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Hans Lambers

Publications and source records attributed to Hans Lambers.

At least 19 recordsLinked to original sources

Carboxylate composition of root exudates does not relate consistently to a crop species' ability to use phosphorus from aluminium, iron or calcium phosphate sources.

* The relationship between carboxylate release from roots and the ability of the species to utilize phosphorus from sparingly soluble forms was studied by comparing Triticum aestivum, Brassica napus, Cicer arietinum, Pisum sativum, Lupinus albus, Lupinus angustifolius and Lupinus cosentinii. * Plants were grown in sand and supplied with 40 mg P kg(-1) in the sparingly soluble forms AlPO(4), FePO(4) or Ca(5)OH(PO(4))(3), or as soluble KH(2)PO(4); control plants received no P. * The ability to utilize sparingly soluble forms of P differed between forms of P supplied and species. Pisum sativum and C. arietinum did not access AlPO(4) or FePO(4) despite releasing carboxylates into the rhizosphere. * Species accessed different forms of sparingly soluble P, but no species was superior in accessing all forms. We conclude that a single trait cannot explain access to different forms of sparingly soluble P, and hypothesize that in addition to carboxylates, rhizosphere pH and root morphology are key factors.

Aluminum↗

Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits.

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.

Phosphorus↗

Root respiratory characteristics associated with plant adaptation to high soil temperature for geothermal and turf-type Agrostis species.

Respiration is a major avenue of carbohydrates loss. The objective of the present study was to examine root respiratory characteristics associated with root tolerance to high soil temperature for two Agrostis species: thermal Agrostis scabra, a species adapted to high-temperature soils in geothermal areas in Yellowstone National Park, and two cultivars ('L-93' and 'Penncross') of a cool-season turfgrass species, A. stolonifera (creeping bentgrass), that differ in their heat sensitivity. Roots of thermal A. scabra and both creeping bentgrass cultivars were exposed to high (37 degrees C) or low soil temperature (20 degrees C). Total root respiration rate and specific respiratory costs for maintenance and ion uptake increased with increasing soil temperatures in both species. The increases in root respiratory rate and costs for maintenance and ion uptake were less pronounced for A. scabra than for both creeping bentgrass cultivars (e.g. respiration rate increased by 50% for A. scabra upon exposure to high temperature for 28 d, as compared with 99% and 107% in 'L-93' and 'Penncross', respectively). Roots of A. scabra exhibited higher tolerance to high soil temperature than creeping bentgrass, as manifested by smaller decreases in relative growth rate, cell membrane stability, maximum root length, and nitrate uptake under high soil temperature. The results suggest that acclimation of respiratory carbon metabolism plays an important role in root survival of Agrostis species under high soil temperatures, particularly for the thermal grass adaptation to chronically high soil temperatures. The ability of roots to tolerate high soil temperatures could be related to the capacity to control respiratory rates and increase respiratory efficiency by lowering maintenance and ion uptake costs.

Acclimatization↗

Specialized 'dauciform' roots of Cyperaceae are structurally distinct, but functionally analogous with 'cluster' roots.

When grown in nutrient solutions of extremely low [P] (<or=1.0 microm), the sedge Schoenus unispiculatus Benth. (Cyperaceae) develops dauciform roots, which are short and carrot shaped, and produce dense numbers of long root hairs. It has been suggested that dauciform roots of monocotyledonous sedges function to acquire P from nutrient-poor, P-fixing soils in a manner similar to that of cluster (proteoid) roots developed by some dicotyledonous species, but without evidence to substantiate this claim. To elucidate the ecophysiological role of dauciform roots, we assessed carboxylate exudation, internal carboxylate and P concentrations and O(2) uptake rates during dauciform root development. We showed that O(2) consumption was fastest [9 nmol O(2) g(-1) fresh mass (FM) s(-1)] and root [P] greatest (0.4 mg P g(-1) FM) when dauciform roots were young and rapidly developing. Citrate was the most abundant carboxylate in root tissues at all developmental stages, and was most concentrated (22.2 micromol citrate g(-1) FM) in young dauciform roots, decreasing by more than half in mature dauciform roots. Peak citrate-exudation rates (1.7 nmol citrate g(-1) FM s(-1)) occurred from mature dauciform roots, and were approximately an order of magnitude faster than those from roots of species without root clusters, and similar to those of mature proteoid (cluster) roots of Proteaceae. Both developing and mature dauciform roots had the capacity to acidify (but not alkalinize) the rhizosphere. Anatomical studies showed that epidermal cells in dauciform roots were greatly elongated in the transverse plane; epidermal cells of parent roots were unmodified. Although structurally distinct, the physiology of dauciform roots in sedges appears to be analogous to that of proteoid roots of Proteaceae and Fabaceae, and hence, dauciform roots would facilitate access to sorbed P and micronutrients from soils of low fertility.

