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1.  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
2.  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
3.  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
4.  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
5.  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
6.  Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris) 
Annals of Botany  2013;112(6):973-982.
Background and Aims
Root architectural phenes enhancing topsoil foraging are important for phosphorus acquisition. In this study, the utility of a novel phene is described, basal root whorl number (BRWN), that has significant effects on topsoil foraging in common bean (Phaseolus vulgaris).
Whorls are defined as distinct tiers of basal roots that emerge in a tetrarch fashion along the base of the hypocotyl. Wild and domesticated bean taxa as well as two recombinant inbred line (RIL) populations were screened for BRWN and basal root number (BRN). A set of six RILs contrasting for BRWN was evaluated for performance under low phosphorus availability in the greenhouse and in the field. In the greenhouse, plants were grown in a sand–soil media with low or high phosphorus availability. In the field, plants were grown in an Oxisol in Mozambique under low and moderate phosphorus availability.
Key Results
Wild bean accessions tended to have a BRWN of one or two, whereas cultivated accessions had BRWN reaching four and sometimes five. BRWN and BRN did not vary with phosphorus availability, i.e. BRWN was not a plastic trait in these genotypes. Greater BRWN was beneficial for phosphorus acquisition in low phosphorus soil. Genotypes with three whorls had almost twice the shoot biomass, greater root length and greater leaf area than related genotypes with two whorls. In low phosphorus soil, shoot phosphorus content was strongly correlated with BRWN (R2 = 0·64 in the greenhouse and R2 = 0·88 in the field). Genotypes with three whorls had shallower root systems with a greater range of basal root growth angles (from 10 to 45 ° from horizontal) than genotypes with two whorls (angles ranged from 60 to 85 ° from horizontal).
The results indicate that BRWN is associated with increased phosphorus acquisition and that this trait may have value for selection of genotypes with better performance in low phosphorus soils.
PMCID: PMC3783229  PMID: 23925972
Basal root whorls; phosphorus acquistion; common bean; Phaseolus vulgaris; root architecture
7.  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
8.  Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems 
Annals of Botany  2012;110(2):329-348.
Carboxylate-releasing cluster roots of Proteaceae play a key role in acquiring phosphorus (P) from ancient nutrient-impoverished soils in Australia. However, cluster roots are also found in Proteaceae on young, P-rich soils in Chile where they allow P acquisition from soils that strongly sorb P.
Unlike Proteaceae in Australia that tend to proficiently remobilize P from senescent leaves, Chilean Proteaceae produce leaf litter rich in P. Consequently, they may act as ecosystem engineers, providing P for plants without specialized roots to access sorbed P. We propose a similar ecosystem-engineering role for species that release large amounts of carboxylates in other relatively young, strongly P-sorbing substrates, e.g. young acidic volcanic deposits and calcareous dunes. Many of these species also fix atmospheric nitrogen and release nutrient-rich litter, but their role as ecosystem engineers is commonly ascribed only to their diazotrophic nature.
We propose that the P-mobilizing capacity of Proteaceae on young soils, which contain an abundance of P, but where P is poorly available, in combination with inefficient nutrient remobilization from senescing leaves allows these species to function as ecosystem engineers. We suggest that diazotrophic species that colonize young soils with strong P-sorption potential should be considered for their positive effect on P availability, as well as their widely accepted role in nitrogen fixation. Their P-mobilizing activity possibly also enhances their nitrogen-fixing capacity. These diazotrophic species may therefore facilitate the establishment and growth of species with less-efficient P-uptake strategies on more-developed soils with low P availability through similar mechanisms. We argue that the significance of cluster roots and high carboxylate exudation in the development of young ecosystems is probably far more important than has been envisaged thus far.
PMCID: PMC3394658  PMID: 22700940
Actinorhizal species; carboxylates; cluster roots; phosphorus nutrition; Cyperaceae; ecosystem engineering; facilitation; Lupinus; Proteaceae
9.  Overexpression of Thellungiella halophila H+-pyrophosphatase Gene Improves Low Phosphate Tolerance in Maize 
PLoS ONE  2012;7(8):e43501.
