Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status

Vesicular-arbuscular mycorrhizae may increase resistance of plants to drought by a number of mechanisms, such as increased root hydraulic conductivity, stomatal regulation, hyphal water uptake and osmotic adjustment. However, a substantial contribution of vesicular-arbuscular mycorrhizal (VAM) hyphae to water uptake has not been demonstrated unequivocally. The objective of this investigation was to examine the contribution of hyphae from two VAM fungi to water uptake and transport by the host plant. Lettuce (Lactuca sativa L.) plants were grown in a container divided by a screen into two compartments. One was occupied by roots, the other only by VAM hyphae, which the screen permitted to pass. Roots were colonized by the VAM fungi Glomus deserticola or Glomus fasciculatum, or were left uninoculated but P-supplemented. Water was supplied to the hyphal compartment at a distance of 10 cm from the screen (root). CO₂ exchange rate, water-use efficiency, transpiration, stomatal conductance and photosynthetic phosphorus-use efficiency of VAM or P-amended control plants were evaluated at three levels of water application in the hyphal compartment. Results indicate that much of the water was taken up by the hyphae in VAM plants. VAM plants, which had access to the hyphal compartment, had higher water and nutrient contents. G. deserticola functioned efficiently under water limitation and mycelium from G. fasciculatum-colonized plants was very sensitive to water in the medium. This discrepancy in VAM behaviour reflects the various abilities of each fungus according to soil water levels. Different abilities of specific mycelia were also expressed in terms of nutritional and leaf gas-exchange parameters. G. fasciculatum caused a significant increase in net photosynthesis and rate of water use efficiency compared to G. deserticola and P-fertilized plants. In contrast, the G. deserticola treatment was the most efficient affecting N, P and K nutrition, leaf conductance and transpiration. Since no differences in the intra- and extra-radical hyphal extension of the two endophytes were found, the results demonstrate that mycorrhizal hyphae can take up water and that there are considerable variations in both the behaviour of these two VAM fungi and in the mechanisms involved in their effects on plant water relations.     

Stimulation of Growth and Nutrient Uptake by VAM Fungi in Brassica Oleracea Var. Capitata

Cabbage (Brassica oleracea, var. capitata, cv. Hercules) seedlings were inoculated with vesicular-arbuscular mycorrhizal (VAM) fungi Glomus fasciculatum, G. aggregatum, and G. mosseae. Differential efficiency in mycorrhizal colonization and the specificity of fungal symbiont to stimulate the growth and nutrient uptake of the host were observed. In addition, there was an increase in phenol, protein, reducing sugar contents, and peroxidase activity in the VAM inoculated seedlings. Since these compounds are known to confer resistance against fungal pathogens, the use of VAM as a biological control agent to protect cabbage against several root diseases is suggested.     

Use of pesticides for mass production of vesicular-arbuscular mycorrhizal inoculum

Nine fungicides, 3 nematicides and 5 insecticides/acaricides were incorporated into the pot cultures of the VAM fungusGlomus fasciculatum in order to study their effect on the mycorrhizal association and the contaminant organisms. All the pesticides were found to be deleterious to VAM at the recommended level. Captan and carbofuran, at half the recommended level (125 mg and 144.5 mg respectively/2.5 litre of the substrate mix), increased significantly the percentage root colonization, extra-matrical chlamydospore number and inoculum potential. Captan and carbofuran at this level also significantly suppressed the contaminant fungi and nematodes in the pot cultures ofG. fasciculatum. The insecticides/acaricides formothion and malathion at half the recommended level, had no deleterious effect onG. fasciculatum but suppressed mites and collumbola in pot cultures.     

