Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field

We present a method to visually score 10 root architectural traits of the root crown of an adult maize plant in the field in a few minutes. Phenotypic profiling of three recombinant inbred line (RIL) populations of maize (Zea mays L.; B73xMo17, Oh43xW64a, Ny821xH99) was conducted in 2008 in a silt loam soil in Pennsylvania and in a sandy soil in Wisconsin, and again in 2009 in Pennsylvania. Numbers, angles and branching pattern of crown and brace roots were assessed visually at flowering. Depending on the soil type in which plants were grown, sample processing took from three (sand) to 8 min (silt-loam). Visual measurement of the root crown required 2 min per sample irrespective of the environment. Visual scoring of root crowns gave a reliable estimation of values for root architectural traits as indicated by high correlations between measured and visually scored trait values for numbers (r ²?=?0.46?C0.97), angles (r ²?=?0.66?C0.76), and branching (r ²?=?0.54?C0.88) of brace and crown roots. Based on the visual evaluation of root crown traits it was possible to discriminate between populations. RILs derived from the cross NY821 x H99 generally had the greatest number of roots, the highest branching density and the most shallow root angles, while inbred lines from the cross between OH43 x W64a generally had the steepest root angles. The ranking of genotypes remained the same across environments, emphasizing the suitability of the method to evaluate genotypes across environments. Scoring of brace roots was better correlated with the actual measurements compared to crown roots. The visual evaluation of root architecture will be a valuable tool in tailoring crop root systems to specific environments.     

Increased seminal root number associated with domestication improves nitrogen and phosphorus acquisition in maize seedlings

Background and AimsDomesticated maize (Zea mays ssp. mays) generally forms between two and six seminal roots, while its wild ancestor, Mexican annual teosinte (Zea mays ssp. parviglumis), typically lacks seminal roots. Maize also produces larger seeds than teosinte, and it generally has higher growth rates as a seedling. Maize was originally domesticated in the tropical soils of southern Mexico, but it was later brought to the Mexican highlands before spreading to other parts of the continent, where it experienced different soil resource constraints. The aims of this study were to understand the impacts of increased seminal root number on seedling nitrogen and phosphorus acquisition and to model how differences in maize and teosinte phenotypes might have contributed to increased seminal root number in domesticated maize.MethodsSeedling root system architectural models of a teosinte accession and a maize landrace were constructed by parameterizing the functional–structural plant model OpenSimRoot using plants grown in mesocosms. Seedling growth was simulated in a low-phosphorus environment, multiple low-nitrogen environments, and at variable planting densities. Models were also constructed to combine individual components of the maize and teosinte phenotypes.Key ResultsSeminal roots contributed ~35 % of the nitrogen and phosphorus acquired by maize landrace seedlings in the first 25 d after planting. Increased seminal root number improved plant nitrogen acquisition under low-nitrogen environments with varying precipitation patterns, fertilization rates, soil textures and planting densities. Models suggested that the optimal number of seminal roots for nutrient acquisition in teosinte is constrained by its limited seed carbohydrate reserves.ConclusionsSeminal roots can improve the acquisition of both nitrogen and phosphorus in maize seedlings, and the increase in seed size associated with maize domestication may have facilitated increased seminal root number.     

Theoretical evidence that root penetration ability interacts with soil compaction regimes to affect nitrate capture

Background and AimsAlthough root penetration of strong soils has been intensively studied at the scale of individual root axes, interactions between soil physical properties and soil foraging by whole plants are less clear. Here we investigate how variation in the penetration ability of distinct root classes and bulk density profiles common to real-world soils interact to affect soil foraging strategies.MethodsWe utilize the functional–structural plant model ‘OpenSimRoot’ to simulate the growth of maize (Zea mays) root systems with variable penetration ability of axial and lateral roots in soils with (1) uniform bulk density, (2) plow pans and (3) increasing bulk density with depth. We also modify the availability and leaching of nitrate to uncover reciprocal interactions between these factors and the capture of mobile resources.Key ResultsSoils with plow pans and bulk density gradients affected overall size, distribution and carbon costs of the root system. Soils with high bulk density at depth impeded rooting depth and reduced leaching of nitrate, thereby improving the coincidence of nitrogen and root length. While increasing penetration ability of either axial or lateral root classes produced root systems of comparable net length, improved penetration of axial roots increased allocation of root length in deeper soil, thereby amplifying N acquisition and shoot biomass. Although enhanced penetration ability of both root classes was associated with greater root system carbon costs, the benefit to plant fitness from improved soil exploration and resource capture offset these.ConclusionsWhile lateral roots comprise the bulk of root length, axial roots function as a scaffold determining the distribution of these laterals. In soils with high soil strength and leaching, root systems with enhanced penetration ability of axial roots have greater distribution of root length at depth, thereby improving capture of mobile resources.     