Low phosphate availability is a major constraint on plant growth and agricultural productivity. Engineering a crop with enhanced low phosphate tolerance by transgenic technique could be one way of alleviating agricultural losses due to phosphate deficiency. In this study, we reported that transgenic maize plants that overexpressed the Thellungiella halophila vacuolar H+-pyrophosphatase gene (TsVP) were more tolerant to phosphate deficit stress than the wild type. Under phosphate sufficient conditions, transgenic plants showed more vigorous root growth than the wild type. When phosphate deficit stress was imposed, they also developed more robust root systems than the wild type, this advantage facilitated phosphate uptake, which meant that transgenic plants accumulated more phosphorus. So the growth and development in the transgenic maize plants were not damaged as much as in the wild type plants under phosphate limitation. Overexpression of TsVP increased the expression of genes involved in auxin transport, which indicated that the development of larger root systems in transgenic plants might be due in part to enhanced auxin transport which controls developmental events in plants. Moreover, transgenic plants showed less reproductive development retardation and a higher grain yield per plant than the wild type plants when grown in a low phosphate soil. The phenotypes of transgenic maize plants suggested that the overexpression of TsVP led to larger root systems that allowed transgenic maize plants to take up more phosphate, which led to less injury and better performance than the wild type under phosphate deficiency conditions. This study describes a feasible strategy for improving low phosphate tolerance in maize and reducing agricultural losses caused by phosphate deficit stress.
PMCID: PMC3431357  PMID: 22952696
10.  Chinese Tallow Trees (Triadica sebifera) from the Invasive Range Outperform Those from the Native Range with an Active Soil Community or Phosphorus Fertilization 
PLoS ONE  2013;8(9):e74233.
Two mechanisms that have been proposed to explain success of invasive plants are unusual biotic interactions, such as enemy release or enhanced mutualisms, and increased resource availability. However, while these mechanisms are usually considered separately, both may be involved in successful invasions. Biotic interactions may be positive or negative and may interact with nutritional resources in determining invasion success. In addition, the effects of different nutrients on invasions may vary. Finally, genetic variation in traits between populations located in introduced versus native ranges may be important for biotic interactions and/or resource use. Here, we investigated the roles of soil biota, resource availability, and plant genetic variation using seedlings of Triadica sebifera in an experiment in the native range (China). We manipulated nitrogen (control or 4 g/m2), phosphorus (control or 0.5 g/m2), soil biota (untreated or sterilized field soil), and plant origin (4 populations from the invasive range, 4 populations from the native range) in a full factorial experiment. Phosphorus addition increased root, stem, and leaf masses. Leaf mass and height growth depended on population origin and soil sterilization. Invasive populations had higher leaf mass and growth rates than native populations did in fresh soil but they had lower, comparable leaf mass and growth rates in sterilized soil. Invasive populations had higher growth rates with phosphorus addition but native ones did not. Soil sterilization decreased specific leaf area in both native and exotic populations. Negative effects of soil sterilization suggest that soil pathogens may not be as important as soil mutualists for T. sebifera performance. Moreover, interactive effects of sterilization and origin suggest that invasive T. sebifera may have evolved more beneficial relationships with the soil biota. Overall, seedlings from the invasive range outperformed those from the native range, however, an absence of soil biota or low phosphorus removed this advantage.
PMCID: PMC3759475  PMID: 24023930
11.  Waterlogging-induced changes in root architecture of germplasm accessions of the tropical forage grass Brachiaria humidicola 
AoB Plants  2014;6:plu017.
Brachiaria humidicola, a tropical forage grass, develops aerenchyma in nodal roots to adapt to waterlogging. A large body of work has focused on the functional role of aerenchyma in nodal roots under waterlogged soil conditions. On the other hand, quantification of responses of lateral roots to waterlogging has been often overlooked in past work. Our data indicated that although waterlogging reduced the overall proportion of lateral roots, its proportion significantly increased in the top 10 cm of the soil. This suggests that soil flooding increases lateral root proliferation of B. humidicola in upper soil layers. This may compensate the reduction of root surface area brought by the restriction of root growth at depths below 30 cm into waterlogged soil.
