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1.  Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays) 
Annals of Botany  2013;113(1):181-189.
Background and Aims
Formation of root cortical aerenchyma (RCA) can be induced by nutrient deficiency. In species adapted to aerobic soil conditions, this response is adaptive by reducing root maintenance requirements, thereby permitting greater soil exploration. One trade-off of RCA formation may be reduced radial transport of nutrients due to reduction in living cortical tissue. To test this hypothesis, radial nutrient transport in intact roots of maize (Zea mays) was investigated in two radiolabelling experiments employing genotypes with contrasting RCA.
In the first experiment, time-course dynamics of phosphate loading into the xylem were measured from excised nodal roots that varied in RCA formation. In the second experiment, uptake of phosphate, calcium and sulphate was measured in seminal roots of intact young plants in which variation in RCA was induced by treatments altering ethylene action or genetic differences.
Key Results
In each of three paired genotype comparisons, the rate of phosphate exudation of high-RCA genotypes was significantly less than that of low-RCA genotypes. In the second experiment, radial nutrient transport of phosphate and calcium was negatively correlated with the extent of RCA for some genotypes.
The results support the hypothesis that RCA can reduce radial transport of some nutrients in some genotypes, which could be an important trade-off of this trait.
PMCID: PMC3864730  PMID: 24249807
Aerenchyma; radial transport; root; nutrient uptake; phosphorus; sulfur; calcium; maize; Zea mays
2.  Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems 
Annals of Botany  2013;112(2):347-357.
A hypothetical ideotype is presented to optimize water and N acquisition by maize root systems. The overall premise is that soil resource acquisition is optimized by the coincidence of root foraging and resource availability in time and space. Since water and nitrate enter deeper soil strata over time and are initially depleted in surface soil strata, root systems with rapid exploitation of deep soil would optimize water and N capture in most maize production environments.
• The ideotype Specific phenes that may contribute to rooting depth in maize include (a) a large diameter primary root with few but long laterals and tolerance of cold soil temperatures, (b) many seminal roots with shallow growth angles, small diameter, many laterals, and long root hairs, or as an alternative, an intermediate number of seminal roots with steep growth angles, large diameter, and few laterals coupled with abundant lateral branching of the initial crown roots, (c) an intermediate number of crown roots with steep growth angles, and few but long laterals, (d) one whorl of brace roots of high occupancy, having a growth angle that is slightly shallower than the growth angle for crown roots, with few but long laterals, (e) low cortical respiratory burden created by abundant cortical aerenchyma, large cortical cell size, an optimal number of cells per cortical file, and accelerated cortical senescence, (f) unresponsiveness of lateral branching to localized resource availability, and (g) low Km and high Vmax for nitrate uptake. Some elements of this ideotype have experimental support, others are hypothetical. Despite differences in N distribution between low-input and commercial maize production, this ideotype is applicable to low-input systems because of the importance of deep rooting for water acquisition. Many features of this ideotype are relevant to other cereal root systems and more generally to root systems of dicotyledonous crops.
PMCID: PMC3698384  PMID: 23328767
Root phenes; ideotype; water; nitrogen; architecture; anatomy
3.  Root cortical burden influences drought tolerance in maize 
Annals of Botany  2013;112(2):429-437.
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.
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.
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.
PMCID: PMC3698389  PMID: 23618897
Root; aerenchyma; respiration; drought; cortex; Zea mays
4.  Integration of root phenes for soil resource acquisition 
Suboptimal availability of water and nutrients is a primary limitation to plant growth in terrestrial ecosystems. The acquisition of soil resources by plant roots is therefore an important component of plant fitness and agricultural productivity. Plant root systems comprise a set of phenes, or traits, that interact. Phenes are the units of the plant phenotype, and phene states represent the variation in form and function a particular phene may take. Root phenes can be classified as affecting resource acquisition or utilization, influencing acquisition through exploration or exploitation, and in being metabolically influential or neutral. These classifications determine how one phene will interact with another phene, whether through foraging mechanisms or metabolic economics. Phenes that influence one another through foraging mechanisms are likely to operate within a phene module, a group of interacting phenes, that may be co-selected. Examples of root phene interactions discussed are: (1) root hair length × root hair density, (2) lateral branching × root cortical aerenchyma (RCA), (3) adventitious root number × adventitious root respiration and basal root growth angle (BRGA), (4) nodal root number × RCA, and (5) BRGA × root hair length and density. Progress in the study of phenes and phene interactions will be facilitated by employing simulation modeling and near-isophenic lines that allow the study of specific phenes and phene combinations within a common phenotypic background. Developing a robust understanding of the phenome at the organismal level will require new lines of inquiry into how phenotypic integration influences plant function in diverse environments. A better understanding of how root phenes interact to affect soil resource acquisition will be an important tool in the breeding of crops with superior stress tolerance and reduced dependence on intensive use of inputs.
