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1.  Cluster-root formation and carboxylate release in three Lupinus species as dependent on phosphorus supply, internal phosphorus concentration and relative growth rate 
Annals of Botany  2013;112(7):1449-1459.
Background and Aims
Some Lupinus species produce cluster roots in response to low plant phosphorus (P) status. The cause of variation in cluster-root formation among cluster-root-forming Lupinus species is unknown. The aim of this study was to investigate if cluster-root formation is, in part, dependent on different relative growth rates (RGRs) among Lupinus species when they show similar shoot P status.
Three cluster-root-forming Lupinus species, L. albus, L. pilosus and L. atlanticus, were grown in washed river sand at 0, 7·5, 15 or 40 mg P kg−1 dry sand. Plants were harvested at 34, 42 or 62 d after sowing, and fresh and dry weight of leaves, stems, cluster roots and non-cluster roots of different ages were measured. The percentage of cluster roots, tissue P concentrations, root exudates and plant RGR were determined.
Key Results
Phosphorus treatments had major effects on cluster-root allocation, with a significant but incomplete suppression in L. albus and L. pilosus when P supply exceeded 15 mg P kg−1 sand. Complete suppression was found in L. atlanticus at the highest P supply; this species never invested more than 20 % of its root weight in cluster roots. For L. pilosus and L. atlanticus, cluster-root formation was decreased at high internal P concentration, irrespective of RGR. For L. albus, there was a trend in the same direction, but this was not significant.
Cluster-root formation in all three Lupinus species was suppressed at high leaf P concentration, irrespective of RGR. Variation in cluster-root formation among the three species cannot be explained by species-specific variation in RGR or leaf P concentration.
PMCID: PMC3806539  PMID: 24061491
Cluster roots; phosphorus acquisition; relative growth rate; Lupinus albus; L. pilosus; L. atlanticus; net assimilation rate
2.  Variation in nutrient-acquisition patterns by mycorrhizal fungi of rare and common orchids explains diversification in a global biodiversity hotspot 
Annals of Botany  2013;111(6):1233-1241.
Background and Aims
Many terrestrial orchids have an obligate requirement for mycorrhizal associations to provide nutritional support from germination to establishment. This study will investigate the ability of orchid mycorrhizal fungi (OMF) to utilize a variety of nutrient sources in the nutrient-impoverished (low organic) soils of the Southwest Australian Floristic Region (SWAFR) in order to effectively compete, survive and sustain the orchid host.
Mycorrhizal fungi representing key OMF genera were isolated from three common and widespread species: Pterostylis recurva, Caladenia flava and Diuris corymbosa, and one rare and restricted species: Drakaea elastica. The accessibility of specific nutrients was assessed by comparing growth including dry biomass of OMF in vitro on basal CN MMN liquid media.
Key Results
Each of the OMF accessed and effectively utilized a wide variety of nutrient compounds, including carbon (C) sources, inorganic and organic nitrogen (N) and inorganic and organic phosphorus (P). The nutrient compounds utilized varied between the genera of OMF, most notably sources of N.
These results suggest that OMF can differentiate between niches (micro-niche specialization) in a constrained, highly resource-limited environment such as the SWAFR. Phosphorus is the most limited macronutrient in SWAFR soils and the ability to access phytate by OMF indicates a characterizing functional capacity of OMF from the SWAFR. Furthermore, compared with OMF isolated from the rare D. elastica, OMF associating with the common P. recurva produced far greater biomass over a wider variety of nutritional sources. This suggests a broader tolerance for habitat variation providing more opportunities for the common orchid for recruitment and establishment at a site.
PMCID: PMC3662510  PMID: 23532043
Carbon; Ceratobasidium; nitrogen; nutrients; orchid mycorrhizal fungi; phosphorus; Sebacina; soil; terrestrial orchid; Tulasnella
3.  Viminaria juncea does not vary its shoot phosphorus concentration and only marginally decreases its mycorrhizal colonization and cluster-root dry weight under a wide range of phosphorus supplies 
Annals of Botany  2013;111(5):801-809.
