Abstract
The traditional milpa system, a polyculture originating in Mesoamerica, centers around maize (Zea mays L.), associated with pumpkin (Cucurbita sp.) and beans (Phaseolus vulgaris L.). The application of plant growth-promoting rhizobacteria (PGPR) under a milpa agrosystem has been little explored. In this study, a maize crop in a milpa system was fertilized with the PGPR Pseudomonas fluorescens UM270 during the 2021 and 2023 seasons, and various phytoparameters (plant height, root length, chlorophyll concentration, root dry weight and total plant dry weight), total production, and grain nutrition were evaluated. The results showed that UM270 improved chlorophyll concentration and increased plant height, root length, and dry weight in maize plants. Co-fertilization with UM270 and diammonium phosphate (DAP) significantly improved plant and corn cob weight compared to controls with single fertilizations in both the 2021 and 2023 seasons. Notably, corn production increased by more than 40% in the corn monoculture inoculated with UM270 compared to the uninoculated plants. The UM270 + DAP cofertilization in the monoculture was also increased by more than 50% in both cycles. When analyzing the nutritional content of the corn cob, nitrogen and phosphorus increased with the inoculation with UM270, while other elements, such as potassium and calcium, were higher in treatments co-inoculated with UM270 + DAP. Based on our research, this study is the first to report the milpa as a suitable model for bioinoculation with PGPR, demonstrating its potential to increase maize yield and benefit other associated crops.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
In the middle of the twentieth century, there was an increase in agricultural production and this exceeded the current increase in population. This transcendental change in agriculture was called “green revolution”, and represented a boost in the world’s most developed and later less developed nations [39, 48]. The main objective was to exponentially increase production through the use of hybrid seeds in large monocultures, planted with heavy machinery. To supply the nutrients required by the plants, different synthetic sources were applied as fertilizers [3, 35].
Maize has been one of the most impactful crops since the beginning of the Green Revolution, due to its nutritional value and high demand in the food, balanced feed, and pharmaceutical industries. In recent years, its use in bioethanol production has further cemented its status as one of the most important cereals worldwide [12]. However, its establishment as a monoculture has increased the presence and resistance of pests and diseases, and the soils are deteriorating and leading to increased soil toxicity due to the large amounts of agrochemicals that are supplied during the development of the crop [5, 26, 40, 50].
Today it is necessary to implement different crop systems that include the use of technologies that are friendly to the environment and counteract the effects caused since the beginning of the green revolution [10, 46]. One of the systems that has regained importance in recent years is the traditional “milpa” system, one of its characteristics is that they apply minimum or zero tillage, do not need irrigation systems, and are based on the establishment of maize cultivation associated with other crops such as beans and pumpkin. [2, 11], where maize serves as a support for the entangling of beans through the production of nodules, increases nitrogen fixation that benefits maize and pumpkin, and the latter provides soil protection by reducing the growth of weeds, which retains moisture, and through the production of allelopathic compounds (cucurbits) released by the leaching of the rain, they keep insects away. It has been one of the most used systems over the years in Mexico, and its importance encompasses cultural, economic, social, biological, and environmental aspects [29, 44]. Additionally, the traditional milpa model system is key to conserving soil biological diversity. Research indicates that the plants in this system have co-evolved with microbial biodiversity, enhancing soil fertility and ecosystem health [13, 49].
The main objective of the milpa system is self-consumption. Due to changes in culture and environmental conditions, productivity has declined. To ensure food security, research into new production methods to increase milpa productivity is essential. One option is the use of microorganisms that promote plant growth, which in recent years has proven effective as biofertilizers, biopesticides, and biofungicides [6, 32].
The interaction between microorganisms and plants depends on the species and age of the plant, soil characteristics, and climate. Plant growth-promoting rhizobacteria (PGPR) are among the plant growth-promoting microorganisms [33, 47, 51]. Mechanisms by which PGPRs act as bioinoculants include phosphate solubilization, nitrogen fixation, phytohormone production, and iron reduction. PGPR protect crops by producing antibiotics, siderophores, lytic enzymes, and volatile organic compounds, and by triggering systemic resistance in plants [27, 38, 52]. However, the survival and proliferation of these non-native microorganisms in the soil are necessary for them to exert their mechanisms on plants [4].
Some of the most studied PGPR genera in the maize rhizosphere include Burkholderia, Bacillus, Azotobacter, Streptomyces, Paenibacillus, Sphingobium, and Pseudomonas. Pseudomonads stand out for their effectiveness as plant growth promoters in maize plants, fungicides against diseases such as Rhizoctonia solani, biostimulants that mitigate water stress, and bioremediators of copper toxicity in maize crops [9, 12, 41, 45]. Pseudomonas fluorescens strain UM270 has various PGP mechanisms, such as the production of siderophores, antibiotics, volatiles, ACC deaminase activity, biofilm formation, and phosphate solubilization. It has been proven that it is an excellent promoter of plant growth in vitro in plants, including Solanum lycopersicum, Physalis ixocarpa, Medicago truncatula, and antagonists of fungal pathogens such as Botrytis cinerea and Fusarium oxysporum [20,21,22,23]. However, its beneficial effects in the field are unknown and under a milpa model. Therefore, the objective of this work was to evaluate the effect of P. fluorescens UM270 inoculation on maize growth, plant nutrition, and production in a milpa agrosystem during two growth cycles (2021 and 2023).