Waterlogging is one of the major factors limiting the productivity of pastures in the humid tropics. Brachiaria humidicola is a forage grass commonly used in zones prone to temporary waterlogging. Brachiaria humidicola accessions adapt to waterlogging by increasing aerenchyma in nodal roots above constitutive levels to improve oxygenation of root tissues. In some accessions, waterlogging reduces the number of lateral roots developed from main root axes. Waterlogging-induced reduction of lateral roots could be of adaptive value as lateral roots consume oxygen supplied from above ground via their parent root. However, a reduction in lateral root development could also be detrimental by decreasing the surface area for nutrient and water absorption. To examine the impact of waterlogging on lateral root development, an outdoor study was conducted to test differences in vertical root distribution (in terms of dry mass and length) and the proportion of lateral roots to the total root system (sum of nodal and lateral roots) down the soil profile under drained or waterlogged soil conditions. Plant material consisted of 12 B. humidicola accessions from the gene bank of the International Center for Tropical Agriculture, Colombia. Rooting depth was restricted by 21 days of waterlogging and confined to the first 30 cm below the soil surface. Although waterlogging reduced the overall proportion of lateral roots, its proportion significantly increased in the top 10 cm of the soil. This suggests that soil flooding increases lateral root proliferation of B. humidicola in the upper soil layers. This may compensate for the reduction of root surface area brought about by the restriction of root growth at depths below 30 cm. Further work is needed to test the relative efficiency of nodal and lateral roots for nutrient and water uptake under waterlogged soil conditions.
PMCID: PMC4038435  PMID: 24876299
Lateral root proportion; oxygen deficiency; rooting depth; root length; soil flooding; vertical root distribution.
12.  Microbial phytases in phosphorus acquisition and plant growth promotion 
Phosphorus (P) is one of the major constituents in energy metabolism and biosynthesis of nucleic acids and cell membranes with an important role in regulation of a number of enzymes. Soil phosphorous is an important macronutrient for plant growth. Phosphorus deficiency in soil is a major problem for agricultural production. Total soil P occurs in either organic or in organic form. Phytic acid as phytate (salts of phytic acid) is the major form of organic phosphorus in soil and it is not readily available to plants as a source of phosphorus because it either forms a complex with cations or adsorbs to various soil components. Phosphate solubilizing microorganisms are ubiquitous in soils and could play an important role in supplying P to plants. Microorganisms utilizing phytate are found in cultivated soils as well as in wetland, grassland and forest soils. Various fungi and bacteria (including plant growth promoting rhizobacteria) hydrolyze this organic form of phosphorus secreting phosphatases such as phytases and acidic/alkaline phosphatases. A large number of transgenic plants have been developed which were able to utilize sodium phytate as sole source of phosphorus. However, the recombinant phytases were similar to their wild type counterparts in terms of their properties. Increased phytase/phosphatase activity in transgenic plants may be an effective approach to promote their phytate-phosphorus utilization. The extracellular phytase activity of transgenic plant roots is a significant factor in the utilization of phosphorus from phytate. Furthermore, this indicated that an opportunity exists for using gene technology to improve the ability of plants to utilize accumulated forms of soil organic phosphorus. This review is focused on the role of phytases and phytase producing microbes in promoting the growth of different plants.
PMCID: PMC3550544  PMID: 23572999
Phytase; Phytate; Plant growth promoting rhizobacteria; Organic phosphorus; Plant growth promotion; Transgenics
13.  Antisense Inhibition of Rubisco Activase Increases Rubisco Content and Alters the Proportion of Rubisco Activase in Stroma and Thylakoids in Chloroplasts of Rice Leaves 
Annals of Botany  2006;97(5):739-744.
• Background and Aims Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase (RCA) is a nuclear-encoded chloroplast protein that modifies the conformation of Rubisco, releases inhibitors from active sites, and increases enzymatic activity. It appears to have other functions, e.g. in gibberellin signalling and as a molecular chaperone, which are related to its distribution within the chloroplast. The aim of this research was to resolve uncertainty about the localization of RCA, and to determine whether the distributions of Rubisco and RCA were altered when RCA content was reduced. The monocotyledon, Oryza sativa was used as a model species.
• Methods Gas exchange and Rubisco were measured, and the sub-cellular locations of Rubisco and RCA were determined using immunogold-labelling electron microscopy, in wild-type and antisense rca rice plants.