Background and Aims
The Australian legume species Viminaria juncea forms both cluster roots and mycorrhizal associations. The aim of this study was to identify if these root specializations are expressed at differential supplies of phosphorus (P) and at different shoot P concentrations [P].
Seedlings were planted in sand and provided with a mycorrhizal inoculum and basal nutrients plus one of 21 P treatments, ranging from 0 to 50 mg P kg−1 dry soil. Plants were harvested after 12 weeks, and roots, shoots and cluster roots were measured for length and fresh and dry weight. The number of cluster roots, the percentage of mycorrhizal colonization, and shoot [P] were determined.
Key Results
Shoot biomass accumulation increased with increasing P supply until a shoot dry weight of 3 g was reached at a P supply of approx. 27·5 mg P kg−1 dry soil. Neither cluster-root formation nor mycorrhizal colonization was fully suppressed at the highest P supply. Most intriguingly, shoot [P] did not differ across treatments, with an average of 1·4 mg P kg−1 shoot dry weight.
The almost constant shoot [P] in V. juncea over the very wide range of P supplies is, to our knowledge, unprecedented. To maintain these stable values, this species down-regulates its growth rate when no P is supplied; conversely, it down-regulates its P-uptake capacity very tightly at the highest P supplies, when its maximum growth rate has been reached. It is proposed that the persistence of cluster roots and mycorrhizal colonization up to the highest P treatments is a consequence of its tightly controlled shoot [P]. This unusual P physiology of V. juncea is surmised to be related to the habitat of this N2-fixing species. Water and nutrients are available at a low but steady supply for most of the year, negating the need for storage of P which would be metabolically costly and be at the expense of metabolic energy and P available for symbiotic N2 fixation.
PMCID: PMC3631325  PMID: 23456689
Cluster roots; legume; shoot phosphorus concentration; mycorrhiza; phosphorus supply; Viminaria juncea
4.  Downregulation of net phosphorus-uptake capacity is inversely related to leaf phosphorus-resorption proficiency in four species from a phosphorus-impoverished environment 
Annals of Botany  2013;111(3):445-454.
Background and Aims
Previous research has suggested a trade-off between the capacity of plants to downregulate their phosphorus (P) uptake capacity and their efficiency of P resorption from senescent leaves in species from P-impoverished environments.
To investigate this further, four Australian native species (Banksia attenuata, B. menziesii, Acacia truncata and A. xanthina) were grown in a greenhouse in nutrient solutions at a range of P concentrations [P]. Acacia plants received between 0 and 500 µm P; Banksia plants received between 0 and 10 µm P, to avoid major P-toxicity symptoms in these highly P-sensitive species.
Key Results
For both Acacia species, the net P-uptake rates measured at 10 µm P decreased steadily with increasing P supply during growth. In contrast, in B. attenuata, the net rate of P uptake from a solution with 10 µm P increased linearly with increasing P supply during growth. The P-uptake rate of B. menziesii showed no significant response to P supply in the growing medium. Leaf [P] of the four species supported this finding, with A. truncata and A. xanthina showing an increase up to a saturation value of 19 and 21 mg P g−1 leaf dry mass, respectively (at 500 µm P), whereas B. attenuata and B. menziesii both exhibited a linear increase in leaf [P], reaching 10 and 13 mg P g−1 leaf dry mass, respectively, without approaching a saturation point. The Banksia plants grown at 10 µm P showed mild symptoms of P toxicity, i.e. yellow spots on some leaves and drying and curling of the tips of the leaves. Leaf P-resorption efficiency was 69 % (B. attenuata), 73 % (B. menziesii), 34 % (A. truncata) and 36 % (A. xanthina). The P-resorption proficiency values were 0·08 mg P g−1 leaf dry mass (B. attenuata and B. menziesii), 0·32 mg P g−1 leaf dry mass (A. truncata) and 0·36 mg P g−1 leaf dry mass (A. xanthina). Combining the present results with additional information on P-remobilization efficiency and the capacity to downregulate P-uptake capacity for two other Australian woody species, we found a strong negative correlation between these traits.
