1. Introduction
The use of arbuscular mycorrhizal fungi (AMF) in agriculture has shown that it substantially improves various components of crop growth and yields. Researchers such as [1] demonstrated these benefits using soybeans against drought stress when inoculating them with AMF and Bradyrhizobium japonicum. Other authors such as (2022) [2] mentioned that the agroecological approach favors the maintenance and balance of microorganisms in the rhizosphere that interact with the host plants [3], in addition to inducing root protection schemes against various pathogens [4]. The interactions between plants and AMF contribute to agricultural sustainability [5], and as a result, benefits are derived and plant survival increases, especially in limiting agroecological conditions [6,7]. Endomycorrhizal fungi are obligate symbionts found in approximately 80% of terrestrial plant roots [8] and embody essential mutualism in the distribution and interaction of both plants and fungi [9,10]. Ref. [11] evaluated the biofertilizers produced from Bradyrhizobium sp., Bacillus subtilis, and AMF in guar plants, noting that the combined inoculation increased the physiological and yield components. Due to the benefits that AMF represents for agriculture and the adaptation of plants to new agroclimatic environments, it is opportune to evaluate their ability to associate with introduced agricultural species, such as lulo.
Lulo or naranjilla (Solanum quitoense Lamarck) (Solanaceae) is a crop of commercial importance in South America, specifically for Ecuador, Colombia, and Peru, with yields of 7 to 15 t ha−1 [12], although its economic importance has also increased in Guatemala and Costa Rica [13]. The lulo plant is an herbaceous perennial (up to 3 years) with a 1 to 3 m height (Figure 1A) and broad and densely pubescent leaves [14] (Figure 1B). The stem is thick and lignescent with purple trichomes [15,16] (Figure 1C). Solanum quitoense grows under a humid mountain forest climate between an altitude of 1000 and 2500 m, featuring temperatures from 15 to 24 °C and precipitation from 2000–3000 mm per year. It prefers acidic (pH 5.5–6.0) and well drained soils [17,18].
One of the factors with the greatest influence on growth is fertilization. Lulo plants require high amounts of nutrients. An inadequate supply of nitrogen (N) causes chlorosis in adult leaves, while a phosphorus deficiency (P) causes downward growth, giving the impression of wilting. Potassium (K) generates yellow mottling, affecting the vegetative growth and causing gas exchange problems [19].
In plant nutrition schemes, the inoculation using arbuscular mycorrhizal fungi (AMF) has shown an efficiency in bioprotection, biofertilization, and bioregulation [20,21]. The plants of the Solanaceae family respond favorably to inoculation using AMF [22,23]. The main morphological characteristic of these is the typical structure of the colonization that the fungus develops inside the cells of the root bark [24]. This facilitates water and nutrient absorption, especially for low mobility nutrients such as P, which occurs through a network of extra radical hyphae that extend from the colonized roots to the surrounding soil and function as a supplementary absorbent system [25].
In Mexico, 143 known AMF species [26] are evaluated in order to improve the production of various tropical crops [27,28,29], from nursery conditions, phytosanitary quality, transplant resistance, height, vigor, as well as fruit quantity and postharvest quality. Based on the above, the growth and development of lulo plants inoculated with mycorrhizal fungi (Funneliformis mosseae and Entrophospora colombiana) accompanied by fertilization using diammonium phosphate (18N-46P-00K) in cloud forest soils was evaluated under the hypothesis that inoculation using AMF contributes to the adaptation and establishment of S. quitoense as an alternative crop in Mexico.
2. Materials and Methods
2.1. Study Site
The study was conducted in Huatusco, Veracruz, Mexico (19°08′56″ N, 96°57′58″ W) at an altitude of 1344 m. The climate was temperate humid with rain in the summer and an average temperature of 19.4 °C (a maximum of 26.3 °C and a minimum of 12.4 °C) [30]. The vegetation was a mountain mesophilic forest with an 85% relative humidity and 2250 mm of annual precipitation. The soils were rich in nutrients with a moderate fertility, coarse texture and fragments of volcanic glass, slightly acidic pH (4.3–6.5), rich organic matter, low Ca contents, and high Fe, Mn, and Zn contents [31].
2.2. Biological Material Used
Lulo seeds were taken from ripe fruits, washed, and dried in the shade. The seeds were sown in trays with 240 cavities (one seed per cavity) using a peat moss® (Baie Sainte-Anne, NB, Canada) and vermiculite® (Mexico City, Mexico) substrate (4:1). After 30 days, the seedlings were transplanted into polyethylene bags with 90 L of soil from the town of Huatusco, Veracruz, Mexico.
2.3. Physicochemical Analysis of Soil
The physicochemical analysis of the soil was obtained from three composite samples of the first 40 cm from random locations. The soil was air dried and sieved through a mesh net (5 mm pore). In the soil samples, the pH, electrical conductivity, and organic matter content were determined using the Walkley and Black method [32], N was determined using the Kjeldahl method [33], and P was determined using the Bray–Kurtz method [34]. The micronutrients were extracted and quantified using wet digestion [35]. The K content was determined using a flame emission spectrophotometer. The Ca and Mg contents were determined using atomic absorption (SavantAA GBC® Scientific Equipment, Keysborough, VIC, Australia). The texture of the soil was determined using the hydrometric method [36].
2.4. Isolation of Mycorrhizal Fungal Spores
The AMF F. mosseae and E. colombiana were isolated from the soil rhizosphere of a mango orchard (Mangifera indica L.) in Manlio Fabio Altamirano, Veracruz, Mexico. The spores were extracted using the methods of wet sieving (sieve numbers: 44, 325, and 400 μm) and decantation [37]. Morphological grouping was performed considering the shape, color, and size [38]. Morphotypes were inoculated in the seedlings of wheat (Triticum aestivum L.; one spore per plant and ten replicates). The monosporic culture was established in pots with a 1.0 L capacity and sterile sand as a substrate. The plants were maintained in a greenhouse at 40 °C. A Steiner nutrient solution [39] modified in P (20%, pH 7.5) was applied using daily irrigation. Through monthly soil sampling, the propagation of the inoculated morphotypes was assessed. In order to multiply the spores and set the symbiosis in the fourth month, one wheat seed was placed per pot for a second crop cycle. In the last two months the plants were maintained with water stress in order to accelerate the symbiosis, and subsequently, the spores of the AMF were extracted following the wet sieving and decantation methods [37].
The identification of F. mosseae and E. colombiana was conducted based on the description of the spore wall groups in semi-permanent preparations using polyvinyl alcohol, lactic acid, and glycerol with and without Melzer’s reagent [40]. For the AMF production, the spores were disinfected on the wall surface with a solution of chloramine T (20 g L−1) and streptomycin (200 mg L−1) and subsequently inoculated into sorghum plants (Sorghum vulgare L.) developed in sterile river sand (120 °C for 3 h for three consecutive days) according to the host plant method [41]. After four months, harvesting and root staining were performed following the method of Phillips and Hayman [42] and the percentage of the mycorrhizal colonization was measured using the quadrant intersection method [43].
