Nodulation and Plant Growth of Shepherdia ×utahensis ‘Torrey’ Topdressed with Controlled-release Fertilizer

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  • 1 Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322
  • 2 University of Nevada, Reno Extension, 4955 Energy Way, Reno, NV 89502
  • 3 Department of Plants, Soils, and Climate, Utah State University, 4820 Old Main Hill, Logan, UT 84322

Shepherdia ×utahensis ‘Torrey’ (‘Torrey’ hybrid buffaloberry) is an actinorhizal plant that can fix atmospheric nitrogen (N2) in symbiotic root nodules with Frankia. Actinorhizal plants with N2-fixing capacity are valuable in sustainable nursery production and urban landscape use. However, whether nodule formation occurs in S. ×utahensis ‘Torrey’ and its interaction with nitrogen (N) fertilization remain largely unknown. Increased mineral N in fertilizer or nutrient solution might inhibit nodulation and lead to excessive N leaching. In this study, S. ×utahensis ‘Torrey’ plants inoculated with soils containing Frankia were irrigated with an N-free nutrient solution with or without added 2 mm ammonium nitrate (NH4NO3) or with 0.0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) to study nodulation and plant morphological and physiological responses. The performance of inoculated plants treated with various amounts of CRF was compared with uninoculated plants treated with the manufacturer’s prescribed rate. Plant growth, gas exchange parameters, and shoot N content increased quadratically or linearly along with increasing CRF application rates (all P < 0.01). No parameters increased significantly at CRF doses greater than 2.1 g·L−1. Furthermore, the number of nodules per plant decreased quadratically (P = 0.0001) with increasing CRF application rates and nodule formation were completely inhibited at 2.9 g·L−1 CRF or by NH4NO3 at 2 mm. According to our results, nodulation of S. ×utahensis ‘Torrey’ was sensitive to N in the nutrient solution or in increasing CRF levels. Furthermore, plant growth, number of shoots, leaf area, leaf dry weight, stem dry weight, root dry weight, and N content of shoots of inoculated S. ×utahensis ‘Torrey’ plants treated with 2.1 g·L−1 CRF were similar to those of uninoculated plants treated with the manufacturer’s prescribed rate. Our results show that S. ×utahensis ‘Torrey’ plants inoculated with soil containing Frankia need less CRF than the prescribed rate to maintain plant quality, promote nodulation for N2 fixation, and reduce N leaching.

Abstract

Shepherdia ×utahensis ‘Torrey’ (‘Torrey’ hybrid buffaloberry) is an actinorhizal plant that can fix atmospheric nitrogen (N2) in symbiotic root nodules with Frankia. Actinorhizal plants with N2-fixing capacity are valuable in sustainable nursery production and urban landscape use. However, whether nodule formation occurs in S. ×utahensis ‘Torrey’ and its interaction with nitrogen (N) fertilization remain largely unknown. Increased mineral N in fertilizer or nutrient solution might inhibit nodulation and lead to excessive N leaching. In this study, S. ×utahensis ‘Torrey’ plants inoculated with soils containing Frankia were irrigated with an N-free nutrient solution with or without added 2 mm ammonium nitrate (NH4NO3) or with 0.0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) to study nodulation and plant morphological and physiological responses. The performance of inoculated plants treated with various amounts of CRF was compared with uninoculated plants treated with the manufacturer’s prescribed rate. Plant growth, gas exchange parameters, and shoot N content increased quadratically or linearly along with increasing CRF application rates (all P < 0.01). No parameters increased significantly at CRF doses greater than 2.1 g·L−1. Furthermore, the number of nodules per plant decreased quadratically (P = 0.0001) with increasing CRF application rates and nodule formation were completely inhibited at 2.9 g·L−1 CRF or by NH4NO3 at 2 mm. According to our results, nodulation of S. ×utahensis ‘Torrey’ was sensitive to N in the nutrient solution or in increasing CRF levels. Furthermore, plant growth, number of shoots, leaf area, leaf dry weight, stem dry weight, root dry weight, and N content of shoots of inoculated S. ×utahensis ‘Torrey’ plants treated with 2.1 g·L−1 CRF were similar to those of uninoculated plants treated with the manufacturer’s prescribed rate. Our results show that S. ×utahensis ‘Torrey’ plants inoculated with soil containing Frankia need less CRF than the prescribed rate to maintain plant quality, promote nodulation for N2 fixation, and reduce N leaching.

Nursery production of native plants has increased tremendously because of increasing interest in using native plants in urban gardens and landscapes (Thomas and Schrock, 2004). The growing interest in native plants is attributable to their ornamental potential, including aesthetic appearance, bio-diversity, and, most importantly, water conservation (Hooper et al., 2008). In the Intermountain West, native plants are used in low-water-use landscapes with sustainable and low-water-use features (Mee et al., 2003). However, it is difficult to establish native plants in disturbed and poorly drained soils (Edmondson et al., 2011; Mee et al., 2003). Native plants in the Intermountain West, such as Arctostaphylos patula (greenleaf manzanita), Artemisia nova (black sagebrush), Ceratoides lanata (syn. Krascheninnikovia lanata) (winterfat), and Cercocarpus montanus (alder-leaf mountain mahogany), are susceptible to overwatering and wet rooting substrates (Mee et al., 2003). Parkinson et al. (2003) also reported that adequate drainage is essential for growing native plants in the Intermountain West, citing Agave parryi (Parry’s agave), Aquilegia caerulea (Colorado blue columbine), Eriogonum niveum (snow buckwheat), and Eriophyllum lanatum (woolly sunflower) as examples.