It is concluded that species that are adapted to extremely P-impoverished soils, such as many south-western Australian Proteaceae species, have developed extremely high P-resorption efficiencies, but lost their capacity to downregulate their P-uptake mechanisms. The results support the hypothesis that the ability to resorb P from senescing leaves is inversely related to the capacity to downregulate net P uptake, possibly because constitutive synthesis of P transporters is a prerequisite for proficient P remobilization from senescing tissues.
PMCID: PMC3579450  PMID: 23293017
Downregulation; nutrient-poor soils; phosphorus toxicity; phosphorus-uptake capacity; Proteaceae; remobilization; resorption; Banksia attenuata; B. menziesii; Acacia truncata; A. xanthina
5.  Adaptive shoot and root responses collectively enhance growth at optimum temperature and limited phosphorus supply of three herbaceous legume species 
Annals of Botany  2012;110(5):959-968.
Background and Aims
Studies on the effects of sub- and/or supraoptimal temperatures on growth and phosphorus (P) nutrition of perennial herbaceous species at growth-limiting P availability are few, and the impacts of temperature on rhizosphere carboxylate dynamics are not known for any species.
The effect of three day/night temperature regimes (low, 20/13 °C; medium, 27/20 °C; and high, 32/25 °C) on growth and P nutrition of Cullen cinereum, Kennedia nigricans and Lotus australis was determined.
Key Results
The highest temperature was optimal for growth of C. cinereum, while the lowest temperature was optimal for K. nigricans and L. australis. At optimum temperatures, the relative growth rate (RGR), root length, root length per leaf area, total P content, P productivity and water-use efficiency were higher for all species, and rhizosphere carboxylate content was higher for K. nigricans and L. australis. Cullen cinereum, with a slower RGR, had long (higher root length per leaf area) and thin roots to enhance P uptake by exploring a greater volume of soil at its optimum temperature, while K. nigricans and L. australis, with faster RGRs, had only long roots (higher root length per leaf area) as a morphological adaptation, but had a higher content of carboxylates in their rhizospheres at the optimum temperature. Irrespective of the species, the amount of P taken up by a plant was mainly determined by root length, rather than by P uptake rate per unit root surface area. Phosphorus productivity was correlated with RGR and plant biomass.
All three species exhibited adaptive shoot and root traits to enhance growth at their optimum temperatures at growth-limiting P supply. The species with a slower RGR (i.e. C. cinereum) showed only morphological root adaptations, while K. nigricans and L. australis, with faster RGRs, had both morphological and physiological (i.e. root carboxylate dynamics) root adaptations.
PMCID: PMC3448422  PMID: 22847657
Australian native legumes; carboxylates; climate change; growth; perennial pastures; phosphorus; photosynthesis; root morphology; temperature; water-use efficiency
6.  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
7.  Morphologies and elemental compositions of calcium crystals in phyllodes and branchlets of Acacia robeorum (Leguminosae: Mimosoideae) 
Annals of Botany  2012;109(5):887-896.
Background and Aims
Formation of calcium oxalate crystals is common in the plant kingdom, but biogenic formation of calcium sulfate crystals in plants is rare. We investigated the morphologies and elemental compositions of crystals found in phyllodes and branchlets of Acacia robeorum, a desert shrub of north-western Australia.
Morphologies of crystals in phyllodes and branchlets of A. robeorum were studied using scanning electron microscopy (SEM), and elemental compositions of the crystals were identified by energy-dispersive X-ray spectroscopy. Distributional patterns of the crystals were studied using optical microscopy together with SEM.
Key Results
According to the elemental compositions, the crystals were classified into three groups: (1) calcium oxalate; (2) calcium sulfate, which is a possible mixture of calcium sulfate and calcium oxalate with calcium sulfate being the major component; and (3) calcium sulfate · magnesium oxalate, presumably mixtures of calcium sulfate, calcium oxalate, magnesium oxalate and silica. The crystals were of various morphologies, including prisms, raphides, styloids, druses, crystal sand, spheres and clusters. Both calcium oxalate and calcium sulfate crystals were observed in almost all tissues, including mesophyll, parenchyma, sclerenchyma (fibre cells), pith, pith ray and cortex; calcium sulfate · magnesium oxalate crystals were only found in mesophyll and parenchyma cells in phyllodes.