PMCID: PMC3771073  PMID: 24062755
root architecture; phenomics; functional traits; ideotype; soil resources
5.  Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures 
Annals of Botany  2012;110(2):521-534.
Background and Aims
During their domestication, maize, bean and squash evolved in polycultures grown by small-scale farmers in the Americas. Polycultures often overyield on low-fertility soils, which are a primary production constraint in low-input agriculture. We hypothesized that root architectural differences among these crops causes niche complementarity and thereby greater nutrient acquisition than corresponding monocultures.
A functional–structural plant model, SimRoot, was used to simulate the first 40 d of growth of these crops in monoculture and polyculture and to determine the effects of root competition on nutrient uptake and biomass production of each plant on low-nitrogen, -phosphorus and -potassium soils.
Key Results
Squash, the earliest domesticated crop, was most sensitive to low soil fertility, while bean, the most recently domesticated crop, was least sensitive to low soil fertility. Nitrate uptake and biomass production were up to 7 % greater in the polycultures than in the monocultures, but only when root architecture was taken into account. Enhanced nitrogen capture in polycultures was independent of nitrogen fixation by bean. Root competition had negligible effects on phosphorus or potassium uptake or biomass production.
We conclude that spatial niche differentiation caused by differences in root architecture allows polycultures to overyield when plants are competing for mobile soil resources. However, direct competition for immobile resources might be negligible in agricultural systems. Interspecies root spacing may also be too large to allow maize to benefit from root exudates of bean or squash. Above-ground competition for light, however, may have strong feedbacks on root foraging for immobile nutrients, which may increase cereal growth more than it will decrease the growth of the other crops. We note that the order of domestication of crops correlates with increasing nutrient efficiency, rather than production potential.
PMCID: PMC3394648  PMID: 22523423
‘Three sisters’; polyculture; root architecture; SimRoot; functional–structural model; nutrient deficiency; maize; bean; squash; niche complementarity; root competition
6.  New roots for agriculture: exploiting the root phenome 
Recent advances in root biology are making it possible to genetically design root systems with enhanced soil exploration and resource capture. These cultivars would have substantial value for improving food security in developing nations, where yields are limited by drought and low soil fertility, and would enhance the sustainability of intensive agriculture. Many of the phenes controlling soil resource capture are related to root architecture. We propose that a better understanding of the root phenome is needed to effectively translate genetic advances into improved crop cultivars. Elementary, unique root phenes need to be identified. We need to understand the ‘fitness landscape’ for these phenes: how they affect crop performance in an array of environments and phenotypes. Finally, we need to develop methods to measure phene expression rapidly and economically without artefacts. These challenges, especially mapping the fitness landscape, are non-trivial, and may warrant new research and training modalities.
PMCID: PMC3321693  PMID: 22527403
root architecture; phenome; plant breeding
7.  Optimizing reproductive phenology in a two-resource world: a dynamic allocation model of plant growth predicts later reproduction in phosphorus-limited plants 
Annals of Botany  2011;108(2):391-404.
Background and Aims
Timing of reproduction is a key life-history trait that is regulated by resource availability. Delayed reproduction in soils with low phosphorus availability is common among annuals, in contrast to the accelerated reproduction typical of other low-nutrient environments. It is hypothesized that this anomalous response arises from the high marginal value of additional allocation to root growth caused by the low mobility of phosphorus in soils.
To better understand the benefits and costs of such delayed reproduction, a two-resource dynamic allocation model of plant growth and reproduction is presented. The model incorporates growth, respiration, and carbon and phosphorus acquisition of both root and shoot tissue, and considers the reallocation of resources from senescent leaves. The model is parameterized with data from Arabidopsis and the optimal reproductive phenology is explored in a range of environments.
Key Results
The model predicts delayed reproduction in low-phosphorus environments. Reproductive timing in low-phosphorus environments is quite sensitive to phosphorus mobility, but is less sensitive to the temporal distribution of mortality risks. In low-phosphorus environments, the relative metabolic cost of roots was greater, and reproductive allocation reduced, compared with high-phosphorus conditions. The model suggests that delayed reproduction in response to low phosphorus availability may be reduced in plants adapted to environments where phosphorus mobility is greater.
Delayed reproduction in low-phosphorus soils can be a beneficial response allowing for increased acquisition and utilization of phosphorus. This finding has implications both for efforts to breed crops for low-phosphorus soils, and for efforts to understand how climate change may impact plant growth and productivity in low-phosphorus environments.
