21111 Lakeshore Road, Ste-Anne-de-Bellevue, Quebec, H9X 3V9, Canada. 3 Central Experimental Farm, Agriculture Canada, Ottawa, Ontario K1A OC6, Canada

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1 Plant and Soil 221: , Kluwer Academic Publishers. Printed in the Netherlands. 157 Mycorrhizae formation and nutrient uptake of new corn (Zea mays L.) hybrids with extreme canopy and leaf architecture as influenced by soil N and P levels A. Liu 1,C.Hamel 1,, R. I. Hamilton 3 and D. L. Smith 2 1 Department of Natural Resource Sciences and 2 Department of Plant Science, Macdonald Campus, McGill University, Lakeshore Road, Ste-Anne-de-Bellevue, Quebec, H9X 3V9, Canada. 3 Central Experimental Farm, Agriculture Canada, Ottawa, Ontario K1A OC6, Canada Received 23 February Accepted in revised form 25 January 2000 Key words: arbuscular mycorrhizal fungi, corn hybrid, extraradical hyphae, mycorrhizal colonization, N/P ratio, nutrient uptake Abstract A study was conducted to evaluate the effect of N and P supply levels on mycorrhizal formation and nutrient uptake in corn hybrids with different architectures and to determine arbuscular mycorrhizal fungal (AMF) development in relation to shoot N/P ratio and shoot:root ratio. Corn pot cultures with a pasteurized medium of two parts sand and one part sandy loam soil were grown in the greenhouse. Marigold plants inoculated or not with Glomus intraradices Schenck & Smith were used to establish an AMF hyphal network in the designated soil pots. Corn hybrids were seeded after removal of the marigold plant. Mycorrhizal colonization of corn hybrids and the quantity of extraradical hyphae produced in soil were greatest at the lowest P level and at the intermediate N level. Root colonization was correlated with shoot N/P ratio only at the intermediate N level. The shoot concentrations of P, Mg, Zn and Cu were significantly higher in mycorrhizal plants than in non-mycorrhizal plants. The corn phenotype with the highest shoot:root ratio had the highest root colonization. The corn hybrid with a leafy normal stature architecture had a greater mycorrhizal colonization than that of other two corn hybrids. This experiment showed that N level in soil influenced shoot N/P ratio, root colonization and extraradical hyphal production, which in turn influenced uptake of other nutrients. Introduction Experiments with several crops such as pearl millet, pea and soybean indicated that arbuscular mycorrhizal fungal (AMF) development varies among genotypes (Daft, 1991; Estaun et al., 1987; Heckman and Angle, 1987). Two newly available corn hybrids, Leafy reduced-stature (LRS) and Leafy normal-stature (LNS) hybrids with extreme root and shoot architectures (Modarres et al., 1997) were developed at the Plant Research Centre, Agri-Food Canada (Ottawa, ON). These hybrids offer an opportunity to test mycorrhizae formation in different phenotypes within a crop species. LRS and LNS have greater above- FAX No: hamel@nrs.mcgill.ca ear leaf area, above-ear leaf number and total leaf number than non-leafy hybrids with the same stature (Modarres et al., 1997). The leaf length and width of LNS are greater than those of LRS. According to an unpublished study (Costa, pers. comm.) on the root architecture of several corn hybrids at early stages of development (up to 20 days) and direct observation of mature plants, the LNS hybrid has a more branched but smaller root system than that of conventional hybrids with the similar height, and LRS has less branched and smaller root system than LNS. Little is known about other root characteristics and mycorrhizal potential. Mycorrhizae are important for optimal root function. The symbiotic association increases uptake of relatively immobile nutrients, such as P, Cu and Zn