2.5. Treatments and Inoculation of Symbiotic Microorganisms
In order to evaluate the growth and development of the lulo plant, four treatments were established: Entrophospora colombiana (350 spores: 10 g plant−1), Funneliformis mosseae (350 spores: 10 g plant−1), DAP fertilization (18-46-00) 5 g plant−1, and a control.
The plants were inoculated with F. mosseae and E. colombiana on the day of transplantation into the bags. A total of 350 spores of each AMF were added per plant in 10 g of substrate–inoculum. The spores were placed over the root system to ensure contact. For the treatment using diammonium phosphate (DAP; NPK 18-46-00 Phosagro® France SAS, PhosAgro Group of Companies, Moscow, Russia), 5 g was applied to each plant. Additionally, and for all the treatments, 5.0 g of a biostimulant (PHC Humex WS® Plant health care de Mexico, Mexico city, México) based on natural humates was applied to each plant, and 25 mL of PHC® YUCCAH® (Plant health care de Mexico, Mexico city, México) as a soil improver and decompactor were applied to the lulo plants.
2.6. Variables
2.6.1. Plant Growth
The plant height was measured monthly up to the fifth month, considering the base of the root neck to the apex of the youngest leaf. The diameter of the stem was recorded using a digital vernier, starting 90 days after germination (dag) and always at the average height of the plant.
2.6.2. Leaf Area Growth
The number of leaves was counted and the leaf area from transplantation (30 dag) to fruit formation was measured monthly. For this evaluation, the equatorial length and width were considered without considering the petiole.
2.6.3. Mycorrhizal Colonization in the Roots
Twelve months after transplantation, the roots of each treatment were sampled. The samples were washed with domestic water, rinsed with KOH (10%), stained with trypan blue (0.05%), and 10 segments of 1.0 cm in length were obtained, which represented a replicate. The segments were placed (randomly) parallel on a slide to determine the mycorrhizal colonization (hyphae, vesicles, and arbuscules) using a microscope at 45×. Three visual fields were examined in each root segment to observe the colonization of F. mosseae and E. colombiana, plus the native mycorrhizae. The percentage of the colonization was calculated as the ratio of the colonized root sections by the observed sections per 100.
2.6.4. Foliar Analysis
The leaves were sampled 12 months after transplantation, and in each treatment the mineral content was quantified. The total N was determined using the Microkjeldahl method [44], P was determined using a spectrophotometer (20D, Milton Roy Co., San Diego, CA, USA), the elements Ca, Mg, Mn, Cu, Zn, and Fe were analyzed using an atomic absorption spectrophotometer, and K was analyzed using flame emission (IL 551, Instrumentation Laboratories, Barcelona, Spain) [44]). Three repetitions per treatment were analyzed.
2.7. Experimental Design and Statistical Analysis
The experiment was conducted in random blocks with four treatments, three repetitions, and five plants for each experimental unit (n = 60 plants). The results were analyzed using an ANOVA and multiple comparisons of a means by Tukey test (α = 0.05) using the RStudio free version and MiniTab version 18 programs.
3. Results
3.1. Soil Analysis
The soil where the lulo plants were established was a clayey Vertisol type, characterized by plastic and moist compaction in the wet season. In the dry season, it formed wide and deep cracks that are typical of tropical climates with defined periods of rain and drought. The soil was slightly acidic (pH 6.39), rich in organic matter, high in Ca and Mg, very high in Fe, Mn, and Cu, but low in N, P, K, and Zn, with a low cation exchange capacity (CEC). Although there was no technical guide for the values of the physicochemical analysis of the soil for the cultivation of lulo, it was conducted based on the standard guide (Table 1).
3.2. Plant Height and Stem Diameter
The growth of lulo plants was recorded monthly (August to December) showing the differences (α = 0.05) between the treatments. The plants inoculated with E. colombiana and those fertilized with DAP (Figure 2A) stood out. During the first month after transplantation (30 dag), the height of the plants inoculated with E. colombiana was 3.54 ± 1.4, F. mosseae was 3.08 ± 0.7, DAP was 2.50 ± 1.0, and the control was 4.18 ± 1.40 cm. At the second month of evaluation, the plants inoculated with E. colombiana and fertilized with DAP achieved the greatest heights with 11.06 ± 2.91 and 9.81 ± 3.3 cm, respectively. At 90 dag, there was a significant increase in plant growth since all the treatments on average increased by 50%, registering the greatest heights for the treatments fertilized with DAP and inoculated with E. colombiana. In the fourth month of evaluation, the plants inoculated with E. colombiana presented the largest increases, with 53.46 ± 6.12 cm in height. After 150 dag, the plants showed heights of 62.40 ± 1.0 for those inoculated with E. colombiana and 61.40 ± 1.0 cm for those fertilized with DAP, which began fruiting and fruit growth.
As shown in Figure 2A, the inoculation using E. colombiana helped increase the height. In contrast, F. mosseae did not promote plant elongation. The stem diameter in all the treatments was evaluated from 90 dag. In this period, the treatments using E. colombiana and DAP exhibited the highest circumference (1.82 ± 0.43 and 1.88 ± 0.50 cm, respectively) (Figure 2B). At the fourth month, there were significant differences in all the treatments, where the plants inoculated with E. colombiana registered 2.39 ± 0.40, F. mosseae registered 1.97 ± 0.39, DAP registered 2.21 ± 0.40, and the control registered 2.12 ± 0.32 cm. However, at the fifth month, all the treatments became similar.
3.3. Number of Leaves and the Leaf Area
The number of leaves per plant during the first month of evaluation ranged from 6.3 ± 1.9 to 8.7 ± 1.1, where the lowest number of leaves was recorded with the inoculation of F. mosseae, while the control had significantly more leaves. In the second and third months of evaluation, all the treatments behaved statistically the same in terms of the number of sheets. However, in the fourth month, the number of leaves per plant showed significant differences since it decreased due to pruning. From the fifth month onwards, new sheets were exposed (Figure 3A). In this case, E. colombiana generated the highest number of leaves (10.33 ± 2.69), and the plants inoculated with F. mosseae had the lowest number (7.66 ± 2.02).
In relation to leaf development (Figure 3B) in the first month, the leaves in all the treatments began to grow while still presenting an oval shape with an average area of 6.5 cm2. In the second month, the leaves showed changes in their shape and color (green on the beam and purple on the underside with densely pubescent surfaces). At this stage, the plants inoculated with F. mosseae registered a smaller leaf area, while the other treatments did not show significant differences. In the third month, the leaf area increased by 90%. The plants inoculated with E. colombiana and DAP exhibited the largest leaf area and maintained this behavior until the fifth month of evaluation, generating areas of 1758.53 and 1666.67 cm2, respectively.