A similar scenario was discovered for Shepherdia species (buffaloberry). Shepherdia argentea (silver buffaloberry) and Shepherdia rotundifolia (roundleaf buffaloberry) are both native plants in the Intermountain West (Mee et al., 2003). Shepherdia rotundifolia is an evergreen shrub with a tidy, rounded form and outstanding drought tolerance, but it is highly sensitive to excessive landscape irrigation (Sriladda, 2011; Sriladda et al., 2014). However, S. argentea is a fast-growing, deciduous shrub that adapts to a wide range of soil conditions, but it is less aesthetically acceptable due to its thorny and unkempt appearance (Sriladda et al., 2016). To enhance the adaptability of Shepherdia to wet and poorly drained soils while maintaining drought tolerance and aesthetic appearance, S. ×utahensis Torrey, an interspecific hybrid cultivar of S. argentea and S. rotundifolia, was created by Sriladda et al. (2016). This hybrid cultivar has the potential for use in low-water landscapes because of its tolerance to drought conditions as well as the occasionally wet soils found in residential landscape environments (Sriladda et al., 2016). Furthermore, S. argentea and S. rotundifolia are actinorhizal plants (Benson and Silvester, 1993), and S ×utahensis ‘Torrey’ can form a symbiotic association with Frankia to fix N2 in its root nodules (J. Chen, unpublished data). This biological N2-fixing capacity may reduce the need for nitrogenous fertilization of nodulated actinorhizal plants, thus solving two primary concerns in the nursery industry: mineral N runoff and leaching to groundwater (Urbano, 1989). For example, nodulated Alnus maritima (seaside alder) had better fertilizer use efficiency when inoculated with soils containing Frankia than uninoculated plants (Beddes and Kratsch, 2010). In another study, Frankia-induced nodulation improved plant performance and N use efficiency of Alnus incana (gray alder) (Sellstedt and Huss-Danell, 1986). Laws and Graves (2005) reported that nodulated A. maritima sustained plant vigor and quality with a lower NH4NO3 concentration than uninoculated plants. Therefore, actinorhizal plants with symbiotic nodules have commercial potential in nursery production and urban landscapes (Kratsch and Graves, 2004).

Slow-release fertilizer and CRF gradually deliver mineral nutrients (mainly N) to plants and have been widely used in nursery production (Adams et al., 2013; Beddes and Kratsch, 2010), but excessive N fertilization reduces nodule formation of actinorhizal plants inoculated with Frankia (Huss-Danell, 1997). For example, A. maritima exhibited a decreased nodule number when NH4NO3 increased from 0 to 8.0 mm (Laws and Graves, 2005). In addition, Beddes and Kratsch (2010) reported that A. maritima plants had a decreased nodule number when CRF (15N–3.9P–10K) levels increased from 0 to 1.8 g·L−1, and 3.6 g·L−1 completely inhibited nodule formation. Unfortunately, although N fertilization significantly influences nodule formation, the impact of fertilizers on plant growth and nodule development of S. ×utahensis ‘Torrey’ is largely unknown. Research investigating the effects of CRF and its application rate on nodulation is needed to inform best practices for nurseries.

The objectives of this research were to 1) investigate the impacts of NH4NO3 and CRF on nodule number and plant growth of S. ×utahensis ‘Torrey’, and 2) to determine CRF application rates that maintain acceptable plant quality with minimal nitrate–nitrogen (NO3-N) leaching. In addition, the effects of inoculation on growth and gas exchange parameters were studied by comparing inoculated S. ×utahensis ‘Torrey’ plants treated with 0 to 8.4 g·L−1 CRF with uninoculated plants treated with the manufacturer’s prescribed rate of 3.2 g·L−1.

Materials and Methods

Shepherdia ×utahensis ‘Torrey’ plants were clonally propagated using cuttings collected from the Utah State University Greenville Research Farm (North Logan, UT) on 16 July 2019. Except for the two to three pairs of leaves at the top, leaves were removed from cuttings. Cuttings were dipped in 1000 mg·L−1 indole-3-butyric acid (Hormodin 1; OHP, Mainland, PA) and placed in a tray filled with perlite (Hess Perlite, Malad City, ID). Trays were kept on a mist bench in a greenhouse with temperatures set at 25/20 °C (day/night). On 1 Oct. 2019, nodule-free rooted cuttings were transplanted into 3.8-L injection-molded, polypropylene containers (PC1D-4; Nursery Supplies, Orange, CA) filled with calcined clay (Turface MVP; Profile Products, Buffalo Grove, IL), which is an inorganic growing substrate that is used for native plants (Beddes and Kratsch, 2009). Plants were irrigated with deionized water before the experiment.

On 15 Oct. 2019, the experiment was initiated and plants of uniform size were randomly assigned to 12 groups. In previous studies, soil collected from the rhizosphere of an actinorhizal plant was used as a source of Frankia inocula (Tortosa and Cusato, 1991). In this study, field soils (≈8 L) were collected from the rhizosphere of a S. ×utahensis ‘Torrey’ plant (lat. 41°45′ N, long. 111°48′ W) at Utah State University Greenville Research Farm. Plants in groups 1 to 10 were inoculated with 50 mL of field soil layered on the surface of the substrate. For groups 1 to 8, each plant was topdressed with 0, 0.5, 1.0, 2.0, 4.0, 8.0, 16.0, and 32.0 g of Osmocote 15N–3.9P–10K (Osmocote Plus 15–9–12; Israel Chemicals, Tel Aviv-Yafo, Israel, hereafter referred to as CRF), resulting in CRF levels of 0, 0.1, 0.3. 0.5, 1.1, 2.1, 4.2, and 8.4 g·L−1, respectively. Plants in groups 9 and 10 were irrigated with 500 mL modified N-free nutrient solution (Bugbee, 2004) supplemented with (N-supplement) or without (N-lacking), respectively, added 2 mm NH4NO3 at pH 7.5 every other day, resulting in NO3-N concentrations of 114.9 ± 6.8 and 13.0 ± 1.1 mg·L−1 (mean ± se), respectively. Plants in group 11 had no inoculation but received 3.2 g·L−1 of CRF following the manufacturer’s recommended application rate for plants in a 3.8-L container. Plants in group 12 were uninoculated and not fertilized to confirm whether uninoculated, unfertilized plants form nodules. Except for the plants in groups 9 and 10, plants were irrigated with 500 mL tap water (pH = 7.8) every other day. A saucer was placed under a container before irrigation to collect leachate for measurements. A NO3-N meter (LAQUA Twin; Horiba, Kyoto, Japan) and a pH meter (LAQUA Twin) were used to record the NO3-N concentration and pH of the leachate weekly. The NO3-N concentration in the leachate of plants treated with CRF was calculated using the difference between NO3-N concentrations in irrigation water and in leachate to correct the variations from background N.