2 158 (Faber et al., 1990; Kothari et al., 1991; Li et al., 1991). Mycorrhizae also enhance uptake and transport of 15 N (Hamel et al., 1991; Johansen et al., 1992, 1993; Tobar et al., 1994) and in contrast, often reduce Mn uptake (Kothari et al., 1991; Posta et al., 1994). Corn has a high demand for N and P nutrients (Jokela and Randall, 1989; Olson and Sander, 1988). In order to get a high yield, large amounts of N and P fertilizers are applied (Barry and Miller, 1989). Consequently, N and P fertilization levels are high in a large percentage of corn fields. This could influence AMF development. Colonization is often negatively correlated with soil P values (Abbott and Robson, 1984). The influence of N on the mycorrhizal association is less consistent than is the influence of P. Several studies have indicated that N fertilization could decrease the proportion of roots colonized by arbuscular mycorrhizal (AM) fungi and the number of spores produced (Hayman, 1970, 1975). In greenhouse studies, N has been reported to either increase (Azcon et al., 1982; Hepper, 1983) or decrease mycorrhizal colonization (Johnson et al., 1980, 1984; Mugnier and Mosse, 1987). Sylvia and Neal (1990) demonstrated that P had a greater effect on root colonization in N-sufficient soils than in N-deficient soils. Little attention has been paid to the interactions between N and P supply and plant phenotype on mycorrhizal formation and nutrient uptake. The objectives of this study were (1) to evaluate the effect of three levels of N and P fertilization on mycorrhizal formation and nutrient uptake in three corn hybrids with highly different architectures, and (2) to determine the potential for AMF colonization and development in these hybrids in relation to shoot:root ratio and the N/P ratio in shoots. Materials and methods Experimental design This experiment was a factorial arranged in a completely randomized design with four replicates. The four factors were three N rates (0, 70 and 140 mg N kg 1 soil), three P rates (0, 40 and 80 mg P kg 1 soil), three hybrids (LNS, LRS and Pioneer 3979) and two mycorrhizal treatments (mycorrhizal and non-mycorrhizal). Establishment of experimental units Two parts sand and one part of a light field soil (coarse -silty, mixed, nonacid, frigid Humaquept) were used as a substrate. This substrate had low N and P levels and allowed the establishment of three N and three P levels ranging from low to high. The KCl extractable NH + 4 and NO 3, and Mehlich-3 (Mehlich, 1984) extractable P, Ca and Mg in the mix were 3.22, 9.30, 42, 143 and 13.2 mg kg 1, respectively. Concentrations of total Fe, Mn, Zn and Cu in the mix were 9600, 204, 38 and 7.0 mg kg 1, and DTPA (Lindsay and Norvell, 1978) extractable Fe, Mn, Zn and Cu were 17.4, 2.42, 0.42 and 0.22 mg kg 1, respectively. Pots (25 cm diameter 22 cm height) were filled with the pasteurized substrate. A network of AMF hyphae was established in the soil of the mycorrhizal treatment prior to corn cultivation to simulate the inoculum status of a field soil under conservation management. Marigold plants were used to establish AMF hyphal networks in pot substrate as follows. One marigold plant was seeded in a30 µm mesh bag filled with the medium inoculated with Glomus intraradices Schenck & Smith, DAOM (isolated from a commercial tree nursery in the 1970s and kept in culture) and placed into the center of each pot to allow hyphae but not the marigold roots to propagate into the medium. The plants grew under greenhouse conditions with 16/8 h day/night regime, 300 µmol 2 s 1 photo flux density, 75% relative humidity and at 26/22 C. Pots were watered to field capacity three times a week. Ammonium nitrate was appliedat20mgnkg 1 soil to all pots. After 2 months of growth, the bags containing the marigold roots were taken out of the pots, leaving behind an established AMF network in the soil of the mycorrhizal treatments. The central holes were filled using the same medium with AMF hyphae taken from extra pots. Non-mycorrhizal treatments were produced in a similar manner, except the medium in the mesh bags did not contain Glomus intraradices. Before corn was grown, an analysis indicated that extractable NH + 4, NO 3 and P were the same in all the pots. Corn seeds were surface sterilized with 30% H 2 O 2 for 10 min and washed several times with distilled water. After they have germinated in Petri dishes for three days, seeds were sown in the prescribed pots. Ammonium nitrate ( NH 4 NO 3 ) and potassium phosphate monobasic (KH 2 PO 4 ) solutions were used to establish target N and P levels, respectively. The cultivation conditions, including temperature, photoperiod, light