3.4. Mycorrhizal Colonization
The analysis of the mycorrhizal colonization after 12 months of transplantation showed the presence of hyphae, vesicles, and arbuscules. The highest values of these structures in the roots were obtained with the inoculation of E. colombiana, achieving a 70.5% total colonization, while the treatment using diammonium phosphate (DAP) had a 63.4% native mycorrhizal colonization. In this case, the addition of the DAP fertilization favored the available content of P, and F. mosseae showed a 59.30% colonization. Since this study aimed to evaluate the adaptability of lulo to soils different from those of its original habitat, the soil was not sterilized to determine the level of colonization, both native and induced by Funneliformis mosseae and Entrophospora colombiana. Table 2 indicates the values of this variable, highlighting the induced colonization with respect to the native colonization. The above suggests that inoculation using these AMF can contribute to the successful establishment of lulo as an agricultural crop in the study region, applying this activity from the nursery.
3.5. Foliar Analysis
Twelve months after transplantation, the leaves inoculated with E. colombiana and F. mosseae showed the highest N contents with values of 3.85 ± 0.21 and 3.54 ± 0.08%, respectively, while the control showed the lowest value (1.85 ± 0.07%) (Figure 4A). The highest content of P was obtained from DAP fertilization, with a value of 0.17 ± 0.0%, which was equivalent to 58.83% more than the control (Figure 4B). The highest concentration of K was recorded in the plants inoculated with E. colombiana (3.57 ± 0.02%), with F. mosseae and DAP (69.54 and 58.94%) achieving higher concentrations than the control (Figure 4C).
The highest content of Ca (3.07 ± 0.04%) in the leaf tissue was observed in the treatment with E. colombiana (Figure 5A), while the lowest content was obtained in the control (1.10 ± 0.03%). The highest Mg content was observed in the plants inoculated with E. colombiana and F. mosseae (0.31 ± 0.01 and 0.28 ± 0.01%), and these concentrations were 46.43 and 53.57% higher than the control (Figure 5B).
The foliar analysis of the micronutrient content showed significant differences between the treatments. The highest content of Mn (40.69%) was observed in the plants inoculated with E. colombiana, and the treatments with F. mosseae and DAP presented 33.6 and 37.1% higher concentrations than the control (Figure 6A).
The Cu concentration of 0.21 ± 0.02 mg kg−1 was the highest and corresponded to the plants inoculated with E. colombiana. The lowest value (0.050 mg kg−1) corresponded to the control (Figure 6B). Regarding Fe, the maximum content was presented by the plants inoculated with E. colombiana and represented a 48.78% higher concentration than in the control (Figure 6C). The highest Zn content (3.0 mg kg−1) was identified from the treatment with E. colombiana. The plants inoculated with F. mosseae and fertilized with DAP showed a content of 2.5 mg kg−1 and the control plants presented a content of 1.0 mg kg−1 (Figure 6D).
4. Discussion
4.1. Soil Analysis
Lulo thrives in slightly acidic soils (pH 6.0–6.4) that are moist, deep, and have good drainage. Interacting with native mycorrhizal fungi improves its development [45]. Despite the “rustic” appearance of the lulo plant, its development depends directly on the nutrition and characteristics of the soil. Generally, the type of soil where it develops best is loam with a good content of organic matter and a clayey–sandy composition [46,47]. Solanum quitoense is used as a colonizer for land from clearings on hillsides, so it is common for it to be planted in virgin soils.
The lulo plant can be adapted to humid mountain forests and can grow in in areas with coffee cultivation (Coffea arabica L.), as was the case for the cloud forest of Huatusco, Veracruz [48,49].
Researchers such as [50] evaluated three bocashi-type organic sources, a treatment using a chemical fertilizer (10 N-30 P-10 K), and a control in a soil derived from volcanic ash that was well drained, soft, or friable, and slightly plastic with a high fertility and loamy texture in order to obtain a better performance in the cultivation of the lulo ‘La Selva’. The researchers recorded that organic matter applications improved the soil characteristics, and with organic matter contents between 172 and 180 g kg−1, chemical fertilization produced contents of 0.5 to 1.54 cmol kg−1 of K, 4.2 to 10.5 cmol kg−1 of Ca, 1.1 to 2.4 cmol kg−1 of Mg, and 990 mg kg−1 of P, which stabilized at a pH of 5.6. With the above, Ref. [50] concluded that the best performance was obtained using a bocashi of poultry manure, which saw a 38.3% increase in fruit productivity that was equivalent to the highest yield of 4.7 t ha−1.
4.2. Plant Height and Stem Diameter
AMF inoculations in S. quitoense var. Septentrionale resulted in an increased in the plant height of 54.7% with Glomus sp. and S. heterogama compared to those that were not inoculated. In addition, shade increased growth by 11.6% compared to the plants exposed to the sun [51].
The biomass in gooseberry plants (Physalis peruviana L.) increased from an inoculation of 200 g of mycorrhiza Glomus sp., Acaulospora sp., and Entrophospora sp. and fertilization using 15-15-15 (N-P-K of 200 g plant−1). AMF increased the landfill capacity of the root system, thereby increasing the photosynthetic rate and growth of the plant [52].
Other researchers evaluated the inoculation of E. colombiana plus the addition of 100N-30P-150K (Heliconia L. f psittacorum × H. spathocircinata) in a reported stimulus or vegetative growth, increase or plant height, stem diameter, number of shoots, leaf area, or chlorophyll content [53]. Additionally, F. mosseae favored the development of the rootstocks of avocados (Persea americana) in nursery conditions, improving the quality and constituting a nutritional alternative for this crop [54].
Fertilization in soil and the foliar applications using biostimulant derivatives of the seaweed extract Ascophyllum nodosum in lulo plants increased the diameter of the stem with respect to the control, registering at 150 days after transplantation with a soil fertilization diameter of 1787 cm. In contrast, the diameter of the foliar fertilization registered as 1.630 cm, the mixture of fertilizers (soil and foliar) registered as 1.877 cm, the control registered as 1.48 cm [55].
In our study, from the application of arbuscular mycorrhizae and DAP, the diameter of the stem was 27.25% greater than the control plants. Similar values were reported by [56] in tomato seedlings (S. lycopersicum L.) whose increased stem diameters ranged between 5.55 and 6.13 cm while the control showed a value of 4.88 cm.
4.3. Number of Leaves and the Leaf Area
The results of the present study coincided with those reported by [56] in tomato plants (S. lycopersicum L.) from inoculation with Rhizophagus irregularis, which generated between 7.10 and 7.70 sheets unlike the control, which generated 6.50 sheets. In relation to leaf development, the length of the leaves were up to 60 cm [57], while Ref. [58] reported lengths between 25 and 30 cm. The evaluations of lulo to determine the effect of NaCl (30 and 60 mM) applied via foliar fertilization in different substrates showed that the highest values of the leaf area corresponded to the control plants grown in peat without NaCl (2900 cm2) [59]. The effect of the fertilization with N (10 and 110 mg N L H2O−1) in greenhouse conditions, treating a group of plants with a foliar urea (250 mg de N L−1), resulted in plants with 110 mg N L−1 and the best performance in waterlogging conditions. The leaf area was 62% greater in the plants with a high N content than in the plants with the lowest concentration [60].