Materials and Methods
Experimental Site
The experiment was conducted in Santa Clara del Cobre, located within the municipality of Salvador Escalante, Michoacán, México (Fig. 1), at 19° 24′ 23″ North and 101° 38′ 24″ West, with an elevation of 2239 m. The climate prevalent in this area is classified as humid subtropical (Köppen climate classification, Cwa). Maize production in this region follows a seasonal pattern, with cultivation of native varieties, including white, black, yellow, and pink maize. Soil analyses were conducted prior to the experiments to determine their physicochemical properties (such pH, textural class, organic matter, elements like P, K, N, Mg, among others), with samples sent to INIFAP-Celaya (Mexico) for processing.
Biological Material
Zea mays L., Phaseolus vulgaris L., and Cucurbita sp. seeds utilized in this experiment were sourced locally from the municipality of Salvador Escalante, Michoacán, México where the study took place and were sourced from local producers. The bioinoculant used was the UM270 strain, which has been previously isolated and characterized [20].
Chemical Fertilizer
Diammonium phosphate (DAP) 18–46-0 was applied. It was purchased from a local company. It is a granular inorganic fertilizer and an excellent source of phosphorus (P) and nitrogen (N), which is highly soluble and dissolves in the soil solution, developing an alkaline pH around the granule.
Inoculum Preparation and Seed Treatments
Inoculum preparation was carried out as follows. Briefly, P. fluorescens strain UM270 was activated by inoculating a bacterial loop into a flask containing 500 mL of Nutrient Broth (BD BIOXON). The flask was then placed on a shaker set to 120 rpm and incubated at 28 °C for 24 h until it reached an optical density at 560–600 nm of 1. Subsequently, the supernatant was separated from the bacterial pellet, and the pellet was resuspended in a solution containing 0.1 mM magnesium sulfate. Finally, colony-forming units (CFUs) per mL were determined.
Seed preparation consisted of a superficial disinfection process involving washing with 70% ethanol, 5% sodium hypochlorite, and sterile distilled water. The seeds used for the treatments in the presence of the bacterial strain were inoculated at a concentration of approximately 1 × 103 − 1 × 104 CFU per seed.
Establishment of the Experiment in the Field
Maize planting was carried out in May during 2021 and 2023, with the entire cultivation stage ending in December of each year. Native maize seeds known as ‘white maize’ were used (Fig. 2). This variety is selected in the area for its characteristics of nixtamalization and tortilla flavor. After two weeks, guide beans and pumpkin were planted. One month after the maize planting, a second inoculation within the same treatment with the UM270 strain at a concentration of 1 × 108 UFC was carried out on the crops with the inoculated seeds, and after another month, a third inoculation was carried out at the same concentration.
The dose of DAP fertilizer applied to the selected crops was 200 kg/ha in the respective treatments. The maize crop was fertilized at the time of sowing; the second fertilization was carried out 1 month later by applying the same doses. Weed management was performed manually through weekly selective weeding, and vegetative development of the plants was monitored every 15 days. The maize harvest was carried out in December, and the bean and pumpkin were harvested when they reached physiological maturity and left to dry in the open air under shade.
The maize phenological scale in which the crop was evaluated included the following stages: emergence stage (VE), stages of development from the first to the nth leaf (V1 to V(n)), panicle stage (VT), reproductive stages that carry out the process from aqueous grain to hard grain (R1 to R5), and finally, the stage of physiological maturity (R6). The evaluated phytometric parameters were chlorophyll concentration, plant height, root length, plant dry weight, root dry weight, and maize ear weight.
Grain Yield and Chemical Composition Analysis
To determine grain yield, the number of maize ears per hectare was calculated by counting the number of ears in an area of 10 m2, and the number of grains per ear was determined by counting the number of rows in each ear and the number of grains per row. The final number of kernels per ear was calculated by multiplying the number of rows by the number of kernels in each row. Finally, the number of grains per hectare and the weight of a thousand grains were measured.
The chemical composition of the maize corn cob was analyzed after the harvest of the crop in December, and the samples obtained were sent to INIFAP-Celaya, Mexico for processing. The parameters evaluated were concentration of nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg), sulfur (S), iron (Fe), zinc (Zn), manganese (Mn), copper (Cu), and sodium (Na). The beans were harvested in September, as soon as they reached physiological maturity and were left to dry under shade in open air until they reached 14% humidity, after which they were weighed. Pumpkins were harvested between July and August as necessary. This crop was harvested twice a week in the form of flowers and green fruits until plant senescence. Afterward, the fruit was weighed, and the number of flowers was counted.