Gas exchange parameters, including the leaf net photosynthesis rate (Pn), stomatal conductance rate (gS), and transpiration rate (E), were recorded for plants treated with 0, 2.0, 8.0, and 32.0 g of CRF 1 week before the experiment was ended. Parameters were recorded using a Portable Photosynthesis System with a PLC3 Universal Leaf Cuvette (CIRAS-3; PP Systems, Amesbury, MA) on a sunny day between 1000 and 1400 hr. Within the cuvette, the intensity of photosynthetic photon flux density was set at 1000 μmol·m−2·s−1 with 38% red, 37% green, and 25% blue light provided from light-emitting diodes, whereas the carbon dioxide level and leaf temperature were controlled at 400 μmol·mol−1 and 25 °C, respectively.

The experiment was ended on 8 Dec. 2019. Plant height was recorded at the initiation and termination of the experiment to determine plant growth. Before all plants were destructively harvested, the number of shoots (longer than 5 cm) was recorded for each plant. All S. ×utahensis ‘Torrey’ plants were destructively harvested, and the leaf area was recorded using a leaf area meter (LI-3000; LI-COR Biosciences, Lincoln, NE). After roots were harvested and washed using deionized water, plants were checked for nodule number. Leaves, stems, and roots were dried in an oven at 80 °C for 3 d, and the dry weight was recorded. Dry leaves and stem samples were ground and analyzed at the Utah State University Analytical Laboratories for N content with an elemental analyzer (vario MAX cube; Elementar Analysensysteme GmbH, Langenselbold, Germany).

The experiment used a randomized complete block design with 10 blocks for all groups. An analysis of variance was performed to test the effects of treatments on plant morphological and physiological responses. The means separation among treatments was adjusted using the Tukey-Kramer method for multiplicity at α = 0.05. All statistical analyses were performed using the PROC Mixed procedure in SAS Studio (SAS Institute, Cary, NC).

Results

Leachate.

The N-supplement and N-lacking treatment led to leachate NO3-N concentrations of 188.3 ± 13.5 and 19.8 ± 1.4 mg·L−1 (mean ± se), respectively. The pH values of the leachate solutions were 7.3 ± 1.3 and 7.6 ± 1.3 (mean ± se) for N-supplement and N-lacking treatment, respectively (data not shown). However, for plants irrigated with tap water, the pH of the leachate solution was 7.9 ± 0.01 (mean ± se). For plants treated with CRF, the NO3-N concentration of leachate solution increased as the applied CRF levels increased (Fig. 1). The NO3-N concentrations of leachate solutions from plants treated with 0 to 2.1 g·L−1 CRF were 28% to 80% less than that from uninoculated plants treated with the manufacturer’s prescribed rate (Fig. 1). However, inoculated plants treated with 4.2 and 8.4 g·L−1 CRF had 42% and 179% greater NO3-N leachate concentrations, respectively, than uninoculated plants treated with the manufacturer’s prescribed rate.

Fig. 1.
Fig. 1.

Nitrate–nitrogen (NO3-N) concentrations of leachate recorded after Shepherida ×utahensis ‘Torrey’ plants topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) were irrigated with tap water. The error bars represent the se of five samples. The background nitrogen in tap water was corrected by calculating the difference between NO3-N concentrations in leachate and tap water.

Citation: HortScience horts 55, 12; 10.21273/HORTSCI15260-20

Plant growth, number of shoots, and leaf area.

Plant growth of S. ×utahensis ‘Torrey’ plants receiving the N-supplement treatment was three times greater than that of plants receiving the N-lacking treatment (Table 1). A regression analysis indicated a quadratic relationship between CRF and plant growth (P = 0.002; R2 = 0.95) (Fig. 2). Plant growth and visual quality are shown in Fig. 3. Plant growth of inoculated S. ×utahensis ‘Torrey’ plants treated with 1.1 to 8.4 g·L−1 CRF increased one to six times compared with plants treated with 0 g·L−1 CRF. A quadratic trend in CRF and the number of shoots of S. ×utahensis ‘Torrey’ (P = 0.003; R2 = 0.95) was observed (Fig. 2). Except for the plants receiving 0.3 g·L−1 CRF, S. ×utahensis ‘Torrey’ plants treated with 0.1 to 8.4 g·L−1 CRF had one to four more shoots than plants treated with 0 g·L−1 CRF. The leaf area of S. ×utahensis ‘Torrey’ plants receiving N-supplement treatment was four times more than that of N-lacking treatment (Table 1). When plants were fertilized with increasing amounts of CRF, a quadratic relationship was found between the leaf area and CRF (P = 0.007; R2 = 0.98) (Fig. 2). When S. ×utahensis ‘Torrey’ plants were treated with 1.1 to 8.4 g·L−1 CRF, the leaf area was one to three times greater than those treated with 0 g·L−1 CRF. No significant difference was found for these parameters of uninoculated S. ×utahensis ‘Torrey’ plants treated with the manufacturer’s prescribed rate and inoculated plants treated with 1.1 and 2.1 g·L−1 CRF.

Table 1.

Plant growth, number of shoots, leaf area, dry weights (DW) of leaf, stem, and root, and number of nodules of inoculated Shepherdia ×utahensis ‘Torrey’ treated with nutrient solution supplemented with (N-supplement) or not supplemented with (N-lacking) 2 mm ammonium nitrate (NH4NO3) for 8 weeks.

Table 1.
Fig. 2.
Fig. 2.

Plant growth (A), number of shoots (B), leaf area (C), leaf dry weight (D), stem dry weight (E), and root dry weight (F) of Shepherdia ×utahensis ‘Torrey’ inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. The round markers represent means of the plants inoculated with Frankia, whereas the square markers represent the uninoculated plants treated with the manufacturer’s prescribed rate of 3.2 g·L−1. A regression analysis was conducted using the plants inoculated with Frankia. The error bars represent the se of 10 samples. No significant difference was found between the inoculated plants treated with 1.1 and 2.1 g·L−1 CRF and uninoculated plants treated with the manufacturer’s prescribed rate according to the Tukey-Kramer method for multiplicity at α = 0.05.

Citation: HortScience horts 55, 12; 10.21273/HORTSCI15260-20

Fig. 3.
Fig. 3.