4.4. Mycorrhizal Colonization
Solanaceae plants such as S. quitoense respond favorably to inoculation with arbuscular mycorrhizal fungi (AMF) [61]. The fungi offer amino acids, nutrients, and water to the host in exchange for photosynthates. Due to this, the photosynthesis and distribution of carbohydrates in the host plant is altered [53]. The efficiency of mycorrhizae depends on the conditions in which it is applied, including the culture and local microbiota in the soil [62]. Colonization with AMF promotes the availability of P in soils with poor concentrations of this element and in clay soils, facilitates the release of this element, and transfers it to the plants through a series of physicochemical and biological reactions, actively transforming P through the processes of mineralization, solubilization, immobilization, and oxidation [63].
Glomus aggregatum was evaluated under greenhouse conditions to determine the dependence of the lulo var. ‘La Selva’. Researchers classified the species as moderately dependent on its association with mycorrhizae with 0.002 mg L−1 de P, with a tendency to decrease when there is an increase in the concentration of P in the soil solution [64]. Other researchers such as [65] evaluated the colonization of the mycorrhizae of G. mosseae and E. colombiana in the papaya (Carica papaya L.) var. Maradol and observed a colonization of 91.5% by G. mosseae, 58.2% by E. colombiana, and 16.5% in the control plants, which indicated that G. mosseae responded favorably to temperate climates and that E. colombiana was effective in tropical climate zones.
4.5. Foliar Analysis
Ref. [60] determined the concentrations of N, P, K, Ca, and Mg in (S. quitoense var. Quitoense), obtaining 3.49% N, which was considered as an adequate value. For P, they reported 0.25%, which was considered a medium level. The average K was 2.9, 2.7, and 3.2% in the plants growing in a peat, sand, and substrate mix, respectively, which was considered low. In Ca, the highest percentage was 2.63%, and for Mg they reported 0.19 to 0.47%. This mineral is relevant because its deficiency affects the structure and integrity of chloroplasts, photosynthesis, sugar accumulation, and various metabolic activities [66].
The physiological response of the Solanum quitoense var. Septentrionale to foliar concentrations of 125, 250 y 500 mg kg−1 of N was evaluated. The results reported that the control plants had a shorter length and a lower dry mass and chlorophyll content in the lower leaves than the plants grown with fertilizer. In addition, they revealed that the lack of nutrients caused more biomass in the roots. These results indicate that a poor nutritional status may limit foliar absorption [67].
The relationship of macro and micronutrients influences the physiological processes of plants, since they intervene in the activity of enzyme systems and participate in oxide reduction reactions, such as nitrate reduction, photosynthesis, N fixation, and oxidations. Cu participates in oxide reduction reactions as a constituent of the enzymes (oxidases, cytochrome oxidase, and others) in photosynthesis, metabolism of the cell walls (synthesis of lignins), nitrogen fixation, and degradation of proteins.
Fe deficiencies are usually induced by inadequate assimilation caused by elevated soil pH, excess Ca ions, bicarbonates in the soil solution, and interactions with other elements. [68]. The Mn concentrations in lulo were lower than those obtained by [69] in pepper (Capsicum annuum L.) from 90 to 250 mg kg−1. However, [70] showed that the Mn content in plants varies widely and that deficiencies are generally observed as those with leaf concentration below 20 mg kg−1. Ref. [71] recommend the application of 135, 86, 126, 9, 4, 4 y 5 g plant−1 of N, P2O5, K2O, Fe, Zn, and B y S, respectively, distributed throughout the year in six applications every two months. Likewise, Ref. [72] found that, by removing Mg from the nutrient solution, the height of the lulo plants decreased significantly and possibly lacked Mn, Mo y Cu.
Other researchers such as [73,74] identified that lulo was significantly susceptible to deficiencies in B, Mg, and Mn, and that P was the cause of delays in growth and the ripening of fruits since this element was considered to be responsible for malformations in the seeds.
5. Conclusions
S. quitoense can grow favorably in and show an adaptability to Vertisol-type clay soils in cloud forests. The composition of macro and microelements increased in K, Ca, Mn, Cu, Zn, and Fe with the inoculation with E. colombiana, and to a lesser extent with F. mosseae, which increased the concentration of N and Mg. The fertilization with DAP increased the content of P. Therefore, the application of mycorrhizae, as well as the application of DAP for seedlings, is a recommended practice for lulo. The results are encouraging to continue with expanding the cultivation areas in the study region, since the components of growth and adaptation in cloud forest soils were attributed to the association with AMF.
Conceptualization: J.C.-I., M.d.L.A.-G. and D.J.-C.; methodology, J.C.-I. and D.J.-C.; software, A.L.O.-H.; validation, C.B.P.-V. and A.L.O.-H.; formal analysis, A.L.O.-H. and C.B.P.-V.; investigation, A.L.O.-H.; resources, M.d.L.A.-G.; data curation, A.L.O.-H. and D.J.-C.; writing—original draft preparation, A.L.O.-H., J.C.-I.; writing—review and editing, A.L.O.-H., M.d.L.A.-G. and J.C.-I.; supervision, M.d.L.A.-G. All authors have read and agreed to the published version of the manuscript.
Not applicable.
The authors wish to thank the Colegio de Postgraduados and the Interdisciplinary Research Group at Sechium edule in Mexico, A.C., for the support with the laboratories, equipment, and biological materials from Lulo for the development of the research.
The authors declare no conflict of interest.
Arbuscular mycorrhizal fungi (AMF), potassium hydroxide (KOH), analysis of variance (ANOVA), liter (L), cation exchange capacity (CEC), diammonium phosphate (DAP), standard error (S.D.), centimoles per kilogram (cmol kg−1), nitrogen (N), phosphorus P), potassium (K), calcium (Ca), magnesium (Mg), copper (Cu), molybdenum (Mo), iron (Fe), boron (B), zinc (Zn), diphosphorus pentaoxy (P2O5), potassium oxide (K2O).
Footnotes
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Enlarge this image.Figure 1. Lulo plant (Solanum quitoense). (A) Structure of the plant. (B) Inflorescences. (C) Fruits in physiological maturity.
Enlarge this image.Figure 2. (A) Total height (±S.D.) of lulo plants (Solanum quitoense) from transplantation to fruiting. (B) Stem diameter (±S.D.) in lulo plants at the third, fourth, and fifth months (fruited) after transplantation. The different letters on the bars indicate a significant difference at each evaluation date (n = 60).
