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Article

Biochemical and Plant Growth Response of the Common Bean to Bioinput Application Under a Drought Stress Period

by
Bruna Arruda
1,
Breno Miranda Bagagi
2,
Nelson Borges de Freitas Junior
2,
Wilfrand Ferney Bejarano Herrera
3,
German Andrés Estrada-Bonilla
4,
Willian Aparecido Leoti Zanetti
2,
Ana Laura Silva Silvério
2 and
Fernando Ferrari Putti
2,*
1
Agricultural Sciences Department, Agronomy Engineering Program, 222 Bogotá Campus, University of Applied and Environmental Sciences (UDCA), Bogotá 111166, Colombia
2
Biosystems Engineering Department, Faculty of Science and Engineering, Tupã campus, São Paulo State University (UNESP), Tupã 17602-496, Brazil
3
Colombian Corporation for Agricultural Research (AGROSAVIA), Obonuco 520038, Colombia
4
Colombian Corporation for Agricultural Research (AGROSAVIA), Tibaitatá 250047, Colombia
*
Author to whom correspondence should be addressed.
Stresses 2025, 5(1), 17; https://doi.org/10.3390/stresses5010017
Submission received: 22 October 2024 / Revised: 24 December 2024 / Accepted: 7 January 2025 / Published: 20 February 2025
(This article belongs to the Collection Feature Papers in Plant and Photoautotrophic Stresses)
Browse Figures
Versions Notes

Abstract

:
The common bean (Phaseolus vulgaris L.) is a global staple, but to guarantee its provision, the crop water supply must be adequate, and bioinput application can benefit plants under drought. The objective was to evaluate the common bean’s response to bioinput application when it was cropped in soils with different water holding capacities submitted to a drought period. The greenhouse experiment used sandy loam and clayey soils. Seeds were sown, and 10 days after emergence (DAE), the treatments were applied: (i) no bioinput application or (ii) bioinput application (Priestia aryabhattai, re-applied at 46 DAE). The first plant growth evaluation was performed at 40 DAE. The irrigation maintained the crops’ needs until the beginning of flowering for all the treatments, when the irrigation was differentiated (for 10 days): (i) maintenance of irrigation or (ii) a drought period. A biochemical analysis was performed of superoxide dismutase activity [SOD], hydrogen peroxide [H2O2], peroxidase activity [POD], and malonaldehyde [MDA] production at 52 DAE. At 57 DAE, the second plant growth evaluation was performed, and the irrigation differentiation ended. Grain harvest followed physiological maturation. Priestia aryabhattai mitigated the drought stress in the common bean cropped in sandy soil by reducing the SOD, H2O2, and MDA production in comparison to no bioinput application. When it was cultivated in the clayey soil, the water availability was maintained for longer, reducing the plant’s dependency on bacteria for stress mitigation.

1. Introduction

In recent years, drought periods have been observed more frequently in different regions of the planet, caused largely by the effects of climate change, which alter the hydrogeological cycle as a whole [1]. Such drought periods negatively affect agricultural production since the full development of plants depends on an adequate supply of water during the different phenological stages, especially during germination and the productive stages of crops, such as flowering [2,3]. A stress condition, such as drought, triggers a sequence of plant responses through the activation of the antioxidative system. However, the activation of the antioxidative system represents an energy expenditure for the plants, reducing their productivity potential. This is especially seen in crops, such as the common bean (Phaseolus vulgaris L.), that are sensitive to water deficits, and specifically require an adequate water supply to avoid stress conditions. The common bean is an important dietary component of a large part of the human population, mainly in developing countries, due to its high protein value with a low cost to consumers. Therefore, common bean production must be guaranteed to avoid food security risks [4].
In this sense, many factors must be considered to provide an adequate water supply to crops. Beyond the rainfall distribution itself, the water availability for crops depends on many other factors, and an understanding of each factor will lead to adequate management of each crop. Once precipitation occurs, the soil may be an important water storage element. However, the water storage capacity of the wide variety of soils spread across the world will depend on their intrinsic features, such as their soil texture. Soil texture refers to the distribution of the soil particles, which are classified according to their diameter: sand (between 2.000 and 0.053 mm), silt (between 0.053 and 0.002 mm), and clay (<0.002 mm). The predominance of a given soil particle class will determine the soil’s porosity, which represents the empty spaces between the soil particles. The soil’s pores may then be occupied by the soil atmosphere or water (soil solution). Soils with predominantly sandy particles present have the majority of their volume being occupied by solids, resulting in a reduction in porosity and so a reduction in the soil’s storage capacity for air and water. On the other hand, soils with predominantly smaller particles in the soil’s volume, such as clay, have more available space between particles, presenting a higher macro- and microporosity and resulting in a strong water retention capacity. Therefore, in general, sandy soils present a low water retention capacity, which favors water losses through leaching, in comparison to silty and clayey soils [5].
When the water supply is not enough to fulfill a crop’s needs, different strategies must be used to guarantee crop production. A solution for the supply of water to various crops, which has been used for many years in areas with deficits in their water distribution, is the implementation of irrigation systems. However, such systems require a high initial investment and availability of quality water. Therefore, in general, irrigation systems are less accessible to small and medium-sized farmers (in family and subsistence agriculture), who represent a high percentage of the common bean farmers in Brazil. An alternative that has been evaluated in recent years is the use of bioinputs, which are biological products applied to crops in order to introduce organisms that have the capacity to provide benefits to plants, such as plant-growth-promoting bacteria (PGPB), whether through growth promotion mechanisms or plant protection, among other mechanisms [6]. The use of microbial applications to manage drought stress is potentially cost-effective and is considered a more eco-friendly approach than other methods [7]. In this sense, previous studies show that some bacteria from the Bacillus genus, with the potential of Bacillus aryabhattai highlighted, currently named Priestia aryabhattai [8], have the potential to mitigate the damage caused by periods of drought in crops such as maize (Zea mays L.) [9,10,11], guinea grass (Megathyrsus maximus Jacq.) [12], pigeon pea (Cajanus cajan L.) [13], and soybean (Glycine max L.) [14]. The Bacillus genus has different regulatory strategies in plants, such as increasing the root biomass and relative water content and decreasing the levels of osmolytes, proline production, glycine-betaine, and antioxidants under drought stress [15]. Although the positive effects of the use of bioinputs on different crops under water deficit conditions have been verified, little is known about the biochemical mechanisms involved in these processes. Considering that an understanding of such mechanisms can facilitate their maximization, their identification is of fundamental importance so their use can be targeted and increased efficiently.
The hypotheses of this study were as follows: (i) the soil texture will influence the water availability to the common bean and hence will affect the response to the bioinput application under a drought stress condition; (ii) the bioinput application can help the common bean in the oxidative response during drought stress, reducing the plant’s energetic expense, allowing the plant to invest resources in productive plant functions.
The objective was to identify the potential biochemical mechanisms, as well as plant growth parameters, related to aspects of drought stress response with Priestia aryabhattai application in common bean subjected to a water deficit period.