The shoot (A) and root (B) of Shepherdia ×utahensis ‘Torrey’ plants inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) and the uninoculated plants that received the manufacturer’s prescribed rate of 3.2 g·L−1. Inoculated S. ×utahensis ‘Torrey’ plants that received 1.1 and 2.1 g·L−1 CRF had plant vigor similar to that of uninoculated plants that received the manufacturer’s prescribed application. Photos were obtained at week 8 of the experiment.

Citation: HortScience horts 55, 12; 10.21273/HORTSCI15260-20

Dry weight of leaf, stem, and root.

Leaf dry weight of S. ×utahensis ‘Torrey’ plants receiving N-supplement treatment was two times greater than plants with the N-lacking treatment (Table 1). A quadratic relationship was found between leaf dry weight and CRF amounts in inoculated plants (P = 0.0002; R2 = 0.97) (Fig. 2). Leaf dry weight of S. ×utahensis ‘Torrey’ plants treated with 2.1, 4.2, and 8.4 g·L−1 CRF was three, four, and five times greater, respectively, than those treated with 0 g·L−1 CRF. The N-supplement treatment increased the stem dry weight of S. ×utahensis ‘Torrey’ plants by 130% compared with plants given the N-lacking treatment (Table 1). When inoculated S. ×utahensis ‘Torrey’ plants were treated with increasing amounts of CRF, a quadratic relationship was found between CRF and stem dry weight (P = 0.03; R2 = 0.98) (Fig. 2). Compared with plants treated with 0 g·L−1 CRF, the stem dry weight of S. ×utahensis ‘Torrey’ treated with 4.2 and 8.4 g·L−1 CRF increased two and three times, respectively. Shepherdia ×utahensis ‘Torrey’ had four times greater root dry weight when N-supplement treatment was applied compared with N-lacking treatment (Table 1). A quadratic relationship was observed between CRF and root dry weight of S. ×utahensis ‘Torrey’ (P = 0.01; R2 = 0.91) (Fig. 2), and the root dry weight increased approximately five times for plants treated with 4.2 and 8.4 g·L−1 CRF compared with plants treated with 0 g·L−1 CRF (Fig. 3). These parameters of uninoculated S. ×utahensis ‘Torrey’ treated with the manufacturer’s prescribed rate were not different from those of inoculated S. ×utahensis ‘Torrey’ plants treated with 1.1 and 2.1 g·L−1 CRF (Fig. 2). However, no significant difference in the root:shoot ratio was observed between inoculated and uninoculated plants receiving no CRF (P = 0.3) (data not shown). In addition, no correlation was observed between the root:shoot ratio and nodule and growth parameters in this study (data not shown).

Gas exchange and shoot N content.

A positive linear relationship was exhibited between CRF and the Pn of S. ×utahensis ‘Torrey’ (P < 0.0001; r2 = 0.74) (Fig. 4). The Pn of S. ×utahensis ‘Torrey’ plants treated with 2.1 and 8.4 g·L−1 CRF increased 12 and 16 times, respectively, compared with plants treated with 0 g·L−1 CRF. The gS of S. ×utahensis ‘Torrey’ increased linearly with increasing CRF (P = 0.004; r2 = 0.66) (Fig. 4), and the gS of plants treated with 8.4 g·L−1 CRF was 72% greater than that of plants treated with 0 g·L−1 CRF. The E of S. ×utahensis ‘Torrey’ had a positive linear trend with increasing CRF (P = 0.005; r2 = 0.69). Shepherdia ×utahensis ‘Torrey’ plants treated with 8.4 g·L−1 CRF had a 54% increase in E compared with plants treated with 0 g·L−1 CRF. No statistical difference was found in the Pn, gS, and E of S. ×utahensis ‘Torrey’ plants receiving 2.1 and 8.4 g·L−1 CRF.

Fig. 4.
Fig. 4.

The photosynthesis rate (Pn) (A), stomatal conductance rate (gS) (B), transpiration rate (E) (C), and nitrogen content of shoot (D) of Shepherdia ×utahensis ‘Torrey’ topdressed with 0 g·L−1, 0.5 g·L−1, 2.1 g·L−1, and 8.4 g·L−1 of controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. The error bars represent the se of four measurements or samples. The round markers represent means of the plants inoculated with Frankia, whereas the square marker in the shoot nitrogen content represents the uninoculated plants that received the manufacturer’s prescribed rate of 3.2 g·L−1 CRF. A regression analysis was conducted using the plants inoculated with Frankia. No significant differences were found in the nitrogen contents of shoots of the inoculated plants treated with 2.1 g·L−1 CRF and uninoculated plants treated with the manufacturer’s prescribed rate according to Tukey-Kramer method for multiplicity at α = 0.05.

Citation: HortScience horts 55, 12; 10.21273/HORTSCI15260-20

The shoot N content of inoculated S. ×utahensis ‘Torrey’ plants increased linearly with CRF (P < 0.0001; r2 = 0.84). When S. ×utahensis ‘Torrey’ was fertilized with 2.1 and 8.4 g·L−1 CRF, the shoot N content increased by 44% and 71%, respectively, compared with plants treated with 0 g·L−1 CRF. There was no statistical difference in the shoot N content of inoculated S. ×utahensis ‘Torrey’ treated with 2.1 or 8.4 g·L−1 CRF and uninoculated plants that received the manufacturer’s prescribed rate (Fig. 4).

Nodulation.

Nodules formed on S. ×utahensis ‘Torrey’ plants inoculated with Frankia-infected soils in our experiment (P < 0.0001), whereas plants without inoculation and treated with 0 g·L−1 CRF did not form any nodules (data not shown). Furthermore, uninoculated plants treated with the manufacturer’s recommended rate did not form nodules. The NH4NO3 in the nutrient solution and CRF affected the nodule number of S. ×utahensis ‘Torrey’ (both P < 0.0001) (data not shown). When the N-supplement treatment was applied, one nodule appeared on 1 out of 10 inoculated S. ×utahensis ‘Torrey’ plants (Table 1). In contrast, for plants receiving N-lacking treatment, all plants formed nodules, with 10 nodules per plant on average. For the inoculated plants treated with CRF, the number of nodules per plant decreased quadratically as CRF increased (P < 0.0001; R2 = 0.74) (Figs. 3 and 5). When inoculated with soils containing infective Frankia strains, S. ×utahensis ‘Torrey’ topdressed with 8.4 g·L−1 CRF did not form any nodules, whereas 1 out of 10 plants treated with 4.2 g·L−1 CRF had one nodule. According to the regression analysis, 2.9 g·L−1 CRF completely inhibited nodule formation. The dry weight of nodules increased quadratically as CRF increased (P = 0.006; R2 = 0.94). The dry weight of nodules on plants treated with 2.1 g·L−1 CRF was 13 times greater than that of plants treated with 0 g·L−1 CRF (Fig. 5).