3 159 intensity, humidity and irrigation for the corn were the same as those for marigold growth. Harvest After 2 months of growth, corn shoots and roots were harvested separately. All roots were collected by sieving with a 2.0 mm mesh screen and washed with tap water to remove any remaining soil. Shoot and root dry weights were determined after drying at 70 Cfor 48 h. Extracting, staining and measuring soil hyphae Hyphal extraction and staining procedures were modified from Miller and Jastrow s (1992) procedure. A moist 20-g soil sub sample from each pot was placed in a 50 ml centrifugation tube containing 40 ml of 2 M sucrose and 2% sodium hexametaphosphate solution. The tube was shaken for 30 min and centrifuged for 15 min at 2000 rpm. The top part of the supernatant containing the hyphae was collected with a pipette after each centrifugation and the tube was filled again with the same solution. The hyphae were extracted from the soil sample three times, recovered on filter paper, rinsed with distilled water and then stained with a 0.2% acid fuchsin solution for 12 h. The line intersect method (Tennant, 1975) was used to estimate the length of hyphae recovered on the filter. Root colonization analysis A 3-g fresh subsample was randomly taken from each corn root system. These samples were cleared with 10% KOH by heating in an autoclave at 121 Cfor 30 min and stained with 0.2% acid fuchsin. The percentage of root length colonized by AM fungi was estimated under a dissecting microscope using the grid line intersect method (Giovannetti and Mosse, 1980). Shoot chemical analysis The dried shoots were ground and digested in concentrated H 2 SO 4 and 30% H 2 O 2 (Thomas et al., 1967). Concentrations of N, P and K were analyzed colorimetrically using a flow injection autoanalyzer (LACHAT AELABCHEM, Milwaukee, WI) and Ca, Mg, Cu, Zn, Mn and Fe by atomic absorption spectrometry (PERKIN-ELMER 5380, Norwalk, CT). Table 1. Main effect of P level on root colonization and extraradical hyphae length of three corn hybrids (colonized) by Glomus intraradices Plevel(mgkg 1 ) Root colonization (%) Extraradical hyphae (m g 1 soil) 0 66 a a 1.40 a b 1.23 a b 0.97 b a Numbers in the same column followed by the same letter are not significantly different at p<0.05 (n=72). Statistical analyses Data were subjected to analysis of variance. A linear regression and correlation between mycorrhizal root colonization percentage and N/P ratio in corn shoots were also analyzed. For variance analysis, the ANOVA procedure of the SAS program was used (SAS Institute, 1990). Statistical significance was determined at the 5% probability level. Means of main effects were compared by the least significant difference (LSD) test following a significant F-test. When there was an interaction between factors, the means of the combinations of each level of the factors were compared by LSD test. Results Root colonization Phosphorus application decreased the percentage of AMF colonization (Table 1). There was an interaction between N application and hybrid (Table 2). Rate of N application had a quadratic influence on root colonization in LNS and LRS hybrids (Figure 1). When 70 mg kg 1 of N was applied, the LNS hybrid had the highest mycorrhizal colonization of all the treatments and its colonization level was significantly higher than treatments with no N addition or with 140 mg N kg 1. The LRS hybrid had the lowest colonization at 0 mg Nkg 1 of all mycorrhizal plants. When 140 mg kg 1 of N was applied, LNS hybrid had the lowest and LRS had the highest root colonization. However, colonization did not significantly change with N application for the Pioneer 3979 hybrid. Root colonization of the LNS hybrid was influenced by N fertilization to a greater extent than that of the other two hybrids (Figure 1). Extraradical mycelium The highest level of P application reduced extraradical hyphae length compared to the other two P levels

4 160 Figure 1. Influence of added N fertilizer on mycorrhizal colonization by Glomus intraradices in three corn hybrids: Pioneer 3979; LNS, Leafy normal stature; LRS, Leafy reduced stature. Vertical bars represent standard error of the mean (n=24). Figure 2. Influence of added N fertilizer on extraradical hyphae of Glomus intraradices in three corn hybrids. Hybrid abbreviations as in Figure 1. Vertical bars represent standard error of the mean (n=24).