2. Results

2.1. Common Bean Vegetative Response of Bioinput Application, Before a Drought Stress Period

At 30 days after bioinput application, during the vegetative stage, no significant differences were observed for plant fresh biomass accumulation (leaf, stem, and root), root dry biomass, root water content, and root volume for both soils tested and in a comparison of the no-bioinput-application treatment with the bioinput application treatment (Figure 1). A similar trend was observed for root length per plant, root surface area per plant, and root average diameter per plant (Table S2).

2.2. Common Bean Biochemical Response of Bioinput Application, During a Drought Stress Period

At 52 DAE, 5 days after the irrigation differentiation, the biochemical response in the sandy loam soil showed changes in the superoxide dismutase [SOD] activity. Plants submitted to a drought stress period without bioinput application (NBA) showed the highest SOD activity, while the application of bioinput (WBA) presented the lowest SOD activity, under drought stress (Figure 2a). When common bean plants were cropped in the clayey soil, no difference in SOD activity was observed for the treatments (Figure 2b).
Regarding the peroxide [H2O2] accumulation, common bean cultivated in the sandy loam soil, when submitted to drought stress conditions, showed the lowest H2O2 accumulation when bioinput was applied (Figure 2c). Conversely, common bean grown in clayey soil displayed no significant differences for the treatments tested here (Figure 2d). When common bean was cultivated in sandy loam soil and submitted to drought stress conditions, the bioinput application reduced the peroxidase activity [POD] (Figure 2e). In the cultivation in the clayey soil under drought stress conditions, the bioinput application did not show any difference in POD activity for the cultivation of common bean in comparison to the treatment without bioinput application (Figure 2f).
Finally, regarding malonaldehyde [MDA] production, growing in the sandy loam soil, stress conditions with bioinput application reduced the MDA accumulation, whereas treatment under drought stress and no bioinput application showed the highest MDA value (Figure 3a). For clayey soil, the bioinput application reduced the MDA production, for both conditions, with and without a stress period, in comparison to the treatment without bioinput application (Figure 3b).

2.3. Common Bean Plant Growth Response of Bioinput Application, at the End of a Drought Stress Period

At 57 DAE, 10 days after irrigation differentiation, common bean, when cultivated in the sandy loam soil and submitted to drought stress and no bioinput application, showed the lowest leaf fresh biomass production. Under this condition, bioinput application slightly reduced the root fresh biomass and slightly increased the leaf fresh biomass production (Figure 4a). When common bean was cultivated in the sandy loam soil, but without the drought stress period, in general, a higher fresh biomass production was observed, in comparison to the condition with the drought stress period, where the no-bioinput-application treatment barely increased the root fresh biomass, and the bioinput application, in general, increased the shoot fresh biomass, leaf and steam (Figure 4a). Regarding the reproductive structures, no differences for the flower fresh biomass were observed, but differences were observed for legume fresh biomass accumulation (Figure 4). When common bean was cultivated in the sandy loam soil, under stress conditions and with no bioinput application, it showed the highest legume fresh biomass. On the other hand, the lowest legume biomass was observed under bioinput application under drought stress (Figure 4a). Regarding root fractionation, no differences were observed for the dry biomass accumulation, but an effect of the treatments was observed for root water content and root volume (Figure 4c,e). Under drought conditions, the bioinput application reduced the root water content and the root volume in comparison to no bioinput application. Under the no-drought condition, no differences were observed in root water content between the bioinput application and no-bioinput-application treatments, and a slight increment was observed in the root volume for the bioinput application treatment in comparison to no bioinput application (Figure 4e). The same trend was observed for root length per plant, root surface area per plant, and root average diameter per plant (Table S4).
When the clayey soil was used for the common bean cultivation, no differences for stem and root fresh biomass were observed, and the highest leaf fresh biomass production was observed under no-drought-stress conditions, but no differences between bioinput applications were observed (Figure 4b). For the clayey soil, the bioinput application increased the legume fresh biomass, in both conditions, with and without drought stress, in comparison to no bioinput application (Figure 4b). For the root parameters, the bioinput application showed an incremental difference in the dry biomass in comparison to no bioinput application both with and without drought stress conditions (Figure 4d). Under the drought stress condition, the bioinput application slightly increased the water content, but under the no-drought-stress conditions, the bioinput application reduced the root water content (Figure 4d). Regarding the root volume, in the clayey soil, no differences were observed for the treatments tested (Figure 4f).

2.4. Common Bean Grain Production Response of Bioinput Application After a Drought Stress Period

No differences were observed for grain production and cycle period regarding the irrigation differentiation and bioinput application, for both types of soils tested (Figure 5).

3. Discussion

3.1. Common Bean Response of Bioinput Application with Cultivation in a Sandy Loam Soil and Submitted to a Drought Stress Period