Spatio-temporal Variations in Axial Conductance of Primary and First-order Lateral Roots of a Maize Crop as Predicted by a Model of the Hydraulic Architecture of Root Systems

Rates at which water can be transported along plant roots (axial pathway) vary through time, in part depending on xylem maturation. Because of experimental constraints, the dynamics of root functional heterogeneity under field conditions remains mostly uncharted territory. Recent advances in mechanistic modelling offer opportunities to bypass such experimental limitations. This paper examines the dynamics of local variations in axial conductance of primary and first-order lateral roots of a maize crop using the architecture-based modelling approach developed by Doussan et al. (Annals of Botany: 81, 213–223, 1998). Specifically, we hypothesised that points of major resistance to long distance water transfers could arise from discrepancies between the hydraulic maturity (or water carrying capacity) of main axes and branch roots. To test this assumption, spatial distributions of root axial conductance were tested after 30, 60 and 100 days at soil depths of 10, 50 and 100 cm under a maize (Zea mays L.) crop sown at a density of 8 plants m⁻². As the crop developed, the corresponding root populations encompassed ever increasing amounts of hydraulically mature first-order laterals (branch roots): after a 100-day growth period, the vast majority of laterals had reached their maximum axial conductance at all soil depths down to 100 cm. In contrast, the axial conductance of a large proportion of main axes (primary roots) remained low, even at shallow soil depths and after 100 days of growth. The imbalance between the hydraulic maturity of primary and lateral roots was most conspicuous at soil depths of 100 cm, where ~10% only of the former compared to ~80% of the latter, had reached their maximum axial conductance after a 100-day growth period.     

Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems

The use of nitrogen (N) fertilizers has contributed to the production of a food supply sufficient for both animals and humans despite some negative environmental impact. Sustaining food production by increasing N use efficiency in intensive cropping systems has become a major concern for scientists, environmental groups, and agricultural policymakers worldwide. In high-yielding maize systems the major method of N loss is nitrate leaching. In this review paper, the characteristic of nitrate movement in the soil, N uptake by maize as well as the regulation of root growth by soil N availability are discussed. We suggest that an ideotype root architecture for efficient N acquisition in maize should include (i) deeper roots with high activity that are able to uptake nitrate before it moves downward into deep soil; (ii) vigorous lateral root growth under high N input conditions so as to increase spatial N availability in the soil; and (iii) strong response of lateral root growth to localized nitrogen supply so as to utilize unevenly distributed nitrate especially under limited N conditions.     

Root cortical burden influences drought tolerance in maize

Background and Aims

Root cortical aerenchyma (RCA) increases water and nutrient acquisition by reducing the metabolic costs of soil exploration. In this study the hypothesis was tested that living cortical area (LCA; transversal root cortical area minus aerenchyma area and intercellular air space) is a better predictor of root respiration, soil exploration and, therefore, drought tolerance than RCA formation or root diameter.

Methods

RCA, LCA, root respiration, root length and biomass loss in response to drought were evaluated in maize (Zea mays) recombinant inbred lines grown with adequate and suboptimal irrigation in soil mesocosms.

Key Results

Root respiration was highly correlated with LCA. LCA was a better predictor of root respiration than either RCA or root diameter. RCA reduced respiration of large-diameter roots. Since RCA and LCA varied in different parts of the root system, the effects of RCA and LCA on root length were complex. Greater crown-root LCA was associated with reduced crown-root length relative to total root length. Reduced LCA was associated with improved drought tolerance.

Conclusions

The results are consistent with the hypothesis that LCA is a driver of root metabolic costs and may therefore have adaptive significance for water acquisition in drying soil.     

Effect of tillage and farming system upon VAM fungus populations and mycorrhizas and nutrient uptake of maize

Low-input agricultural systems that do not rely on fertilizers may be more dependent on vesicular-arbuscular mycorrhizal [VAM] fungi than conventionally managed systems. We studied populations of spores of VAM fungi, mycorrhiza formation and nutrient utilization of maize (Zea mays L.) grown in moldboard plowed, chisel-disked or no-tilled soil under conventional and low-input agricultural systems. Maize shoots and roots were collected at four growth stages. Soils under low-input management had higher VAM fungus spore populations than soils under conventional management. Spore populations and colonization of maize roots by VAM fungi were higher in no-tilled than in moldboard plowed or chisel-disked soil. The inoculum potential of soil collected in the autumn was greater for no-till and chisel-disked soils than for moldboard plowed soils and greater for low-input than conventionally farmed soil. The effects of tillage and farming system on N uptake and utilization varied with growth stage of the maize plants. The effect of farming system on P use efficiency was significant at the vegetative stages only, with higher efficiencies in plants under low-input management. The effect of tillage was consistent through all growth stages, with higher P use efficiencies in plants under moldboard plow and chisel-disk than under no-till. Plants grown in no-tilled soils had the highest shoot P concentrations throughout the experiment. This benefit of enhanced VAM fungus colonization, particularly in the low-input system in the absence of effective weed control and with likely lower soil temperatures, did not translate into enhanced growth and yield.     