Experimental Design
The experiment was implemented over an area of 5600 m2. The experimental design was completely randomized with 10 treatments, where the three crops were planted at various densities. According to recommendations from the producers in the region, eight Maize plants m2 were planted. The composition of the polycultures was calculated as follows: planting a Maize plant is equivalent to 0.75 bean plants and 0.25 pumpkin plants.
The treatments evaluated were:
-
(1)
Zea mays L. (M)
-
(2)
Zea mays L. + Phaseolus vulgaris L. (M + P)
-
(3)
Zea mays L. + Cucurbita sp. (M + C)
-
(4)
Zea mays L., Phaseolus vulgaris L., Cucurbita sp. (TM)
-
(5)
Zea mays L. + diammonium phosphate (M + DAP)
-
(6)
Zea mays L. + UM270 (M + UM270)
-
(7)
Zea mays L. + UM270 + Phaseolus vulgaris L. (M + P + UM270)
-
(8)
Zea mays L. + UM270 + Cucurbita sp. (M + C + UM270)
-
(9)
Zea mays L. + UM270 + Phaseolus vulgaris L. + Cucurbita sp. (TM + UM270)
-
(10)
Zea mays L. + UM270 + diammonium phosphate (M + DAP + UM270)
Statistical Analysis
The data obtained were analyzed by analysis of variance, and the variables showing significant differences were further analyzed using Tukey’s test (p < 0.05) with STATISTICA 12 software. Additionally, correlation analysis and a heat map were performed using the METABOANALYST 6.0 platform. The data were subjected to t-test ANOVA with autoscale samples and a Pearson distance measure with a complete clustering method.
Results
Physicochemical Traits of the Soil
The physicochemical characteristics of the soil are presented in Table 1, where it can be observed that the pH levels are 5.42 and 6.2, organic matter was measured at 7.18 and 7.9 respectively, and phosphorus levels were low. Additionally, calcium, manganese, copper, magnesium, and zinc levels were found to be in a moderately low range. K and Fe levels were within the medium range. However, for the establishment of corn, soils with a pH range of 5.5–7.8 were required. Beyond these values, the crop may exhibit symptoms of excess micronutrient toxicity. Corn’s adaptability to various soil types contributed to successful cultivation in the conditions described in this study (cycles 2021 and 2023).
Maize Growth Promotion by Biofertilization with Strain UM270
During both corn crop cycles, different parameters were evaluated, such as plant height, root length, chlorophyll concentration (SDAP units), root dry weight, total plant dry weight and corn cob weight (Suppl. Table 1 and Figs. 3 and 4). In general, all treatments under the different milpa systems, with and without inoculum, showed an increase in chlorophyll concentration compared to the corn monoculture control treatment (without inoculum). The monoculture treatments fertilized with DAP, the Mesoamerican triad model (TM), and the corn-squash coculture increased the chlorophyll concentration by more than 50% during both cycles (Fig. 3A-A2), where significant differences were found between treatments (p < 0.05).
The height of the plants for both cycles increased in the treatments inoculated with the UM270 strain, highlighting the treatments of monoculture fertilized with DAP, TM, and corn-squash co-culture, which increased by more than 26% and by up to 56% during both cycles (Fig. 3B-B2), and significant differences were found between the treatments (p < 0.05). Similarly, root length increased in treatments inoculated with strain UM270, with an increase of more than 27% in each cycle (Fig. 3C-C2).
The dry weight of the plant with respect to the TM increased by more than 100% in the treatments inoculated with the UM270 strain, including the corn-squash co-culture, TM, and corn monoculture fertilized with DAP. for both cycles (Fig. 4D-D2). However, regardless of the type of milpa model with or without inoculum or DAP fertilization, there were significant differences (p < 0.05), and the dry weight of the plant increased with respect to the corn control treatment for both cycles.
There were no significant differences in the root dry weight after inoculation with strain UM270 (Fig. 4E-E2). Curiously, the dry weight of the corn cob presented significantly different (p < 0.05), highlighting the treatments inoculated with UM270, which included corn monoculture, corn-bean co-culture, and fertilized corn monoculture were found. with DAP, which increased their weight by more than 40% during the 2021 cycle. In the 2023 cycle, treatments inoculated with UM270 included corn monocultures with and without DAP; on the other hand, the corn monoculture fertilized with DAP without inoculum increased by 56%, 42%, and 25%, respectively (Fig. 4F-F2).
Based on the correlation analysis between treatments, it can be determined that during the 2021 cycle, the corn-bean co-culture and the corn monoculture, both inoculated with UM270, were positively correlated. In the same way the corn monoculture fertilized with DAP and the TM, both inoculated with UM270, were positively correlated (Fig. 5).
During the 2023 cycle, the TM, corn monoculture, and fertilized DAP were positively correlated, and both treatments were inoculated with UM270 (Fig. 5).