The formation of most crystals was biologically induced, as confirmed by studying the crystals formed in the phyllodes from seedlings grown in a glasshouse. The crystals may have functions in removing excess calcium, magnesium and sulfur, protecting the plants against herbivory, and detoxifying aluminium and heavy metals.
PMCID: PMC3310486  PMID: 22294477
Acacia robeorum; biomineralization; calcium oxalate; calcium sulfate; crystal sand; druses; Leguminosae; magnesium oxalate; Mimosoideae; prisms; raphides; styloids
8.  Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments 
Journal of Experimental Botany  2013;64(6):1731-1743.
Phosphite () induces a range of physiological and developmental responses in plants by disturbing the homeostasis of the macronutrient phosphate. Because of its close structural resemblance to phosphate, phosphite impairs the sensing, membrane transport, and subcellular compartmentation of phosphate. In addition, phosphite induces plant defence responses by an as yet unknown mode of action. In this study, the acclimation of Arabidopsis thaliana plants to a sustained phosphite supply in the growth medium was investigated and compared with plants growing under varying phosphate supplies. Unlike phosphate, phosphite did not suppress the formation of lateral roots in several Arabidopsis accessions. In addition, the expression of well-documented phosphate-starvation-induced genes, such as miRNA399d and At4, was not repressed by phosphite accumulation, whilst the induction of PHT1;1 and PAP1 was accentuated. Thus, a mimicking of phosphate by phosphite was not observed for these classical phosphate-starvation responses. Metabolomic analysis of phosphite-treated plants showed changes in several metabolite pools, most prominently those of aspartate, asparagine, glutamate, and serine. These alterations in amino acid pools provide novel insights for the understanding of phosphite-induced pathogen resistance.
PMCID: PMC3617837  PMID: 23404904
Arabidopsis; phosphate; phosphate-starvation response; phosphite
9.  Development and persistence of sandsheaths of Lyginia barbata (Restionaceae): relation to root structural development and longevity 
Annals of Botany  2011;108(7):1307-1322.
Background and Aims
Strongly coherent sandsheaths that envelop perennial roots of many monocotyledonous species of arid environments have been described for over a century. This study, for the first time, details the roles played by the structural development of the subtending roots in the formation and persistence of the sheaths.
The structural development of root tissues associated with persistent sandsheaths was studied in Lyginia barbata, native to the Western Australian sand plains. Cryo-scanning electron microscopy CSEM, optical microscopy and specific staining methods were applied to fresh, field material. The role of root hairs was clarified by monitoring sheath development in roots separated from the sand profile by fine mesh.
Key Results and Conclusions
The formation of the sheaths depends entirely on the numerous living root hairs which extend into the sand and track closely around individual grains enmeshing, by approx. 12 cm from the root tip, a volume of sand more than 14 times that of the subtending root. The longevity of the perennial sheaths depends on the subsequent development of the root hairs and of the epidermis and cortex. Before dying, the root hairs develop cellulosic walls approx. 3 µm thick, incrusted with ferulic acid and lignin, which persist for the life of the sheath. The dead hairs remain in place fused to a persistent platform of sclerified epidermis and outer cortex. The mature cortex comprises this platform, a wide, sclerified inner rim and a lysigenous central region – all dead tissue. We propose that the sandsheath/root hair/epidermis/cortex complex is a structural unit facilitating water and nutrient uptake while the tissues are alive, recycling scarce phosphorus during senescence, and forming, when dead, a persistent essential structure for maintenance of a functional stele in the perennial Lyginia roots.