Carboxylic Acids↗

Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere.

The relationship between carboxylate release and the ability of plants to access phosphorus from AlPO4 and to detoxify aluminium was studied by comparing species with a low and high rate of carboxylate release, Triticum aestivum (wheat) and Lupinus albus (white lupin), respectively. Species were supplied with P at 10, 20, 40 or 100 mg P kg-1 sand in the form of sparingly soluble AlPO4 or soluble KH2PO4; control plants did not receive any P. Triticum aestivum was significantly better than L. albus at accessing P from AlPO4, despite accumulating fewer carboxylates in its rhizosphere. Rhizosphere pH of L. albus did not vary with form or level of P supply, while the rhizosphere pH of T. aestivum increased with the level of P supplied. Based on the evidence in the present study, a model is proposed to explain the poor performance of L. albus, whereby the release of carboxylates and associated protons reduces the chelating ability of exuded carboxylates, thus reducing P acquisition and increasing Al toxicity.

Aluminum Compounds↗

Assimilation and allocation of carbon and nitrogen of thermal and nonthermal Agrostis species in response to high soil temperature.

We studied whether changes in the assimilation and allocation of carbon and nitrogen are associated with plant tolerance to high soil temperatures. Two Agrostis species, thermal Agrostis scabra, a species adapted to high-temperature soils in geothermal areas in Yellowstone National Park (USA), and two cultivars of a cool-season species, Agrostis stolonifera, L-93 and Penncross, were exposed to soil temperatures of 37 or 20 degrees C, while shoots were exposed to 20 degrees C. Net photosynthesis rate, photochemical efficiency, NO(3) (-)-assimilation rate and root viability decreased with increasing soil temperatures in both species. However, the decreases were less pronounced for A. scabra than for both A. stolonifera cultivars. Carbon investment in growth of plants exposed to 37 degrees C decreased more dramatically in both A. stolonifera cultivars than in A. scabra. Nitrogen allocation to shoots was greater in A. scabra than in both creeping bentgrass cultivars at 37 degrees C soil temperature. Our results demonstrate that plant tolerance to high soil temperature is related to efficient expenditure and adjustment of C- and N-allocation patterns between growth and respiration.

Agrostis↗

Functional significance of dauciform roots: exudation of carboxylates and acid phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae).

Caustis blakei produces an intriguing morphological adaptation by inducing dauciform roots in response to phosphorus (P) deficiency. We tested the hypothesis that these hairy, swollen lateral roots play a similar role to cluster roots in the exudation of organic chelators and ectoenzymes known to aid the chemical mobilization of sparingly available soil nutrients, such as P. Dauciform-root development and exudate composition (carboxylates and acid phosphatase activity) were analysed in C. blakei plants grown in nutrient solution under P-starved conditions. The distribution of dauciform roots in the field was determined in relation to soil profile depth and matrix. The percentage of dauciform roots of the entire root mass was greatest at the lowest P concentration ([P]) in solution, and was suppressed with increasing solution [P], while in the field dauciform roots were predominantely located in the upper soil horizons, and decreased with increasing soil depth. Citrate was the major carboxylate released in an exudative burst from mature dauciform roots, which also produced elevated levels of acid phosphatase activity. Malonate was the dominant internal carboxylate present, with the highest concentration in young dauciform roots. The high concentration of carboxylates and phosphatases released from dauciform roots, combined with their prolific distribution in the organic surface layer of nutrient-impoverished soils, provides an ecophysiological advantage for enhancing nutrient acquisition.

Acid Phosphatase↗

Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of 'P toxicity'.