Drought resistance of wheat plants inoculated with vesicular-arbuscular mycorrhizae

Summary Drought resistance of wheat (Triticum aestivum L.) as influenced by two vesiculararbuscular mycorrhizal (VAM) fungi,Glomus fasciculatum ¹⁰ andGlomus deserticola ¹⁹, was evaluated. Soil columns 0.15 m diam. by 1.20 m length were used to reduce the influence of limited rooting space. With initial soil water at 0.5 MPa (0.145 kg kg^–1), plants were subjected to low-level water stress throughout the experiment and severe water stress for 24 h at one (55 days after transplanting, Feekes scale 10.1) two (55 and 63 days, Feekes 10.1 and 10.2), or three (55, 63, and 70 days, Feekes 10.1, 10.1, and 10.2) periods. After each stress period, one set of plants was watered and grown to maturity without subsequent water stress. A second set of plants was harvested 1 week after stress.G. fasciculatum-inoculated plants harvested 7 days after stress at 55 days had greater leaf area and leaf, total plant, and root weight than non-VAM plants.G. deserticola-inoculated plants had greater leaf area and leaf weight than non-VAM plants. After stress at 55 and 63 days, leaf area, and leaf and total dry weight were again greater for VAM than for non-VAM plants. However, after stress at 55, 63, and 70 days, differences in aboveground biomass between VAM and non-VAM plants were not significant at P=0.05. Aboveground biomass was not affected by VAM species in plants stressed at 55 or 55 and 63 days, butG. fasciculatum-inoculated plants produced more tillers atter stress at 55 days. When grown to maturity, VAM plants which had undergone three stress periods had twice the biomass and grain yield as non-VAM plants subjected to the same stress. The three stress periods reduced number of heads and kernel numbers of weight of non-VAM plants compared to VAM plants.G. fasciculatum-inoculated plants consistently had increased root weight and rooting depth.Contribution from the Agricultural Research Service, USDA, in cooperation with the Nebr. Agric. Exp. Stn., Univ. Nebr.-Lincoln, Lincoln, Nebr. Published as Paper No. 7571 Journal Series, Nebr. Agric. Exp. Stn.     

Development of two endomycorrhizal symbioses on soybean and comparison with phosphorus fertilization

Summary Soybean (Glycine max L. Merr. cv. Amsoy 71) plants were grown in a greenhouse in a soil very low in plant-available P, and plants were harvested 5 times over a 21-week growth period. Soybeans were inoculated with one of two species of VAM fungi or received daily one of three nutrient solutions of different P concentrations (0.0, 0.2, or 1.0mMP). Until week 9, the dry weights, leaf areas and developmental stage of soybeans inoculated withG. fasciculatum orG. mosseae were similar to the 1.0 or 0.2mMP-treated plants, respectively. Phosphorus concentrations were significantly lower in VAM plants at weeks 6 and 9 as compared to non-VAM soybeans given 1.0mMP, suggesting P input in VAM plants was immediately used for new growth. Total P input for VAM plants was linear over 21 weeks, and the average rate of P uptake for these plants was 0.19mg P d⁻¹. Estimated specific P uptake rates (SPUR) for the mycorrhizae (VAM roots) were twice that of the control (0.0mMP) roots. The calculated SPURs forG. fasciculatum andG. mosseae hyphae were 95 and 120μg P g⁻¹ VAM d⁻¹ respectively, a 4 to 5 fold increase over non-inoculated roots, indicating more attention must be paid to P assimilation by VAM fungi in P-fixing substrates. Contribution from the Western Regional Research Center, USDA-ARS (CRIS No. 5325-20580-003).     

Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogenPhytophthora fragariae

Three strawberry cultivars Elsanta, Cambridge Favourite and Rhapsody were inoculated with eitherGlomus fasciculatum orGlomus etunicatum and their growth compared with non-inoculated plants. The roots of all inoculated plants were 55 to 70% colonised after 98 days. Increases in both root and shoot dry weights were measured. Root architecture was also determined and increases in branching were evident in AMF colonised root systems. The remaining plants were then inoculated with the root pathogenPhytophthora fragariae and allowed to grow for a further 58 days before harvest. In two of the cultivars, Cambridge Favourite and Elsanta, AMF reduced root necrosis by approximately 60 and 30% respectively. Only in the least susceptible cultivar, Rhapsody, was no reduction measured in AMF colonised plants. There were differences in the control conferred by the two arbuscular mycorrhizal fungi and this suggests there may be practical benefits of inoculation. Relationships between the presence of roots of different orders, on inoculation with the pathogen, and subsequent necrosis provided a mechanism for identifying root-architecture driven alteration to susceptibility. Root system necrosis was positively correlated with the proportion of the root system made up of higher order roots (3° to 4°) in non-colonised plants and negatively correlated in AMF colonised plants. These data suggest that root-architecture changes are not important per se but factors expressed concurrently may be.     

Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (<Emphasis Type="Italic">Solanum lycopersicum</Emphasis>) plants infected with necrotrophic or hemibiotrophic pathogens

A study was performed to determine the effect of the systemin polypeptide on the bio-protective effect of arbuscular mycorrhizal fungi (AMF) in tomato plants infected with Alternaria solani, Phytophthora infestans or P. parasitica. Before infection, tomato plants were colonized with two different AMF, Glomus fasciculatum or G. clarum. In addition, a group of inoculated plants was treated with systemin, just after emergence. The exogenous application of systemin marginally suppressed the resistance against A. solani leaf blight observed in G. fasciculatum mycorrhizal plants but significantly enhanced it in plants colonized with G. clarum. Systemin induced resistance to P. parasitica in leaves of G. fasciculatum mycorrhizal plants, in which AMF colonization alone was shown to have no protective effect. Conversely, none of the treatments led to resistance to root or stem rots caused by P. infestans or P. parasitica. The above effects did not correlate with changes in the activity levels of β-1,3-glucanase (BG), chitinase (CHI), peroxidase (PRX), and phenylalanine ammonium lyase (PAL) in leaves of infected plants. However, they corroborated previous reports showing that colonization by AMF can lead to a systemic resistance response against A. solani. Systemic resistance to A. solani was similarly observed in non-mycorrhizal systemin-treated plants, which, in contrast, showed increased susceptibility to P. infestans and P. parasitica. The results indicated that the pattern of systemic disease resistance conferred by mycorrhizal colonization was dependent on the AMF employed and could be altered by the exogenous application of systemin, by means of a still undefined mechanism.     

Real‐time PCR Suggests that Aphanomyces euteiches is Associated with Reduced Amounts of Phytophthora medicaginis in Alfalfa that is Co‐inoculated with Both Pathogens

Aphanomyces euteiches and Phytophthora medicaginis are two pathogens of seedling and mature alfalfa (Medicago sativa L.) that are frequently found in the same field sites. In order to investigate possible interactions of these two pathogens, two greenhouse experiments were conducted on seedling alfalfa from check populations representing the phenotypic classes of dual susceptibility and dual resistance to both pathogens. Seedlings were challenged with multiple inoculum concentrations of A. euteiches and P. medicaginis. Separate real‐time PCR assays specific for A. euteiches and P. medicaginis were used to quantify the amount of each pathogen in root tissue. For both pathogens, significantly more pathogen DNA was detected in the susceptible check population Saranac than in the resistant check population WAPH‐1 in all treatment combinations. In general, co‐inoculation with both A. euteiches and P. medicaginis resulted in significantly reduced amounts of P. medicaginis DNA detected when compared with amounts detected from inoculations with P. medicaginis alone. This relationship was observed for the analysis of bulked plant samples and also for individual plants. Co‐infestation by both pathogens did not reduce the quantity of A. euteiches detected. Possible mechanisms responsible for the inhibition of accumulation of P. medicaginis by A. euteiches are discussed.     

Preparation of gel-entrapped mycorrhizal inoculum in the presence or absence of Yarowia lipolytica

Two arbuscular mycorrhizal fungi (Glomus deserticola and Glomus fasciculatum) were entrapped in calcium alginate, alone or in combination with a phosphate-solubilizing yeast (Yarowia lipolytica) and, after storage for 60 days, were inoculated into soil microcosms with tomato as the test plant. The average extent of root colonization by gel-entrapped G. deserticola and G. fasciculatum were 32 ± 5.6 and 24 ± 12.1%, respectively. Improved infective potential and colonization efficiency were observed when Y. lipolytica was co-entrapped with the mycorrhizal fungi. The best value, 49%, of mycorrhizal colonization was in roots of plants inoculated with G. deserticola co-entrapped with Y. lipolytica.     