PMCID: PMC3197463  PMID: 21969258
CSEM; lignified and suberized root hairs; Lyginia barbata; perennial drought-tolerant roots; persistent root hairs; phosphorus recycling; Restionaceae; rhizosheaths; root hair histochemistry; sandbinding roots
10.  Precipitation of Calcium, Magnesium, Strontium and Barium in Tissues of Four Acacia Species (Leguminosae: Mimosoideae) 
PLoS ONE  2012;7(7):e41563.
Precipitation of calcium in plants is common. There are abundant studies on the uptake and content of magnesium, strontium and barium, which have similar chemical properties to calcium, in comparison with those of calcium in plants, but studies on co-precipitation of these elements with calcium in plants are rare. In this study, we compared morphologies, distributional patterns, and elemental compositions of crystals in tissues of four Acacia species grown in the field as well as in the glasshouse. A comparison was also made of field-grown plants and glasshouse-grown plants, and of phyllodes of different ages for each species. Crystals of various morphologies and distributional patterns were observed in the four Acacia species studied. Magnesium, strontium and barium were precipitated together with calcium, mainly in phyllodes of the four Acacia species, and sometimes in branchlets and primary roots. These elements were most likely precipitated in forms of oxalate and sulfate in various tissues, including epidermis, mesophyll, parenchyma, sclerenchyma (fibre cells), pith, pith ray and cortex. In most cases, precipitation of calcium, magnesium, strontium and barium was biologically induced, and elements precipitated differed between soil types, plant species, and tissues within an individual plant; the precipitation was also related to tissue age. Formation of crystals containing these elements might play a role in regulating and detoxifying these elements in plants, and protecting the plants against herbivory.
PMCID: PMC3405136  PMID: 22848528
11.  Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments 
Annals of Botany  2010;105(5):755-767.
Background and Aims
Many Australian legumes have evolved in low-phosphorus (P) soils and low-rainfall areas. Therefore a study was made of the interaction of soil [P] and water availability on growth, photosynthesis, water-use efficiency (WUE) and P nutrition of two Australian native legumes with pasture potential, Cullen australasicum and C. pallidum, and the widely grown exotic pasture legume, lucerne (Medicago sativa).
Plants were grown in a glasshouse at 3, 10 and 30 mg P kg−1 dry soil for 5 months. At week 10, two drought treatments were imposed, total pot dried (all-dry) and only top soil dried (top-dry), while control pots were maintained at field capacity.
Key Results
Shoot dry weight produced by lucerne was never higher than that of C. australasicum. For C. pallidum only, shoot dry weight was reduced at 30 mg P kg−1 dry soil. The small root system of the Cullen species was quite plastic, allowing plants to access P and moisture efficiently. Lucerne always had a higher proportion of its large root system in the top soil layer compared with Cullen species. All species showed decreased photosynthesis, leaf water potential and stomatal conductance when exposed to drought, but the reductions were less for Cullen species, due to tighter stomatal control, and consequently they achieved a higher WUE. All species showed highest rhizosphere carboxylate concentrations in the all-dry treatment. For lucerne only, carboxylates decreased as P supply increased. Citrate was the main carboxylate in the control and top-dry treatments, and malate in the all-dry treatment.
Multiple adaptive responses of Cullen species and lucerne favoured exploitation of low-P soils under drought. The performance of undomesticated Cullen species, relative to that of lucerne, shows their promise as pasture species for environments such as in south-western Australia where water and P are limiting, especially in view of a predicted drying and warming climate.
PMCID: PMC2859915  PMID: 20421234
Australian native legumes; carboxylates; climate change; Cullen spp.; drought; Medicago sativa; novel crops; perennial pastures; phosphorus; photosynthesis; root distribution; water-use efficiency
12.  Localized application of soil organic matter shifts distribution of cluster roots of white lupin in the soil profile due to localized release of phosphorus 
Annals of Botany  2010;105(4):585-593.
Background and Aims
Phosphorus (P) is a major factor controlling cluster-root formation. Cluster-root proliferation tends to concentrate in organic matter (OM)-rich surface-soil layers, but the nature of this response of cluster-root formation to OM is not clear. Cluster-root proliferation in response to localized application of OM was characterized in Lupinus albus (white lupin) grown in stratified soil columns to test if the stimulating effect of OM on cluster-root formation was due to (a) P release from breakdown of OM; (b) a decrease in soil density; or (c) effects of micro-organisms other than releasing P from OM.
