Soil Strength.

Increased soil strength due to soil compaction or soil drying is a major limitation to root growth and crop productivity. Roots need to exert higher penetration force, resulting in increased penetration stress when elongating in soils of greater strength. This study aimed to quantify how the genotypic diversity of root tip geometry and root diameter influences root elongation under different levels of soil strength and to determine the extent to which roots adjust to increased soil strength. Fourteen wheat (Triticum aestivum) varieties were grown in soil columns packed to three bulk densities representing low, moderate, and high soil strength. Under moderate and high soil strength, smaller root tip radius-to-length ratio was correlated with higher genotypic root elongation rate, whereas root diameter was not related to genotypic root elongation. Based on cavity expansion theory, it was found that smaller root tip radius-to-length ratio reduced penetration stress, thus enabling higher root elongation rates in soils with greater strength. Furthermore, it was observed that roots could only partially adjust to increased soil strength. Root thickening was bounded by a maximum diameter, and root tips did not become more acute in response to increased soil strength. The obtained results demonstrated that root tip geometry is a pivotal trait governing root penetration stress and root elongation rate in soils of greater strength. Hence, root tip shape needs to be taken into account when selecting for crop varieties that may tolerate high soil strength.

Genetic Diversity under Soil Compaction in Wheat: Root Number as a Promising Trait for Early Plant Vigor.

Soil compaction of arable land, caused by heavy machinery constitutes a major threat to agricultural soils in industrialized countries. The degradation of soil structure due to compaction leads to decreased (macro-) porosity resulting in increased mechanical impedance, which adversely affects root growth and crop productivity. New crop cultivars, with root systems that are adapted to conditions of increased soil strength, are needed to overcome the limiting effects of soil compaction on plant growth. This study aimed (i) to quantify the genetic diversity of early root system development in wheat and to relate this to shoot development under different soil bulk densities and (ii) to test whether root numbers are suitable traits to assess the genotypic tolerance to soil compaction. Fourteen wheat genotypes were grown for 3 weeks in a growth chamber under low (1.3 g cm-3), moderate (1.45 g cm-3), and high soil bulk density (1.6 g cm-3). Using X-ray computed tomography root system development was quantified in weekly intervals, which was complemented by weekly measurements of plant height. The development of the root system, quantified via the number of axial and lateral roots was strongly correlated (0.78 < r < 0.88, p < 0.01) to the development of plant height. Furthermore, significant effects (p < 0.01) of the genotype on root system development and plant vigor traits were observed. Under moderate soil strength final axial and lateral root numbers were significantly correlated (0.57 < r < 0.84, p < 0.05) to shoot dry weight. Furthermore, broad-sense heritability of axial and lateral root number was higher than 50% and comparable to values calculated for shoot traits. Our results showed that there is genetic diversity in wheat with respect to root system responses to increased soil strength and that root numbers are suitable indicators to explain the responses and the tolerance to such conditions. Since root numbers are heritable and can be assessed at high throughput rates under laboratory and field conditions, root number is considered a promising trait for screening toward compaction tolerant varieties.

Artificial macropores attract crop roots and enhance plant productivity on compacted soils.

The structure of compacted soils is characterised by decreased (macro-)porosity, which leads to increased mechanical impedance and decreased fluid transport rates, resulting in reduced root growth and crop productivity. Particularly in soils with high mechanical impedance, macropores can be used by roots as pathways of least resistance. This study investigated how different soil physical states relate to whole plant growth and whether roots grow towards spots with favourable soil physical conditions. Experiments were conducted under controlled and field conditions. Soybean (Glycine max L.), wheat (Triticum aestivum L.) and maize (Zea mays L.) were grown on uncompacted soil, compacted soil and compacted soil with artificial macropores. The interactions between roots and artificial macropores were quantified using X-ray computed tomography. Active growth of roots towards artificial macropores was observed for all three species. Roots grew either into macropores (predominantly in maize) or crossed them (predominantly in wheat). The presence of artificial macropores in compacted soil enabled all three species to compensate for decreased early vigour at later developmental stages. These results show that roots sense their physical environment, enabling them to grow towards spots with favourable soil conditions. The different kinds of root-macropore interaction indicated that macropores serve as a path of least resistance and a source of oxygen, both resulting in increased crop productivity on compacted soils.

Root responses of triticale and soybean to soil compaction in the field are reproducible under controlled conditions.

Soil compaction includes a set of underlying stresses that limit root growth such as increased impedance and limited oxygen availability. The aims of the present study were to (i) find acclimations of triticale (× Triticosecale) and soybean (Glycine max L.) roots to compacted soils in the field; (ii) reproduce these under controlled conditions; and (iii) associate these responses with soil physical properties. To this end, plants were grown at two different soil bulk densities in the field and under controlled conditions representing mature root systems and the seedling stage respectively. Diameters, lateral branching densities, the cortical proportion within the total root cross-section and the occurrence of cortical aerenchyma of main roots were quantified. Soil compaction caused decreasing root branching and increasing cortical proportions in both crops and environments. In triticale, root diameters and the occurrence of aerenchyma increased in response to compaction in the field and under controlled conditions. In soybean, these acclimations occurred at an initial developmental stage but due to radial root growth not in mature roots. These results showed that responses of root systems to compacted soils in the field are, to a large extent, reproducible under controlled conditions, enabling increased throughput, phenotyping-based breeding programs in the future. Furthermore, the occurrence of aerenchyma clearly indicated the important role of limited oxygen availability in compacted soils on root growth.

Rapid phenotyping of crop root systems in undisturbed field soils using X-ray computed tomography.

BACKGROUND: X-ray computed tomography (CT) has become a powerful tool for root phenotyping. Compared to rather classical, destructive methods, CT encompasses various advantages. In pot experiments the growth and development of the same individual root can be followed over time and in addition the unaltered configuration of the 3D root system architecture (RSA) interacting with a real field soil matrix can be studied. Yet, the throughput, which is essential for a more widespread application of CT for basic research or breeding programs, suffers from the bottleneck of rapid and standardized segmentation methods to extract root structures. Using available methods, root segmentation is done to a large extent manually, as it requires a lot of interactive parameter optimization and interpretation and therefore needs a lot of time. RESULTS: Based on commercially available software, this paper presents a protocol that is faster, more standardized and more versatile compared to existing segmentation methods, particularly if used to analyse field samples collected in situ. To the knowledge of the authors this is the first study approaching to develop a comprehensive segmentation method suitable for comparatively large columns sampled in situ which contain complex, not necessarily connected root systems from multiple plants grown in undisturbed field soil. Root systems from several crops were sampled in situ and CT-volumes determined with the presented method were compared to root dry matter of washed root samples. A highly significant (P < 0.01) and strong correlation (R(2) = 0.84) was found, demonstrating the value of the presented method in the context of field research. Subsequent to segmentation, a method for the measurement of root thickness distribution has been used. Root thickness is a central RSA trait for various physiological research questions such as root growth in compacted soil or under oxygen deficient soil conditions, but hardly assessable in high throughput until today, due to a lack of available protocols. CONCLUSIONS: Application of the presented protocol helps to overcome the segmentation bottleneck and can be considered a step forward to high throughput root phenotyping facilitating appropriate sample sizes desired by science and breeding.