• Key Results In antisense rca plants, net photosynthetic rate and the initial Rubisco activity decreased much less than RCA content. Immunocytolocalization showed that Rubisco in wild-type and antisense plants was localized in the stroma of chloroplasts. However, the amount of Rubisco in the antisense rca plants was greater than in the wild-type plants. RCA was detected in both the chloroplast stroma and in the thylakoid membranes of wild-type plants. The percentage of RCA labelling in the thylakoid membrane was shown to be substantially decreased, while the fraction in the stroma was increased, by the antisense rca treatment.
• Conclusions From the changes in RCA distribution and alterations in Rubisco activity, RCA in the stroma of the chloroplast probably contributes to the activation of Rubisco, and RCA in thylakoids compensates for the reduction of RCA in the stroma, allowing steady-state photosynthesis to be maintained when RCA is depleted. RCA may also have a second role in protecting membranes against environmental stresses as a chaperone.
PMCID: PMC2803410  PMID: 16478766
Antisense rca rice plants; Rubisco; Rubisco activase (RCA); cellular localization
14.  Training health care professionals in root cause analysis: a cross-sectional study of post-training experiences, benefits and attitudes 
Root cause analysis (RCA) originated in the manufacturing engineering sector but has been adapted for routine use in healthcare to investigate patient safety incidents and facilitate organizational learning. Despite the limitations of the RCA evidence base, healthcare authorities and decision makers in NHS Scotland – similar to those internationally - have invested heavily in developing training programmes to build local capacity and capability, and this is a cornerstone of many organizational policies for investigating safety-critical issues. However, to our knowledge there has been no systematic attempt to follow-up and evaluate post-training experiences of RCA-trained staff in Scotland. Given the significant investment in people, time and funding we aimed to capture and learn from the reported experiences, benefits and attitudes of RCA-trained staff and the perceived impact on healthcare systems and safety.
We adapted a questionnaire used in a published Australian research study to undertake a cross sectional online survey of health care professionals (e.g. nursing & midwifery, medical doctors and pharmacists) formally trained in RCA by a single territorial health board region in NHS Scotland.
A total of 228/469 of invited staff completed the survey (48%). A majority of respondents had yet to participate in a post-training RCA investigation (n=127, 55.7%). Of RCA-experience staff, 71 had assumed a lead investigator role (70.3%) on one or more occasions. A clear majority indicated that their improvement recommendations were generally or partly implemented (82%). The top three barriers to RCA success were cited as: lack of time (54.6%), unwilling colleagues (34%) and inter-professional differences (31%). Differences in agreement levels between RCA-experienced and inexperienced respondents were noted on whether a follow-up session would be beneficial after conducting RCA (65.3% v 39.4%) and if peer feedback on RCA reports would be of educational value (83.2% v 37.0%). Comparisons with the previous research highlighted significant differences such as less reported difficulties within RCA teams (P<0.001) and a greater proportion of respondents taking on RCA leadership roles in this study (P<0.001).
This study adds to our knowledge and understanding of the need to improve the effectiveness of RCA training and frontline practices in healthcare settings. The overall evidence points to a potential organisational learning need to provide RCA-trained staff with continuous development opportunities and performance feedback. Healthcare authorities may wish to look more critically at whom they train in RCA, and how this is delivered and supported educationally to maximize cost-benefits, organizational learning and safer patient care.
PMCID: PMC3574857  PMID: 23391260
15.  Trees, soils, and food security 
Trees have a different impact on soil properties than annual crops, because of their longer residence time, larger biomass accumulation, and longer-lasting, more extensive root systems. In natural forests nutrients are efficiently cycled with very small inputs and outputs from the system. In most agricultural systems the opposite happens. Agroforestry encompasses the continuum between these extremes, and emerging hard data is showing that successful agroforestry systems increase nutrient inputs, enhance internal flows, decrease nutrient losses and provide environmental benefits: when the competition for growth resources between the tree and the crop component is well managed. The three main determinants for overcoming rural poverty in Africa are (i) reversing soil fertility depletion, (ii) intensifying and diversifying land use with high-value products, and (iii) providing an enabling policy environment for the smallholder farming sector. Agroforestry practices can improve food production in a sustainable way through their contribution to soil fertility replenishment. The use of organic inputs as a source of biologically-fixed nitrogen, together with deep nitrate that is captured by trees, plays a major role in nitrogen replenishment. The combination of commercial phosphorus fertilizers with available organic resources may be the key to increasing and sustaining phosphorus capital. High-value trees, 'Cinderella' species, can fit in specific niches on farms, thereby making the system ecologically stable and more rewarding economically, in addition to diversifying and increasing rural incomes and improving food security. In the most heavily populated areas of East Africa, where farm size is extremely small, the number of trees on farms is increasing as farmers seek to reduce labour demands, compatible with the drift of some members of the family into the towns to earn off-farm income. Contrary to the concept that population pressure promotes deforestation, there is evidence that demonstrates that there are conditions under which increasing tree planting is occurring on farms in the tropics through successful agroforestry as human population density increases.