Lupin plants were grown in three-layer stratified soil columns where P was applied at 0 or 330 mg P kg−1 to create a P-deficient or P-sufficient background, and OM, phytate mixed with OM, or perlite was applied to the top or middle layers with or without sterilization.
Key Results
Non-sterile OM stimulated cluster-root proliferation and root length, and this effect became greater when phytate was supplied in the presence of OM. Both sterile OM and perlite significantly decreased cluster-root formation in the localized layers. The OM position did not change the proportion of total cluster roots to total roots in dry biomass among no-P treatments, but more cluster roots were concentrated in the OM layers with a decreased proportion in other places.
Localized application of non-sterile OM or phytate plus OM stimulated cluster-root proliferation of L. albus in the localized layers. This effect is predominantly accounted for by P release from breakdown of OM or phytate, but not due to a change in soil density associated with OM. No evidence was found for effects of micro-organisms in OM other than those responsible for P release.
PMCID: PMC2850796  PMID: 20150198
Citrate exudation; cluster-root formation; root proliferation; Lupinus albus; phosphorus; soil patch; soil micro-organisms; soil organic matter
13.  Effects of phosphorus supply on growth, phosphate concentration and cluster-root formation in three Lupinus species 
Annals of Botany  2009;105(3):365-374.
Background and Aims
In some lupin species, phosphate deficiency induces cluster-root formation, which enhances P uptake by increasing root surface area and, more importantly, the release of root exudates which enhances P availability.
Three species of Lupinus, L. albus, L. atlanticus and L. micranthus, with inherently different relative growth rates were cultivated under hydroponics in a greenhouse at four phosphate concentrations (1, 10, 50 and 150 µm) to compare the role of internal P in regulating cluster-root formation.
Key Results
The highest growth rate was observed in L. atlanticus, followed by L. albus and L. micranthus. At 1 µm P, cluster-root formation was markedly induced in all three species. The highest P uptake and accumulation was observed in L. micranthus, followed by L. atlanticus and then L. albus. Inhibition of cluster-root formation was severe at 10 µm P in L. atlanticus, but occurred stepwise with increasing P concentration in the root medium in L. albus.
In L. atlanticus and L. albus cluster-root formation was suppressed by P treatments above 10 µm, indicating a P-inducible regulating system for cluster-root formation, as expected. By contrast, production of cluster roots in L. micranthus, in spite of a high internal P concentration, indicated a lower sensitivity to P status, which allowed P-toxicity symptoms to develop.
PMCID: PMC2826247  PMID: 20037142
Cluster roots; lupin; Lupinus; phosphate nutrition; toxicity; uptake
14.  Change in Uptake, Transport and Accumulation of Ions in Nerium oleander (Rosebay) as Affected by Different Nitrogen Sources and Salinity 
Annals of Botany  2008;102(5):735-746.
Background and Aims
The source of nitrogen plays an important role in salt tolerance of plants. In this study, the effects of NaCl on net uptake, accumulation and transport of ions were investigated in Nerium oleander with ammonium or nitrate as the nitrogen source in order to analyse differences in uptake and cycling of ions within plants.
Plants were grown in a greenhouse in hydroponics under different salt treatments (control vs. 100 mm NaCl) with ammonium or nitrate as the nitrogen source, and changes in ion concentration in plants, xylem sap exuded from roots and stems, and phloem sap were determined.
Key Results
Plant weight, leaf area and photosynthetic rate showed a higher salt tolerance of nitrate-fed plants compared with that of ammonium-fed plants. The total amount of Na+ transported in the xylem in roots, accumulated in the shoot and retranslocated in the phloem of ammonium-fed plants under salt treatment was 1·8, 1·9 and 2·7 times more, respectively, than that of nitrate-treated plants. However, the amount of Na+ accumulated in roots in nitrate-fed plants was about 1·5 times higher than that in ammonium-fed plants. Similarly, Cl− transport via the xylem to the shoot and its retranslocation via the phloem (Cl− cycling) were far greater with ammonium treatment than with nitrate treatment under conditions of salinity. The uptake and accumulation of K+ in shoots decreased more due to salinity in ammonium-fed plants compared with nitrate-fed plants. In contrast, K+ cycling in shoots increased due to salinity, with higher rates in the ammonium-treated plants.