Enlarge this image.Figure 3. (A) Number of leaves (±S.D.) in lulo plants (Solanum quitoense) from transplant to fruiting. The different letters on the bars indicate a significant difference at each evaluation date (n = 60). (B) Leaf area (±S.D.). The different letters on the bar indicate a significant difference at each evaluation date (n = 60).
Enlarge this image.Figure 4. Percentages (±S.D.) of N (A), P (B), and K (C) in the leaf tissue of lulo plants (Solanum quitoense) twelve months after transplantation. The different letters on the bars indicate a significant difference in the concentration of each element between the treatments (n = 12).
Enlarge this image.Figure 5. Concentrations (±S.D.) of Ca (A) and Mg (B) in the leaf tissue of lulo plants (Solanum quitoense) twelve months after transplantation. The different letters on the bars indicate a significant difference in the concentration of each element between the treatments (n = 12).
Enlarge this image.Figure 6. Concentrations of Mn (A), Cu (B), Fe (C), and Zn (D) in the leaf tissue of lulo plants (Solanum quitoense) twelve months after transplantation. The different letters on the bars indicate a significant difference in the concentration of each element between the treatments (n = 12).
Physicochemical characteristics of the soil of the experimental location for twelve-month-old plants in a reproductive stage.
| Variable | Content (mg kg−1) | Interpretation |
|---|---|---|
| N | 14.3 | Low |
| P | 11.3 | Low |
| K | 63.0 | Low |
| Ca | 3010 | High |
| Mg | 570 | High |
| Fe | 52.12 | Very high |
| Zn | 1.45 | Low |
| Mn | 57.30 | Very high |
| Cu | 3.04 | Very high |
| CEC | 14.64 cmol kg−1 | Low |
| Texture | ||
| Organic matter | 4.02 (%) | Rich |
| Arena | 17.16 (%) | Clay soil |
| Limo | 13.08 (%) | |
| Clay | 69.76 (%) | |
| pH | 6.39 | Slightly acidic |
Mycorrhizal colonization in the roots of lulo plants (Solanum quitoense). The different letters indicate a significant difference at each evaluation date (n = 60).
| Treatment | Hyphae (%) | Vesicles (%) | Arbuscules (%) | Colonization |
|---|---|---|---|---|
| Entrophospora colombiana | 63.20 a | 32.10 a | 36.50 a | 70.50 a |
| Funneliformis mosseae | 53.12 b | 10.70 b | 24.78 b | 59.30 b |
| Diammonium phosphate (DAP), native colonization | 59.70 a | 14.70 b | 28.70 b | 63.40 a |
| Control (native colonization) | 21.36 c | 1.47 c | 0.98 c | 9.74 c |
References
1. Sheteiwy, M.S.; Ali, D.F.I.; Xiong, Y.C.; Brestic, M.; Skalicky, M.; Hamoud, Y.A.; Ulhassan, Z.; Shaghaleh, H.; AbdElgawad, H.; Farooq, M. et al. Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biol.; 2021; 21, 195. [DOI: https://dx.doi.org/10.1186/s12870-021-02949-z] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33888066]
2. Reyes, J.R.; Morales, J.A.R.; de la Torre, D.D.J.P.; Pérez, M.A.F.; Morales, P.M.; García, A.M.; Medina, J.F.A. Diversidad y estructura arbórea de los árboles de sombra asociados a Coffea arabica L. en el Soconusco, Chiapas. Rev. Mex. Cienc. For.; 2022; 13, pp. 4-27. [DOI: https://dx.doi.org/10.29298/rmcf.v13i71.1191]
3. Baldi, E. Soil-plant interaction: Effects on plant growth and soil biodiversity. Agronomy; 2021; 11, 2378. [DOI: https://dx.doi.org/10.3390/agronomy11122378]
4. Bhale, S.A.; Bansode, A.; Singh, S. Multifactorial Role of Arbuscular Mycorrhizae in Agroecosystem. Fungi and their Role in Sustainable Development: Current Perspectives; Gehlot, P.; Singh, J. Springer: Singapore, 2018; pp. 2005-2020. [DOI: https://dx.doi.org/10.1007/978-981-13-0393-7_12]
5. Devi, S.H.; Bhupenchandra, I.; Sinyorita, S.; Chongtham, S.; Devi, E.L. Mycorrhizal fungi and sustainable agriculture. Nitrogen in Agriculture−Physiological, Agricultural and Ecological Aspects; Ohyama, T.; Inubushi, K. IntechOpen: London, UK, 2021; pp. 1-19. [DOI: https://dx.doi.org/10.5772/intechopen.99262]
6. Agnolucci, M.L.; Avio, A.; Pepe, A.; Turrini, C.; Cristani, P.; Bonini, P.; Giovannetti, M. Bacteria associated with a commercial mycorrhizal inoculum: Community composition and multifunctional activity as assessed by illumina sequencing and culture-dependent tools. Front. Plant Sci.; 2019; 9, 1956. [DOI: https://dx.doi.org/10.3389/fpls.2018.01956] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30693008]
7. Lara-Capistran, L.; Zulueta-Rodriguez, R.; Murillo-Amador, B.; Preciado-Rangel, P.; Verdecia-Acosta, D.M.; Hernandez-Montiel, L.G. Biodiversity of AM fungi in Coffee cultivated on eroded soil. Agronomy; 2021; 11, 567. [DOI: https://dx.doi.org/10.3390/agronomy11030567]
8. Zou, Y.N.; Wu, Q.S.; Kuča, K. Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biol.; 2021; 23, pp. 50-57. [DOI: https://dx.doi.org/10.1111/plb.13161] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32745347]
9. Tedersoo, L.; Anslan, S.; Bahram, M.; Drenkhan, R.; Pritsch, K.; Buegger, F.; Abarenkov, K. Regional-scale in-depth analysis of soil fungal diversity reveals strong pH and plant species effects in Northern Europe. Front. Microbiol.; 2020; 11, 1953. [DOI: https://dx.doi.org/10.3389/fmicb.2020.01953]
10. Janowski, D.; Leski, T. Factors in the distribution of mycorrhizal and soil fungi. Diversity; 2022; 14, 1122. [DOI: https://dx.doi.org/10.3390/d14121122]
11. El-Sawah, A.M.; El-Keblawy, A.; Ali, D.F.I.; Ibrahim, H.M.; El-Sheikh, M.A.; Sharma, A.; Alhaj Hamoud, Y.; Shaghaleh, H.; Brestic, M.; Skalicky, M. et al. Arbuscular Mycorrhizal Fungi and Plant Growth-Promoting Rhizobacteria Enhance Soil Key Enzymes, Plant Growth, Seed Yield, and Qualitative Attributes of Guar. Agriculture; 2021; 11, 194. [DOI: https://dx.doi.org/10.3390/agriculture11030194]
12. Duarte-Alvarado, D.; Lagos-Burbano, T.C.; Lagos-Santander, L.K.; Benavides-Cardona, C.A. General and specific combining abilities in a diallel cross of lulo (Solanum quitoense Lam.). Rev. Colomb. Cienc. Hortícolas; 2021; 15, e11976. [DOI: https://dx.doi.org/10.17584/rcch.2021v15i1.11976]
13. Andrade-Cuvi, M.J.; Guijarro-Fuertes Figueroa, J.L. Evaluación fisicoquímica y antioxidante de naranjilla (Solanum quitoense Lam.) durante la maduración. Rev. Iberoam. Tecnol. Postcosecha; 2021; 22, pp. 145-164.