When Priestia aryabhattai was applied to common bean in a sandy loam soil, no change was observed in the plant growth during the vegetative stage compared to the control of no bioinput application, indicating no plant growth bacteria effect.
However, after five days of the drought stress condition, a biochemical response was observed. The initial plant response to a stress condition is the production of reactive oxygen species (ROS) such as superoxide (O2•−), 1O2, and HO [16]. The ROS accumulation will lead to cell lipid peroxidation, which is the incorporation of molecular oxygen in the cell membrane fatty acids. To avoid the peroxidation, plants trigger the dismutation processes, catalyzing the enzyme superoxide dismutase (SOD, EC 1.15.1.1) within the cell [17]. The results showed that the treatment submitted to a drought stress condition without bioinput application presented an increase in the SOD activity, which may be a response to the lack of water. As sandy soil has low water retention capacity, after four days of drought conditions, low or even no water was available to the plants, which increased the ROS production and hence triggered the SOD activity. Also, sandy soils have larger macropores, resulting in greater permeability compared to fine-textured soils. Prolonged drought can significantly affect the activity and structure of soil microbial communities [18]. The action of the SOD prompts the reduction of the ROS, producing hydrogen peroxide (H2O2). As a consequence of the higher SOD activity under the water deficit condition and no bioinput application, a higher H2O2 accumulation was observed [19]. However, the accumulation of H2O2 is toxic to the plant and must be decomposed into H2O and O2. For this, peroxidase enzymes (POD, EC 1.11.1) are activated. Due to the high H2O2 production, high peroxidase [POD], under the stress condition, was required. One of the final products of polyunsaturated fatty acids’ peroxidation in plants is the overproduction of malondialdehyde (MDA), which is used as a stress marker because of oxidative damage, and under the drought stress condition, the treatment that showed the highest accumulation of MDA was no bioinput application [20].
Under drought conditions, the bioinput application showed very promising results for the mitigation of the plant biochemical response. Under the stress condition with bioinput application, there were lower levels of SOD, H2O2, POD, and MDA in comparison to no bioinput application. This indicates that even under drought conditions, the common bean that received the bioinput was aided by the bacteria and did not activate the ROS production, which in turn did not trigger the SOD production, reducing the H2O2 accumulation, and hence, less POD enzyme activity was required. Finally, low MDA was found, indicating that the plants with the application of Priestia aryabhattai suffered a low level of stress. Yasmin et al. [21] found that plant-growth-promoting bacteria may decrease malondialdehyde levels in plants under drought stress, enhance proline production and associated hormones, and markedly augment plant drought resistance. Priestia aryabhattai is isolated from areas prone to drought and is adapted to this stress condition. When used for agricultural purposes, the bacteria are found to help the plant and mitigate the stress under drought [22].
The potential of bacteria from the Bacillus genus has shown promise in mitigating stress condition effects. Zhou et al. [23] studied the effects of Bacillus cereus on cucumber seedlings under salt stress; observed that the H2O2 and MDA production of seedlings treated with B. cereus was significantly reduced, indicating a regulation of the antioxidant metabolism of cucumber seedlings; and concluded that this bioinput could alleviate salt-induced inhibition of growth and photosynthesis. In the same way, Duo et al. [24] evaluated the alleviation of drought stress in turfgrass by the combined application of nano-compost and microbes from compost, identified as Bacillus cereus, Lysinibacillus sp., and Rhodotorula glutinis, and found that the nanocompost-treated and inoculated seedlings showed lower MDA production compared to a nontreated control under drought stress, indicating the capacity to eliminate toxic reactive oxygen species (ROS). A reduction in the hydrogen peroxide (H2O2) and malondialdehyde (MDA) in rice leaves under drought stress was observed when plants were treated with plant-growth-promoting rhizobacteria (PGPR), including Bacillus cereus BSB 38 (14B) [25]. Our results also agreed with the drought stress amelioration with the inoculation of Bacillus spp. in maize, showing the antioxidant response to bacterial inoculation reduced the malondialdehyde level by 59.14% and the formation of hydrogen peroxide by 45.75% in both the control and water stress condition [26].
Regarding the application of Priestia aryabhattai, positive results in the mitigation of the effect of stress conditions were also observed in Chinese cabbage under heat and drought stresses [27], Chinese cabbage seedlings under high-temperature stress [28], induction of drought tolerance on sugarcane seedlings [29], and onion bulb development and maturation under drought stress [30].

3.2. Common Bean Response of Bioinput Application with Cultivation in a Clayey Soil and Submitted to a Drought Stress Period

Similarly, to the sandy loam soil, no differences were observed in the clayey soil for the first sampling of fresh biomass production. Additionally, no differences were observed among the treatments of irrigation differentiation and bioinput application for SOD activity and H2O2 accumulation. This may be due to the clayey soil’s potential to store water and, after four days without the input of water, still retain available water for the plants [31]. This result shows the low dependency of the plants on the bioinput bacteria [32], even in a condition where there is no water entry in the system. Consequently, for POD, under drought conditions, no effect of the bioinput application was observed. POD in optimum levels serves as a signaling molecule for plant growth [33]. However, the common bean plants under water deficit and no bioinput showed an increase in the MDA production, indicating a stress event. Gaafar et al. [34] reported a significant increase (by 88.6%) in malondialdehyde (MDA) in common bean leaves from plants under water stress, compared to the well-watered control.
After 10 days of drought stress, no differences were observed between the treatments with or without bioinput application for plant fresh biomass accumulation. In the treatment that maintained the irrigation, the bioinput application was effective in increasing the legume fresh biomass, an important productive parameter for common bean. This may be related to the influence of bacteria on plant growth. The promotion of drought tolerance is mainly attributed to the capacity of PGPB to synthesize plant hormones, such as auxin, which enhances the development of lateral roots and root hairs and promotes greater root growth, thereby augmenting water and nutrient uptake, supporting plants in mitigating environmental stresses, and enhancing their growth and yield [35]. This result demonstrates that the use of microorganisms can improve plant yield and serve as a complement to mineral fertilization [36].

3.3. Limitations and Outlooks

Despite the trend of the biochemical response of the common bean to the drought stress being markedly different between the soil types tested, the biomass production achieved for each soil was on different scales. These results may be due to the difference in the chemical fertility, even with the soils corrected and fertilized for common bean according to each soil type, highlighting the importance of integrated soil fertility management for optimal agricultural outcomes [37]. In the present study, the sandy loam soil, initially, presented higher chemical fertility than the clayey soil, and the biological potential of the bioinput inoculation had a significant effect in the sandy soil. Arruda et al. [38] studied the application of a bioinput (Herbaspirillum frisingense AP21) in common beans to mitigate stresses caused by a period of drought in a sandy loam and clayey soil, in Colombia, and the clayey soil showed an initial higher chemical fertility; those authors observed that while the addition of the bioinput had an effect in the clayey soil, no effect was observed for the sandy soil. This indicates that the integrative fertility is fundamental, where the potential of the biological effect may be dependent on the chemical soil properties.
We demonstrate the significant impact of the external application of Priestia aryabhattai in safeguarding plant growth during drought periods. The application of this bacteria into the soil markedly mitigated the suppression of biomass production under drought conditions. Another point to be highlighted is that, in implementing a greenhouse experiment, evidence of biochemical response can be identified under controlled conditions. Further research is necessary to attribute shifts in common bean grain production influenced by Priestia aryabhattai application under field experiments. Such information could be used to connect the potential of the bioinput to mitigate the drought effect in a production environment closely aligned with farmers’ realities.