PMCID: PMC1691986
Agroforestry Systems Soil Fertility Food Security Tree Domestication Environmental Benefits Enabling Policy Environment
16.  Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding 
Annals of Botany  2012;112(2):331-345.
Rice is the world's most important cereal crop and phosphorus (P) and zinc (Zn) deficiency are major constraints to its production. Where fertilizer is applied to overcome these nutritional constraints it comes at substantial cost to farmers and the efficiency of fertilizer use is low. Breeding crops that are efficient at acquiring P and Zn from native soil reserves or fertilizer sources has been advocated as a cost-effective solution, but would benefit from knowledge of genes and mechanisms that confer enhanced uptake of these nutrients by roots.
This review discusses root traits that have been linked to P and Zn uptake in rice, including traits that increase mobilization of P/Zn from soils, increase the volume of soil explored by roots or root surface area to recapture solubilized nutrients, enhance the rate of P/Zn uptake across the root membrane, and whole-plant traits that affect root growth and nutrient capture. In particular, this review focuses on the potential for these traits to be exploited through breeding programmes to produce nutrient-efficient crop cultivars.
Few root traits have so far been used successfully in plant breeding for enhanced P and Zn uptake in rice or any other crop. Insufficient genotypic variation for traits or the failure to enhance nutrient uptake under realistic field conditions are likely reasons for the limited success. More emphasis is needed on field studies in mapping populations or association panels to identify those traits and underlying genes that are able to enhance nutrient acquisition beyond the level already present in most cultivars.
PMCID: PMC3698374  PMID: 23071218
Adventitious roots; deoxymugineic acid; marker-assisted selection; nutrient-use efficiency; phosphorus transporters; phosphorus uptake; zinc uptake; low-molecular-weight organic acids; radial oxygen loss; radical oxygen stress; root hairs; quantitative trait loci; QTL
17.  Responses of root architecture development to low phosphorus availability: a review 
Annals of Botany  2012;112(2):391-408.
Phosphorus (P) is an essential element for plant growth and development but it is often a limiting nutrient in soils. Hence, P acquisition from soil by plant roots is a subject of considerable interest in agriculture, ecology and plant root biology. Root architecture, with its shape and structured development, can be considered as an evolutionary response to scarcity of resources.
This review discusses the significance of root architecture development in response to low P availability and its beneficial effects on alleviation of P stress. It also focuses on recent progress in unravelling cellular, physiological and molecular mechanisms in root developmental adaptation to P starvation. The progress in a more detailed understanding of these mechanisms might be used for developing strategies that build upon the observed explorative behaviour of plant roots.
The role of root architecture in alleviation of P stress is well documented. However, this paper describes how plants adjust their root architecture to low-P conditions through inhibition of primary root growth, promotion of lateral root growth, enhancement of root hair development and cluster root formation, which all promote P acquisition by plants. The mechanisms for activating alterations in root architecture in response to P deprivation depend on changes in the localized P concentration, and transport of or sensitivity to growth regulators such as sugars, auxins, ethylene, cytokinins, nitric oxide (NO), reactive oxygen species (ROS) and abscisic acid (ABA). In the process, many genes are activated, which in turn trigger changes in molecular, physiological and cellular processes. As a result, root architecture is modified, allowing plants to adapt effectively to the low-P environment. This review provides a framework for understanding how P deficiency alters root architecture, with a focus on integrated physiological and molecular signalling.
