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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.  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
4.  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
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.  Genetic Variability in Phosphorus Responses of Rice Root Phenotypes 
Rice  2016;9:29.
Low phosphorus availability is a major factor limiting rice productivity. Since root traits determine phosphorus acquisition efficiency, they are logical selection targets for breeding rice with higher productivity in low phosphorus soils. Before using these traits for breeding, it is necessary to identify genetic variation and to assess the plasticity of each trait in response to the environment. In this study, we measured phenotypic variation and effect of phosphorus deficiency on root architectural, morphological and anatomical traits in 15 rice (Oryza sativa) genotypes. Rice plants were grown with diffusion-limited phosphorus using solid-phase buffered phosphorus to mimic realistic phosphorus availability conditions.
Shoot dry weight, tiller number, plant height, number of nodal roots and shoot phosphorus content were reduced under low phosphorus availability. Phosphorus deficiency significantly reduced large lateral root density and small and large lateral root length in all genotypes, though the degree of plasticity and relative allocation of root length between the two root classes varied among genotypes. Root hair length and density increased in all genotypes in response to low phosphorus. Nodal root cross-sectional area was significantly less under low phosphorus availability, and reduced cortical area was disproportionately responsible for this decline. Phosphorus deficiency caused a 20 % increase in the percent cortical area converted to aerenchyma. Total stele area and meta-xylem vessel area responses to low phosphorus differed significantly among genotypes. Phosphorus treatment did not significantly affect theoretical water conductance overall, but increased or reduced it in a few genotypes. All genotypes had restricted water conductance at the base of the nodal root compared to other positions along the root axis.
There was substantial genetic variation for all root traits investigated. Low phosphorus availability significantly affected most traits, often to an extent that varied with the genotype. With the exception of stele and meta-xylem vessel area, root responses to low phosphorus were in the same direction for all genotypes tested. Therefore, phenotypic evaluations conducted with adequate fertility should be useful for genetic mapping studies and identifying potential sources of trait variation, but these should be confirmed in low-phosphorus environments.
Electronic supplementary material
The online version of this article (doi:10.1186/s12284-016-0102-9) contains supplementary material, which is available to authorized users.
PMCID: PMC4905936  PMID: 27294384
Aerenchyma; Root anatomy; Lateral roots; Oryza sativa; Phosphorus; Root hairs; Stele; Xylem
7.  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
8.  Liming can decrease legume crop yield and leaf gas exchange by enhancing root to shoot ABA signalling 
Journal of Experimental Botany  2015;66(8):2335-2345.
This paper describes a novel mechanistic understanding of how recommended rates of liming to manage soil pH may cause reduced gas exchange and growth in legumes.
To meet future requirements for food production, sustainable intensive agricultural systems need to optimize nutrient availability to maximize yield, traditionally achieved by maintaining soil pH within an optimal range (6–6.5) by applying lime (calcium carbonate). However, a field trial that applied recommended liming rates to a sandy loam soil (increasing soil pH from 5.5 to 6.2) decreased pod yield of field bean (Vicia faba L. cv. Fuego) by ~30%. Subsequent pot trials, with liming that raised soil pH to 6.3–6.7, reduced stomatal conductance (g s) by 63, 26, and 59% in V. faba, bean (Phaseolus vulgaris), and pea (Pisum sativum), respectively. Furthermore, liming reduced shoot dry biomass by 16–24% in these species. Ionomic analysis of root xylem sap and leaf tissue revealed a decrease in phosphorus concentration that was correlated with decreased g s: both reductions were partially reversed by adding superphosphate fertilizer. Further analysis of pea suggests that leaf gas exchange was reduced by a systemic increase (roots, xylem sap, and leaves) in the phytohormone abscisic acid (ABA) in response to lime-induced suboptimal plant phosphorus concentrations. Supplying synthetic ABA via the transpiration stream to detached pea leaves, at the same xylem sap concentrations induced by liming, decreased transpiration. Furthermore, the g s of the ABA-deficient mutant pea wilty was unresponsive to liming, apparently confirming that ABA mediates some responses to low phosphorus availability caused by liming. This research provides a detailed mechanistic understanding of the physiological processes by which lime application can limit crop yields, and questions the suitability of current liming recommendations.