5 161 Table 2. Summary of F significance from analysis of variance of Host (H), Nitrogen (N), Phosphorus (P) and Mycorrhizae (M) Sources DF RCP a EHL SDW RDW S/R Nutrient concentrations in corn shoots N P K Ca Mg Cu Zn Mn H 2 * ns ns N 2 ns ns P 2 ns ns ns M 1 ns ns ns ns H N 4 ns ns ns ns ns ns ns ns H P 4 ns ns ns ns ns ns ns ns ns ns ns ns ns H M 2 ns ns ns ns ns ns ns ns ns ns ns N P 4 ns ns ns ns ns ns N M 2 ns ns ns ns ns ns ns ns ns ns ns ns ns P M 2 ns ns ns ns ns ns ns ns ns ns ns ns ns H N P 8 ns ns ns ns ns ns ns ns ns ns ns ns ns H P M 4 ns ns ns ns ns ns ns ns ns ns ns ns ns N P M 4 ns ns ns ns ns ns ns ns ns ns ns ns H N P M 8 ns ns ns ns ns ns ns ns ns ns ns ns ns a RCP, root colonization percentage; EHL, extraradical hyphal length; SDW, shoot dry weight; RDW, root dry weight; S/R, shoot:root ratio; ns, not significant; P < 0.05; P < Table 3. The influence of mycorrhizae on shoot dry weight, root dry weight and shoot:root ratio in three corn hybrids Mycorrhizal Shoots (g plant 1 ) Root (g plant 1 ) Shoot:Root status P3979 a LNS LRS P3979 LNS LRS P3979 LNS LRS Myc ab b 22.6 a 17.4 c 5.66 a 5.17 ab 5.21 ab 3.85 b 4.37 a 3.34 c Myc ab 19.6 b 14.9 d 5.44 a 5.25 ab 4.50 b 3.86 b 3.73 b 3.31 c a P3979, Pioneer 3979; LNS, Leafy normal stature; LRS, Leafy reduced stature. b Means followed by the same letter in a group are not significantly different at P<0.05 (n=36). (Table 1). There was an interaction between N level and hybrid on the length of extraradical hyphae (Table 2). Extraradical hyphal length had a quadratic response to N application for all hybrids (Figure 2). Extraradical hyphal length was significantly influenced by all N levels for LNS and LRS hybrids, while, in contrast, the hyphal length associated with Pioneer 3979 hybrid was not changed between 0 and 70 mg N kg 1 (Figure 2). The maximum length of extraradical hyphae was recovered at the intermediate N level for the LNS hybrid. Shoot and root dry weight Mycorrhizal plants had significantly higher shoot dry weights than non-mycorrhizal plants except the Pioneer 3979 hybrid, which did not respond to mycorrhizal inoculation (Table 3). Inoculation had no influence on root dry weight for all hybrids, but significantly increased shoot:root ratios of LNS (Table 3). After corn hybrids were inoculated with AM fungi, LNS had a higher shoot:root ratio than the other two hybrids. Nitrogen application significantly increased the shoot dry weight of all three hybrids (Table 4). There was interaction of N and P on shoot dry weight (Table 5). When N supply was increased from 0 to 70 mg kg 1 soil/sand mix, shoot growth was sharply increased; continued increase of N supply either decreased shoot growth (at 0mgPkg 1 substrate) or did not change shoot growth (at 40 or 80 P mg kg 1 substrate). Nutrient concentration and N/P ratio in shoots Mycorrhizal plants had significantly higher concentrations of P, Mg, Zn and Cu and lower Mn in shoots than non-mycorrhizal plants, but there were no significant changes in shoot N, K and Ca concentrations (Table 6). The LNS hybrid had higher shoot concentrations of N, P and K than Pioneer 3979, and had higher shoot concentrations of P, Ca and Zn than LRS (Table 6).

6 162 Figure 3. Influence of added N fertilizer on Mn concentration in shoots of three corn hybrids. Hybrid abbreviations as in Figure 1. Vertical bars represent standard error of the mean (n=24). Table 4. Influence of N level applied on shoot dry weight (g plant 1 ) of three corn hybrids Nlevel(mgkg 1 ) Hybrid P3979 a LNS LRS e b 5.0 e 4.6 e b 29.3 b 18.0 d a 24.4 c 19.8 d a P3979, Pioneer 3979; LNS, Leafy normal stature; LRS, Leafy reduced stature. b Means followed by the same letter are not significantly different at P<0.05 (n=24). Table 5. Influence of N and P levels on shoot dry weight (g plant 1 ) of three corn hybrids Nlevel(mgkg 1 ) Plevel (mg kg 1 ) de a 13.8 d 12.1 e b 24.8 a 23.2 ab c 25.0 a 24.4 a a Means followed by the same letter are not significantly different at P<0.05 (n=24). The shoot concentration of Mn was the lowest when Nwasappliedat70mgkg 1 in LNS and LRS hybrids (Figure 3). LNS had the lowest shoot Mn concentration of the three hybrids at all N application rates. There were significant interactions between N and P supply on shoot Cu, Zn and Mn concentrations (Table 2). The impact of N-P combinations on concentrations of these micronutrients in shoots was different for different micronutrients (Table 7). Correlations between N/P ratios in shoots and root colonization Root colonization was negatively correlated (R 2 =0.48) with N/P ratios in corn shoots only when N was appliedat70mgkg 1 (Figure 4). However, correlations were not significant when 0 mg N kg 1 or 140 mg N kg 1 was applied, or when the data from all N levels were pooled (data not shown). Discussion Our experiment revealed that the mycorrhizal corn hybrid with higher shoot:root ratio, LNS, had greater root colonization and extraradical hyphal length except at excessive N availability. Plants with higher shoot:root ratio have higher photosynthetic potential and smaller root capacity to support a potentially larger shoot demand than those with a lower shoot:root ratio. Thus,