Proteomic Profiling Unravels Insights into the Molecular Background Underlying Increased <Emphasis Type="Italic">Aphanomyces euteiches</Emphasis>-Tolerance of <Emphasis Type="Italic">Medicago truncatula</Emphasis>

To investigate the molecular mechanisms underlying susceptibility of legumes to the root pathogen Aphanomyces euteiches (oomycota), comparative proteomic studies have been carried out. In a first approach, we have analysed two Medicago truncatula lines of the French CORE collection (F83.005-5 (R2002) and F83.005-9 (R2002)), which showed either increased or decreased susceptibility to A. euteiches as compared to the widely adopted line A17. Several proteins were identified to be differentially induced after pathogen challenge in the two M. truncatula accessions with altered disease susceptibility, whereof proteins with increased abundances in the more resistant line F83.005-9 could be involved in mechanisms that lead to an improved disease resistance. Among these proteins, we identified two proteasome alpha subunits, which might be involved in defense response. To broaden our studies on A. euteiches-tolerance of M. truncatula, we investigated two other phenomena that lead to an either increased A. euteiches-resistance or to an enhanced susceptibility. The topic of an enhanced plant resistance to A. euteiches was studied in plants showing a bioprotective effect of a pre-established arbuscular mycorrhiza (AM) symbiosis. Evaluation of root fresh weights and pathogen spreading in the root system clearly indicate that mycorrhizal plants show increased A. euteiches-resistance as compared to non-mycorrhizal plants. Proteome analyses revealed the induction of similar protein patterns as in the M. truncatula accessions with comparatively high resistance level to A. euteiches. In a third approach, increased A. euteiches susceptibility was effected by exogenous abscisic acid (ABA) application prior to root infection. Evaluation of the abundance levels of a group of pathogenesis related class 10 (PR10)-like proteins, which were previously identified to be regulated after A. euteiches infection, revealed a correlation between the abundance levels of these proteins and the A. euteiches infection level or severity. Requests concerning seeds from the Medicago truncatula lines F83.005-5 and F83.005-9 should be addressed to Jean-Marie Prospéri, INRA-SGAP Laboratory, Laboratoire de Ressources Génétiques et d’Amélioration des Luzernes méditerranéennes, Mauguio, France, jean-marie.prosperi@ensam.inra.fr.     

Biological control of root-rot disease complex of chickpea by AM fungi

Abstract

Six species AM fungi, namely Glomus fasciculatum, G. constrictum, G. intraradices sp., Gigaspora margarita, Acaulospora sp. and Sclerocystis sp., were used for the biological control of root-rot disease complex of chickpea caused by Meloidogyne incognita and Macrophomina phaseolina. Application of these AM fungi increase plant growth, pod number, chlorophyll, nitrogen, phosphorus and potassium contents in diseased plants and also reduced nematode multiplication and root-rot index. G. fasciculatum caused greater increase in plant growth, pod number, chlorophyll, nitrogen, phosphorus and potassium contents of pathogen inoculated plants followed by G. intaradices, G. constrictum, Sclerocystis, G. margarita and Acaulospora sp. Percent root colonization caused by G. fasciculatum was high followed by G. intaradices, G. constrictum, Sclerocystis sp., G. margarita and Acaulospora sp. Glomus fasciculatum also caused higher reduction in root-rot index, galling and nematodes multiplication while Acaulospora sp. produced the least.     

Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intraradices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches

 The effects of inorganic phosphate levels and the presence of arbuscular mycorrhiza on disease severity of Aphanomyces euteiches in pea roots were studied. Disease severity on roots and epicotyl as well as the oospore number within infected root tissue were correlated with the phosphorus (P) level in the growth medium. The arbuscular mycorrhizal fungus Glomus intraradices increased P uptake and the P concentration in the plant but reduced disease development in peas. Polyacrylamide gel electrophoresis followed by densitometry of glucose-6-phosphate dehydrogenase specific to A.euteiches was used to measure the activity of the pathogen in roots. The enzyme activity increased with disease severity and disease incidence, except in plants supplemented with P at the highest level, where a peak in activity was seen 12 days after inoculation with the pathogen, followed by a decrease in activity. The epicotyl of mycorrhizal plants showed a reduction in disease severity although this part of the plants was not mycorrhizal. Thus, an induced systemic factor may be responsible for increased resistance in mycorrhizal plants. Accepted: 21 August 1998     

Induced Resistance in the Biocontrol of Pythium aphanidermatum by Pseudomonas spp. on Cucumber