Fig. 5.
Fig. 5.

The number of nodules per plant (A) and nodule dry weight (B) of Shepherdia ×utahensis ‘Torrey’ inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. A regression analysis was conducted using the plants inoculated with Frankia. The error bars represent the se of 10 samples.

Citation: HortScience horts 55, 12; 10.21273/HORTSCI15260-20

Discussion

Leachate.

Factors such as environmental temperature and physical properties of CRF coating affect the release rate of CRF; however, generally, Osmocote has a relatively rapid release rate initially, followed by a steadily decreasing rate of release over time (Adams et al., 2013). A similar pattern was found in our study; leachate NO3-N concentrations increased at an early stage of the experiment and then decreased over time in plants receiving 2.1 to 8.4 g·L−1 CRF (Fig. 1). The trend of increasing NO3-N concentrations in the leachate at the early stage of the experiment followed by declining concentrations was also reported by Glenn et al. (2000) and Niemiera and Leda (1993). This pattern was also reported for A. maritima plants grown in a substrate containing peat and vermiculite and treated with CRF; the NO3-N concentration in the leachate increased from days 1 to 14 for plants receiving 3.6 and 7.3 g·L−1 Osmocote 15N–3.9P–10K and then decreased (Beddes and Kratsch, 2010). The increasing NO3-N concentration in growing substrates during the early period of the experiment could delay nodule formation.

Morphological and physiological responses.

In our study, although morphological parameters of S. ×utahensis ‘Torrey’ increased quadratically with increasing CRF levels, these parameters did not change significantly when fertilizer levels exceeded 2.1 g·L−1 CRF (≈0.3 g·L−1 N) (Fig. 2). This may be because plant growth responses do not correlate well with nutrient availability when the substrate nutrient concentration exceeds a certain range (Taiz et al., 2015). For example, for morphological parameters, the shoot dry weight of Salvia farinacea (mealycup sage) increased quadratically with Osmocote 39N–0P–0K, increasing from 0.5 to 3.0 g·L−1 N, but increasing the rate of Osmocote 39N–0P–0K did not contribute to the shoot dry weight when it exceeded 2.0 g·L−1 N (Knowles et al., 1993). Beddes and Kratsch (2010) also reported that leaf area, shoot dry weight, and root dry weight of A. maritima did not increase when Osmocote 15N–3.9P–10K was more than 3.6 g·L−1 (≈0.5 g·L−1 N).

Physiological parameters of S. ×utahensis ‘Torrey’ increased linearly with increasing CRF levels (Fig. 4), which is inconsistent with a previous report indicating that a quadratic relationship generally occurs between plant growth and nutrient availability (Taiz et al., 2015). Actually, our data points strongly resemble quadratic trends (Fig. 4) because the physiological parameters did not change significantly when CRF levels exceeded 2.1 g·L−1 CRF (≈0.3 g·L−1 N). This discrepancy might have resulted from numerous variations in the physiological data that were recorded and the limited number of treatments. The Pn of Abies fraseri (fraser fir), Picea glauca (white spruce), Picea pungens (blue spruce), and Pinus strobus (eastern white pine) increased when Osmocote 15N–3.9P–10K ranged from 0.25 to 0.5 g·L−1 N, but it did not change at levels greater than 0.5 g·L−1 N (Klooster et al., 2010). In a study by Zhang et al. (2011), the Pn of Hosta clausa (hosta) did not increase when controlled-release N fertilizer 46N–0P–0K exceeded 0.3 g·L−1 (≈0.1 g·L−1 N) at 90 and 120 d after treatment. Therefore, it is important to define the minimum application rate of CRF to maintain plant vigor and photosynthesis while reducing fertilizer costs and the potential for groundwater contamination (Poole and Conover, 1989). Based on the results of our study, an effective CRF application rate for inoculated S. ×utahensis ‘Torrey’ is 2.1 g·L−1 (≈0.3 g·L−1 N) for maintaining plant vigor and reducing NO3-N leaching.

Nitrogen content and nodulation.

The N concentrations in plant tissues in our study increased linearly with increasing fertilizer levels. Klooster et al. (2010) reported that the N contents of A. fraseri, P. glauca, P. pungens, and P. strobus needles increased when the Osmocote 15N–3.9P–10K application increased from 0.25 and 0.5 g·L−1 N . The N contents of Pilea ‘Silver Tree’, Aphelandra squarrosa (zebra plant), Chamaedorea elegans (parlor palm), and Dieffenbachia maculata ‘Camille’ (‘Camille’ dumb cane) increased linearly with the 14N–6.2P–11.6K slow-release fertilizer level increasing from 0.5 to 1.5 g·L−1 (≈0.07 to 0.2 g·L−1 N) (Poole and Conover, 1989). In the study by Knowles et al. (1993), the shoot N content of Salvia farinacea showed a quadratic trend with increasing Osmocote 39N–0P–0K. The N content of A. maritima increased quadratically with increasing application rates of Osmocote 15N–3.9P–10K, but the shoot N contents of nodulated A. maritima plants receiving 0.9 to 1.8 g·L−1 CRF (≈0.1 to 0.3 g·L−1 N) were not different from those of uninoculated plants receiving the manufacturer’s prescribed rate of 2.7 g·L−1 CRF (≈0.4 g·L−1 N) because of the N2-fixing ability of Frankia (Beddes and Kratsch, 2010). The leaf N content of A. maritima plants also increased along with NH4NO3 levels in the nutrient solution (Laws and Graves, 2005). In our study, the shoot N content of nodulated S. ×utahensis ‘Torrey’ plants fertilized with 2.1 g·L−1 CRF was similar to that of uninoculated plants receiving the manufacturer’s prescribed rate of 3.2 g·L−1. These results indicate that nodulation induced by Frankia may help accumulate N. Because the N2-fixation of Frankia enhances the N content, inducing nodules in novel actinorhizal plants using field soil is a preferred practice to reduce fertilizer applications in sustainable nurseries concerned with the economic and ecological impacts of chemical fertilizers (Kratsch and Graves, 2004).