The faster growth of nitrate-fed plants under conditions of salinity was associated with a lower transport and accumulation of Na+ and Cl− in the shoot, whereas in ammonium-fed plants accumulation and cycling of Na+ and Cl− in shoots probably caused harmful effects and reduced growth of plants.
PMCID: PMC2712379  PMID: 18772147
Mineral cycling; Nerium oleander; nitrogen source; salinity; xylem and phloem transport
15.  Plant Growth Modelling and Applications: The Increasing Importance of Plant Architecture in Growth Models 
Annals of Botany  2008;101(8):1053-1063.
Modelling plant growth allows us to test hypotheses and carry out virtual experiments concerning plant growth processes that could otherwise take years in field conditions. The visualization of growth simulations allows us to see directly and vividly the outcome of a given model and provides us with an instructive tool useful for agronomists and foresters, as well as for teaching. Functional–structural (FS) plant growth models are nowadays particularly important for integrating biological processes with environmental conditions in 3-D virtual plants, and provide the basis for more advanced research in plant sciences.
In this viewpoint paper, we ask the following questions. Are we modelling the correct processes that drive plant growth, and is growth driven mostly by sink or source activity? In current models, is the importance of soil resources (nutrients, water, temperature and their interaction with meristematic activity) considered adequately? Do classic models account for architectural adjustment as well as integrating the fundamental principles of development? Whilst answering these questions with the available data in the literature, we put forward the opinion that plant architecture and sink activity must be pushed to the centre of plant growth models. In natural conditions, sinks will more often drive growth than source activity, because sink activity is often controlled by finite soil resources or developmental constraints.
This viewpoint paper also serves as an introduction to this Special Issue devoted to plant growth modelling, which includes new research covering areas stretching from cell growth to biomechanics. All papers were presented at the Second International Symposium on Plant Growth Modeling, Simulation, Visualization and Applications (PMA06), held in Beijing, China, from 13–17 November, 2006. Although a large number of papers are devoted to FS models of agricultural and forest crop species, physiological and genetic processes have recently been included and point the way to a new direction in plant modelling research.
PMCID: PMC2710283  PMID: 18387970
Biomechanics; carbon allocation; functional–structural plant models; meristem; nitrogen; phenotypic plasticity; root architecture; simulation; sink; source; PMA06
16.  Short-term and long-term root respiratory acclimation to elevated temperatures associated with root thermotolerance for two Agrostis grass species 
Journal of Experimental Botany  2008;59(14):3803-3809.
This study was designed to investigate whether thermotolerant roots exhibit respiratory acclimation to elevated temperatures. Root respiratory acclimation traits in response to increasing temperatures were compared between two Agrostis species contrasting in heat tolerance: thermal A. scabra and heat-sensitive A. stolonifera. Roots of both species were exposed to 17, 27, or 37 °C. Root RGR declined with increasing temperatures from 17 °C to 37 °C in both species; however, root growth of A. scabra maintained a significantly higher RGR than A. stolonifera at 27 °C or 37°C. A. scabra exhibited a significantly higher respiration acclimation potential to elevated temperatures, both in the short term (60 min) and in the long term (7–28 d) as compared with A. stolonifera, when temperatures increased from 17 °C to 27 °C or from 27 °C to 37 °C. Thermal A. scabra also maintained a significantly lower maintenance cost than A. stolonifera as temperatures increased to 27 °C or 37 °C. The results suggested that root thermotolerance of thermal A. scabra was associated with both short-term and long-term respiratory acclimation to changes in temperatures. The superior ability of adjusting the rate of root respiration to compensate for increases in carbon demand during short- or long-term temperature increases in the heat-tolerant A. scabra may result in the reduction in carbon expenditure or costs for maintenance, leading to extended root survivability in high temperature soils.