Grevillea crithmifolia R. Br. is a species of Proteaceae that is resistant to developing P-toxicity symptoms at phosphorus supplies in the root environment that induce P-toxicity symptoms in the closely related Hakea prostrata (Proteaceae). It was discovered previously that development of P-toxicity symptoms in H. prostrata is related to its low capacity to down-regulate net P-uptake rates (i.e. its low plasticity). The plasticity of net P-uptake rates and whole-plant growth responses in G. crithmifolia has now been assessed in two separate experiments: (i) a range of P, from 0 to 200 micromol P d-1, was supplied to whole root systems; (ii) using a split-root design, one root half was supplied with 0, 3, 75, or 225 micromol P d-1, while the other root half invariably received 3 micromol P d-1. Fresh mass was significantly greater in G. crithmifolia plants that had received a greater daily P supply during the pretreatments, but symptoms of P toxicity were never observed. Cluster-root growth decreased from about half the total root fresh mass when the leaf [P] was lowest (c. 0.1 mg P g-1 DM) to complete suppression of cluster-root growth when leaf [P] was 1-2 mg P g-1 DM. Split-root studies revealed that cluster-root initiation and growth, and net P-uptake rates by roots were regulated systemically, possibly by shoot P concentration. It is concluded that, in response to higher P supply, G. crithmifolia does not develop symptoms of P toxicity because of (i) greater plasticity of its net P-uptake capacity, and (ii) its greater plasticity for allocating P to growth and P storage in roots. This ecologically important difference in plasticity is most probably related to a slightly higher nutrient availability in the natural habitat of G. crithmifolia when compared with that of H. prostrata.

Acclimatization↗

Genetic and physiological architecture of early vigor in Aegilops tauschii, the D-genome donor of hexaploid wheat. A quantitative trait loci analysis.

Plant growth can be studied at different organizational levels, varying from cell, leaf, and shoot to the whole plant. The early growth of seedlings is important for the plant's establishment and its eventual success. Wheat (Triticum aestivum, genome AABBDD) seedlings exhibit a low early growth rate or early vigor. The germplasm of wheat is limited. Wild relatives constitute a source of genetic variation. We explored the physiological and genetic relationships among a range of early vigor traits in Aegilops tauschii, the D-genome donor. A genetic map was constructed with amplified fragment-length polymorphism and simple sequence repeat markers, and quantitative trait loci (QTL) analysis was performed on the F(4) population of recombinant inbred lines derived from a cross between contrasting accessions. The genetic map consisted of 10 linkage groups, which were assigned to the seven chromosomes and covered 68% of the D genome. QTL analysis revealed 87 mapped QTLs (log of the odds >2.65) in clusters, 3.1 QTLs per trait, explaining 32% of the phenotypic variance. Chromosomes 1D, 4D, and 7D harbored QTLs for relative growth rate, biomass allocation, specific leaf area, leaf area ratio, and unit leaf rate. Chromosome 2D covered QTLs for rate and duration of leaf elongation, cell production rate, and cell length. Chromosome 5D harbored QTLs for the total leaf mass and area and growth rate of the number of leaves and tillers. The results show that several physiological correlations between growth traits have a genetic basis. Genetic links between traits are not absolute, opening perspectives for identification of favorable alleles in A. tauschii to improve early vigor in wheat.

Biomass↗

Effects of water stress on respiration in soybean leaves.

The effect of water stress on respiration and mitochondrial electron transport has been studied in soybean (Glycine max) leaves, using the oxygen-isotope-fractionation technique. Treatments with three levels of water stress were applied by irrigation to replace 100%, 50%, and 0% of daily water use by transpiration. The levels of water stress were characterized in terms of light-saturated stomatal conductance (g(s)): well irrigated (g(s) > 0.2 mol H(2)O m(-2) s(-1)), mildly water stressed (g(s) between 0.1 and 0.2 mol H(2)O m(-2) s(-1)), and severely water stressed (g(s) < 0.1 mol H(2)O m(-2) s(-1)). Although net photosynthesis decreased by 40% and 70% under mild and severe water stress, respectively, the total respiratory oxygen uptake (V(t)) was not significantly different at any water-stress level. However, severe water stress caused a significant shift of electrons from the cytochrome to the alternative pathway. The electron partitioning through the alternative pathway increased from 10% to 12% under well-watered or mild water-stress conditions to near 40% under severe water stress. Consequently, the calculated rate of mitochondrial ATP synthesis decreased by 32% under severe water stress. Unlike many other stresses, water stress did not affect the levels of mitochondrial alternative oxidase protein. This suggests a biochemical regulation (other than protein synthesis) that causes this mitochondrial electron shift.

Adenosine Triphosphate↗

The occurrence of dauciform roots amongst Western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae).