Increased nutrient supply facilitates acclimation to high-water level in the marsh plant Deyeuxia angustifolia: The response of root morphology

Both water level and nutrient availability are important factors influencing the growth of wetland plants. Increased nutrient supply might counteract the negative effects of flooding on the growth of the fast-growing species. Experimental evidence is scarce and the mechanism is far from clear. The aim of this study is to identify the role of nutrient availability in acclimation to high-water level by investigating the growth and root morphology of the marsh plant Deyeuxia angustifolia, one of the dominant species in the Sanjiang Plain, China. Experimental treatments included two water levels (0 and 10 cm, relative to soil surface) and three levels of nutrient supply (0, 0.5 and 1 g fertilizer per container). High-water level usually led to decreased biomass accumulation, shoot mass and root mass, whereas biomass accumulation was unaffected by water level at the highest nutrient level, indicating that high-nutrient availability played a role in compensating for the growth loss induced by the high-water level. Increased nutrient supply led to decreased root length in 0 cm water-level treatments, but root length increased with nutrient supply in the 10 cm water-level treatments. High-water level usually led to a lower lateral root density, lateral root:main root length ratio and the diameter of main roots and laterals, whereas increased nutrient supply resulted in thicker main roots or laterals, and a higher total root length, lateral root density and lateral root:main root length ratio. These data indicate that the growth of D. angustifolia is restrained by high-water level, and that increased nutrient supply not only ameliorates root characteristics to acclimate to high-water level but also results in a high-total root length to facilitate nutrient acquisition.     

Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability

Background and Aims

The formation of root cortical aerenchyma (RCA) reduces root respiration and nutrient content by converting living tissue to air volume. It was hypothesized that RCA increases soil resource acquisition by reducing the metabolic and phosphorus cost of soil exploration.

Methods

To test the quantitative logic of the hypothesis, SimRoot, a functional–structural plant model with emphasis on root architecture and nutrient acquisition, was employed. Sensitivity analyses for the effects of RCA on the initial 40 d of growth of maize (Zea mays) and common bean (Phaseolus vulgaris) were conducted in soils with varying degrees of phosphorus availability. With reference to future climates, the benefit of having RCA in high CO₂ environments was simulated.

Key Results

The model shows that RCA may increase the growth of plants faced with suboptimal phosphorus availability up to 70 % for maize and 14 % for bean after 40 d of growth. Maximum increases were obtained at low phosphorus availability (3 µm). Remobilization of phosphorus from dying cells had a larger effect on plant growth than reduced root respiration. The benefit of both these functions was additive and increased over time. Larger benefits may be expected for mature plants. Sensitivity analysis for light-use efficiency showed that the benefit of having RCA is relatively stable, suggesting that elevated CO₂ in future climates will not significantly effect the benefits of having RCA.

Conclusions

The results support the hypothesis that RCA is an adaptive trait for phosphorus acquisition by remobilizing phosphorus from the root cortex and reducing the metabolic costs of soil exploration. The benefit of having RCA in low-phosphorus soils is larger for maize than for bean, as maize is more sensitive to low phosphorus availability while it has a more ‘expensive’ root system. Genetic variation in RCA may be useful for breeding phosphorus-efficient crop cultivars, which is important for improving global food security.     

Root anatomy of <Emphasis Type="Italic">Pinus taeda</Emphasis> L.: seasonal and environmental effects on development in seedlings