Plants of Cucumis sativus cv. Corona were grown in rockwool, with the root systems split into two separate pots. B pots were treated with water or a cell suspension of Pseudomonas corrugata isolate 13 or P. fluorescens biovar C isolate 15, two rhizosphere isolates effective as biocontrol agents against Pythium aphanidermatum. The P pot was treated with water or a suspension of zoospores of P. aphanidermatum applied at the same time (simultaneous treatment) or 1 week after B pot treatments. Most of the bacterial treatments reduced disease incidence and disease severity. Simultaneous treatment with isolate 15 increased shoot dry weight, leaf area, and number of fruit of inoculated plants in one trial. Some treatments with isolate 13 or 15 also increased root volume or root dry weight in B or P pots, compared to the inoculated plants where the B pot was treated with water only (Pythium control). Lower population densities of P. aphanidermatum in P pots were detected in some treatments to which bacteria were applied to the B pot, but only in the early stages of the experiment. This is the first report of systemic-induced resistance against a root pathogen in cucumber obtained by application of Pseudomonas spp. to a root system spatially separated from the pathogen-inoculated root.     

Histological, Physiological and Biochemical Interactions between Vesicular-Arbuscular Mycorrhizae and Thielaviopsis basicola in Tobacco Plants

Interactions between the mycorrhizal fungus Glomus monosporum and the root rot pathogen Thielaviopsis basicola and their effects on tobacco plants were investigated over a 4 week period. Mycorrhizal tobacco plants, obtained by preinoculation with G. monosporum, showed a better tolerance to T. basicola than non-mycorrhizal seedlings. Root and leaf dry weights of mycorrhizal plants were greater than those of controls. Mycorrhizal plants inoculated with T. basicola showed higher root and leaf dry weights than non-mycorrhizal infected plants, but lower values than mycorrhizal plants which were not infected. No appreciable differences in free aminoacid composition were observed among the different treatments with two exceptions: proline content was higher in infected and mycorrhizal infected plants compared to control and mycorrhizal plants; arginine content was higher in infected and mycorrhizal infected plants compared to control and mycorrhizal plants; arginine content was higher in mycorrhizal plants than in all the other treatments. The mechanisms by which (VAM) fungi can reduce disease incidence and pathogen development are discussed.     

Effect of arbuscular mycorrhizal fungi and Pseudomonas fluorescens on root-rot and wilt,growth and yield of Coleus forskohlii

Root-rot and wilt caused by Fusarium chlamydosporum affects the cultivation of Coleus forskohlii, a medicinal plant grown for its roots, which contain a pharmaceutically important compound called forskolin. In this study, management of this disease under low and high inoculum levels was assessed with four arbuscular mycorrhizal (AM) fungi and a strain of Pseudomonas fluorescens. The AM fungus Glomus fasciculatum and P. fluorescens were the most effective treatments that reduced the severity of root-rot and wilt of C. forskohlii by 56–65% and 61–66%, respectively, under lower and higher levels of pathogen F. chlamydosporum. G. fasciculatum increased the dry shoot and root weight by 108–241% and 92–204%, respectively, while in plants treated with P. fluorescens, an increase of 97–223% and 97–172% in dry shoot and root weight, respectively, was observed. Although P. fluorescens was effective, it gave higher root yields only under lower inoculum level of the pathogen. G. fasciculatum performed equally well under both lower and higher inoculum levels. Increase in yields with both the biocontrol agents was accompanied by increase in P uptake (230–303%) and in K uptake (270–335%). The forskolin content of the roots was significantly increased (14–21%) by G. fasciculatum, P. fluorescens or G. mosseae under lower inoculum level of pathogen.     

Interaction of Vesicular-Arbuscular Mycorrhizae and Cultivars of Alfalfa Susceptible and Resistant to Meloidogyne hapla

The interaction between vesicular-arbuscular mycorrhizal (VAM) fungi and the root-knot nematode (Meloidogyne hapla) was investigated using both nematode-susceptible (Grasslands Wairau) and nematode-resistant (Nevada Synthetic XX) cultivars of alfalfa (Medicago sativa) at four levels of applied phosphate. Mycorrhizal inoculation improved plant growth and reduced nematode numbers and adult development in roots in dually infected cultures of the susceptible cultivar. The tolerance of plants to nematode infection and development when preinfected with mycorrhizal fungi was no greater than when they were inoculated with nematodes and mycorrhizal fungi simultaneously. Growth of plants of the resistant cultivar was unaffected by nematode inoculation but was improved by mycorrhizal inoculation. Numbers of nematode juveniles were lower in the roots of the resistant than of the susceptible cultivar and were further reduced by mycorrhizal inoculation, although no adult nematodes developed in any resistant cultivar treatment. Inoculation of alfalfa with VAM fungi increased the tolerance and resistance of a cultivar susceptible to M. hapla and improved the resistance of a resistant cultivar.     