PMCID: PMC3698383  PMID: 23267006
Low phosphate; phosphorus acquisition; primary root; lateral root; root hair; cluster root; sugars; auxins; ethylene; cytokinins; nitric oxide; reactive oxygen species
18.  Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone 
BMC Plant Biology  2012;12:89.
Phosphorus (P) is an essential macronutrient for all living organisms. Maize (Zea mays) is an important human food, animal feed and energy crop throughout the world, and enormous quantities of phosphate fertilizer are required for maize cultivation. Thus, it is important to improve the efficiency of the use of phosphate fertilizer for maize.
In this study, we analyzed the maize root response to phosphate starvation and performed a transcriptomic analysis of the 1.0-1.5 cm lateral root primordium zone. In the growth of plants, the root-to-shoot ratio (R/L) was reduced in both low-phosphate (LP) and sufficient-phosphate (SP) solutions, but the ratio (R/L) exhibited by the plants in the LP solution was higher than that of the SP plants. The growth of primary roots was slightly promoted after 6 days of phosphate starvation, whereas the numbers of lateral roots and lateral root primordia were significantly reduced, and these differences were increased when associated with the stress caused by phosphate starvation. Among the results of a transcriptomic analysis of the maize lateral root primordium zone, there were two highlights: 1) auxin signaling participated in the response and the modification of root morphology under low-phosphate conditions, which may occur via local concentration changes due to the biosynthesis and transport of auxin, and LOB domain proteins may be an intermediary between auxin signaling and root morphology; and 2) the observed retardation of lateral root development was the result of co-regulation of DNA replication, transcription, protein synthesis and degradation and cell growth.
These results indicated that maize roots show a different growth pattern than Arabidopsis under low-phosphate conditions, as the latter species has been observed to halt primary root growth when the root tip comes into contact with low-phosphate media. Moreover, our findings enrich our understanding of plant responses to phosphate deficits and of root morphogenesis in maize.
PMCID: PMC3463438  PMID: 22704465
Maize; Phosphate starvation; Root development; Transcriptomic analysis
19.  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
20.  Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils 
SpringerPlus  2013;2:587.
Phosphorus is the second important key element after nitrogen as a mineral nutrient in terms of quantitative plant requirement. Although abundant in soils, in both organic and inorganic forms, its availability is restricted as it occurs mostly in insoluble forms. The P content in average soil is about 0.05% (w/w) but only 0.1% of the total P is available to plant because of poor solubility and its fixation in soil (Illmer and Schinner, Soil Biol Biochem 27:257-263, 1995). An adequate supply of phosphorus during early phases of plant development is important for laying down the primordia of plant reproductive parts. It plays significant role in increasing root ramification and strength thereby imparting vitality and disease resistance capacity to plant. It also helps in seed formation and in early maturation of crops like cereals and legumes. Poor availability or deficiency of phosphorus (P) markedly reduces plant size and growth. Phosphorus accounts about 0.2 - 0.8% of the plant dry weight.
To satisfy crop nutritional requirements, P is usually added to soil as chemical P fertilizer, however synthesis of chemical P fertilizer is highly energy intensive processes, and has long term impacts on the environment in terms of eutrophication, soil fertilility depletion, carbon footprint. Moreover, plants can use only a small amount of this P since 75–90% of added P is precipitated by metal–cation complexes, and rapidly becomes fixed in soils. Such environmental concerns have led to the search for sustainable way of P nutrition of crops. In this regards phosphate-solubilizing microorganisms (PSM) have been seen as best eco-friendly means for P nutrition of crop. Although, several bacterial (pseudomonads and bacilli) and fungal strains (Aspergilli and Penicillium) have been identified as PSM their performance under in situ conditions is not reliable and therefore needs to be improved by using either genetically modified strains or co-inoculation techniques. This review focuses on the diversity of PSM, mechanism of P solubilization, role of various phosphatases, impact of various factors on P solubilization, the present and future scenario of their use and potential for application of this knowledge in managing a sustainable environmental system.
PMCID: PMC4320215
Soil phosphorus; PSM; P solubilization; Biodiversity; Biofertilizers
21.  Nitrogen regulation of transpiration controls mass-flow acquisition of nutrients 
Journal of Experimental Botany  2013;65(1):159-168.