The results of the heat map that considers the six phytometric parameters show that the treatment of the corn monoculture inoculated with UM270 and fertilized with DAP presented the highest values of all the parameters in both cycles. The treatments where UM270 biofertilization was applied increased the values of the parameters depending on the type of model evaluated (Fig. 6). Based on the results of the principal component analysis, it can be determined that the first axis of the PCA explains 30.5 and 30% of the variation and the second 16.6 and 16.2% for the 2021 and 2023 cycles, respectively. During the first cycle, they grouped the height of the plant, root growth, and chlorophyll concentration during the second cycle, only the dry weight of the plant was not grouped with the other phytometric parameters (Fig. 7).
Maize Yield
The increase in maize yield was evaluated at the end of the harvest in both cycles. During the first cycle, the treatments that showed an increase in maize yield were those inoculated with UM270, maize in co-culture with bean plants, and maize fertilized with DAP by 41.96%, 28.28%, and 58.13%, respectively, in comparison with the maize plants controls (uninoculated) (Table 2). During the second cycle, the corn monocultures inoculated with the UM270 strain and the co-fertilized one (UM270-DAP) were the ones that presented the greatest increase in production by 42.03% and 56.59%, respectively (Table 2). This result indicates that biofertilization with P. fluorescens UM270 has great potential to increase maize crop yield.
Phaseolus vulgaris L. and Cucurbita sp. Yield
Bean yield was determined under the milpa model; the interaction, given in the corn-bean co-culture inoculated with the UM270 strain increased by 12.5% and 13.32% in the 2021 and 2023 cycles, respectively, compared to the corn-bean co-culture without inoculum (Table 3). Biofertilization with the UM270 strain increased pumpkin yield, indicating the treatment of the TM with an increase of 30.27% and 20.90% in the 2021 and 2023 cycles, respectively, compared to the corn-squash co-culture without inoculum (Table 4).
Nutritional Composition of the Maize Corn Cob
The nutritional composition of maize grains is presented as the mean of the two seasons (Table 5). One of the elements analyzed was the concentration of total N, which presented significant differences (p > 0.05) between treatments. Notably, maize co-cultured with pumpkin and inoculated with the UM270 strain showed an 18.8% increase in nitrogen concentration compared to the maize control treatment and the traditional TM system. The same behavior was observed, but with an increase of 14.87%.
P is another of the treatments that was evaluated, and in this case the treatments of the TM, that of maize fertilized with DAP, and that of maize in co-culture with beans and inoculated with the bacterial strain, stood out for presenting the highest concentration, increasing by 52.94%, 43.38%, and 45.58% compared to the maize control treatment. In this case, we determined that even without inoculation with the bacterial strain, the TM system could increase P concentration.
K increased in maize treatments inoculated with strain UM270 and in maize inoculated and fertilized with DAP, showing an increase of 20.47% and 16.5%, respectively, compared to the control treatment of maize alone. Ca presented its highest concentration in the maize treatment inoculated with the strain and added with DAP fertilizer, increasing by 56% compared to the maize control treatment. Mg, Zn, Mg, Cu, and Na did not show significant differences between the treatments. S had the highest concentration in the TM treatment, increasing by 41.09%. Fe presented its highest concentration in the maize treatment co-cultivated with beans, where it increased by 509.48% compared with the maize control treatment.
The correlation analysis between the different milpa models in the nutritional content of the corn cob, the treatments without TM inoculum, corn, corn-bean co-culture, and corn monoculture fertilized with DAP were positively correlated, whereas the treatments inoculated with the TM, strain UM270, and corn-bean co-culture were positively correlated (Fig. 8A). In the heat map based on the elements in the corn cob, it was observed that Fe had the highest values in the control treatment of the corn monoculture, even though there was no increase in the values given by the inoculation of the UM270 strain, which can be determined depending on the type of system, and the different parameters evaluated increased in different ways (Fig. 8B).
Discussion
Corn is one of the most important cereals worldwide, and its nutritional value makes it key to food security including its cultivation via the Milpa model, which is key to generating a variety of agricultural products in a small space and stimulating soil biodiversity [18, 19, 44]. No agrochemicals were applied in the milpa; therefore, its production was highly eco-friendly. However, the threat of pathogens and their cultivation in nutrient-poor soils can reduce their efficient production. Therefore, it is necessary to use and apply biological fertilizers and fungicides to naturally restore agroecosystems [16, 17, 42].
The results of this study demonstrate that the application of a biofertilizer based on the PGPR P. fluorescens UM270 under the Milpa model (TM or Mesoamerican Triad), among other treatments, including corn-pumpkin co-inoculation, managed to increase all analyzed parameters (e.g., concentration of chlorophyll, biomass, root length, corn plant height, and corn cob weight) compared to the control treatment of corn monoculture without bacterial inoculum. Similar beneficial effects have been observed in corn crops under a monoculture system with the application of biocapsules formulated with chitosan and PS2 and PS10 (Bacillus spp.) [7]. The effect of P. fluorescens UM270 on maize plants also increased the chlorophyll concentration, regardless of the type of Milpa system treatment established in the field.