PMCID: PMC4407654  PMID: 25740925
Abscisic acid; ionome; liming; phosphorus; stomatal conductance; wilty.
9.  Root adaptations to soils with low fertility and aluminium toxicity 
Annals of Botany  2016;118(4):593-605.
Background Plants depend on their root systems to acquire the water and nutrients necessary for their survival in nature, and for their yield and nutritional quality in agriculture. Root systems are complex and a variety of root phenes have been identified as contributors to adaptation to soils with low fertility and aluminium (Al) toxicity. Phenotypic characterization of root adaptations to infertile soils is enabling plant breeders to develop improved cultivars that not only yield more, but also contribute to yield stability and nutritional security in the face of climate variability.
Scope In this review the adaptive responses of root systems to soils with low fertility and Al toxicity are described. After a brief introduction, the purpose and focus of the review are outlined. This is followed by a description of the adaptive responses of roots to low supply of mineral nutrients [with an emphasis on low availability of nitrogen (N) and phosphorus (P) and on toxic levels of Al]. We describe progress in developing germplasm adapted to soils with low fertility or Al toxicity using selected examples from ongoing breeding programmes on food (maize, common bean) and forage/feed (Brachiaria spp.) crops. A number of root architectural, morphological, anatomical and metabolic phenes contribute to the superior performance and yield on soils with low fertility and Al toxicity. Major advances have been made in identifying root phenes in improving adaptation to low N (maize), low P (common bean) or high Al [maize, common bean, species and hybrids of brachiariagrass, bulbous canarygrass (Phalaris aquatica) and lucerne (Medicago sativa)].
Conclusions Advanced root phenotyping tools will allow dissection of root responses into specific root phenes that will aid both conventional and molecular breeders to develop superior cultivars. These new cultivars will play a key role in sustainable intensification of crop–livestock systems, particularly in smallholder systems of the tropics. Development of these new cultivars adapted to soils with low fertility and Al toxicity is needed to improve global food and nutritional security and environmental sustainability.
PMCID: PMC5055624  PMID: 27255099
aluminium; breeding; interspecific hybridization; low soil fertility; nitrogen; nutrient acquisition; phosphorus; problem soils; root phenes; root physiology
10.  The mitochondrial malate dehydrogenase 1 gene GhmMDH1 is involved in plant and root growth under phosphorus deficiency conditions in cotton 
Scientific Reports  2015;5:10343.
Cotton, an important commercial crop, is cultivated for its natural fibers, and requires an adequate supply of soil nutrients, including phosphorus, for its growth. Soil phosporus exists primarily in insoluble forms. We isolated a mitochondrial malate dehydrogenase (MDH) gene, designated as GhmMDH1, from Gossypium hirsutum L. to assess its effect in enhancing P availability and absorption. An enzyme kinetic assay showed that the recombinant GhmMDH1 possesses the capacity to catalyze the interconversion of oxaloacetate and malate. The malate contents in the roots, leaves and root exudates was significantly higher in GhmMDH1-overexpressing plants and lower in knockdown plants compared with the wild-type control. Knockdown of GhmMDH1 gene resulted in increased respiration rate and reduced biomass whilst overexpression of GhmMDH1 gave rise to decreased respiration rate and higher biomass in the transgenic plants. When cultured in medium containing only insoluble phosphorus, Al-phosphorus, Fe-phosphorus, or Ca-phosphorus, GhmMDH1-overexpressing plants produced significantly longer roots and had a higher biomass and P content than WT plants, however, knockdown plants showed the opposite results for these traits. Collectively, our results show that GhmMDH1 is involved in plant and root growth under phosphorus deficiency conditions in cotton, owing to its functions in leaf respiration and P acquisition.
PMCID: PMC4503954  PMID: 26179843
11.  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
12.  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
13.  Root foraging elicits niche complementarity-dependent yield advantage in the ancient ‘three sisters’ (maize/bean/squash) polyculture 
Annals of Botany  2014;114(8):1719-1733.
Background and Aims
Since ancient times in the Americas, maize, bean and squash have been grown together in a polyculture known as the ‘three sisters’. This polyculture and its maize/bean variant have greater yield than component monocultures on a land-equivalent basis. This study shows that below-ground niche complementarity may contribute to this yield advantage.