To test whether N regulates transpiration, Phaseolus vulgaris was grown with N placed at one of six distances behind a root-impenetrable mesh whilst control plants intercepted the N-source. N-availability regulated transpiration-driven mass-flow of nutrients from soil zones that were inaccessible
Transpiration may enhance mass-flow of nutrients to roots, especially in low-nutrient soils or where the root system is not extensively developed. Previous work suggested that nitrogen (N) may regulate mass-flow of nutrients. Experiments were conducted to determine whether N regulates water fluxes, and whether this regulation has a functional role in controlling the mass-flow of nutrients to roots. Phaseolus vulgaris were grown in troughs designed to create an N availability gradient by restricting roots from intercepting a slow-release N source, which was placed at one of six distances behind a 25 μm mesh from which nutrients could move by diffusion or mass-flow (termed ‘mass-flow’ treatment). Control plants had the N source supplied directly to their root zone so that N was available through interception, mass-flow, and diffusion (termed ‘interception’ treatment). ‘Mass-flow’ plants closest to the N source exhibited 2.9-fold higher transpiration (E), 2.6-fold higher stomatal conductance (g s), 1.2-fold higher intercellular [CO2] (C i), and 3.4-fold lower water use efficiency than ‘interception’ plants, despite comparable values of photosynthetic rate (A). E, g s, and C i first increased and then decreased with increasing distance from the N source to values even lower than those of ‘interception’ plants. ‘Mass-flow’ plants accumulated phosphorus and potassium, and had maximum concentrations at 10mm from the N source. Overall, N availability regulated transpiration-driven mass-flow of nutrients from substrate zones that were inaccessible to roots. Thus when water is available, mass-flow may partially substitute for root density in providing access to nutrients without incurring the costs of root extension, although the efficacy of mass-flow also depends on soil nutrient retention and hydraulic properties.
PMCID: PMC3883293  PMID: 24231035
Interception; phosphate; potassium; urea; water flux; water use efficiency.
22.  Phosphate solubilizers enhance NPK fertilizer use efficiency in rice and legume cultivation 
3 Biotech  2011;1(4):227-238.
It has been reported that phosphate solubilizing bacteria (PSB) are the most promising bacteria among the plant growth promoting rhizobacteria (PGPR); which may be used as biofertilizers for plant growth and nutrient use efficiency. Moreover, these soil micro-organisms play a significant role in regulating the dynamics of organic matter decomposition and the availability of plant nutrients such as nitrogen (N), phosphorus (P), potassium (K) and other nutrients. Through this study, the management of nutrient use efficiency by the application of PSB was targeted in order to make the applied nutrients more available to the plants in the rice (Oryza sativa) and yardlong bean (Vigna unguiculata) cultivation. Results have shown that the treatments with PSB alone or in the form of consortia of compatible strains with or without the external application of chemical NPK gave more germination index (G. I.) from 2.5 to 5 in rice and 2.7 to 4.8 in bean seeds. They also showed a higher growth in both shoot and root length and a higher biomass as compared to the control. This gives us an idea about the potentiality of these PSB strains and their application in rice and yardlong bean cultivation to get a better harvest index. Their use will also possibly reduce the nutrient runoff or leaching and increase in the use efficiency of the applied fertilizers. Thus, we can conclude that the NPK uptake and management can be improved by the use of PSB in rice and yardlong bean cultivation, and their application may be much more beneficial in the agricultural field.
PMCID: PMC3339586  PMID: 22558541
Fertilizer; Phosphate solubilizing bacteria; Oryza sativa; Vigna unguiculata; Germination index; Plant growth; Chemistry; Stem Cells; Biotechnology; Biomaterials; Agriculture; Bioinformatics; Cancer Research