14. Ramírez, F.; Kallarackal, J.; Davenport, T.L. Lulo (Solanum quitoense Lam.) reproductive physiology: A review. Sci. Hortic.; 2018; 238, pp. 163-176. [DOI: https://dx.doi.org/10.1016/j.scienta.2018.04.046]
15. Daunay, M.C.; Rousselle-Bourgeois, F.; Lester, R.N.; Peron, J.Y. Known and less known Solanum species for fresh market. Int. Symp. Solanacea Fresh Mark.; 1995; 412, pp. 293-305. [DOI: https://dx.doi.org/10.17660/ActaHortic.1995.412.34]
16. Chiarini, F.E.; Barboza, G.E. Fruit anatomy of species of Solanum sect. Acanthophora (Solanaceae). Flora-Morphology, Distribution, Functional Ecology of Plants; Elsevier: Amsterdam, The Netherlands, 2009; Volume 204, pp. 146-156. [DOI: https://dx.doi.org/10.1016/j.flora.2008.01.010]
17. González-Espinosa, M.; Meave, J.A.; Ramírez-Marcial, N.; Toledo-Aceves, T.; Lorea-Hernández, F.G.; Ibarra-Manríquez, G. Los bosques de niebla de México: Conservación y restauración de su componente arbóreo. Ecosistemas; 2012; 21, pp. 36-54.
18. Muñoz, J.A.; Rodríguez, L.F.; Bermúdez, L.T. Análisis de competitividad del sistema de producción de lulo (Solanum quitoense Lam.) en tres municipios de Nariño. Rev. Colomb. Cienc. Hortícolas; 2013; 7, pp. 173-185.
19. Lim, T.K. Solanum quitoense. Edible Medicinal and Non-Medicinal Plants; Springer: Dordrecht, The Netherlands, 2013; Volume 6, pp. 419-423. [DOI: https://dx.doi.org/10.1007/978-94-007-5628-1_46]
20. Varela, J.C.; Velásquez, J.C.; de Tafur, M.S.M. Respuesta fisiológica del lulo (Solanum quitoense Lam.) a diferentes concentraciones de N, P, K, Ca y Mg en la solución nutritiva. Acta Agron.; 2002; 51, pp. 53-59. [DOI: https://dx.doi.org/10.15446/acag]
21. Di Barbaro, G.; Andrada, H.; González Basso, V.; Alurralde, A.L.; Del Valle, E.; Brandán de Weht, C. Micorrizas arbusculares y hongos septados oscuros nativos en topinambur (Helianthus tuberosus L.) en Catamarca, Argentina. Rev. Cienc. Agric.; 2017; 34, pp. 98-106. [DOI: https://dx.doi.org/10.22267/rcia.173402.75]
22. Tedersoo, L.; Bahram, M.; Zobel, M. How mycorrhizal associations drive plant population and community biology. Science; 2020; 367, eaba1223. [DOI: https://dx.doi.org/10.1126/science.aba1223]
23. Avio, L.; Turrini, A.; Giovannetti, M.; Sbrana, C. Designing the ideotype mycorrhizal symbionts for the production of healthy food. Front. Plant Sci.; 2018; 9, 1089. [DOI: https://dx.doi.org/10.3389/fpls.2018.01089]
24. Arocha-Rodríguez, M.D.L.C.; Pérez-Ortega, E.; Fernández-Suárez, K.; Haesaert, G. Efecto del pH del medio de cultivo en el crecimiento pre simbiótico de Rhizoglomus irregulare. Cultiv. Trop.; 2019; 40, pp. 1-12.
25. Ferlian, O.; Biere, A.; Bonfante, P.; Buscot, F.; Eisenhauer, N.; Fernandez, I.; Martinez-Medina, A. Growing research networks on mycorrhizae for mutual benefits. Trends Plant Sci.; 2018; 23, pp. 975-984. [DOI: https://dx.doi.org/10.1016/j.tplants.2018.08.008] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30241736]
26. Loor, M.J.B.; Zambrano, L.J.S. Evaluación de la infectividad de comunidades de hongos micorrízicos arbusculares. Pro Sci. Rev. Prod. Cienc. Investig.; 2019; 3, pp. 1-5.
27. Peñuelas-Rubio, O.; Trejo-Aguilar, D.; Cervantes-Gámez, R.G.; Maldonado-Mendoza, I.E. Análisis microbiómico de hongos micorrízicos arbusculares asociados a papaya, inoculada con consorcios de dos ecosistemas naturales. Sci. Fungorum; 2021; 51, e1292. [DOI: https://dx.doi.org/10.33885/sf.2021.51.1292]
28. Raya-Montaño, Y.A.; Apáez-Barrios, P.; Aguirre- Paleo, S.; Vargas -Sandoval, M.; Paz-Da Silva, R.; Lara-Chávez, M.B.N. Identificación de hongos micorrizógenos arbusculares en huertos de aguacate de Uruapan, Michoacán. Rev. Mex. Cienc. Agrícolas; 2019; 10, pp. 267-276. [DOI: https://dx.doi.org/10.29312/remexca.v0i23.2026]
29. Hernández-Acosta, E.; Trejo-Aguilar, D.; Rivera-Fernández, A.; Ferrera-Cerrato, R. La micorriza arbuscular como biofertilizante en cultivo de café. Terra Latinoam.; 2020; 38, pp. 613-628. [DOI: https://dx.doi.org/10.28940/terra.v38i3.659]
30. Vázquez-Hernández, M.V.; Arévalo-Galarza, M.D.L.; Jaen-Contreras, D.; Escamilla-García, J.L.; Luna-Esquivel, G. Calidad y almacenamiento de frutos de papaya procedentes de plantas inoculadas con Glomus mosseae. Rev. Mex. Cienc. Agrícolas; 2020; 11, pp. 1163-1170. [DOI: https://dx.doi.org/10.29312/remexca.v11i5.2280]
31. SMN-CONAGUA. Servicio Meteorológico Nacional. Comisión Nacional del Agua. 2022; Available online: https://smn.conagua.gob.mx/es/ (accessed on 21 October 2022).
32. Cadena-Iñiguez, J.; Soto-Hernández, M.; Arévalo-Galarza, M.; Avendaño-Arrazate, C.H.; Aguirre-Medina, J.F.; Ruiz-Posadas, L.D.M. Caracterización bioquímica de variedades domesticadas de chayote Sechium edule (Jacq.) Sw. comparadas con parientes silvestres. Revista Chapingo. Ser. Hortic.; 2011; 17, pp. 45-55.