* The incidence of species that develop specialised 'dauciform' lateral roots, which are hypothesised to be important for phosphorus (P) acquisition, is uncertain. We investigated their occurrence in Australian reed, rush and sedge species, grown at low P concentration in nutrient solution, and studied the response of Schoenus unispiculatus (Cyperaceae) to a range of P concentrations. * We assessed the fraction of root biomass invested in dauciform roots, their respiration and net P-uptake rate, and the P status of roots and leaves. * Dauciform-root development occurred only in particular genera of Cyperaceae when grown at low P supply. Increased P supply was associated with increased growth of S. unispiculatus and increased leaf [P]. Dauciform-root growth was reduced by increased P supply, and reduced P uptake co-occurred with the complete suppression of dauciform roots. * The P-induced suppression of dauciform roots in Cyperaceae is similar to that observed for proteoid roots in members of Proteaceae and Lupinus albus. The response of dauciform roots to altered P supply and their absence from root systems of some sedge species are discussed in terms of managed and natural systems.

Cyperaceae↗

A genetic analysis of relative growth rate and underlying components in Hordeum spontaneum.

Species from productive and unproductive habitats differ inherently in their relative growth rate (RGR) and a wide range of correlated quantitative traits. We investigated the genetic basis of this trait complex, and specifically assessed whether it is under the control of just one or a few genes that can act as 'master switches' by simultaneously affecting a range of traits in the complex. To address this problem, we crossed two Hordeum spontaneum lines originating from two habitats that differ in productivity. The F3 offspring, in which parental alleles are present in different combinations due to recombination and segregation, was analysed for RGR and its underlying components (leaf area ratio, unit leaf rate, photosynthesis, respiration), as well as a number of other physiological and morphological parameters. For this intra-specific comparison, we found a complex of positively and negatively correlated traits, which was quite similar to what is generally observed across species. A quantitative trait loci (QTL) analysis showed three major and one minor QTL for RGR. Most other variables of the growth-trait complex showed fewer QTLs that were typically scattered over various locations on the genome. Thus, at least in H. spontaneum, we found no evidence for regulation of the trait complex by one or two master switches.

Crosses, Genetic↗

From individual leaf elongation to whole shoot leaf area expansion: a comparison of three Aegilops and two Triticum species.

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.

Biomass↗

Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase.

Harsh hakea (Hakea prostrata R.Br.) is a member of the Proteaceae family, which is highly represented on the extremely nutrient-impoverished soils in southwest Australia. When phosphorus is limiting, harsh hakea develops proteoid or cluster roots that release carboxylates that mobilize sparingly soluble phosphate in the rhizosphere. To investigate the physiology underlying the synthesis and exudation of carboxylates from cluster roots in Proteaceae, we measured O2 consumption, CO2 release, internal carboxylate concentrations and carboxylate exudation, and the abundance of the enzymes phosphoenolpyruvate carboxylase and alternative oxidase (AOX) over a 3-week time course of cluster-root development. Peak rates of citrate and malate exudation were observed from 12- to 13-d-old cluster roots, preceded by a reduction in cluster-root total protein levels and a reduced rate of O2 consumption. In harsh hakea, phosphoenolpyruvate carboxylase expression was relatively constant in cluster roots, regardless of developmental stage. During cluster-root maturation, however, the expression of AOX protein increased prior to the time when citrate and malate exudation peaked. This increase in AOX protein levels is presumably needed to allow a greater flow of electrons through the mitochondrial electron transport chain in the absence of rapid ATP turnover. Citrate and isocitrate synthesis and accumulation contributed in a major way to the subsequent burst of citrate and malate exudation. Phosphorus accumulated by harsh hakea cluster roots was remobilized during senescence as part of their efficient P cycling strategy for growth on nutrient impoverished soils.

Carbon Dioxide↗

Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae).

Storage of phosphorus (P) in stem tissue is important in Mediterranean Proteaceae, because proteoid root growth and P uptake is greatest during winter, whereas shoot growth occurs mostly in summer. This has prompted the present investigation of the P distribution amongst roots, stems, and leaves of Hakea prostrata R.Br. (Proteaceae) when grown in nutrient solutions at ten P-supply rates. Glasshouse experiments were carried out during both winter and summer months. For plants grown in the low-P range (0, 0.3, 1.2, 3.0, or 6.0 micromol d(-1)) the root [P] was > stem and leaf [P]. In contrast, leaf [P] > stem and root [P] for plants grown in the high-P range (6.0, 30, 60, 150, or 300 micromol P d(-1)). At the highest P-supply rates, the capacity for P storage in stems and roots appears to have been exceeded, and leaf [P] thereafter increased dramatically to approximately 10 mg P g(-1) dry mass. This high leaf [P] was coincident with foliar symptoms of P toxicity which were similar to those described for many other species, including non-Proteaceae. The published values (tissue [P]) at which P toxicity occurs in a range of species are summarized. X-ray microanalysis of frozen, full-hydrated leaves revealed that the [P] in vacuoles of epidermal, palisade and bundle-sheath cells were in the mM range when plants were grown at low P-supply, even though very low leaf [P] was measured in bulk leaf samples. At higher P-supply rates, P accumulated in vacuoles of palisade cells which were associated with decreased photosynthetic rates.