23.  Phosphate solubilizers enhance NPK fertilizer use efficiency in rice and legume cultivation 
3 Biotech  2011;1(4):227-238.
It has been reported that phosphate solubilizing bacteria (PSB) are the most promising bacteria among the plant growth promoting rhizobacteria (PGPR); which may be used as biofertilizers for plant growth and nutrient use efficiency. Moreover, these soil micro-organisms play a significant role in regulating the dynamics of organic matter decomposition and the availability of plant nutrients such as nitrogen (N), phosphorus (P), potassium (K) and other nutrients. Through this study, the management of nutrient use efficiency by the application of PSB was targeted in order to make the applied nutrients more available to the plants in the rice (Oryza sativa) and yardlong bean (Vigna unguiculata) cultivation. Results have shown that the treatments with PSB alone or in the form of consortia of compatible strains with or without the external application of chemical NPK gave more germination index (G. I.) from 2.5 to 5 in rice and 2.7 to 4.8 in bean seeds. They also showed a higher growth in both shoot and root length and a higher biomass as compared to the control. This gives us an idea about the potentiality of these PSB strains and their application in rice and yardlong bean cultivation to get a better harvest index. Their use will also possibly reduce the nutrient runoff or leaching and increase in the use efficiency of the applied fertilizers. Thus, we can conclude that the NPK uptake and management can be improved by the use of PSB in rice and yardlong bean cultivation, and their application may be much more beneficial in the agricultural field.
PMCID: PMC3339586  PMID: 22558541
Fertilizer; Phosphate solubilizing bacteria; Oryza sativa; Vigna unguiculata; Germination index; Plant growth
24.  Impacts of environmental factors on fine root lifespan 
The lifespan of fast-cycling roots is a critical parameter determining a large flux of plant carbon into soil through root turnover and is a biological feature regulating the capacity of a plant to capture soil water and nutrients via root-age-related physiological processes. While the importance of root lifespan to whole-plant and ecosystem processes is increasingly recognized, robust descriptions of this dynamic process and its response to changes in climatic and edaphic factors are lacking. Here we synthesize available information and propose testable hypotheses using conceptual models to describe how changes in temperature, water, nitrogen (N), and phosphorus (P) availability impact fine root lifespan within a species. Each model is based on intrinsic responses including root physiological activity and alteration of carbohydrate allocation at the whole-plant level as well as extrinsic factors including mycorrhizal fungi and pressure from pathogens, herbivores, and other microbes. Simplifying interactions among these factors, we propose three general principles describing fine root responses to complex environmental gradients. First, increases in a factor that strongly constrains plant growth (temperature, water, N, or P) should result in increased fine root lifespan. Second, increases in a factor that exceeds plant demand or tolerance should result in decreased lifespan. Third, as multiple factors interact fine root responses should be determined by the most dominant factor controlling plant growth. Moving forward, field experiments should determine which types of species (e.g., coarse vs. fine rooted, obligate vs. facultative mycotrophs) will express greater plasticity in response to environmental gradients while ecosystem models may begin to incorporate more detailed descriptions of root lifespan and turnover. Together these efforts will improve quantitative understanding of root dynamics and help to identify areas where future research should be focused.
PMCID: PMC4032987  PMID: 24904605
ecosystem; root longevity; belowground; priming; nitrogen; phosphorus; climate change; mycorrhizal fungi
25.  Disentangling who is who during rhizosphere acidification in root interactions: combining fluorescence with optode techniques 
Plant–soil interactions can strongly influence root growth in plants. There is now increasing evidence that root–root interactions can also influence root growth, affecting architecture and root traits such as lateral root formation. Both when species grow alone or in interaction with others, root systems are in turn affected by as well as affect rhizosphere pH. Changes in soil pH have knock-on effects on nutrient availability. A limitation until recently has been the inability to assign species identity to different roots in soil. Combining the planar optode technique with fluorescent plants enables us to distinguish between plant species grown in natural soil and in parallel study pH dynamics in a non-invasive way at the same region of interest (ROI). We measured pH in the rhizosphere of maize and bean in rhizotrons in a climate chamber, with ROIs on roots in proximity to the roots of the other species as well as not-close to the other species. We found clear dynamic changes of pH over time and differences between the two species in rhizosphere acidification. Interestingly, when roots of the two species were interacting, the degree of acidification or alkalization compared to bulk soil was less strong then when roots were not growing in the vicinity of the other species. This cutting-edge approach can help provide a better understanding of plant–plant and plant–soil interactions.
PMCID: PMC3797519  PMID: 24137168
plant roots; interaction; green fluorescent protein; pH planar optodes; rhizotrons; rhizosphere; maize; bean

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