33. Walkley, A.; Black, I.A. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci.; 1934; 37, pp. 29-38. [DOI: https://dx.doi.org/10.1097/00010694-193401000-00003]
34. Bremner, J.M.; Mulvaney, C.S. Nitrogen-total. Methods of Soil Analysis, Part 2. Agronomy Monograph 9; Page, A.L.; Miller, H.; Keeny, D.R. American Society of Agronomy: Madison, WI, USA, 1982; pp. 56-59.
35. Boschetti, G.; Quintero, C.; Diaz-Zorita, M.; Barraco, M. Determinación del fósforo disponible en el suelo por el método de Bray. Argentina. Actividad del comité de química de la AACS. Inf. Agron. Cono Sur; 2003; 17, pp. 6-9.
36. Chapman, H.D. Cation exchange capacity. Methods of Soil Analysis. Part 2. Agronomy Monograph 9; Black, C.A. American Society of Agronomy: Madison, WI, USA, 1965; pp. 891-901. [DOI: https://dx.doi.org/10.2134/agronmonogr9.2.c6]
37. Bouyoucos, G.J. Directions for making mechanical analyses of soils by the hydrometer method. Soil Sci.; 1936; 42, pp. 225-230. [DOI: https://dx.doi.org/10.1097/00010694-193609000-00007]
38. Gerdemann, J.W.; Nicolson, T.H. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc.; 1963; 46, pp. 235-244. [DOI: https://dx.doi.org/10.1016/S0007-1536(63)80079-0]
39. INVAM. International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi. Species Descriptions from Reference Cultures; West Virginia University: Morgantown, WV, USA, 2016; Available online: https://invam.ku.edu/species-descriptions (accessed on 23 January 2023).
40. Steiner, A.A. Selective compacity of tomato plants for ions in a nutrient solution. Proceedings of the 3d International Congress on Soilless Culture; Sassari, Cerdeña, Italy, 7–12 May 1973; pp. 43-54.
41. Schenck, N.C.; Pérez, Y. Manual for the Identification of VA Mycorrhizal Fungi; 3rd ed. Synergistic Publications: Gainesville, FL, USA, 1990; 286p.
42. Sieverding, E. Manual de Métodos para la Investigación de la Micorriza Vesículo-Arbuscular en el Laboratorio; Centro Internacional de Agricultura Tropical: Cali, Colombia, 1983; 121.
43. Phillips, J.M.; Hayman, D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc.; 1970; 55, 158-IN18. [DOI: https://dx.doi.org/10.1016/S0007-1536(70)80110-3]
44. Giovannetti, M.; Mosse, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol.; 1980; 84, pp. 489-500. [DOI: https://dx.doi.org/10.1111/j.1469-8137.1980.tb04556.x]
45. Chapman, H.D.; Pratt, P.F. Métodos de Análisis para Suelo, Plantas y Agua; Trillas: Mexico city, Mexico, 1973.
46. Duarte Alvarado, D.E.; Lagos Burbano, T.C.; Vallejo Cabrera, F.A.; y Lagos Santander, L.K. Agronomic evaluation of lulo introductions Solanum quitoense Lamarck. Acta Agron.; 2021; 70, pp. 66-72. [DOI: https://dx.doi.org/10.15446/acag.v70n1.84150]
47. Gómez-Merino, F.C.; Trejo-Téllez, L.I.; García-Albarado, J.C.; Cadeña-Íñiguez, J. Lulo (Solanum quitoense [Lamarck.]) as new landscape crop in the Mexican agro-ecosystem. Rev. Mex. Cienc. Agrícolas; 2014; 5, pp. 1741-1753. [DOI: https://dx.doi.org/10.29312/remexca.v0i9.1061]
48. Lagos-Santander, L.K.; Lagos-Burbano, T.C.; Duarte-Alvarado, D.E.; Criollo-Escobar, H.; Angulo-Ramos, N.F. Evaluación del rendimiento y calidad del fruto de parentales e híbridos de lulo de Castilla. Rev. UDCA Act. Div. Cient.; 2019; 22, e1344. [DOI: https://dx.doi.org/10.31910/rudca.v22.n2.2019.1344]
49. Medina, C.C.I.; Lobo, A.M.; Martínez, B.E. State of knowledge review on the productive function of lulo (Solanum quitoense Lam.) in Colombia. Rev. Corpoica-Cienc. Tecnol. Agropecu.; 2009; 10, pp. 167-179. [DOI: https://dx.doi.org/10.21930/rcta.vol10_num2_art:139]
50. Coronado, A.C.M.; Fagua, A.D.P.R.; Coronado, Y.M. Morphological Characterization of Lulo (Solanum quitoense Lam.) in the Municipality for Pachavita, Boyacá. Acta Biol. Colomb.; 2019; 24, pp. 291-298. [DOI: https://dx.doi.org/10.15446/abc.v24n2.75832]
51. Ramírez-Builes, V.H.; Duque, N.N. Respuesta del lulo La Selva (Solanum quitoense x Solanum hirtum) a la aplicación de fermentados aeróbicos tipo bocashi y fertilizante químico. Acta Agron.; 2010; 59, pp. 155-161.
52. Casierra-Posada, F.; Peña-Olmos, J.; Peñaloza, J.; Roveda, G. Influencia de la sombra y de las micorrizas sobre el crecimiento de plantas de lulo (Solanum quitoense Lam.). Rev. UDCA Actual. Divulg. Cienti.; 2013; 16, pp. 61-70.
53. Miranda, D.; Fischer, G.; Ulrichs, C. The influence of arbuscular mycorrhizal colonization on the growth parameters of cape gooseberry (Physalis peruviana L.) plants grown in a saline soil. J. Soil Sci. Plant Nutr.; 2011; 11, pp. 18-30. [DOI: https://dx.doi.org/10.4067/S0718-95162011000200003]
54. Baltazar-Bernal, O.; Jaén-Contreras, D. Hongos micorrízicos arbusculares y fertilización en Heliconia psittacorum L. f.× H. spathocircinata cv. tropics. Rev. Fitotec. Mex.; 2020; 43, pp. 45-52. [DOI: https://dx.doi.org/10.35196/rfm.2020.1.45]
55. Sánchez, L.R.F.; Espinosa, R.R.; Cárdenas, J.V.M.; Puig, A.C.; Hernández, A.T. Utilización de cepas eficientes de hongos micorrízicos arbusculares en el desarrollo de portainjertos de aguacate en un sustrato suelo-cachaza. Cultiv. Trop.; 2011; 32, pp. 23-29.