The presence of the arbuscular mycorrhizal fungus Glomus intraradices influences enzymatic activities of the root pathogen Aphanomyces euteiches in pea roots

 Fungal enzyme activities were quantified in an interaction study between the fungus Glomus intraradices and the pea pathogen Aphanomyces euteiches. Fungal and host enzymes were separated by polyacrylamide gel electrophoresis and the activity of A. euteiches–specific glucose-6-phosphate dehydrogenase (Gd), phosphoglucomutase and peptidase (PEP) enzymes were quantified by densitometry. The activity of A. euteiches–specific enzymes increased until 14 days after inoculation with A. euteiches, and then decreased. The plants preinoculated with G. intraradices showed no symptoms of severe root rot even though the pathogen was present and active in these plants. Thus, plants preinoculated with G. intraradices were more tolerant of infection with A. euteiches than non-mycorrhizal plants. This effect was evident even though the A. euteiches infection levels of mycorrhizal and non-mycorrhizal plants were the same. A. euteiches enzyme activities in the mycorrhizal plants were different to those in non-mycorrhizal plants. The peaks of PEP and Gd enzyme activity of A. euteiches were lower and the development of A. euteiches PEP activity was later in the mycorrhizal plants than in the non-mycorrhizal plants. Accepted: 14 November 1996     

Field response of mycorrhizal and nonmycorrhizal Medicago sativa var. local in the F1 generation

Seeds were collected from plants of Medicago sativa var. local inoculated with Glomus macrocarpum and G. fasciculatum separately in pot experiments. These seeds were sown in garden soil and the percentage germination, general health and yield of subsequent plants (the F1 generation) were studied. The percentage germination was highest in seeds of G. macrocarpum-inoculated parents followed by those inoculated with G. fasciculatum; seeds of uninoculated parent plants showed the lowest germination. Vegetative yield of the progeny decreased in the order of plants inoculated with G. fasciculatum, with G. macrocarpum, and uninoculated. On the other hand, reproductive yield was highest for plants whose parents were inoculated with G. macrocarpum, followed by G. fascicullatum, and lowest for seeds of uninoculated parent plants.     

Effects of vesicular-arbuscular mycorrhizal inoculation at different soil P availabilities on growth and nutrient uptake of in vitro propagated coffee (Coffea arabica L.) plants

 In a pot experiment, the growth and the nutrient status of in vitro propagated coffee (Coffea arabica L.) microcuttings were investigated for 5 months following vesicular-arbuscular mycorrhizal (VAM) inoculation with either Acaulospora melleae or Glomus clarum at four soil P availabilities. Control plants remained P-deficient even at the highest soil P availability while mycorrhizal plants were P-sufficient at all soil P availabilities. Growth of control plants was only improved at the highest soil P availability. In P-deficient soil, neither of the two VAM species improved plant growth. Plant growth increased by 50% following inoculation with either A. melleae or G. clarum when P availability went from deficient to low. No further plant growth improvement was induced by either VAM species at intermediate and high soil P levels. Nevertheless, growth of plants inoculated with G. clarum was still significantly greater than that of non-mycorrhizal plants at the highest soil P availability. Root colonization by G. clarum increased with increasing soil P availability while root colonization by A. mellea decreased with soil P level increasing above low P availability. Soil P availability also affected Zn nutrition through its influence on VAM symbiosis. With increasing soil P availability, foliar Zn status increased with G. clarum or decreased with A. mellea in parallel to root colonization by VAM. This study demonstrates the beneficial effects of VAM inoculation on in vitro propagated Arabica coffee microcuttings, as shown previously for seedlings. This study also demonstrates differences in tolerance to soil P availability between VAM species, most likely resulting from their differing abilities to enhance coffee foliar P status. Accepted: 14 November 1996