4. Materials and Methods

4.1. Experimental Conditions and Setup of the Experiment

The greenhouse (alveolar polycarbonate; 10 mm thick; with treatment against ultraviolet rays; Van Der HoevenTM) experiment (21 ± 3 °C; 60 ± 10% humidity) was conducted at São Paulo State University (UNESP), Tupã campus, in pots (10 L capacity) containing 7 kg (dry basis) of two types of soil, differentiated according to the texture classification (Figure 6): sandy loam, sampled in Tupã-SP (21°55′44.1″ S 50°29′19.7″ W) and clayey, sampled in Botucatu–SP (22°50′48.0″ S 48°26′09.0″ W), classified as Nitisol and Alisol [39], respectively.
Chemical fertility analyses of both soils are presented in Table 1, based on which the correction and fertilization of each soil was carried out according to the recommendations for common bean (Phaseolus vulgaris L.; BRS Estilo variety), for the São Paulo state region, Brazil [40].
At the setup of the experiment, four common bean seeds (Phaseolus vulgaris L.; BRS Estilo variety) were sown per pot. Three days after emergence (DAE), a thinning was performed, maintaining one plant per pot.

4.2. Experimental Treatments

Two treatments were used for bioinput application: (i) no bioinput application, as a negative control; and (ii) with bioinput application, where two applications were performed along the crop cycle. The first application (Priestia aryabhattai CMAA 1363; Auras®; concentration 1 × 108 CFU mL−1) occurred at 10 DAE (V2—primary leaves [41]) and was performed using a water solution (150 mL pot−1), and the reapplication occurred at 46 DAE (R5—pre-flowering period [41]), according to the treatments, as previously described.
Regarding the water supply, all the pots received irrigation to satisfy the common bean demand, according to the available water capacity (AWC). The AWC of each soil was determined by adding water to soil samples (7 kg of dried basis soil (DSW); n = 4) using pots with drainage holes in the bottom. The water was added until the water started to drain. When the water stopped draining, the weight of the water-saturated soil (SSW) was obtained. The AWC was estimated by the following Equation (1):
AWC = SSW − DSW
The sandy loam soil presented an AWC of 243 mL kg−1 (100%), and the clayey soil presented an AWC of 371 mL kg−1 (100%). Common bean plants were irrigated at 80% of the AWC for each soil. The irrigation differentiation (for 10 days) was set at 47 DAE (R6 flowering [41]) according to the following treatments: (i) no stress period, where the irrigation water was kept during the irrigation differentiation period; and (ii) with a stress period, where the irrigation was completely paused, and no water was provided to the crop during the irrigation differentiation period. At 58 DAE, before the permanent wilting point, the irrigation differentiation was finished, and the water supply was resumed for all the treatments.

4.3. Sampling and Analysis

The experiment had four replicates (n = 4) per treatment, totaling 80 experimental units (pots), to comprise the 1st destructive sampling (n = 16); 2nd destructive sampling (n = 32), and final grain harvest (n = 32), as described in Table 2.
At 30 days after bioinput application, during the vegetative stage (40 DAE), the first destructive sampling (n = 32) was performed, where the common bean plants were removed from the soil and separated into the shoot (stem and leaf) and roots, and the fresh mass of each part was obtained. Additionally, the root samples were scanned using a LA2400 Scanner (Expression 12000XL, SEIKO EPSONTM, Suwa, Japan), and the root length per plant, root surface area per plant, root average diameter per plant, and root volume were evaluated using the WinRHIZOTM software (version Arabidopsis 2022, Regent Instruments, Quebec, Canada) image analysis system. Then, the root samples were dried (40 °C; until constant weight) to obtain the root dry biomass (RDB). Root water content (RWC) was estimated by Equation (2):
RWC = RFW − RDW
where RFW is root fresh biomass.
At 52 DAE, 5 days after irrigation differentiation started, two leaves (composed of three leaflets each) per plant, located in the middle third of the plants, were sampled (n = 4). The trefoils were stored (−80 °C) for analysis of the antioxidant system: superoxide dismutase activity [SOD], determined according to the methodology proposed by Del Longo et al. [42] and Giannopolitis and Ries [43] (1.5 g leaf material: 4 mL extractant); hydrogen peroxide production [H2O2], determined using the methodology described by Alexieva et al. [44] (0.4 g leaf material: 4 mL extractant); peroxidase activity [POD] determined according the methods propose by Teisseire and Guy [45] (0.1 g leaf material: 5 mL extractant); and malonaldehyde [MDA] production, determined by the methodology described by Heath and Packer [46] (0.4 g leaf material: 4 mL extractant).
At 57 DAE, 10 days after irrigation differentiation, the second destructive sampling (n = 32) was performed, where the common bean plants were removed from the soil and separated into shoots (stem, leaf, flower, and legume) and roots, and the fresh mass of each part was obtained. The root fractionation (dry biomass and water content) and root volume were obtained, as described previously.
The common bean grain harvest was performed according to the physiological maturation of each experimental unit (one plant per pot; n = 4), which occurred in the interval of 88 and 109 DAE.

4.4. Statistical Analysis

The results were analyzed separately per soil type (sandy loam and clayey soil). The data were submitted to analysis of variance (ANOVA), and where there was a significant effect, the means were compared using the Duncan test, at a 5% probability of error. The statistical analysis was performed using the SAS software (version 9.4, SAS Institute, Cary, NC, USA), and the graphics were made using SigmaPlot software (version 12.5, Systat Software Inc., San Jose, CA, USA).

5. Conclusions

The bioinput application influenced the common bean’s response to drought stress conditions, and the results depended on the soil type. Priestia aryabhattai showed promising results for the mitigation of drought stress in the sandy soil, characterized by lower water holding capacity, by reducing the SOD activity, POD activity, and MDA production compared to no bioinput application, indicating effective stress mitigation using the bacteria. When common bean was cropped in the clayey soil, characterized by higher water holding capacity in comparison to sandy soils, water availability to plants was maintained for longer, hence diminishing the plant dependence on the bacteria for stress mitigation. Thus, the introduction of bioinput in the common bean cultivation enhanced the stress tolerance and was demonstrated to be an effective strategy for improving the water stress resilience and productivity of P. vulgaris. Therefore, Priestia aryabhattai may be implemented as a bioinoculant to enhance crop development under drought stress scenarios. Nevertheless, these findings require verification under field conditions.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/stresses5010017/s1, Table S1: Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil), following the treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence-DAE). Plant sampling was performed at 40 DAE; Table S2: Common bean root parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil), following the treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence-DAE). Plant sampling was performed at 40 DAE; Table S3: Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil), following the treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence-DAE). Plant sampling was performed at 52 DAE; Table S4: Common bean root growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil), following the treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence-DAE). Plant sampling was performed at 52 DAE.