56. Díaz-Leguizamón, J.J.; Chingaté-Cruz, O.F.; Sánchez-Reinoso, A.D.; Restrepo-Díaz, H. The effect of foliar applications of a bio-stimulant derived from algae extract on the physiological behavior of lulo seedlings (Solanum quitoense cv. Septentrionale). Cienc. Investig. Agrar.; 2016; 43, pp. 25-37. [DOI: https://dx.doi.org/10.4067/S0718-16202016000100003]
57. Ramos-Otiniano, C.C.; Hidalgo Rodríguez, J.E.M.; Vera Vega, M.Á.; Pedro Huaman, J.J.; Rodríguez Seminario, C.E.; Chaman Medina, M.E. Efecto del NaCl y micorrizas (Rhizophagus irregularis) en el crecimiento de “tomate” Solanum lycopersicum L. (Solanaceae). Arnaldoa; 2021; 28, pp. 675-692.
58. Dennis, F.G., Jr.; Herner, R.C.; Camacho, S. Naranjilla: A potential cash crop for the small farmer in Latin America. Proceedings of the X African Symposium on Horticultural Crops; Addis Ababa, Ethiopia, 16–21 January 1984; Volume 158, pp. 475-481. [DOI: https://dx.doi.org/10.17660/ActaHortic.1985.158.55]
59. Almanza-Fandiño, M.T.A. Management of Bombus atratus Bumblebees to pollinate lulo (Solanum quitoense L), a Native Fruit from the Andes of Colombia; Cuvillier Verlag: Göttingen, Germany, 2007; Volume 50, pp. 50-112.
60. Flórez, S.L.; Miranda, D.; Chaves, B. Nutrient dynamic in the vegetative growth phase of lulo (Solanum quitoense Lam.) in response to NaCl salinity. Agron. Colomb.; 2008; 26, pp. 205-216.
61. Flórez-Velasco, N.; Balaguera-López, H.E.; Restrepo-Díaz, H. Effects of foliar urea application on lulo (Solanum quitoense cv. septentrionale) plants grown under different waterlogging and nitrogen conditions. Sci. Hortic.; 2015; 186, pp. 154-162. [DOI: https://dx.doi.org/10.1016/j.scienta.2015.02.021]
62. Aranguren, Y.A.; Castellanos, L.; Escalante, J.C. Hongos formadores de micorrizas arbusculares (HMA) en frutales de Colombia y su comparación con investigaciones internacionales: Arbuscular mycorrhizal fungi (AMF) in Colombian fruit trees and their comparability with international research. Cienc. Tecnol. Agropecu.; 2020; 5, pp. 27-37.
63. Carreón-Abud, Y.; Vega-Fraga, M.; Gavito, M.E. Interaction of arbuscular mycorrhizal inoculants and chicken manure in avocado rootstock production. J. Soil Sci. Plant Nutr.; 2015; 15, pp. 867-881. [DOI: https://dx.doi.org/10.4067/S0718-95162015005000060]
64. Arias-Mota, R.M.; Romero Fernández, A.D.J.; Bañuelos Trejo, J.; Cruz Elizondo, Y.D.L. Inoculation of phosphorus solubilizing fungi and arbuscular mycorrhizae in tomato plants. Rev. Mex. Cienc. Agric.; 2019; 10, pp. 1747-1757. [DOI: https://dx.doi.org/10.29312/remexca.v10i8.1558]
65. González, O.; Osorio, W. Determinación de la dependencia micorrizal del lulo. Acta Biol. Colomb.; 2008; 13, pp. 163-174.
66. Vázquez-Hernández, M.V.; Arévalo-Galarza, L.; Jaen-Contreras, D.; Escamilla-García, J.L.; Mora-Aguilera, A.; Hernández-Castro, E.; Téliz-Ortiz, D. Effect of Glomus mosseae and Entrophospora colombiana on plant growth, production, and fruit quality of ‘Maradol’papaya (Carica papaya L.). Sci. Hortic.; 2011; 128, pp. 255-260. [DOI: https://dx.doi.org/10.1016/j.scienta.2011.01.031]
67. Yang, G.H.; Yang, L.T.; Jiang, H.X.; Li, Y.; Wang, P.; Chen, L.S. Physiological impacts of magnesium-deficiency in Citrus seedlings: Photosynthesis, antioxidant system and carbohydrates. Trees; 2012; 26, pp. 1237-1250. [DOI: https://dx.doi.org/10.1007/s00468-012-0699-2]
68. Parra-Coronado, A.; Ardila-Roa, G.H.; Restrepo-Díaz, H. The physiological response of lulo plants (Solanum quitoense var. Septentrionale) to soil and foliar applications of nutrients. Int. J. Fruit Sci.; 2015; 15, pp. 148-160. [DOI: https://dx.doi.org/10.1080/15538362.2014.978638]
69. Cavallaro Júnior, M.L.; Trani, P.E.; Passos, F.A.; Kuhn Neto, J.; Tivelli, S.W. Produtividade de rúcula e tomate em função da adubação N e P orgânica e mineral. Bragantia; 2009; 68, pp. 347-356. [DOI: https://dx.doi.org/10.1590/S0006-87052009000200008]
70. Schroeder, M.A.; Martínez, G.C. Concentraciones foliares de microelementos en Pimiento (Capsicum annuum L.). Agrotecnia; 2004; 13, pp. 17-21. [DOI: https://dx.doi.org/10.30972/agr.013446]
71. Loué, A. Los Microelementos en Agricultura; Mundi Prensa: Madrid, Spain, 1986; 166p.
72. Herrera, J.G.A.; Guerrero, M.J.; Fischer, G. Aspectos de la fisiología y el cultivo del lulo (Solanum quitoense LAM.) en Colombia: Una revisión. Rev. Investig. Agrar. Ambient.; 2022; 13, pp. 131-148. [DOI: https://dx.doi.org/10.22490/21456453.4641]
73. Bolívar, M.I.V.; Medellín, L.A.C.; Trujillo, M.M.P. Efecto de las deficiencias de algunos nutrientes en plantas de lulo (Solanum quitoense var. quitoense) en etapa de vivero. Rev. Fac. Cienc. Básicas; 2009; 5, pp. 64-81. [DOI: https://dx.doi.org/10.18359/issn.1900-4699]
74. Cabezas, M.; Botía, T.; Medina, L.M. Determinación de síntomas de deficiencia inducida de nutrimentos en lulo (Solanum quitoense Lam.). IV Seminario Nacional de Frutales de Clima Frío Moderado; Corpoica: Mosquera, Colombia, 2003; pp. 176-181. Available online: http://hdl.handle.net/20.500.12324/13648 (accessed on 11 February 2023).
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Details
; Cadena-Iñiguez, Jorge 2
; Jaén-Contreras, David 1 ; Peña-Valdivia, Cecilia B 1
1 Colegio de Postgraduados, Campus Montecillo, Fisiología Vegetal. Km. 36.5 Carretera México, Texcoco 56264, Estado de México, Mexico;
2 Colegio de Postgraduados, Campus San Luis Potosí, Salinas de Hidalgo 78600, San Luis Potosí, Mexico