Plant height growth increased only in the treatments in which the UM270 strain was inoculated. Similarly, root growth increased only in the treatments inoculated with the UM270 strain, which indicated that the plant-microorganism interaction promoted the growth of maize plants roots, regardless of which Milpa model was established. The dry weight of the plant increased only in the treatments inoculated with the UM270 strain in corn-squash, TM and corn monoculture fertilized with DAP, with the results of this parameter it can be determined that depending on the established Milpa system, the weight increases of plant height by the end of the cycle. Likewise, previous studies have shown that in maize crops under a monoculture system by inoculating consortia of plant growth-promoting bacterial strains such as Bacillus and Pseudomonas, they increase the growth of maize plants compared to the treatments where only an inoculant was applied [37]. Strains like Pseudomonas geniculata, Pseudomonas psychrotolerans, Bacillus circulans, Pseudomonas putida, and Pseudomonas pseudoalcaligenes, increase the growth of corn plants through various mechanisms under abiotic conditions both in vitro and in the field; however, it is worth mentioning that the majority of crops where bioinoculants are applied are under the establishment of hybrid seeds in monoculture systems and through irrigation systems, which contrasts with the system established in this work, where native seeds were used in a traditional and agro-sustainable system [8, 14, 28, 43, 45, 54].
The correlations between treatments during both cycles allowed to determine that the treatments with the UM270 bioinoculum correlate with each other, as is the case of the corn monoculture with the corn-bean co-culture. On the other hand, the monoculture fertilized with DAP was correlated with the TM. The heat map shows that the highest parameters during both cycles are presented in the same way in the treatments with the inoculum. This indicated that the strain’s effect on corn growth depends on the interaction between plants, and plants with microorganisms.
One of the most important parameters for field crops is the dry weight of the cob, which directly influences grain yield. In the TM, corn production increased by 12.56 and 5.91% compared with the control treatment during the 2021 and 2023 cycles, respectively. By adding the UM270 inoculum to the corn monoculture, the production increased by 41.96 and 42.03 for 2021 and 2023 cycles, respectively. respectively. Similarly, in the co-cultivation of corn and beans with the UM270 inoculum, it was determined that there was an increase in production of 28.28 and 23.56 during both cycles.
Previous reports have shown that inoculation with PGPR such as Sinorhizobium sp. A15, Bacillus sp. A28 and Sphingomonas spp. A55, isolated from the maize rhizosphere in the same area and inoculated separately, increased maize growth and grain yield between 22 and 29% [8]. The increase in corn yield is determined due to abiotic and biotic factors, but it has been proven that through the application of PGPR, corn yield increases even under stress conditions in the field [15, 34, 41]. In addition, promoting corn yield through the establishment of multispecies cropping increases productivity per unit area and, in turn, reduces the number of weeds and pathogens present [36].
Regarding bean production, it can be observed that the corn-bean interaction and the UM270 bioinoculant increased bean production by 13.32%, compared to the corn-bean co-culturepl. For its part, the pumpkin yield increased in the biofertilized treatments by 30.29% (2021 cycle) and 20.90% (2023 cycle). In previous field studies, the effect of plant promotion in wheat crops was determined due to the effect of bioinoculation of the B. subtilis strain [25]. Furthermore, under controlled conditions, the benefits of plant–plant interactions have been observed in intercrops such as corn-bean, where nodulation in broad bean was stimulated. In Cajanus cajan-Zea mays co-culture, an increase in the production of corn proteins and in the corn-bean co-culture, the induction of genes for nodulation in bean plants was determined, and in the case of maize genes for the degradation of mucilage and feluric acid, among other compounds [1, 30, 53].
The chemical composition of the grain provides a basic parameter for determining its nutritional quality [31]. Calcium, phosphorus, potassium, and nitrogen are among the elements with the greatest nutritional importance. Here, an increase was observed in certain elements, such as N and P, whereas K and Ca improved in treatments with UM270 + DAP. In a recently published study, Pereira et al. (2020) observed an increase in N and P in maize plants when inoculating with two PGPR, Cupriavidus necator 1C2 and P. fluorescens S3X. Although the nutritional grade of the corn grain was not analyzed, only that of the plants under conditions of water deficit was analyzed. In our study, it is possible that the UM270 strain, which is a phosphate solubilizer, increases its nutrient use efficiency, shoot biomass, and concentration in the grain cob. The nutritional value of seeds enhanced by bacterial inoculation has also been tested in other crops, such as faba beans [55] and wheat [24], among others.
Conclusions
Incorporating biofertilizers, such as the P. fluorescens strain UM270, into Milpa models not only enhances plant growth promoting parameters and improves grain nutrition by providing specific elements (e.g. K and P), but also boosts overall crop yield. This approach offers significant economic and agroecological benefits to local farmers by providing an alternative to reducing dependency on synthetic fertilizers and leading to more sustainable agricultural practices.