Author Contributions

Conceptualization, B.A., W.F.B.H., G.A.E.-B. and F.F.P.; formal analysis, B.M.B., N.B.d.F.J., W.A.L.Z. and A.L.S.S.; investigation, B.A.; resources, B.A. and F.F.P.; data curation, B.A.; writing—original draft preparation, B.A.; writing—review and editing, B.A., W.F.B.H., G.A.E.-B. and F.F.P.; supervision, B.A. and F.F.P.; project administration, F.F.P.; funding acquisition, B.A. and F.F.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Council for Scientific and Technological Development (CNPq), project MCTI/CNPq/CT-AGRO number 32/2022 (Process number 406288/2022-4). B.A. was funded (post-doctoral grant) by São Paulo State University (UNESP) (Project number 4428); B.M.B. was funded (undergraduate grant) by The São Paulo Research Foundation, FAPESP (Project number 2023/03839-3); N.B.d.F.J. was funded (undergraduate grant) by National Council for Scientific and Technological Development (CNPq) (Process number 180024/2023-0).

Data Availability Statement

Data are contained within the article.

Acknowledgments

The authors thank São Paulo State University (UNESP), Tupã, for the infrastructure support. Also, the authors thank Bruno Braga da Silva and Leandro de Souza Rosa for their support during the greenhouse experiment conduction. Thanks are also due to Yasmin Saegusa Tadayozzi for the support in the laboratory analysis. Also, the authors thank Cyan Turner for the English review.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of this study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Gitz, V.; Meybeck, A.; Lipper, L.; Young, C.D.; Braatz, S. Climate change and food security: Risks and responses. Food Agric. Organ. United Nations (FAO) Rep. 2016, 110, 3–36. [Google Scholar]
  2. Fraire-Velázquez, S.; Balderas-Hernández, V.E. Abiotic stress in plants and metabolic responses. Abiotic Stress—Plant Responses Appl. Agric. 2013, 1, 25–48. [Google Scholar]
  3. CHARY, G.R.; Gopinath, K.; Kumar, P.R.; Bhaskar, S.; Singh, V.; Deepika, S.; Kumari, V.V.; Sridhar, K.; Narsimlu, B.; RASUL11, B.R.K.A.A. Management of major abiotic stresses in field crops. Indian J. Agron. 2021, 66, S258–S278. [Google Scholar]
  4. Reichert, J.M.; Rodrigues, M.F.; Awe, G.O.; Riquelme, U.F.B.; Kaiser, D.R.; Reinert, D.J. Common bean in highly variable weather conditions, on sandy soils, and food security in a subtropical environment. Food Energy Secur. 2015, 4, 219–237. [Google Scholar] [CrossRef]
  5. Brady, N.C.; Weil, R.R. Elements of the Nature and Properties of Soils; Pearson Prentice Hall: New Jersey, NY, USA, 2010. [Google Scholar]
  6. Buitrago, R.B.; de Bashan, L.E.G.; Pedraza, R.O. Bacterias Promotoras de Crecimiento Vegetal; Corporacion Colombiana de Investigacion Agropecuaria (Corpoica): Mosquera, Cundinamarca, Colombia, 2021. [Google Scholar]
  7. Jatav, S.S.; Parihar, M.; Patra, A.; Singh, S.K.; Chitara, M.K.; Mohapatra, K.K.; Rana, K. Soil microbes in plant growth promotion and for mitigation of abiotic stress of drought. Soil Microbiomes Sustain. Agric. Funct. Annot. 2021, 175–201. [Google Scholar]
  8. Gupta, R.S.; Patel, S.; Saini, N.; Chen, S. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: Description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int. J. Syst. Evol. Microbiol. 2020, 70, 5753–5798. [Google Scholar] [PubMed]
  9. Moreno-Galván, A.; Romero-Perdomo, F.A.; Estrada-Bonilla, G.; Meneses, C.H.S.G.; Bonilla, R.R. Dry-caribbean Bacillus spp. strains ameliorate drought stress in maize by a strain-specific antioxidant response modulation. Microorganisms 2020, 8, 823. [Google Scholar] [CrossRef] [PubMed]
  10. Deng, C.; Zhang, N.; Liang, X.; Huang, T.; Li, B. Bacillus aryabhattai LAD impacts rhizosphere bacterial community structure and promotes maize plant growth. J. Sci. Food Agric. 2022, 102, 6650–6657. [Google Scholar] [CrossRef] [PubMed]
  11. Akhtar, S.S.; Amby, D.B.; Hegelund, J.N.; Fimognari, L.; Großkinsky, D.K.; Westergaard, J.C.; Müller, R.; Moelbak, L.; Liu, F.; Roitsch, T. Bacillus licheniformis FMCH001 increases water use efficiency via growth stimulation in both normal and drought conditions. Front. Plant Sci. 2020, 11, 297. [Google Scholar] [CrossRef] [PubMed]
  12. Mendoza-Labrador, J.; Romero-Perdomo, F.; Abril, J.; Hernández, J.-P.; Uribe-Vélez, D.; Buitrago, R.B. Bacillus strains immobilized in alginate macrobeads enhance drought stress adaptation of guinea grass. Rhizosphere 2021, 19, 100385. [Google Scholar] [CrossRef]
  13. Devi, N.S.A.; Kumutha, K.; Anandham, R.; Krishnamoorthy, R. Induction of moisture stress tolerance by Bacillus and Paenibacillus in pigeon pea (Cajanus cajan. L). 3 Biotech 2021, 11, 355. [Google Scholar] [CrossRef]
  14. Park, Y.-G.; Mun, B.-G.; Kang, S.-M.; Hussain, A.; Shahzad, R.; Seo, C.-W.; Kim, A.-Y.; Lee, S.-U.; Oh, K.Y.; Lee, D.Y. Bacillus aryabhattai SRB02 tolerates oxidative and nitrosative stress and promotes the growth of soybean by modulating the production of phytohormones. PLoS ONE 2017, 12, e0173203. [Google Scholar] [CrossRef] [PubMed]
  15. Lahlali, R.; Ezrari, S.; Radouane, N.; Belabess, Z.; Jiang, Y.; Mokrini, F.; Tahiri, A.; Peng, G. Bacillus spp.-Mediated drought stress tolerance in plants: Current and future prospects. In Bacilli in Agrobiotechnology: Plant Stress Tolerance, Bioremediation, and Bioprospecting; Springer: Berlin/Heidelberg, Germany, 2022; pp. 487–518. [Google Scholar]
  16. Babaei, K.; Moghaddam, M.; Farhadi, N.; Pirbalouti, A.G. Morphological, physiological and phytochemical responses of Mexican marigold (Tagetes minuta L.) to drought stress. Sci. Hortic. 2021, 284, 110116. [Google Scholar] [CrossRef]
  17. Gill, S.S.; Anjum, N.A.; Gill, R.; Yadav, S.; Hasanuzzaman, M.; Fujita, M.; Mishra, P.; Sabat, S.C.; Tuteja, N. Superoxide dismutase—mentor of abiotic stress tolerance in crop plants. Environ. Sci. Pollut. Res. 2015, 22, 10375–10394. [Google Scholar] [CrossRef]
  18. Siebielec, S.; Siebielec, G.; Klimkowicz-Pawlas, A.; Gałązka, A.; Grządziel, J.; Stuczyński, T. Impact of water stress on microbial community and activity in sandy and loamy soils. Agronomy 2020, 10, 1429. [Google Scholar] [CrossRef]
  19. Ullah, A.; Akbar, A.; Luo, Q.; Khan, A.H.; Manghwar, H.; Shaban, M.; Yang, X. Microbiome diversity in cotton rhizosphere under normal and drought conditions. Microb. Ecol. 2019, 77, 429–439. [Google Scholar] [CrossRef]
  20. Abiala, M.; Sadhukhan, A.; Muthuvel, J.; Shekhawat, R.S.; Yadav, P.; Sahoo, L. Rhizosphere Priestia species altered cowpea root transcriptome and enhanced growth under drought and nutrient deficiency. Planta 2023, 257, 11. [Google Scholar] [CrossRef] [PubMed]
  21. Yasmin, H.; Rashid, U.; Hassan, M.N.; Nosheen, A.; Naz, R.; Ilyas, N.; Sajjad, M.; Azmat, A.; Alyemeni, M.N. Volatile organic compounds produced by Pseudomonas pseudoalcaligenes alleviated drought stress by modulating defense system in maize (Zea mays L.). Physiol. Plant. 2021, 172, 896–911. [Google Scholar] [CrossRef] [PubMed]