7 163 Table 6. Influence of mycorrhizae and corn hybrid on nutrient concentration in corn shoots Factor Level a Concentration of nutrients in shoots N P K Ca Mg Zn Cu Mn (g kg 1 ) (g kg 1 ) (g kg 1 ) (g kg 1 ) (g kg 1 ) (mg kg 1 ) (mg kg 1 ) (mg kg 1 ) Mycorrhizal Myc a b 3.39 a 44.1 a 6.07 a 1.80 a 70 a 13 a 68 b status Myc a 3.13 b 44.0 a 6.14 a 1.07 b 63 b 10 b 74 a P b 3.14 b 39.8 b 6.59 a 1.45 a 69 a 12 a - Hybrid LNS 18.5 a 3.46 a 46.2 a 6.45 a 1.45 a 71 a 12 a - LRS 19.0 a 3.19 b 46.3 a 5.28 b 1.41 a 59 b 12 a - a Myc+, mycorrhizal; Myc-, non-mycorrhizal; P3979, Pioneer 3979; LNS, Leafy normal stature; LRS, Leafy reduced stature. b Means followed by the same letter within the same factor are not significantly different at P<0.05 (Mycorrhizal status, n=108; Hybrid, n=72). plants with a high shoot:root ratio may enhance uptake of minerals with high mycorrhizal development. Baylis (1975) also postulated that plants with a high shoot:root ratio are more dependent on AMF extraradical mycelia for extraction of nutrients from the soil. Our previous greenhouse experiment has shown that the LNS had the highest total leaf area (1825 cm 2 ) in 10 corn hybrids (unpublished). This indicates that LNS has the highest ability to produce and supply organic C to mycorrhizae. This may lead to increased root colonization and extraradical mycelium growth and, in turn, enhanced uptake and translocation of nutrients by mycorrhizae to the host plants. The relatively small but highly ramified root system of LNS may also be related to increased AMF development. The increase in shoot:root ratio by mycorrhizal inoculation, as was observed with the LNS hybrid, may be indicative of the efficiency of the symbiosis (Bryla and Koide, 1990a, b). The genotype whose shoot:root ratio is increased most by AMF inoculation may form a more efficient symbiosis. More experimentation is needed before a generalization can be made. Mycorrhizal colonization is a complex multi-step processes, in which the mycorrhizal association is influenced not only by both the host plant and the AM fungi, but also by soil and other environmental conditions (Barea, 1991). If any one of these factors is inhibitory to AM fungi, the symbiosis will be inhibited even if other factors are optimum. Much experimental evidence shows that mycorrhizal colonization is reduced in plants having a high level of phosphorus (Koide and Li, 1990). However, plant P level is influenced by soil P level. The mechanism by which soil P regulates mycorrhizal colonization has been studied (Graham et al., 1981; Lu et al., 1994; Schwab et al., 1983), but it is not yet clearly under- Table 7. Influence of N and P levels in soils on concentrations (mg kg 1 ) of Cu, Zn and Mn in shoots of three corn hybrids Nlevel Cu Zn Mn (mg kg 1 ) P level(mg kg 1 ) P level(mg kg 1 ) P level(mg kg 1 ) b a 8.7 c 13 a 69 bc 63 c 64 c 69 b 71 b 84 a a 11 b 13 a 83 a 74 b 51 d 47 d 56 c 69 b b 9.2 c 10 bc 52 d 65 c 76 b 87 a 86 a 68 b a Means followed by the same letter are not significantly different at P<0.05 (n=24). stood. According to membrane permeability models, root exudation would be regulated by the leakiness of the plasmalemma of root cortical cells, which, in turn, is determined by levels of cellular P. The amount of cellular P in roots is likely related not only to the abundance of P in soil, but also to the abundance of N (Guttay, 1983; Hepper, 1983). Under conditions where N was sufficient in soil, i.e. the intermediate N application, N uptake and P translocation and utilization in biomass production were increased. This resulted in increased growth, dilution of P in root tissues and an increased shoot N/P ratio as compared to plants growing in N deficient soils. The roots may have become leaky, resulting in an abundance of exudates that presumably stimulate the growth of AM fungi and increase subsequent colonization. In this condition, the higher the N/P ratio in shoots, the greater the root colonization. In agreement with our results, Onguene and Habte (1995) showed that the percentage of root colonization in Leucaena leucocephala increased with increasing N levels up to 100 mg N kg 1. In our experiment, the N/P ratio in shoots was related to root colonization only when N supply was adequate.