PMCID: PMC2576646  PMID: 18977747
Acclimation; grass; heat tolerance; high temperature; root respiration
17.  Root Structure and Functioning for Efficient Acquisition of Phosphorus: Matching Morphological and Physiological Traits 
Annals of Botany  2006;98(4):693-713.
• Background Global phosphorus (P) reserves are being depleted, with half-depletion predicted to occur between 2040 and 2060. Most of the P applied in fertilizers may be sorbed by soil, and not be available for plants lacking specific adaptations. On the severely P-impoverished soils of south-western Australia and the Cape region in South Africa, non-mycorrhizal species exhibit highly effective adaptations to acquire P. A wide range of these non-mycorrhizal species, belonging to two monocotyledonous and eight dicotyledonous families, produce root clusters. Non-mycorrhizal species with root clusters appear to be particularly effective at accessing P when its availability is extremely low.
• Scope There is a need to develop crops that are highly effective at acquiring inorganic P (Pi) from P-sorbing soils. Traits such as those found in non-mycorrhizal root-cluster-bearing species in Australia, South Africa and other P-impoverished environments are highly desirable for future crops. Root clusters combine a specialized structure with a specialized metabolism. Native species with such traits could be domesticated or crossed with existing crop species. An alternative approach would be to develop future crops with root clusters based on knowledge of the genes involved in development and functioning of root clusters.
• Conclusions Root clusters offer enormous potential for future research of both a fundamental and a strategic nature. New discoveries of the development and functioning of root clusters in both monocotyledonous and dicotyledonous families are essential to produce new crops with superior P-acquisition traits.
PMCID: PMC2806175  PMID: 16769731
Actinorhizal; capillaroid roots; carboxylates; Casuarinaceae; cluster roots; Cyperaceae; dauciform roots; exudation; Fabaceae; Proteaceae; proteoid roots; Restionaceae
18.  From Individual Leaf Elongation to Whole Shoot Leaf Area Expansion: a Comparison of Three Aegilops and Two Triticum Species 
Annals of Botany  2004;94(1):99-108.
• Background and Aims Rapid leaf area expansion is a desirable trait in the early growth stages of cereal crops grown in low‐rainfall areas. In this study, the traits associated with inherent variation in early leaf area expansion rates have been investigated in two wheat species (Triticum aestivum and T. durum) and three of its wild relatives (Aegilops umbellulata, A. caudata and A. tauschii) to find out whether the Aegilops species have a faster leaf area expansion in their early developmental stage than some of the current wheat species.
• Methods Growth of individual leaves, biomass allocation, and gas exchange were measured on hydroponically grown plants for 4 weeks.
• Key Results Leaf elongation rate (LER) was strongly and positively correlated with leaf width but not with leaf elongation duration (LED). The species with more rapidly elongating leaves showed a faster increase with leaf position in LER, leaf width and leaf area, higher relative leaf area expansion rates, and more biomass allocation to leaf sheaths and less to roots. No differences in leaf appearance rate were found amongst the species.
• Conclusions Aegilops tauschii was the only wild species with rapid leaf expansion rates similar to those of wheat, and it achieved the highest photosynthetic rates, making it an interesting species for further study.
PMCID: PMC4242366  PMID: 15155374
Aegilops; biomass allocation; leaf elongation duration; leaf elongation rate; leaf expansion; leaf width; photosynthesis; relative growth rate; Triticum; wheat; wild relatives
19.  Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species 
Plant, Cell & Environment  2013;37(6):1276-1298.
Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A. thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus (‘delayed greening’), with young leaves having very low levels of chlorophyll and Calvin–Benson cycle enzymes. In mature leaves, soluble protein and Calvin–Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A. thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin–Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.
PMCID: PMC4260170  PMID: 24895754
Banksia; carbon metabolism; delayed greening; glucose 6-phosphate; Hakea; PPUE; Rubisco; shikimate dehydrogenase

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