The environmental and seasonal effects on anatomical traits of Pinus taeda L. seedling roots were studied in the laboratory in three contrasting root growth media and also in typical outdoor nursery culture. Growth media with lower water regimen and high penetration resistance caused a reduction in lengths of the white and condensed tannin (CT) zones and acceleration of development of suberin lamellae in the endodermis. As a possible counter to this reduction in zone lengths, second-order laterals were produced closer to the tips of first-order laterals. This suggested there may be an advantage to producing more shorter roots under stressful conditions. Under outdoor nursery conditions (June to mid-December) the white zone was always a rather small part of the root system surface area (4.5% in December), but it dominated as a provider of cortical plasmalemma surface area (CPSA) in contact with modified soil solution (65% in December) because of its live cortex and capacity to increase nearly three fold the amount of CPSA per unit root length. The CT zone always provided most of the total root surface area (80% in December). Although it had no live cortex, a few cells of the CT zone endodermis remained non-suberized passage cells, perhaps giving this major part of the root system some capacity for ion and water absorption. A late summer increase in CPSA was due largely to the rapid production of mycorrhizae. Root systems were capable of very rapid replacement of roots lost due to undercutting and lateral root pruning. The great variation in CPSA per unit root length contained in the white, mycorrhizal and CT zones suggested a capacity to adapt rapidly to changing conditions.     

Focus Issue on Roots: Low Crown Root Number Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize

In developing nations, low soil nitrogen (N) availability is a primary limitation to crop production and food security, while in rich nations, intensive N fertilization is a primary economic, energy, and environmental cost to crop production. It has been proposed that genetic variation for root architectural and anatomical traits enhancing the exploitation of deep soil strata could be deployed to develop crops with greater N acquisition. Here, we provide evidence that maize (Zea mays) genotypes with few crown roots (crown root number [CN]) have greater N acquisition from low-N soils. Maize genotypes differed in their CN response to N limitation in greenhouse mesocosms and in the field. Low-CN genotypes had 45% greater rooting depth in low-N soils than high-CN genotypes. Deep injection of ¹⁵N-labeled nitrate showed that low-CN genotypes under low-N conditions acquired more N from deep soil strata than high-CN genotypes, resulting in greater photosynthesis and plant N content. Under low N, low-CN genotypes had greater biomass than high-CN genotypes at flowering (85% in the field study in the United States and 25% in South Africa). In the field in the United States, 1.8× variation in CN was associated with 1.8× variation in yield reduction by N limitation. Our results indicate that CN deserves consideration as a potential trait for genetic improvement of N acquisition from low-N soils.Maize (Zea mays) is one of the world’s most important crops and is a staple food in Latin America and Africa. Maize production requires a large amount of fertilizer, especially nitrogen (N). In the United States, N fertilizers represent the greatest economic and energy costs for maize production (Ribaudo et al., 2011). However, on-farm studies across the northcentral United States revealed that more than half of applied N is not taken up by maize plants and is vulnerable to losses from volatilization, denitrification, and leaching, which pollute air and water resources (Cassman et al., 2002). Conversely, in developing countries, suboptimal N availability is a primary limitation to crop yields and, therefore, food security (Azeez et al., 2006). Increasing yield in these areas is an urgent concern, since chemical fertilizers are not affordable (Worku et al., 2007). Cultivars with greater N acquisition from low-N soils could help alleviate food insecurity in poor nations as well as reduce environmental degradation from excessive fertilizer use in developed countries.The two major soil N forms available to plants are ammonium and nitrate. Nitrate is the main N form in most maize production environments (Miller and Cramer, 2004). Nitrate is highly mobile in soil, and the spatiotemporal availability of soil N is rather complex. In the simplest case, N fertilizers applied to the soil and/or N released from the mineralization of soil organic matter are rapidly converted to nitrate by soil microbes. After irrigation and precipitation events, nitrate moves with water to deeper soil strata. Leaching of nitrate from the root zone has been shown to be a significant cause of low recovery of N fertilizer in commercial agricultural systems (Raun and Johnson, 1999; Cassman et al., 2002). Differences in root depth influence the ability of plants to acquire N. Studies using ¹⁵N-labeled nitrate placed at different soil depths showed that only plants with deep rooting can acquire N sources from deep soil strata, which would otherwise have been lost through leaching (Kristensen and Thorup-Kristensen, 2004a, 2004b). Therefore, selection for root traits enhancing rapid deep soil exploration could be used as a strategy to improve crop N efficiency.The maize root system consists of embryonic and postembryonic components. The embryonic root system consists of two distinct root classes: a primary root and a variable number of seminal roots formed at the scutellar node. The postembryonic root system consists of roots that are formed at consecutive shoot nodes and lateral roots, which are initiated in the pericycle of all root classes. Shoot-borne or nodal roots that are formed belowground are called crown roots, whereas those that are formed aboveground are designated brace roots (Hochholdinger, 2009). While the primary root and seminal roots are essential for the establishment of seedlings after germination, nodal roots and particularly crown roots make up most of the maize root system and are primarily responsible for soil resource acquisition later in development (Hoppe et al., 1986).Lynch (2013) proposed an ideotype for superior N and water acquisition in maize called Steep, Cheap, and Deep (SCD), which integrates root architectural, anatomical, and physiological traits to increase rooting depth and, therefore, the capture of N in leaching environments. One such trait is crown root number (CN). CN is an aggregate trait consisting of the number of belowground nodal whorls and the number of roots per whorl. The crown root system dominates resource acquisition during vegetative growth after the first few weeks and remains important during reproductive development (Hochholdinger et al., 2004). CN in maize ranges from five to 50 under fertile conditions (Trachsel et al., 2011). At the low end of this range, crown roots may be too spatially dispersed to sufficiently explore the soil. There is also a risk of root loss to herbivores and pathogens. If roots are lost in low-N plants, there may be too few crown roots left to support the nutrient, water, and anchorage needs of the plant. At the high end, a large number of crown roots may compete with each other for water and nutrients as well as incur considerable metabolic costs for the plant (Fig. 1). The SCD ideotype proposes that there is an optimal CN for N capture in maize (Lynch, 2013). Under low-N conditions, resources for root growth and maintenance are limiting, and nitrate is a mobile resource that can be captured by a dispersed root system. The optimal CN should tend toward the low end of the phenotypic variation to make resources available for the development of longer, deeper roots rather than more crown roots. According to the SCD ideotype, in low-N soils, maize genotypes with fewer crown roots could explore soils at greater depth, resulting in greater N acquisition, growth, and yield than genotypes with many crown roots.Open in a separate windowFigure 1.Visualization of the maize root system of low- and high-CN genotypes at 40 d after germination. Crown roots are colored in blue, and seminal roots are in red. The CN is eight in the low-CN genotype and 46 in the high-CN genotype. (Image courtesy of Larry M. York.)The objective of this study was to test the hypotheses that (1) low-CN genotypes have greater rooting depth than high-CN genotypes in low-N soils; (2) low-CN genotypes are better at acquiring deep soil N than high-CN genotypes; and (3) low-CN genotypes have greater biomass and yield than high-CN genotypes in low-N conditions.     