Soils from actinorhizal plant habitats have dense populations of infective Frankia, and host plants are the primary factor amplifying Frankia populations in the soil (Benson and Silvester, 1993; Schwencke and Caru, 2001). In our study, soil used for inoculation was collected from the rhizosphere of a S. ×utahensis ‘Torrey’ in North Logan, UT. Our results suggest that this soil has infective Frankia to induce symbiotic nodules of S. ×utahensis ‘Torrey’, which is similar to previous reports indicating that soils collected from wild populations have significant effects on inducing nodules on actinorhizal plants (Beddes and Kratsch, 2010; Jeong and Myrold, 2001; Laws and Graves, 2005).

Although soil can induce nodules on S. ×utahensis ‘Torrey’, such nodule formation was inhibited by 2.9 g·L−1 CRF (≈0.4 g·L−1 N) or 2 mm NH4NO3. This might be associated with the significant impact of N fertilizer on the infection process of actinorhizal plants. Depending on the host plant species, Frankia strains infect host plants by either root hair infection or intercellular penetration (Schwencke and Caru, 2001). Nitrate has a negative effect on root hair development; therefore, the nodule number is more sensitive to nitrate in actinorhizal plants with root hair infection. For instance, Alnus glutinosa (black alder), Casuarina cunninghamiana (river oak), and Myrica cerifera (southern wax myrtle) are infected by Frankia via root hair infection, and their nodule formation is more sensitive to nitrate when compared with Elaeagnus angustifolia (Russian olive), which is infected by Frankia via intercellular penetration (Kohls and Baker, 1989). Ammonium ions in substrate may impact nodule formation, but the substrate used for growing S. ×utahensis ‘Torrey’ is well-drained, a condition under which N fertilizer tends to transform to nitrate (Norton and Ouyang, 2019). This nitrate, together with those released from fertilizer, would significantly inhibit the Frankia infection process of S. × utahensis ‘Torrey’. However, further investigations should be conducted to confirm the mechanism of Frankia strains infecting S. ×utahensis ‘Torrey’ because they infect most Shepherdia species via intercellular penetration (Racette and Torrey, 1989) and, therefore, would not be sensitive to nitrate.

Additionally, the reliance of host plants on the symbiont decreases when the plant N status increases; therefore, autoregulation is triggered to suppress nodule formation and prevent excessive export of photosynthate (Kratsch and Graves, 2004). The sensitivity of nodule formation to N is different among actinorhizal plants. Thomas and Berry (1989) reported that the nodule number on Ceanothus griseus (carmel ceanothus) was significantly reduced at 0.714 mm NH4NO3 and completely inhibited at 2.68 mm NH4NO3. However, Purshia mexicana (Mexican cliffrose) and Purshia tridentata (antelope bitterbrush) did not form nodules when exposed to 6 mm NH4NO3 (Righetti et al., 1986). For A. maritima, the nodule number decreased linearly when the NH4NO3 concentration increased from 0.25 to 4 mm, and it was completely inhibited at 8 mm NH4NO3 (Laws and Graves, 2005). In another study, the nodule number of A. maritima declined when Osmocote 15N–3.9P–10K exceeded 1.8 g·L−1 (≈0.3 g·L−1 N), and it was completely inhibited at 3.6 g·L−1 CRF (≈0.5 g·L−1 N) (Beddes and Kratsch, 2010). Compared with A. maritima, the nodule formation of S. ×utahensis ‘Torrey’ is completely inhibited by a relatively lower concentration of NH4NO3 or CRF level. Therefore, S. ×utahensis ‘Torrey’ may be sensitive to environmental N content.

Apart from N, mineral nutrients in the CRF and substrate pH might also affect the nodule number of S. ×utahensis ‘Torrey’. Although NO3-N and ammonium–nitrogen (NH4NO3-N) are the primary nutrients in Osmocote 15N–3.9P–10K, it also contains mineral nutrients such as phosphate and iron (Adams et al., 2013). A previous study has documented that phosphate, cobalt, iron, calcium, and sodium affect the nodule number of actinorhizal plants (Huss-Danell, 1997). For instance, low phosphorus availability significantly impaired the nodule formation of Discaria trinervis (Valverde et al., 2002). Although substrate pH was not controlled in this experiment, it might affect the availability of macronutrients and micronutrients to inhibit nodulation (Huss-Danell, 1997; Taiz et al., 2015).

However, the N fixing ability of actinorhizal plants is related to nodule biomass instead of nodule number (Dawson and Gordon, 1979; Gordon and Wheeler, 1987). For S. ×utahensis ‘Torrey’, nodule dry weight increased with increasing CRF levels (Fig. 5), and a similar result was reported by Beddes and Kratsch (2010). These results indicate that the N fixation ability of S. ×utahensis ‘Torrey’ may increase with increasing CRF levels up to 2.1 g·L−1. Although the N2 fixation capacity of nodules of S. ×utahensis ‘Torrey’ was undefined in our study, our results indicate that Frankia inoculation could improve plant performance and reduce fertilizer use. Further investigations are needed to test the N2 fixation of S. ×utahensis ‘Torrey’ using acetylene reduction assays or 15N-labeling techniques (Huss-Danell, 1997; Laws and Graves, 2005).

For acceptable plant quality and minimal NO3-N concentrations in leachate, Beddes and Kratsch (2010) concluded that 0.9 g·L−1 Osmocote 15N–3.9P–10K was the proper application rate for producing nodulated A. maritima. In addition, NH4NO3 at 0.5 to 2.0 mm in nutrient solution was recommended by Laws and Graves (2005) for A. maritima with symbiotic nodules to enhance leaf N as well as maintain plant vigor. In our research, plant growth was similar between the inoculated plants fertilized with 1.1 g and 2.1 g·L−1 CRF and the uninoculated plants receiving the manufacturer’s prescribed rate. Furthermore, inoculated plants treated with 2.1 g·L−1 CRF had tissue N content similar to that of the uninoculated plants receiving the manufacturer’s prescribed rate. Therefore, 1.1 or 2.1 g·L−1 CRF may be the proper application rate for the production of nodulated S. ×utahensis ‘Torrey’.