  22. Xu, H.; Gao, J.; Portieles, R.; Du, L.; Gao, X.; Borras-Hidalgo, O. Endophytic bacterium Bacillus aryabhattai induces novel transcriptomic changes to stimulate plant growth. PLoS ONE 2022, 17, e0272500. [Google Scholar] [CrossRef]
  23. Zhou, Y.; Sang, T.; Tian, M.; Jahan, M.S.; Wang, J.; Li, X.; Guo, S.; Liu, H.; Wang, Y.; Shu, S. Effects of Bacillus cereus on photosynthesis and antioxidant metabolism of cucumber seedlings under salt stress. Horticulturae 2022, 8, 463. [Google Scholar] [CrossRef]
  24. Duo, L.; Liu, C.; Zhao, S. Alleviation of drought stress in turfgrass by the combined application of nano-compost and microbes from compost. Russ. J. Plant Physiol. 2018, 65, 419–426. [Google Scholar] [CrossRef]
  25. Gusain, Y.S.; Singh, U.; Sharma, A. Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr. J. Biotechnol. 2015, 14, 764–773. [Google Scholar]
  26. Azeem, M.; Haider, M.Z.; Javed, S.; Saleem, M.H.; Alatawi, A. Drought stress amelioration in maize (Zea mays L.) by inoculation of Bacillus spp. strains under sterile soil conditions. Agriculture 2022, 12, 50. [Google Scholar] [CrossRef]
  27. Yoo, S.-J.; Hong, J.K.; Weon, H.-Y.; Song, J.; Sang, M.K. Effect of Bacillus aryabhattai H26-2 and B. siamensis H30-3 on growth promotion and alleviation of heat and drought stresses in Chinese cabbage. Plant Pathol. J. 2019, 35, 178. [Google Scholar]
  28. Lee, Y.H.; Jang, S.J.; Han, J.-H.; Bae, J.S.; Shin, H.; Park, H.J.; Sang, M.K.; Han, S.H.; Kim, K.S.; Han, S.-W. Enhanced tolerance of Chinese cabbage seedlings mediated by Bacillus aryabhattai H26-2 and B. siamensis H30-3 against high temperature stress and fungal infections. Plant Pathol. J. 2018, 34, 555. [Google Scholar] [CrossRef] [PubMed]
  29. May, A.; Moreira, B.R.A.; Mascarin, G.M.; Viana, R.S.; Santos, M.S.; Silva, E.H.F.M.; Ramos, N.P.; de MELO, I.S. Induction of drought tolerance by inoculation of Bacillus aryabhattai on sugarcane seedlings. Científica 2019, 47, 400–410. [Google Scholar] [CrossRef]
  30. Moon, H.J.; Yoo, S.-J.; Sang, M.K. Bacillus aryabhattai H19-1-Mediated Mitigation of Drought Stress in Onion Bulb Development and Maturation. Res. Plant Dis. 2023, 29, 200–203. [Google Scholar] [CrossRef]
  31. Reichert, J.M.; Rodrigues, M.F.; Peláez, J.J.Z.; Lanza, R.; Minella, J.P.G.; Arnold, J.G.; Cavalcante, R.B.L. Water balance in paired watersheds with eucalyptus and degraded grassland in Pampa biome. Agric. For. Meteorol. 2017, 237, 282–295. [Google Scholar] [CrossRef]
  32. Compant, S.; Cambon, M.C.; Vacher, C.; Mitter, B.; Samad, A.; Sessitsch, A. The plant endosphere world–bacterial life within plants. Environ. Microbiol. 2021, 23, 1812–1829. [Google Scholar] [CrossRef] [PubMed]
  33. Afzal, S.; Chaudhary, N.; Singh, N.K. Role of soluble sugars in metabolism and sensing under abiotic stress. Plant Growth Regul. Signal. Under Stress Cond. 2021, 305–334. [Google Scholar]
  34. Gaafar, A.A.; Ali, S.I.; El-Shawadfy, M.A.; Salama, Z.A.; Sękara, A.; Ulrichs, C.; Abdelhamid, M.T. Ascorbic acid induces the increase of secondary metabolites, antioxidant activity, growth, and productivity of the common bean under water stress conditions. Plants 2020, 9, 627. [Google Scholar] [CrossRef] [PubMed]
  35. Steiner, F.; da Silva Oliveira, C.-E.; Zoz, T.; Zuffo, A.-M.; de Freitas, R. Co-Inoculation of common bean with Rhizobium and Azospirillum enhance the drought tolerance. Russ. J. Plant Physiol. 2020, 67, 923–932. [Google Scholar] [CrossRef]
  36. Ke, J.; Wang, B.; Yoshikuni, Y. Microbiome engineering: Synthetic biology of plant-associated microbiomes in sustainable agriculture. Trends Biotechnol. 2021, 39, 244–261. [Google Scholar] [CrossRef] [PubMed]
  37. Bayu, T. Review on contribution of integrated soil fertility management for climate change mitigation and agricultural sustainability. Cogent Environ. Sci. 2020, 6, 1823631. [Google Scholar] [CrossRef]
  38. Arruda, B.; Bejarano-Herrera, W.F.; Ortega-Cepeda, M.C.; Campo-Quesada, J.M.; Toro-Tobón, G.; Estrada-Bonilla, G.A.; Silva, A.M.M.; Ferrari Putti, F. Bioinput Inoculation in Common Beans to Mitigate Stresses Caused by a Period of Drought. Stresses 2023, 3, 842–857. [Google Scholar] [CrossRef]
  39. Food and Agriculture Organization of the United Nations. World Reference Base for soil resources world soil resource. In Reports FAO, ISRIC, ISSS, Rome; Food and Agriculture Organization of the United Nations: Rome, Italy, 1998. [Google Scholar]
  40. Raij, B.V.; Cantarella, H.; Quaggio, J.A.; Furlani, A. Recomendações de Adubação e Calagem para o Estado de São Paulo; Instituto Agronômico/Fundação IAC Campinas: Campinas, Brazil, 1997.
  41. Fernández, F. Etapas de Desarrollo de la Planta de Fríjol Común: Guía de Estudio; CIAT: Colombia, UK, 1982. [Google Scholar]
  42. Del Longo, O.T.; González, C.A.; Pastori, G.M.; Trippi, V.S. Antioxidant defences under hyperoxygenic and hyperosmotic conditions in leaves of two lines of maize with differential sensitivity to drought. Plant Cell Physiol. 1993, 34, 1023–1028. [Google Scholar]
  43. Giannopolitis, C.N.; Ries, S.K. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 1977, 59, 309–314. [Google Scholar] [CrossRef]
  44. Alexieva, V.; Sergiev, I.; Mapelli, S.; Karanov, E. The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ. 2001, 24, 1337–1344. [Google Scholar] [CrossRef]
  45. Teisseire, H.; Guy, V. Copper-induced changes in antioxidant enzymes activities in fronds of duckweed (Lemna minor). Plant Sci. 2000, 153, 65–72. [Google Scholar] [CrossRef]
  46. Heath, R.L.; Packer, L. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys. 1968, 125, 189–198. [Google Scholar] [CrossRef]
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Figure 1. Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE). Plant sampling was performed at 40 DAE: (a) plant fresh biomass per plant (leaf, stem, or root), for sandy loam soil; (b) plant fresh biomass per plant (leaf, stem, or root), for clayey soil; (c) root fractionation per plant, for sandy loam soil; (d) root fractionation per plant, for clayey soil; (e) root volume per plant, for sandy loam soil; (f) root volume per plant, for clayey soil. ns: non-significant difference (p ≥ 0.05) by analysis of variance (ANOVA). Errors of the mean of the results showed in (a–d) are presented in Supplementary Materials (Table S1). Error bars (e,f) represent the standard error of the mean (n = 4).
Figure 1. Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE). Plant sampling was performed at 40 DAE: (a) plant fresh biomass per plant (leaf, stem, or root), for sandy loam soil; (b) plant fresh biomass per plant (leaf, stem, or root), for clayey soil; (c) root fractionation per plant, for sandy loam soil; (d) root fractionation per plant, for clayey soil; (e) root volume per plant, for sandy loam soil; (f) root volume per plant, for clayey soil. ns: non-significant difference (p ≥ 0.05) by analysis of variance (ANOVA). Errors of the mean of the results showed in (a–d) are presented in Supplementary Materials (Table S1). Error bars (e,f) represent the standard error of the mean (n = 4).