Evaluation in field conditions of a three-dimensional architectural model of the maize root system: Comparison of simulated and observed horizontal root maps

Most existing water and nutrient uptake models are based on the assumption that roots are evenly distributed in the soil volume. This assumption is not realistic for field conditions, and significantly alters water or nutrient uptake calculations. Therefore, development of models of root system growth that account for the spatial distribution of roots is necessary.The objective of this work was to test a three dimensional architectural model of the maize root system by comparing simulated horizontal root maps with observed root maps obtained from the field. The model was built using the current knowledge on maize root system morphogenesis and parameters obtained under field conditions. Simulated root maps (0.45 × 0.75 m) of horizontal cross sections at 3 depths and 3 dates were obtained by using the model for a plant population. Actual root maps were obtained in a deep, barrier-free clay-loamy soil by digging pits, preparing selected horizontal planes and recording root contacts on plastic sheets.Results showed that both the number of cross-sections of axile roots, and their spatial distribution characterized with the R-index value of Clark and Evans (1954), were correctly accounted for by the model at all dates and depths. The number of cross-sections of laterals was also correctly predicted. However, laterals were more clustered around axile roots on simulated root maps than on observed root maps. Although slight discrepancies appeared between simulated and observed root maps in this respect, it was concluded that the model correctly accounted for the general colonization pattern of the soil volume by roots under a maize crop.     

Coping with low nutrient availability and inundation: root growth responses of three halophytic grass species from different elevations along a flooding gradient

We describe the responses of three halophytic grass species that dominate the low (Spartina anglica), middle (Puccinellia maritima) and high (Elymus pycnanthus) parts of a salt marsh, to soil conditions that are believed to favour contrasting root-growth strategies. Our hypotheses were: (1) individual lateral root length is enhanced by N limitations in the soil but restricted by oxygen limitations, (2) the density of root branching within a species is inversely related to the length of the lateral roots, and (3) species from high elevations (i.e. the driest parts of a marsh) are the most responsive to changing soil conditions. Plant growth responses and soil parameters showed that the contrasting but uniformly applied soil treatments were effective. All three species showed a small but significant shift towards a finer root diameter distribution when N was limiting, partly because of the finer diameters of the laterals (Elymus and Spartina) and partly because of increased length of individual 1st-order laterals (Elymus and Puccinellia). The increased length of the 1st-order laterals of Elymus and Puccinellia grown under low N indicates that the first part of hypothesis 1 may be true. However, lack of effect of flooding and reduced soil conditions lead us to reject the second part of hypothesis 1. Hypothesis 2 was rejected for these three halophytes, as the branch density of 1st- and 2nd-order laterals appears to be controlled by other factors than length of individual laterals. Hypothesis 3 may be true for specific root characteristics (e.g. length of individual 1st-order laterals), but cannot be generalised (e.g. branch density and topological index). In conclusion, the present data on root growth in contrasting but homogeneous soil conditions indicate that morphological responsiveness of the root systems of these halophytic grass species is limited, regardless of their location along the elevational gradient.     