Monocultures and polycultures of maize, bean and squash were grown in two seasons in field plots differing in nitrogen (N) and phosphorus (P) availability. Root growth patterns of individual crops and entire polycultures were determined using a modified DNA-based technique to discriminate roots of different species.
Key Results
The maize/bean/squash and maize/bean polycultures had greater yield and biomass production on a land-equivalent basis than the monocultures. Increased biomass production was largely caused by a complementarity effect rather than a selection effect. The differences in root crown architecture and vertical root distribution among the components of the ‘three sisters’ suggest that these species have different, possibly complementary, nutrient foraging strategies. Maize foraged relatively shallower, common bean explored the vertical soil profile more equally, while the root placement of squash depended on P availability. The density of lateral root branching was significantly greater for all species in the polycultures than in the monocultures.
It is concluded that species differences in root foraging strategies increase total soil exploration, with consequent positive effects on the growth and yield of these ancient polycultures.
PMCID: PMC4416130  PMID: 25274551
‘Three sisters’; niche complementarity; polyculture; intercropping; nitrogen; phosphorus; plant nutrition; root architecture; root foraging; maize; bean; squash; Zea mays; Phaseolus vulgaris; Cucurbita
14.  The effects of nitrogen form on root morphological and physiological adaptations of maize, white lupin and faba bean under phosphorus deficiency 
AoB Plants  2016;8:plw058.
Root morphological/physiological modifications are important for phosphorus (P) acquisition of plants under P deficiency, but strategies differ among plant species. Detailed studies on the response of maize roots to P deficiency are limited. Nitrogen (N) form influences root morphology/physiology, and thus may influence root responses to P deficiency. This work investigated adaptive mechanisms of maize roots to low P by comparison with white lupin and faba bean supplied with two N forms. Plants were grown for 7–16 days in hydroponics with sufficient (250 µmol L−1) and deficient P supply (1 µmol L−1) under supply of NH4NO3 or Ca(NO3)2. Plant growth and P uptake were measured, and release of protons and organic acid anions, and acid phosphatase activity in the root were monitored. The results showed that P deficiency significantly decreased shoot growth while increased root growth and total root length of maize and faba bean, but not white lupin. It enhanced the release of protons and organic acid anions, and acid phosphatase activity, from the roots of both legumes but not maize. Compared with Ca(NO3)2, NH4NO3 dramatically increased proton release by roots but did not alter root morphology or physiology of the three species in response to low P. It is concluded that the N form did not fundamentally change root morphological/physiological responses of the three species to P deficiency. Morphological variation in maize and morpho-physiological modifications in white lupin and faba bean were the main adaptive strategies to P deficiency.
PMCID: PMC5018397  PMID: 27519912
Low P availability; organic acids; rhizosphere; root exudation; root morphology; species variation
15.  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
16.  Assess suitability of hydroaeroponic culture to establish tripartite symbiosis between different AMF species, beans, and rhizobia 
BMC Plant Biology  2009;9:73.
Like other species of the Phaseoleae tribe, common bean (Phaseolus vulgaris L.) has the potential to establish symbiosis with rhizobia and to fix the atmospheric dinitrogen (N2) for its N nutrition. Common bean has also the potential to establish symbiosis with arbuscular mycorrhizal fungi (AMF) that improves the uptake of low mobile nutrients such as phosphorus, from the soil. Both rhizobial and mycorrhizal symbioses can act synergistically in benefits on plant.
The tripartite symbiosis of common bean with rhizobia and arbuscular mycorrhizal fungi (AMF) was assessed in hydroaeroponic culture with common bean (Phaseolus vulgaris L.), by comparing the effects of three fungi spp. on growth, nodulation and mycorrhization of the roots under sufficient versus deficient P supplies, after transfer from initial sand culture. Although Glomus intraradices Schenck & Smith colonized intensely the roots of common bean in both sand and hydroaeroponic cultures, Gigaspora rosea Nicolson & Schenck only established well under sand culture conditions, and no root-colonization was found with Acaulospora mellea Spain & Schenck under either culture conditions. Interestingly, mycorrhization by Glomus was also obtained by contact with mycorrhized Stylosanthes guianensis (Aubl.) sw in sand culture under deficient P before transfer into hydroaeroponic culture. The effect of bean genotype on both rhizobial and mycorrhizal symbioses with Glomus was subsequently assessed with the common bean recombinant inbreed line 7, 28, 83, 115 and 147, and the cultivar Flamingo. Significant differences among colonization and nodulation of the roots and growth among genotypes were found.