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Figure 2. Common bean antioxidative stress parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) superoxide dismutase [SOD] in leaf, for sandy loam soil; (b) superoxide dismutase [SOD] in leaf, for clayey soil; (c) hydrogen peroxide [H2O2] in leaf, for sandy loam soil; (d) hydrogen peroxide [H2O2] in leaf, for clayey soil; (e) peroxidase [POD] in leaf, for sandy loam soil; (f) peroxidase [POD] in leaf, for clayey soil; ns: non-significant difference (p ≥ 0.05). Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Error bars represent the standard error of the mean (n = 4).
Figure 2. Common bean antioxidative stress parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) superoxide dismutase [SOD] in leaf, for sandy loam soil; (b) superoxide dismutase [SOD] in leaf, for clayey soil; (c) hydrogen peroxide [H2O2] in leaf, for sandy loam soil; (d) hydrogen peroxide [H2O2] in leaf, for clayey soil; (e) peroxidase [POD] in leaf, for sandy loam soil; (f) peroxidase [POD] in leaf, for clayey soil; ns: non-significant difference (p ≥ 0.05). Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Error bars represent the standard error of the mean (n = 4).
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Figure 3. Common bean antioxidative stress parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) malonaldehyde [MDA] production in leaf, for sandy loam soil; (b) malonaldehyde [MDA] production in leaf, for clayey soil. Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Error bars represent the standard error of the mean (n = 4).
Figure 3. Common bean antioxidative stress parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) malonaldehyde [MDA] production in leaf, for sandy loam soil; (b) malonaldehyde [MDA] production in leaf, for clayey soil. Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Error bars represent the standard error of the mean (n = 4).
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Figure 4. Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) plant fresh biomass per plant (legume, flower, leaf, stem, or root), for sandy loam soil; (b) plant fresh biomass per plant (legume, flower, leaf, stem, or root), for clayey soil; (c) root fractionation, for sandy loam soil; (d) root fractionation, for clayey soil; (e) root volume, for sandy loam soil; (f) root volume, for clayey soil. ns: non-significant difference (p ≥ 0.05) by analysis of variance (ANOVA). Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Errors of the mean of the results showed in (a–d) are presented in Supplementary Materials (Table S3). Error bars (e,f) represent the standard error of the mean (n = 4).
Figure 4. Common bean plant growth parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Trefoil sampling was performed at 52 DAE: (a) plant fresh biomass per plant (legume, flower, leaf, stem, or root), for sandy loam soil; (b) plant fresh biomass per plant (legume, flower, leaf, stem, or root), for clayey soil; (c) root fractionation, for sandy loam soil; (d) root fractionation, for clayey soil; (e) root volume, for sandy loam soil; (f) root volume, for clayey soil. ns: non-significant difference (p ≥ 0.05) by analysis of variance (ANOVA). Bars that have the same letters at the top do not differ significantly among treatments by the Duncan test (p ≥ 0.05). Errors of the mean of the results showed in (a–d) are presented in Supplementary Materials (Table S3). Error bars (e,f) represent the standard error of the mean (n = 4).
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Figure 5. Common bean production parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Grain harvest was performed at 88–109 DAE: (a) grain biomass production, for sandy loam soil; (b) grain biomass production, for clayey soil; (c) cycle, for sandy loam soil; (d) cycle, for clayey soil. ns: non-significant difference (p ≥ 0.05) analysis of variance (ANOVA)Error bars represent the standard error of the mean (n = 4).
Figure 5. Common bean production parameters from a greenhouse experiment, using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE), under a stress period (red stripe) and no stress period. Grain harvest was performed at 88–109 DAE: (a) grain biomass production, for sandy loam soil; (b) grain biomass production, for clayey soil; (c) cycle, for sandy loam soil; (d) cycle, for clayey soil. ns: non-significant difference (p ≥ 0.05) analysis of variance (ANOVA)Error bars represent the standard error of the mean (n = 4).
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Figure 6. Texture of two soils for conducting a greenhouse experiment: (a) sandy loam soil; (b) clayey soil.
Figure 6. Texture of two soils for conducting a greenhouse experiment: (a) sandy loam soil; (b) clayey soil.
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Table 1. Chemical fertility analysis of two soils, sandy loam soil and clayey soil, collected from the 0–20 cm layer for conducting a greenhouse experiment.
Table 1. Chemical fertility analysis of two soils, sandy loam soil and clayey soil, collected from the 0–20 cm layer for conducting a greenhouse experiment.
Soil
Texture
Classification		pHCaCl2SOMPresinaAl3+H+AlKCaMgSBCECVSBCuFeMnZn
g dm−3mg dm−3mmolc dm−3%mg dm−3
Sandy loam5.52.00.2009.20.7216.374.1721.26307050.070.428.563.920.12
Clayey4.35.60.13-35.70.172.000.863.03398-0.140.486.380.210.23
SOM: soil organic matter; SB: sum of basis; CEC: cation exchange capacity; V: basis saturation.
Table 2. Sampling scheme used in the greenhouse experiment with common bean using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE); with drought stress period (WSP) and no drought stress period (NSP).
Table 2. Sampling scheme used in the greenhouse experiment with common bean using two types of soil (sandy loam soil and clayey soil) and the following treatments: no bioinput application (NBA) and with bioinput application (WBA; Priestia aryabhattai; applied 10 and 46 days after emergence—DAE); with drought stress period (WSP) and no drought stress period (NSP).
Soil
Texture Classification		Bioinput * Application
10 and 46 DAE		Drought
Stress Period
47–57 DAE		1st Plant Sampling
40 DAE		Leaves Sampling
52 DAE		2nd Plant Sampling
57 DAE		Harvest
88–109 DAE
Replications §
Sandy
loam		NBAWSP-444
WBAWSP-444
NBANSP4444
WBANSP4444
ClayeyNBA WSP-444
WBAWSP-444
NBA NSP4444
WBANSP4444
16323232
DAE: days after emergence. * Priestia aryabhattai (Auras®); § each repetition represents a pot.
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Arruda, B.; Bagagi, B.M.; de Freitas Junior, N.B.; Bejarano Herrera, W.F.; Estrada-Bonilla, G.A.; Leoti Zanetti, W.A.; Silva Silvério, A.L.; Ferrari Putti, F. Biochemical and Plant Growth Response of the Common Bean to Bioinput Application Under a Drought Stress Period. Stresses 2025, 5, 17. https://doi.org/10.3390/stresses5010017