Reduced Root Cortical Cell File Number Improves Drought Tolerance in Maize

We tested the hypothesis that reduced root cortical cell file number (CCFN) would improve drought tolerance in maize (Zea mays) by reducing the metabolic costs of soil exploration. Maize genotypes with contrasting CCFN were grown under well-watered and water-stressed conditions in greenhouse mesocosms and in the field in the United States and Malawi. CCFN ranged from six to 19 among maize genotypes. In mesocosms, reduced CCFN was correlated with 57% reduction of root respiration per unit of root length. Under water stress in the mesocosms, genotypes with reduced CCFN had between 15% and 60% deeper rooting, 78% greater stomatal conductance, 36% greater leaf CO₂ assimilation, and between 52% to 139% greater shoot biomass than genotypes with many cell files. Under water stress in the field, genotypes with reduced CCFN had between 33% and 40% deeper rooting, 28% lighter stem water oxygen isotope enrichment (δ¹⁸O) signature signifying deeper water capture, between 10% and 35% greater leaf relative water content, between 35% and 70% greater shoot biomass at flowering, and between 33% and 114% greater yield than genotypes with many cell files. These results support the hypothesis that reduced CCFN improves drought tolerance by reducing the metabolic costs of soil exploration, enabling deeper soil exploration, greater water acquisition, and improved growth and yield under water stress. The large genetic variation for CCFN in maize germplasm suggests that CCFN merits attention as a breeding target to improve the drought tolerance of maize and possibly other cereal crops.Drought is a primary constraint to global crop production (Schmidhuber and Tubiello, 2007), and global climate change is likely to increase the risk of drought, especially in rain-fed agriculture (Battisti and Naylor, 2009; Burke et al., 2009; Mishra and Cherkauer, 2010; Lobell et al., 2011). Therefore, the development of crops with greater drought tolerance is an important global objective. Yield under drought is often not an efficient selection criterion in drought breeding programs, since yield is affected by many elements of the phenotype and the environment, interacting in complex and often unknown ways. Trait-based selection or ideotype breeding is generally a more efficient selection strategy, permitting the identification of useful sources of variation among lines that have poor agronomic adaptation, elucidation of genotype-by-environment interactions, and informed trait stacking (Araus et al., 2002, 2008; Manschadi et al., 2006; Lynch, 2007b, 2011; York et al., 2013).In most agroecosystems, the topsoil dries before the subsoil as drought progresses. In such environments, plants with deeper roots are able to acquire water available in deeper soil domains that may not be available to plants with shallower roots (Ludlow and Muchow, 1990; Ho et al., 2005; Hammer et al., 2009). An ideotype has been proposed to guide the breeding of crops with deeper roots and, therefore, greater water acquisition from drying soil, called Steep, Cheap, and Deep, integrating architectural, anatomical, and physiological phenes (Lynch, 2013). The term Cheap denotes phenes that reduce the metabolic cost of soil exploration, which is an important limitation to the acquisition of scarce soil resources, including water in dry soil (Fan et al., 2003; Lynch, 2007b; Zhu et al., 2010; Postma and Lynch, 2011a, 2011b; Jaramillo et al., 2013). Plant resource allocation to root growth typically increases under drought to enhance water acquisition; therefore, the metabolic cost of root growth becomes a significant component of plant fitness and adaptation under drought (Lynch, 2007b, 2013). Therefore, a plant that is able to access water in deep soil domains at reduced metabolic cost will have superior productivity, because it will have more metabolic resources available for further resource acquisition, growth, and reproduction. Evidence in support of this hypothesis comes from empirical and modeling studies for maize (Zea mays) under water and edaphic stress (Lynch, 2007a; Zhu et al., 2010; Postma and Lynch, 2011a, 2011b; Jaramillo et al., 2013).Root cortical aerenchyma (RCA) is the enlarged air space in the root cortex that forms either through cell death or cell separation (Evans, 2004). RCA is associated with a disproportionate reduction of root respiration in maize by converting living cortical tissue to air volume (Fan et al., 2003; Zhu et al., 2010). Reduction of root metabolic costs permits more internal resources to be allocated to greater root growth and, consequently, greater soil resource acquisition. RCA formation is also associated with a reduction of phosphorus content in root tissue on a volume basis, since air spaces do not contain phosphorus (Fan et al., 2003), and with improved growth in low-phosphorus soil (Lynch, 2011). RCA also reduces the nitrogen content of root tissue and is beneficial for nitrogen capture and maize growth on low-nitrogen soils (Saengwilai, 2014a). Modeling studies suggest that RCA improves crop adaptation to suboptimal nutrient availability by reducing the metabolic costs of soil exploration (Postma and Lynch, 2011a, 2011b). Under drought, Zhu et al. (2010) found that maize genotypes with more RCA had five times greater biomass and eight times greater yield than genotypes with less RCA. Living cortical area (LCA) is total transverse root cortical area minus RCA area. Jaramillo et al. (2013) found that root respiration is positively correlated with LCA, and a 3.5-fold reduction in LCA is associated with a 2.5-fold improvement in plant growth under drought. These results indicate that the metabolic demand of living cortical tissue is a primary determinant of root growth, soil exploration, and resource acquisition in soil environments with suboptimal resource availability.This study builds on earlier studies indicating that substantial reduction of root metabolic cost is associated with variation in LCA. The cortex of the maize root is composed of several concentric layers of parenchyma cells, the number of which we refer to as the cortical cell file number (CCFN). Recently, Burton et al. (2013) reported that there is 3-fold variation for CCFN in Zea spp. In that study, the variation was wider in maize landraces (six to 16 cell files) than in wild Zea spp. (seven to 13 cell files). It has been proposed that reduced CCFN would decrease the metabolic costs of root growth and maintenance, in terms of both the carbon cost of root respiration and the nutrient content of living tissue, by reducing the proportion of root volume occupied by living cortical tissue, which has greater metabolic demands than the stele (Lynch, 2013). However, the physiological utility of CCFN has not been explored.The objective of this study was to test the hypothesis that reduced CCFN would reduce root respiration, permitting greater rooting depth, thereby enhancing water acquisition and improving both plant growth and yield under water stress.     