The hydroaeroponic culture is a valuable tool for further scrutinizing the physiological interactions and nutrient partitioning within the tripartite symbiosis.
PMCID: PMC2713235  PMID: 19534785
17.  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
18.  Maize Varieties Released in Different Eras Have Similar Root Length Density Distributions in the Soil, Which Are Negatively Correlated with Local Concentrations of Soil Mineral Nitrogen 
PLoS ONE  2015;10(3):e0121892.
Larger, and deeper, root systems of new maize varieties, compared to older varieties, are thought to have enabled improved acquisition of soil resources and, consequently, greater grain yields. To compare the spatial distributions of the root systems of new and old maize varieties and their relationships with spatial variations in soil concentrations of available nitrogen (N), phosphorus (P) and potassium (K), two years of field experiments were performed using six Chinese maize varieties released in different eras. Vertical distributions of roots, and available N, P and K in the 0–60 cm soil profile were determined in excavated soil monoliths at silking and maturity. The results demonstrated that new maize varieties had larger root dry weight, higher grain yield and greater nutrient accumulation than older varieties. All varieties had similar total root length and vertical root distribution at silking, but newer varieties maintained greater total root length and had more roots in the 30–60 cm soil layers at maturity. The spatial variation of soil mineral N (Nmin) in each soil horizon was larger than that of Olsen-P and ammonium-acetate-extractable K, and was inversely correlated with root length density (RLD), especially in the 0–20 cm soil layer. It was concluded that greater acquisition of mineral nutrients and higher yields of newer varieties were associated with greater total root length at maturity. The negative relationship between RLD and soil Nmin at harvest for all varieties suggests the importance of the spatial distribution of the root system for N uptake by maize.
PMCID: PMC4370465  PMID: 25799291
19.  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
20.  The Expression of TaRca2-α Gene Associated with Net Photosynthesis Rate, Biomass and Grain Yield in Bread Wheat (Triticum aestivum L.) under Field Conditions 
PLoS ONE  2016;11(8):e0161308.
Improvement in activation of Rubisco by Rubisco activase can potentially enhance CO2 assimilation and photosynthetic efficiency in plants. The three homoeologous copies of TaRca2-α were identified on chromosomes 4AL, 4BS and 4DS (TaRca2-α-4AL, TaRca2-α-4BS, and TaRca2-α-4DS) in bread wheat. Expression patterns of the three copies at heading (Z55), anthesis (Z67) and grain-filling (Z73) stages were investigated through qRT-PCR analyses in a panel of 59 bread wheat genotypes and their effects on net photosynthesis rate (Pn), biomass plant-1 (BMPP) and grain yield plant-1 (GYPP) were further explored. Different but similar expression patterns were observed for the three copies of TaRca2-α at the three growth stages with highest expression at grain-filling stage. TaRca2-α-4BS expressed higher at the three stages than TaRca2-α-4AL and TaRca2-α-4DS. The 59 genotypes could be clustered into three groups as high (7 genotypes), intermediate (41 genotypes) and low (11 genotypes) expression based on the expression of the three copies of TaRca2-α at three growth stages. Significant variations (P<0.01) were observed among the three groups of bread wheat genotypes for Pn, BMPP and GYPP. Generally, the genotypes with higher TaRca2-α expression also showed higher values for Pn, BMPP and GYPP. The expressions of the three copies of TaRca2-α at heading, anthesis and grain-filling stages were positively correlated with Pn, BMPP and GYPP (P<0.01) with stronger association for TaRca2-α-4BS at grain-filling stage. These results revealed that the expression of TaRca2-α contribute substantially to Pn, BMPP and GYPP, and suggested that manipulating TaRca-α expression may efficiently improve Pn, BMPP and GYPP in bread wheat and detecting TaRca-α expression levels with emphasis on TaRca2-α-4BS may be a positive strategy for selection in improving photosynthetic efficiency and grain yield of bread wheat.