References
Aguirre-noyola JL, Rosenblueth M, Santiago-martínez MG (2021) Transcriptomic responses of rhizobium phaseoli to root exudates reflect its capacity to colonize maize and common bean in an intercropping system. Front Microbiol. https://doi.org/10.3389/fmicb.2021.740818
Álvarez-Buylla ER, Carreón-García A, San Vicente-Tello A (2011) Haciendo milpa, Primera ed. México
Álvarez-Buylla E-R, Piñeyro Nelson A (2013) El maíz en peligro ante los transgénicos: un análisis integral sobre el caso de México
Barajas LNA, Noya YEN, Guido MLL (2021) Impact of a bacterial consortium on the soil bacterial community structure and maize (Zea mays L .) cultivation. Sci Rep. https://doi.org/10.1038/s41598-021-92517-0
Camacho EC (2017) “Revolución Verde” Agricultura y suelos, aportes y controversias. Rev la Carrera Ing Agronómica - UMSA 3:844–859
Castillo-López E, Marín-Collí EE, López-Tolentino G et al (2020) Perspectivas del sistema milpa en Yucatán. Bioagrociencias 14(2):13–22
Chaudhary P, Khati P, Gangola S et al (2021) Impact of nanochitosan and Bacillus spp. on health, productivity and defence response in Zea mays under field condition. 3 Biotech 11:1–11. https://doi.org/10.1007/s13205-021-02790-z
Chen L, Hao Z, Li K et al (2021) Effectsof growth-promoting rhizobacteria on maize growth and rhizosphere microbial community under conservation tillage in Northeast China. Microb Biotechnol 14:535–550. https://doi.org/10.1111/1751-7915.13693
Chu TN, Van BL, Hoang MTT (2020) Pseudomonas PS01 isolated from maize rhizosphere alters root system architecture and promotes plant growth. Microorganisms 8:1–23. https://doi.org/10.3390/microorganisms8040471
Dellepiane AV, Sánchez Vallduví GE, Tamagno LN (2015) Sustainability of monoculture and intercropping Helianthus annuus L. (sunflower) with Trifolium pratense, Trifolium repens or Lotus corniculatus in La Plata, Argentina. Evaluation using indicators. / Sustentabilidad del monocultivo e intercultivo de Helia. Rev la Fac Agron (La Plata) 114:85–94
Ebel R, Pozas J, Soria F, Cruz J (2017) Manejo orgánico de la milpa: rendimiento de maíz, frijol y calabaza en monocultivo y policultivo Organic milpa: yields of maize, beans, and squash in mono-and polycropping systems. Terra Latinoam 35:149–160
Edoghogho-Imade E, Olubukola-Oluranti B (2021) Biotechnological utilization: the role of Zea mays rhizospheric bacteria in ecosystem sustainability. Appl Microbiol Biotechnol 105:4487–4500. https://doi.org/10.1007/s00253-021-11351-6
FAO (2007) Guía Metodológica La milpa del siglo XXI. Colección Guías Metod del Programa Espec para la Segur Aliment Guatemala 1:66
Gao C, El-Sawah AM, Ismail Ali DF et al (2020) The integration of bio and organic fertilizers improve plant growth, grain yield, quality and metabolism of hybrid maize (Zea mays L.). Agronomy 10:1–25. https://doi.org/10.3390/agronomy10030319
García González MT, Rojas Rojas JA, Castellanos González L et al (2013) Policultivos para el manejo de Spodoptera frugiperda ( J. E. Smith ) en maíz en un agroecosistema pre montañoso. Rev Cent Agrícola 40:41–45
Gastélum G, Rocha J (2020) La milpa como modelo para el estudio de la microbiodiversidad e interacciones planta-bacteria. TIP Rev Espec en Ciencias Químico-Biológicas 23:1–13. https://doi.org/10.22201/fesz.23958723e.2020.0.254
Gómez Betancur LM, Márquez Girón SM, Restrepo Betancur LF (2018) La milpa como alternativa de conversión agroecológica de sistemas agrícolas convencionales de frijol (Phaseolus vulgaris), en el municipio El Carmen de Viboral, Colombia. Idesia (Chile) 36:123–131. https://doi.org/10.4067/s0718-34292018000100123
Gómez-Martínez E, Álvarez-Buylla RE, Carreón García A et al (2020) La milpa: sistema de resiliencia campesina. Estudio de dos organizaciones campesinas en Chiapas. Rev Geogr Agrícola 12:1–17. https://doi.org/10.19136/era.a7n1.2244
Hernández Galindo HS, Alanís García E, Omaña Covarrubias A (2022) La Dieta de La Milpa: como una alternativa en salud pública en el Valle del Mezquital Hidalguense, después de la pandemia de la covid-19. Educ y Salud Boletín Científico Inst Ciencias la Salud Univ Autónoma del Estado Hidalgo 10:7–20. https://doi.org/10.29057/icsa.v10i20.8362