Root and leaf traits, water use and drought tolerance of maize genotypes

The main components of drought tolerance of six maize genotypes were studied to evaluate crop performance in water limiting environments: (1) the postponement of dehydration by reduced transpiration rate (TR) and an increased efficiency of water acquisition from soil; (2) the tolerance of dehydration by effective physiological water use. The aim was to describe the genotype dependent response to drought in leaf and root traits and water relations using data from controlled environment and field experiments, and using dynamic simulation by the Swedish Coup model. High genetic variation was detected in the root density, acquisition efficiency and water use among the genotypes. The female parent lines had the greatest TR with the smallest dry matter accumulation in water deficiency, whereas hybrids could acquire more water from dryer soil while maintaining a lower TR. Hybrid Mv 444 increased water potential more strongly in leaves than hybrid Norma. The postponement of dehydration was observed for Norma, while more tolerance to dehydration characterized Mv 444. Simulation was an effective tool for testing hypotheses considering water acquisition efficiency and for summarizing the results of the measurements in a formalized structure; it helped to quantify the dynamics of water availability and the impact of drought on the growth of the maize genotypes.     

Soil textures rather than root hairs dominate water uptake and soil–plant hydraulics under drought

Although the role of root hairs (RHs) in nutrient uptake is well documented, their role in water uptake and drought tolerance remains controversial. Maize (Zea mays) wild-type and its hair-defective mutant (Mut; roothairless 3) were grown in two contrasting soil textures (sand and loam). We used a root pressure chamber to measure the relation between transpiration rate (E) and leaf xylem water potential (ψ_{leaf_x}) during soil drying. Our hypotheses were: (1) RHs extend root–soil contact and reduce the ψ_{leaf_x} decline at high E in dry soils; (2) the impact of RHs is more pronounced in sand; and (3) Muts partly compensate for lacking RHs by producing longer and/or thicker roots. The ψ_{leaf_x}(E) relation was linear in wet conditions and became nonlinear as the soils dried. This nonlinearity occurred more abruptly and at less negative matric potentials in sand (ca. −10 kPa) than in loam (ca. −100 kPa). At more negative soil matric potentials, soil hydraulic conductance became smaller than root hydraulic conductance in both soils. Both genotypes exhibited 1.7 times longer roots in loam, but 1.6 times thicker roots in sand. No differences were observed in the ψ_{leaf_x}(E) relation and active root length between the two genotypes. In maize, RHs had a minor contribution to soil–plant hydraulics in both soils and their putative role in water uptake was smaller than that reported for barley (Hordeum vulgare). These results suggest that the role of RHs cannot be easily generalized across species and soil textures affect the response of root hydraulics to soil drying.