PMCID: PMC3143053  PMID: 21712299
Dynamic allocation budget; optimization; Arabidopsis thaliana; flowering phenology; root–shoot partitioning; phosphorus availability
8.  Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability 
Annals of Botany  2010;107(5):829-841.
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.
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.
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.
PMCID: PMC3077978  PMID: 20971728
Zea mays; Phaseolus vulgaris; root cortical aerenchyma; phosphorus deficiency; SimRoot; functional structural modelling; carbon economy
9.  Assessment of Inequality of Root Hair Density in Arabidopsis thaliana using the Gini Coefficient: a Close Look at the Effect of Phosphorus and its Interaction with Ethylene 
Annals of Botany  2004;95(2):287-293.
• Background and Aims Root hair density (i.e. the number of root hairs per unit root length) in Arabidopsis thaliana varies among individual plants in response to different nutrient stresses. The degree of such variation, defined as inequality, serves as a unique indicator of the uniformity of response within a plant population to nutrient availability.
• Methods Using the Gini coefficient (G) as an inequality index, the inequality of root hair density in Arabidopsis thaliana ‘Columbia’ was evaluated under conditions of nutrient stresses; in particular the effect of phosphorus and its interaction with ethylene.
• Key Results With decreasing phosphorus concentration, root hair density increased while inequality decreased logarithmically. The addition of the ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC) under high phosphorus increased root hair density and decreased inequality by 7-fold. Inhibition of ethylene action with 1-methylcyclopropene (MCP) and silver thiosulphate (STS) under low phosphorus decreased root hair density, and increased inequality by 9-fold and 4-fold, respectively. The ethylene action inhibitors had little effect on root hair density under high phosphorus, but inequality increased 3-fold in the presence of MCP and decreased 2-fold in the presence of STS. Compared with the control, deficiencies in S, N and K increased inequality of root hair density, whereas deficiencies in P, Ca, B, Mn, Fe, Zn, Cu and Mg decreased inequality. In particular, the inequality of root hair density increased by over 2-fold under deficiencies of N or K, but decreased 14-fold under phosphorus deficiency.
• Conclusions The inequality analysis indicates a strong correlation between prevalent signals from the environment (i.e. phosphorus stress) and the response of the plant, and the role of ethylene in this response. As the environmental signals become stronger, an increasing proportion of individuals respond, resulting in a decrease in variation in responsiveness among individual plants as indicated by reduced inequality.
PMCID: PMC4246827  PMID: 15546931
Arabidopsis thaliana; root hairs; nutrient deficiencies; phosphorus; ethylene; Gini coefficient; inequality; Lorenz curve
10.  Modelling Applicability of Fractal Analysis to Efficiency of Soil Exploration by Roots 
Annals of Botany  2004;94(1):119-128.
• Background and Aims Fractal analysis allows calculation of fractal dimension, fractal abundance and lacunarity. Fractal analysis of plant roots has revealed correlations of fractal dimension with age, topology or genotypic variation, while fractal abundance has been associated with root length. Lacunarity is associated with heterogeneity of distribution, and has yet to be utilized in analysis of roots. In this study, fractal analysis was applied to the study of root architecture and acquisition of diffusion‐limited nutrients. The hypothesis that soil depletion and root competition are more closely correlated with a combination of fractal parameters than by any one alone was tested.
• Model The geometric simulation model SimRoot was used to dynamically model roots of various architectures growing for up to 16 d in three soil types with contrasting nutrient mobility. Fractal parameters were calculated for whole roots, projections of roots and vertical slices of roots taken at 0, 2·5 and 5 cm from the root origin. Nutrient depletion volumes, competition volumes, and relative competition were regressed against fractal parameters and root length.
• Key Results Root length was correlated with depletion volume, competition volume and relative competition at all times. In analysis of three‐dimensional, projected roots and 0 cm slices, log(fractal abundance) was highly correlated with log(depletion volume) when times were pooled. Other than this, multiple regression yielded better correlations than regression with single fractal parameters. Correlations decreased with age of roots and distance of vertical slices from the root origin. Field data were also examined to see if fractal dimension, fractal abundance and lacunarity can be used to distinguish common bean genotypes in field situations. There were significant differences in fractal dimension and fractal abundance, but not in lacunarity.
• Conclusions These results suggest that applying fractal analysis to research of soil exploration by root systems should include fractal abundance, and possibly lacunarity, along with fractal dimension.
PMCID: PMC4242372  PMID: 15145791
Fractal dimension; fractal abundance; lacunarity; phosphorus; depletion; competition; Phaseolus vulgaris; SimRoot; simulation modelling

Results 1-10 (10)