Hernández-León R, Rojas-Solís D, Contreras-Pérez M et al (2015) Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol Control 81:83–92. https://doi.org/10.1016/j.biocontrol.2014.11.011
Hernández-Salmerón JE, Hernández-Flores BR, del Rocha-Granados MC et al (2018) Hongos fitopatógenos modulan la expresión de los genes antimicrobianos phlD y hcnC de la rizobacteria Pseudomonas fluorescens UM270. Biotecnia 20:110–116. https://doi.org/10.18633/biotecnia.v20i2.609
Hernández-Salmerón JE, Hernández-León R, Orozco-Mosqueda MDC et al (2016) Draft genome sequence of the biocontrol and plant growth-promoting rhizobacterium pseudomonas fluorescens strain UM270. Stand Genomic Sci. https://doi.org/10.1186/s40793-015-0123-9
Hernández-Salmerón JE, Moreno-Hagelsieb G, Santoyo G (2017) Genome comparison of pseudomonas fluorescens UM270 with related fluorescent strains unveils genes involved in rhizosphere competence and colonization. J Genomics 5:91–98. https://doi.org/10.7150/jgen.21588
Hussain A, Ahmad M, Nafees M et al (2020) Plant-growth-promoting Bacillus and Paenibacillus species improve the nutritional status of Triticum aestivum L. PLoS ONE 15:1–14. https://doi.org/10.1371/journal.pone.0241130
Ibarra-villarreal AL, Villarreal-delgado MF, Isela F et al (2023) Effect of a native bacterial consortium on growth, yield, and grain quality of durum wheat (Triticum turgidum L . subsp. durum ) under different nitrogen rates in the Yaqui Valley. Mexico Plant Signal Behav. https://doi.org/10.1080/15592324.2023.2219837
Jasso-Miranda M, Soria-Ruiz J, Antonio-Némiga X (2022) Pérdida de superficies cultivadas de maíz de temporal por efecto de heladas en el valle de Toluca. Rev Mex Ciencias Agrícolas 13:207–222. https://doi.org/10.29312/remexca.v13i2.2587
Keswani C, Sarma BK, Singh HB (2016) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia
Kubi HAA, Khan MA, Adhikari A et al (2021) Silicon and plant growth-promoting rhizobacteria pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture. https://doi.org/10.3390/agriculture11030272
Ku-Pech EM, Mijangos-Cortés JO, Andueza-Noh RH et al (2019) Estrategias de manejo de la milpa maya en Xoy, Peto, Yucatán. Ecosistemas y Recur Agropecu 7:1–8. https://doi.org/10.19136/era.a7n1.2244
Li B, Li Y, Wu H et al (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1523580113
Martínez-Cruz M, Ortiz-Pérez R, Raigón MD (2018) Contenido De Fósforo, Potasio, Zinc, Hierro, Sodio, Calcio Y Magnesio, Análisis De Su Variabilidad En Accesiones Cubanas De Maíz. Cultiv Trop 38:92–101
Martínez-Pérez DY, Sánchez-Escudero J, de las Rodríguez-Mendoza MN, Astier-Calderón M (2020) Sustentabilidad de agroecosistemas de milpa en La Trinidad Ixtlán. Oaxaca. Rev la Fac Agron 119:048
Molina-Romero D, del Bustillos-Cristales M, Rodríguez-Andrade O et al (2015) Mecanismos de fitoestimulación por rizobacterias, aislamientos en América y potencial biotecnológico. Biológicas 17:24–34
Mubeen M, Bano A, Ali B et al (2021) Effect of plant growth promoting bacteria and drought on spring maize (Zea mays l.). Pakistan J Bot 53:731–739. https://doi.org/10.30848/PJB2021-2(38)
Murillo-Cuevas F, Adame-García J, Cabrera-Mireles H, et al (2020) Edaphic fauna and insects associated to weeds in persian lemon, monoculture and intercropping. Ecosistemas y Recur Agropecu https://doi.org/10.19136/era.a7n2.2508
Nunez L, Lucati L, Pietrarelli L (2021) Evaluación del cultivo agroecológico de maíz, poroto y zapallito en policultivo. Rev difusión socio-tecnológica Nexo-Agropecuario 9:96–104
Olanrewaju O-S, Babalola O-O (2019) Bacterial consortium for improved maize (Zea mays L .) Production. Microorganisms 7:19. https://doi.org/10.3390/microorganisms711051
Pereira SIA, Abreu D, Moreira H et al (2020) Plant growth-promoting Rhizobacteria (PGPR) improve the growth and nutrient use efficiency in maize (Zea mays L.) under water deficit conditions. Heliyon. https://doi.org/10.1016/j.heliyon.2020.e05106
Pichardo González B (2006) La revolucion verde en México. Agraria 40–68
Prasad R, Gunn SK, Rotz CA et al (2018) Projected climate and agronomic implications for corn production in the Northeastern United States. PLoS ONE 13:1–20. https://doi.org/10.1371/journal.pone.0198623