Cells, Cultured↗

Maintenance of growth rate at low temperature in rice and wheat cultivars with a high degree of respiratory homeostasis is associated with a high efficiency of respiratory ATP production.

Some plants have the ability to maintain similar respiratory rates (measured at the growth temperature) when grown at different temperatures. This phenomenon is referred to as respiratory homeostasis. Using wheat and rice cultivars with different degrees of respiratory homeostasis (H), we previously demonstrated that high-H cultivars maintained shoot and root growth at low temperature [Kurimoto et al. (2004) Plant Cell Environ., 27: 853]. Here, we assess the relationship between respiratory homeostasis and the efficiency of respiratory ATP production, by measuring the levels of alternative oxidase (AOX) and uncoupling protein (UCP), which have the potential to decrease respiratory ATP production per unit of oxygen consumed. We also measured SHAM- and CN-resistant respiration of intact roots, and the capacity of the cytochrome pathway (CP) and AOX in isolated mitochondria. Irrespective of H, SHAM-resistant respiration of intact roots and CP capacity of isolated root mitochondria were larger when plants were grown at low temperature, and the maximal activity and relative amounts of cytochrome c oxidase showed a similar trend. In contrast, CN-resistant respiration of intact roots and relative amounts of AOX protein in mitochondria isolated from those roots, were lower in high-H plants grown at low temperature. In the roots of low-H cultivars, relative amounts of AOX protein were higher at low growth temperature. Relative amounts of UCP protein showed similar trends to AOX. We conclude that maintenance of growth rate in high-H plants grown at low temperature is associated with both respiratory homeostasis and a high efficiency of respiratory ATP production.

Adenosine Triphosphate↗

Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation.

The effects were studied of both nitrogen and phosphorus limitation and irradiance on the performance and operation of photosynthesis in tomato leaves (Lycopersicon esculentum Mill.). Plants were grown at low N, high N, low P or high P supply and at two irradiances. Using mature leaves, measurements were made of the irradiance dependencies of the relative quantum efficiencies of photosystems I and II, and of the rate of carbon dioxide fixation. Measurements were also made of foliar starch and chlorophyll concentrations. The results showed that photosynthetic light-harvesting and electron-transport activity acclimate to nutrient stress and growth irradiance such that the internal relationships between electron transport by photosystems I and II do not change; the linear relationship between PhiPSII, and PhiPSI was not affected. It was also evident that under N stress photosynthesis was reduced by a decreased light absorption and by the decreased utilization of assimilates, while P stress mainly affected the carboxylation capacity. Under N stress foliar starch levels increased and the oxygen sensitivity of CO2 fixation decreased, whereas P stress resulted in decreased starch levels and increased oxygen sensitivity of CO2 fixation. The relationship between starch accumulation and oxygen sensitivity (increased starch correlated with decreased oxygen sensitivity) was always the same across the nutrient treatments. These results are consistent with N deprivation producing an increasing limitation of photosynthesis, possibly by feedback from the leaf carbohydrate pool, whereas, although P deprivation produces a decreased rate of CO2 fixation, this is accompanied by a increase in oxygen sensitivity, suggesting that feedback limitation is decreased under P stress.

Acclimatization↗

Role of sugars and organic acids in regulating the concentration and activity of the alternative oxidase in Poa annua roots.

Detached roots of Poa annua were used to study alternative oxidase protein expression upon the addition of sucrose, glucose, fructose, inositol, mannitol, citrate or malate, at a concentration of 1 or 10 mM for 24 h. After 24 h the capacity of cytochrome c oxidase was decreased equally in all treatments. Only citrate induced the expression of the alternative oxidase, especially at a concentration of 1 mM (15-fold). The activity of the alternative pathway (measured with the (18)O-fractionation technique) was not affected by the addition of sucrose for 24 h as compared with time zero. However, after the addition of citrate or mannitol the activity of the alternative pathway decreased to almost zero. The discrepancy between the large increase in alternative oxidase protein concentration when citrate was applied and the concomitant decrease in alternative pathway activity is discussed.

Carbohydrates↗