Conclusions

Although growth and physiological responses of S. ×utahensis ‘Torrey’ were improved by increasing CRF, increased CRF led to higher NO3-N concentrations in the leachate. No significant differences in morphological and physiological parameters and shoot N contents were observed in the inoculated plants when CRF levels exceeded 2.1 g·L−1. Furthermore, compared with the uninoculated plants treated with the manufacturer’s prescribed rate, nodulated plants treated with 1.1 g·L−1 CRF had similar morphological and growth responses, and nodulated plants at 2.1 g·L−1 had similar shoot N contents. The number of nodules on S. ×utahensis ‘Torrey’ was inhibited with increased CRF application rates, and it was completely inhibited by 2.9 g·L−1 of CRF or 2 mm NH4NO3. Therefore, when nodulated S. ×utahensis ‘Torrey’ plants are produced in the nursey, CRF lower than 2.9 g·L−1 or NH4NO3 lower than 2 mm should be applied. Rates between 1.1 and 2.1 g·L−1 CRF may be sufficient for nodulated S. ×utahensis ‘Torrey’ to sustain acceptable visual quality and promote nodulation for N2 fixation with minimal nitrate leachate.

Literature Cited

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Contributor Notes

This research was supported in part by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Hatch project UTA01381, New Faculty Start-Up Funds from the Utah State University Office of Research and Graduate Studies, and the Center for Water-Efficient Landscaping. It was approved as the UAES journal paper number 9359. We are grateful for valuable comments from anonymous reviewers. The content is solely the responsibility of the authors and does not necessarily represent the official views of the funding agencies. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by the USDA or the American Society for Horticultural Science and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

Y.S. and J.C. are the corresponding authors. E-mail: youping.sun@usu.edu or jijhong.chen@gmail.com.

  • View in gallery

    Nitrate–nitrogen (NO3-N) concentrations of leachate recorded after Shepherida ×utahensis ‘Torrey’ plants topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) were irrigated with tap water. The error bars represent the se of five samples. The background nitrogen in tap water was corrected by calculating the difference between NO3-N concentrations in leachate and tap water.

  • View in gallery

    Plant growth (A), number of shoots (B), leaf area (C), leaf dry weight (D), stem dry weight (E), and root dry weight (F) of Shepherdia ×utahensis ‘Torrey’ inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. The round markers represent means of the plants inoculated with Frankia, whereas the square markers represent the uninoculated plants treated with the manufacturer’s prescribed rate of 3.2 g·L−1. A regression analysis was conducted using the plants inoculated with Frankia. The error bars represent the se of 10 samples. No significant difference was found between the inoculated plants treated with 1.1 and 2.1 g·L−1 CRF and uninoculated plants treated with the manufacturer’s prescribed rate according to the Tukey-Kramer method for multiplicity at α = 0.05.

  • View in gallery

    The shoot (A) and root (B) of Shepherdia ×utahensis ‘Torrey’ plants inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) and the uninoculated plants that received the manufacturer’s prescribed rate of 3.2 g·L−1. Inoculated S. ×utahensis ‘Torrey’ plants that received 1.1 and 2.1 g·L−1 CRF had plant vigor similar to that of uninoculated plants that received the manufacturer’s prescribed application. Photos were obtained at week 8 of the experiment.

  • View in gallery

    The photosynthesis rate (Pn) (A), stomatal conductance rate (gS) (B), transpiration rate (E) (C), and nitrogen content of shoot (D) of Shepherdia ×utahensis ‘Torrey’ topdressed with 0 g·L−1, 0.5 g·L−1, 2.1 g·L−1, and 8.4 g·L−1 of controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. The error bars represent the se of four measurements or samples. The round markers represent means of the plants inoculated with Frankia, whereas the square marker in the shoot nitrogen content represents the uninoculated plants that received the manufacturer’s prescribed rate of 3.2 g·L−1 CRF. A regression analysis was conducted using the plants inoculated with Frankia. No significant differences were found in the nitrogen contents of shoots of the inoculated plants treated with 2.1 g·L−1 CRF and uninoculated plants treated with the manufacturer’s prescribed rate according to Tukey-Kramer method for multiplicity at α = 0.05.

  • View in gallery

    The number of nodules per plant (A) and nodule dry weight (B) of Shepherdia ×utahensis ‘Torrey’ inoculated with soil containing infective Frankia and topdressed with 0 to 8.4 g·L−1 controlled-release fertilizer (CRF; 15N–3.9P–10K) for 8 weeks. A regression analysis was conducted using the plants inoculated with Frankia. The error bars represent the se of 10 samples.

  • Adams, C., Frantz, J. & Bugbee, B. 2013 Macro- and micronutrient-release characteristics of three polymer-coated fertilizers: Theory and measurement J. Plant Nutr. Soil Sci. 176 76 88

    • Search Google Scholar
    • Export Citation
  • Beddes, T. & Kratsch, H.A. 2009 Seed germination of roundleaf buffaloberry (Shepherdia rotundifolia) and silver buffaloberry (Shepherdia argentea) in three substrates J. Environ. Hort. 27 129 133

    • Search Google Scholar
    • Export Citation
  • Beddes, T. & Kratsch, H.A. 2010 Nodulation of seaside alder topdressed with controlled-release fertilizer HortTechnology 20 740 745

  • Benson, D.R. & Silvester, W.B. 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants Microbiol. Rev. 57 293 319

  • Bugbee, B. 2004 Nutrient management in recirculating hydroponic culture Acta Hort. 648 99 112

  • Dawson, J.O. & Gordon, J.C. 1979 Nitrogen fixation in relation to photosynthesis in Alnus glutinosa Bot. Gaz. 140 70 75

  • Edmondson, J.L., Davies, Z.G., McCormack, S.A., Gaston, K.J. & Leake, J.R. 2011 Are soils in urban ecosystems compacted? A citywide analysis Biol. Lett. 7 771 774