8 164 Figure 4. Relationship between the N/P ratio in shoots of three corn hybrids and mycorrhizal colonization by Glomus intraradices at the intermediate level (70 mg N kg 1 added) of N supply. When N level is very low in soil, N shortage may limit root colonization (Aziz and Habte, 1990), as observed here for plants not fertilized with N. The AM fungi have a high N requirement for the synthesis of protein and chitin, the main constituents of its cell walls (Bethlenfalvay and Ames, 1987). It appears that colonization would be reduced under any conditions in which N does not promote growth, such as extremely low or extremely high fertility (Koide and Li, 1990). An extremely high N level in soil may directly repress AM fungi. When N was applied at a rate of 140 mg kg 1, AM fungi were inhibited and the length of extraradical mycelium was reduced. These results suggest that excessive amounts of N in soil negatively affect AMF activity. Onguene and Habte (1995) did not find a correlation between shoot N/P ratio and root colonization level, but they did not consider levels of soil available N limiting or directly suppressing AM fungi. In contrast, we found significant correlation between root colonization and N/P ratio in shoots only at the intermediate level of N application. Furthermore, we also found that the greatest root colonization and most abundant extraradical hyphal growth occurred at the intermediate N level, indicating that this level was favorable to mycorrhizal development. This suggests that root colonization is related to the N/P ratio in shoots only when soil conditions are conducive to mycorrhizal development and not under conditions limiting or inhibitory to AMF development. Mycorrhizal colonization, extraradical hyphae and Mn concentration in shoots were always quadratically related to the amount of applied N. The curves of mycorrhizal colonization and extraradical hyphae were similar, but opposite to that of shoot Mn concentration. This indicates that the higher the rate of colonization, the greater the development of extraradical hyphae and the lower the uptake of Mn which is associated with a lower concentration of Mn in shoots. When the intermediate level of N was applied in this experiment, root colonization level and extraradical hyphal length of the LNS hybrid were highest, and shoot Mn concentrations were lowest. Posta et al. (1994) found that AM fungi could reduce Mn-reducing microbial populations. From their information and our results, it appears that soil available N level can influence mycorrhizal development, rhizospheric Mn-reducing microbial populations and, as a result, plant uptake of Mn. In our experiment, shoot Mg concentration in mycorrhizal plants was higher than that in nonmycorrhizal plants. Before planting, the available Mg in the growth substrate was low compared with normal field soil. When the soil Mg is high, mass flow can supply a large percentage of Mg to root surfaces (Tisdale

9 165 et al., 1993). However, as in the case with P, when the Mg level is low, diffusion is an important way to move Mg to plant roots. In the latter situation, reduced Mg diffusion distance or increased absorption area by extraradical hyphae of AM fungi may have facilitated uptake of Mg. Acknowledgements The authors thank Dr. X M Zhou for her assistance. This project was financially supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant held by Dr. D L Smith. References Abbott L K and Robson A D 1984 The effect of VA mycorrhizae on plant growth. In VA Mycorrhiza. Eds C L Powell and D J Bagyaraj. pp CRC Press, Boca Raton, Florida. Azcon R, Gomez-Ortega M and Barea J M 1982 Comparative effects of foliar- or soil-applied nitrate on vesicular-arbuscular mycorrhizal infection in maize. New Phytol. 92, Aziz T and Habte M 1990 Enhancement of endomycorrhizal activity through nitrogen fertilization in cowpea grown in an oxisol subjected to simulated erosion. 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