PMCID: PMC4993480  PMID: 27548477
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.  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
23.  Competition between Free-Floating Plants Is Strongly Driven by Previously Experienced Phosphorus Concentrations in the Water Column 
PLoS ONE  2016;11(9):e0162780.
Nutrients can determine the outcome of the competition between different floating plant species. The response of floating plants to current phosphorus levels may be affected by previously experienced phosphorus concentrations because some species have the ability to store excess phosphorus for later use. This might have an impact on their competition. Here, we investigate the effect of previous and actual phosphorus concentrations on the growth rate of free-floating plant species (Azolla filiculoides, Lemna minor/gibba and Ricciocarpus natans)and the effect of phosphorus history on the competition between L. minor/gibba and A. filiculoides and between L. minor/gibba and R. natans. As expected, plant growth was lower when previously kept at low instead of high phosphorus concentrations. Growth of L. minor/gibba and A. filiculoides with a phosphorus rich history was comparable for low and high actual phosphorus concentrations, however, internal phosphorus concentrations were significantly lower with low actual phosphorus concentration. This indicates that both species perform luxury phosphorus uptake. Furthermore, internal P concentration in Azolla and Lemna increased within two weeks after a period of P deficit without a strong increase in growth. A. filiculoides in a mixture with L. minor/gibba grew faster than its monoculture. Morphological differences may explain why A. filiculoides outcompeted L. minor/gibba and these differences may be induced by phosphorus concentrations in the past. Growth of L. minor/gibba was only reduced by the presence of A. filiculoides with a high phosphorus history. Growth of L. minor/gibba and R. natans in mixtures was positively affected only when they had a high phosphorus history themselves and their competitor a low phosphorus history. These observations clearly indicate that phosphorus history of competing plants is important for understanding the outcome of the competition. Therefore, actual and previously experienced phosphorus concentrations should be taken into account in future studies dealing with competition between plants.
PMCID: PMC5021290  PMID: 27622519
24.  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.
25.  The Plastid Casein Kinase 2 Phosphorylates Rubisco Activase at the Thr-78 Site but Is Not Essential for Regulation of Rubisco Activation State 
Rubisco activase (RCA) is essential for the activation of Rubisco, the carboxylating enzyme of photosynthesis. In Arabidopsis, RCA is composed of a large RCAα and small RCAβ isoform that are formed by alternative splicing of a single gene (At2g39730). The activity of Rubisco is controlled in response to changes in irradiance by regulation of RCA activity, which is known to involve a redox-sensitive disulfide bond located in the carboxy-terminal extension of the RCAα subunit. Additionally, phosphorylation of RCA threonine-78 (Thr-78) has been reported to occur in the dark suggesting that phosphorylation may also be associated with dark-inactivation of RCA and deactivation of Rubisco. In the present study, we developed site-specific antibodies to monitor phosphorylation of RCA at the Thr-78 site and used non-reducing SDS-PAGE to monitor the redox status of the RCAα subunit. By immunoblotting, phosphorylation of both RCA isoforms occurred at low light and in the dark and feeding peroxide or DTT to leaf segments indicated that redox status of the chloroplast stroma was a critical factor controlling RCA phosphorylation. Use of a knockout mutant identified the plastid-targeted casein kinase 2 (cpCK2α) as the major protein kinase involved in RCA phosphorylation. Studies with recombinant cpCK2α and synthetic peptide substrates identified acidic residues at the –1, +2, and +3 positions surrounding Thr-78 as strong positive recognition elements. The cpck2 knockout mutant had strongly reduced phosphorylation at the Thr-78 site but was similar to wild type plants in terms of induction kinetics of photosynthesis following transfer from darkness or low light to high light, suggesting that if phosphorylation of RCA Thr-78 plays a direct role it would be redundant to redox regulation for control of Rubisco activation state under normal conditions.
PMCID: PMC4814456  PMID: 27064346
Rubisco; Rubisco activase; redox regulation; protein phosphorylation; modification-specific antibodies

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