Rana A, Sahgal M, Kumar P (2019) Biocontrol prospects of pseudomonas fluorescens AS15 against banded leaf and sheath blight disease of maize under field condition in conducive soil. Natl Acad Sci Lett. https://doi.org/10.1007/s40009-018-0772-5
Regalado-López J, Castellanos-Alanis A, Pérez-Ramírez N, et al (2020) Modelo asociativo y de organización para transferir la tecnología milpa intercalada en árboles frutales (MIAF). Estudios Sociales Revista de Alimentación Contemporánea y Desarrollo Regional https://doi.org/10.24836/es.v30i56.983
Rezazadeh S, Ilkaee M, Aghayari F et al (2019) The physiological and biochemical responses of directly seeded and transplanted maize (Zea mays L.) supplied with plant growth-promoting Rhizobacteria (PGPR) under water stress. Iran J Plant Physiol 10:3009–3021
Rodríguez A, Arias de Reyna L (2014) La Milpa y el Maizal: Retos al Desarrollo Rural en México y Perú. Etnobiología 12:76–89
Sah S, Singh N, Singh R (2017) Iron acquisition in maize (Zea mays L.) using Pseudomonas siderophore. 3 Biotech 7:1–7. https://doi.org/10.1007/s13205-017-0772-z
de Salazar Barrientos LL, MagañaMagañaAguilarJiménez MÁAN et al (2016) Ecosistemas y recursos agropecuarios. Ecosistemas y Recur Agropecu 3:391–400
dos Santos ML, Berlitz DL, Wiest SLF et al (2018) Benefits associated with the interaction of endophytic bacteria and plants. Brazilian Arch Biol Technol 61:1–11. https://doi.org/10.1590/1678-4324-2018160431
Sobalvarro H, Karina K, Lina A, et al (2018) La revolución verde Green revolution. 1040–1046
Torres-Calderón S, Huaraca-Férnandez J, Peso D-L, Calderón R-C (2018) Asociación de cultivos, maíz y leguminosas para la conservación de la fertilidad del suelo. Rev Investig Ciencia, Tecnol y Desarro 4:15–22. https://doi.org/10.4067/s0718-34292018000100123
Ureta C, González EJ, Espinosa A et al (2020) Maize yield in Mexico under climate change. Agric Syst 177:102697. https://doi.org/10.1016/j.agsy.2019.102697
Vandana UK, Singha B, Gulzar ABM, Mazumder PB (2020) Molecular mechanisms in plant growth promoting bacteria (PGPR) to resist environmental stress in plants. In: Vandana UK, Singha B, Gulzar ABM, Mazumder PB (eds) Molecular aspects of plant beneficial microbes in agriculture. Elsevier, pp 221–233
Vejan P, Khadiran T, Abdullah R et al (2019) Encapsulation of plant growth promoting Rhizobacteria—prospects and potential in agricultural sector: a review. J Plant Nutr 42:2600–2623. https://doi.org/10.1080/01904167.2019.1659330
Vora SM, Ankati S, Patole C et al (2021) Alterations of primary metabolites in root exudates of intercropped Cajanus cajan—Zea mays modulate the adaptation and proteome of Ensifer (Sinorhizobium) fredii NGR234. Microb Ecol. https://doi.org/10.1007/s00248-021-01818-4
Yasmin H, Rashid U, Hassan MN et al (2021) Volatile organic compounds produced by Pseudomonas pseudoalcaligenes alleviated drought stress by modulating defense system in maize (Zea mays L.). Physiol Plant 172:896–911. https://doi.org/10.1111/ppl.13304
Youseif SH, Fayrouz HAEM, Saleh SA (2017) Improvement of faba bean yield using rhizobium/agrobacterium inoculant in low-fertility sandy soil. Agronomy 7:1–12. https://doi.org/10.3390/agronomy7010002
Acknowledgements
This work was supported by the ICTI-Michoacán (Project: ICTI-PICIR23-105), CONAHCYT-México [Proposal: A1-S-15956], and CIC-UMSNH (Project: 2023–2024). Blanca Sánchez-Rojas received a PhD scholarship from CONAHCYT-México. The technical assistance of Jose Luis Avila Oviedo is also acknowledged.
Author information
Authors and Affiliations
Contributions
BRS: investigation, methodology and formal analysis. MCOM and GS: Conceptualization, resources, supervision, writing, review, and editing. All the authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Rojas-Sánchez, B., Orozco-Mosqueda, M.d.C. & Santoyo, G. Field Assessment of a Plant Growth-Promoting Pseudomonas on Phytometric, Nutrient, and Yield Components of Maize in a Milpa Agrosystem. Agric Res (2024). https://doi.org/10.1007/s40003-024-00756-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s40003-024-00756-0