    • Search Google Scholar
    • Export Citation
  • Gordon, J.C. & Wheeler, C.T. 1987 Whole plant studies on photosynthesis and acetylene reduction in Alnus glutinosa New Phytol. 80 179 186

  • Glenn, J.S., Gilliam, C.H., Edwards, J.H., Keever, G.J. & Knight, P.R. 2000 Recycled waste paper mulch reduces available container N J. Environ. Hort. 18 188 191

    • Search Google Scholar
    • Export Citation
  • Hooper, V.H., Endter-Wada, J. & Johnson, C.W. 2008 Theory and practice related to native plants: A case study of Utah landscape professionals Landsc. J. 27 1 8

    • Search Google Scholar
    • Export Citation
  • Huss-Danell, K. 1997 Actinorhizal symbioses and their N2 fixation New Phytol. 136 375 405

  • Jeong, S.C. & Myrold, D.D. 2001 Population size and diversity of Frankia in soils of Ceanothus velutinus and Douglas-fir stands Soil Biol. Biochem. 33 931 941

    • Search Google Scholar
    • Export Citation
  • Klooster, W.S., Cregg, B.M., Fernandez, R.T. & Nzokou, P. 2010 Growth and photosynthetic response of pot-in-pot-grown conifers to substrate and controlled-release fertilizer HortScience 45 36 42

    • Search Google Scholar
    • Export Citation
  • Knowles, T.C., Hipp, B.W. & Hegemann, M.A. 1993 Container medium and slow-release nitrogen fertilizer influence growth and quality of Salvia farinacea HortScience 28 623 625

    • Search Google Scholar
    • Export Citation
  • Kohls, S.J. & Baker, D.D. 1989 Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants Plant Soil 118 171 179

    • Search Google Scholar
    • Export Citation
  • Kratsch, H.A. & Graves, W.R. 2004 Nitrogen fixation as a stress-avoidance strategy among actinorhizal (non-legume) trees and shrubs J. Crop Improv. 10 281 304

    • Search Google Scholar
    • Export Citation
  • Laws, M.T. & Graves, W.R. 2005 Nitrogen inhibits nodulation and reversibly suppresses nitrogen fixation in nodule of Alnus maritina J. Amer. Soc. Hort. Sci. 130 496 499

    • Search Google Scholar
    • Export Citation
  • Mee, W., Barnes, J., Kjelgren, R., Sutton, R., Cerny, T. & Johnson, C. 2003 Water wise: Native plants for intermountain landscapes. Utah State University Press, Logan, UT

  • Niemiera, A.X. & Leda, C.E. 1993 Nitrogen leaching from Osmocote-fertilized pine bark at leaching fractions of 0 to 0.4 J. Environ. Hort. 11 75 77

  • Norton, J. & Ouyang, Y. 2019 Controls and adaptive management of nitrification in agricultural soils Front. Microbiol. 10 1931

  • Parkinson, H., DeBolt, A., Rosentreter, R. & Geertson, V. 2003 Landscaping with native plants of the Intermountain Region. U.S. Bureau of Land Management, Boise, ID

  • Poole, R.T. & Conover, C.A. 1989 Fertilization of four indoor foliage plants with Osmocote or Nutricote J. Environ. Hort. 7 102 108

  • Racette, S. & Torrey, J.G. 1989 Root nodule initiation in Gymnostoma (Casuarinaceae) and Shepherida (Elaeagnaceae) induced by Frankia strain HFPGpI1 Can. J. Bot. 67 2873 2879

    • Search Google Scholar
    • Export Citation
  • Righetti, T.L., Chard, C.H. & Backhaus, R.A. 1986 Soil and environmental factors related to nodulation in Cowania and Purshia Plant Soil 91 147 160

  • Schwencke, J. & Caru, M. 2001 Advances in actinorhizal symbiosis: Host pant-Frankia interactions, biology, and applications in arid land reclamation. A review Arid Land Res. Manage. 154 283 327

    • Search Google Scholar
    • Export Citation
  • Sellstedt, A. & Huss-Danell, K. 1986 Biomass production and nitrogen utilization by Alnus incana when grown on N2 or NH4 + made available at the same rate Planta 167 387 394

    • Search Google Scholar
    • Export Citation
  • Sriladda, C. 2011 Ecophysiology and genetic variation in domestication of shpaeralcea and shepherdia species for the Intermountain West. Utah State University, Logan, UT. 2 June 2020. <https://digitalcommons.usu.edu/cgi/viewcontent.cgi?article=2027&context=etd>

  • Sriladda, C., Kratsch, H.A., Larson, S.R., Monaco, T.A., Shen, F. & Kjelgren, R.K. 2016 Interspecific hybrid of xeric Shepherdia rotundifolia and riparian Shepherdia argentea: Description, and traits suitable for low-water urban landscapes HortScience 51 822 828

    • Search Google Scholar
    • Export Citation
  • Sriladda, C., Kjelgren, R., Kratsch, H., Monaco, T., Larson, S. & Shen, F. 2014 Ecological adaptation of the endemic Shepherdia rotundifolia to conditions in its Colorado Plateau range West. N. Amer. Nat. 74 79 91

    • Search Google Scholar
    • Export Citation
  • Taiz, L., Zeiger, E., Møller, I.M. & Murphy, A. 2015 Plant physiology and development. 6th ed. Sinauer Associates, Sunderland, MA

  • Thomas, A.L. & Schrock, D. 2004 Performance of 67 native midwestern U.S. perennials in a low-maintenance landscape HortTechnology 14 381 388

  • Thomas, K.A. & Berry, A.M. 1989 Effects of continuous nitrogen application and nitrogen preconditioning on nodulation and growth of Ceanothus griseus var horizontalis Plant Soil 118 181 187

    • Search Google Scholar
    • Export Citation
  • Tortosa, R.D. & Cusato, M. 1991 Effective nodulation of rhamnaceous actinorhizal plants induced by air dry soils Plant Soil 131 229 233

  • Urbano, C.C. 1989 The environmental debate: An industry issue. Amer. Nurseryman 169:69–73, 76–79, 81, 83, 85

  • Valverde, C., Ferrai, A. & Wall, L.G. 2002 Phosphorus and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501 New Phytol. 153 43 51

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