Root hairs of maize do not show evident contribution to root growth, water uptake, and soil–plant hydraulics, whereas soil textures affect the response of root hydraulics to soil drying.     

Changes in root system structure,leaf water potential and gas exchange of maize and triticale seedlings affected by soil compaction

The physiological reasons associated with differential sensitivity of C₃ and C₄ plant species to soil compaction stress are not well explained and understood. The responses of growth characteristics, changes in leaf water potential and gas exchange in maize and triticale to a different soil compaction were investigated. In the present study seedlings of triticale and maize, representative of C₃ and C₄ plants were subjected to low (L – 1.10 g cm⁻³), moderate (M – 1.34 g cm⁻³) and severe (S – 1.58 g cm⁻³) soil compaction level. Distinct differences in distribution of roots in the soil profile were observed. Plants of treatments M or S in comparison to treatment L, showed a decrease in leaf number, dry mass of stem, leaves and roots, and an increase in the shoot to root ratio. A drastic decrease in root biomass in M and S treatments in the soil profile on depth from 15 to 40 cm was observed. Any level of soil compaction did not influence the number of seminal and seminal-adventitious roots but decreased their length. The number and total length of nodal roots decreased with compaction. Changes of growth traits in M and S treatments in comparison to the L were greater for maize than for triticale and were accompanied by daily changes in water potential (ψ) and gas exchange parameters (P_N, E, g_s). Differences between M and S treatments in daily changes in ψ for maize were in most cases statistically insignificant, whereas for triticale, they were statistically significant. Differences in the responses of maize and triticale to soil compaction were found in P_N, E and g_s in particular for the measurements taken at 12:00 and 16:00. The highest correlation coefficients were obtained for the relationship between leaf water potential and stomatal conductance, both for maize and triticale, which indicates the close association between stomata behavior and changes in leaf water status.     

Morphological plasticity of wheat and barley roots in response to spatial variation in soil strength

Root systems of individual crop plants may encounter large variations in mechanical impedance to root penetration. Split-root experiments were conducted to compare the effects of spatial variation in soil strength on the morphological plasticity of wheat and barley roots, and its relationship to shoot growth. Plants of spring barley (Hordeum vulgare cv Prisma) and spring wheat (Triticum aestivum cv Alexandria) were grown for 12 days with their seminal roots divided between two halves of a cylinder packed with sandy loam soil. Three treatment combinations were imposed: loose soil where both halves of the cylinder were packed to 1.1 g cm^–3 (penetrometer resistance 0.3 MPa), dense soil where both halves were packed to 1.4 g cm^–3 (penetrometer resistance 1 MPa), and a split-root treatment where one half was packed to 1.1 and the other to 1.4 g cm^–3. In barley, uniform high soil strength restricted the extension of main seminal root axes more than laterals. In the split-root treatment, the length of laterals and the dry weight of main axes and laterals were increased in the loose soil half and reduced in the dense soil half compared with their respective loose and dense-soil controls. No such compensatory adjustments between main axis and laterals and between individual seminal roots were found in wheat. Variation in soil strength had no effect on the density of lateral roots (number per unit main axis length) in either barley or wheat. The nature and extent of wheat root plasticity in response to variation in soil strength was very different from that in response to changes in N-supply in previous experiments. In spite of the compensatory adjustments in growth between individual seminal roots of barley, the growth of barley shoots, as in wheat, was reduced when part of the root system was in compacted soil.     

Neutron imaging reveals internal plant water dynamics

Background and aims

Knowledge of plant water fluxes is critical for assessing mechanistic processes linked to biogeochemical cycles, yet resolving root water transport dynamics has been a particularly daunting task. Our objectives were to demonstrate the ability to non-invasively monitor individual root functionality and water fluxes within Zea mays L. (maize) and Panicum virgatum L. (switchgrass) seedlings using neutron imaging.

Methods

Seedlings were propagated for 1–3 weeks in aluminum chambers containing sand. Pulses of water or deuterium oxide were then tracked through the root systems by collecting consecutive radiographs during exposure to a cold-neutron source. Water flux was manipulated by cycling on a growth lamp to alter foliar demand for water.

Results

Neutron radiography readily illuminated root structure, root growth, and relative plant and soil water content. After irrigation there was rapid root water uptake from the newly wetted soil, followed by hydraulic redistribution of water through the root system to roots terminating in dry soil. Water flux within individual roots responded differentially to foliar illumination based on supply and demand of water within the root system.

Conclusions

Sub-millimeter scale image resolution revealed timing and magnitudes of root water uptake, redistribution within the roots, and root-shoot hydraulic linkages—relationships not well characterized by other techniques.