AMA Style

Arruda B, Bagagi BM, de Freitas Junior NB, Bejarano Herrera WF, Estrada-Bonilla GA, Leoti Zanetti WA, Silva Silvério AL, Ferrari Putti F. Biochemical and Plant Growth Response of the Common Bean to Bioinput Application Under a Drought Stress Period. Stresses. 2025; 5(1):17. https://doi.org/10.3390/stresses5010017

Chicago/Turabian Style

Arruda, Bruna, Breno Miranda Bagagi, Nelson Borges de Freitas Junior, Wilfrand Ferney Bejarano Herrera, German Andrés Estrada-Bonilla, Willian Aparecido Leoti Zanetti, Ana Laura Silva Silvério, and Fernando Ferrari Putti. 2025. "Biochemical and Plant Growth Response of the Common Bean to Bioinput Application Under a Drought Stress Period" Stresses 5, no. 1: 17. https://doi.org/10.3390/stresses5010017

APA Style

Arruda, B., Bagagi, B. M., de Freitas Junior, N. B., Bejarano Herrera, W. F., Estrada-Bonilla, G. A., Leoti Zanetti, W. A., Silva Silvério, A. L., & Ferrari Putti, F. (2025). Biochemical and Plant Growth Response of the Common Bean to Bioinput Application Under a Drought Stress Period. Stresses, 5(1), 17. https://doi.org/10.3390/stresses5010017

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