ACC deaminase-producing bacteria mitigate water deficit in tomato seedsABSTRACT:
Bacteria that modulate ethylene levels through the enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase are a promising strategy to mitigate the effects of water stress. The aim of this study was to assess the effect of these bacteria on the germination and growth of tomato seedlings subjected to water deficit. The experiment was conducted using a completely randomized design and 6x5 factorial scheme, with six seed treatments (four bacterial isolates and two controls) and five PEG 6000-induced osmotic potentials (0.0, -0.2, -0.4, -0.6, and -0.8 MPa), with four replications of 50 seeds. Germination, radicle protrusion, first germination count (FGC), germination speed index (GSI), and the fresh weight, root and shoot length of seedlings were evaluated. The results indicated that bacteria with ACC-deaminase activity favored germination and seedling development under water stress. Although water deficit reduced germination, isolate RZ-1 effectively mitigated these effects at -0.4 MPa. Strains E-154 and E-24 promoted the highest root and shoot growth.
Index terms:
aminocyclopropane-1-carboxylate-deaminase; ethylene; osmotic potential; PEG 6000; Solanum lycopersicum L
RESUMO:
O uso de bactérias moduladoras dos níveis de etileno por meio da enzima 1-aminociclopropano-1-carboxilato (ACC) desaminase surge como estratégia promissora para mitigar os efeitos do estresse hídrico. O objetivo deste trabalho foi avaliar o impacto dessas bactérias na germinação e no crescimento de plântulas de tomateiro sob condições de déficit hídrico. O experimento foi conduzido em delineamento inteiramente casualizado e esquema fatorial 6x5, com seis tratamentos de sementes (quatro isolados bacterianos e dois controles) e cinco potenciais osmóticos (0,0; -0,2; -0,4; -0,6; e -0,8 MPa) induzidos por PEG 6000, com quatro repetições de 50 sementes. Foram avaliados a germinação, protrusão radicular, primeira contagem de germinação, índice de velocidade de germinação, massa fresca, e comprimentos de raiz e parte aérea das plântulas. Os resultados indicaram que as bactérias com atividade ACC-desaminase favoreceram a germinação e o desenvolvimento de plântulas sob estresse hídrico. Embora o déficit hídrico tenha reduzido a germinação, o isolado RZ-1 foi eficaz na mitigação desses efeitos a -0,4 MPa. As cepas E-154 e E-24 destacaram-se na promoção do crescimento radicular e da parte aérea.
Termos para indexação:
aminociclopropano-1-carboxilato-desaminase; etileno; PEG 6000; potenciais osmóticos; Solanum lycopersicum L
INTRODUCTION
Water plays a crucial role in seed germination by promoting the resumption of embryo growth, leading to radicle protrusion. It is also responsible for reserve translocation and mobilization, essential for seed germination and seedling growth (Bewley et al., 2013; Marcos-Filho, 2015; Obroucheva et al., 2017). Thus, water deficit can significantly decrease the germination percentage, cause poor root and shoot formation and development, delay seedling growth and, in extreme cases, result in embryo death (Farooq et al., 2009). Water deficit during germination can be induced by polyethylene glycol (PEG) 6000 which, in general, simulates water deficiency without penetrating the seed coat, making it ideal for use in the early stages of seed germination (Masetto et al., 2016).
Inoculation with plant growth-promoting bacteria (PGPB) can mitigate the effects of water deficit, provide beneficial properties to plants, and colonize the rhizosphere, improving the performance of tomato plants under environmental stress (Candido et al., 2015). Moreover, this group of microorganisms can increase and stimulate plant resistance to pests and pathogens (Goswami and Deka, 2020).
Abiotic factors such as water deficit and salt and thermal stress have the greatest influence on plant performance and trigger peaks in ethylene production. Plants’ response to ethylene is complex and depends on factors such as the concentration of the hormone, plant development stage, and environmental conditions. This hormone plays a significant role in different plant physiological processes, including germination, tissue differentiation, flowering onset, pollination, lateral bud development, flower opening, and leaf and fruit senescence and abscission (Orozco-Mosqueda et al., 2020; Singh et al., 2022; Shahid et al., 2023; Kour et al., 2024; Reshma et al., 2024).
Ethylene can induce responses in plants at very low concentrations (< 1.0 µL.L-1) (Lynch and Brown, 1997; Choudhary, 2017). Conversely, at high levels, especially when triggered by biotic and abiotic stresses, the effects can be harmful, leading to root elongation, chlorophyll degradation, and leaf senescence and abscission (Glick et al., 2007; Singh et al., 2022).
The effect of ethylene stress on plants can be mitigated by multifunctional bacteria, which can facilitate plant growth and development through a wide range of mechanisms, such as modulating plant hormone levels (Glick, 2012). This is because certain bacteria can modulate endogenous ethylene by expressing the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase, which cleaves the ethylene precursor (ACC) into α-ketobutyrate and ammonia. This reduces substrate availability for ethylene biosynthesis and minimizes its harmful effects (Glick, 2014; Chandra et al., 2020). Studies on different crops have shown an increase in seed vigor and germination as a result of reduced ethylene concentrations (Siddiqui et al., 2015; Safari et al., 2018; Sarkar et al., 2018; Zhou et al., 2022).
Preliminary characterization studies of bacteria isolated from the internal tissues and rhizosphere of banana plants from municipalities in northern Minas Gerais and Bahia states identified strains capable of producing indole compounds, gibberellins, siderophores, and lytic enzymes, solubilizing phosphate, fixing nitrogen, and exhibiting ACC deaminase activity. These findings indicate multiple traits that may have a cumulative effect in promoting plant growth under stress (Souza et al., 2017; Silva, 2018).
Given that tomato plants are sensitive to water deficit, this study aimed to validate the effect of bacteria with ACC deaminase activity on the germination and physiological performance of tomato seeds (cv. Kada) under water deficit conditions.
MATERIAL AND METHODS
The experiment was carried out at the Plant Pathology and Seed Analysis laboratories on the Janaúba Campus of UNIMONTES in Minas Gerais state (MG), Brazil. A 6x5 factorial design was used, with the first factor corresponding to microbiolization of ‘Santa Cruz’ tomato seeds using four bacterial isolates (Bacillus pumilus-RZ-1; B. thuringiensis-E-24, Bacillus sp.-E-37 and B. pumilus-E-154), seeds disinfected with saline solution (no bacteria) and an absolute control (no disinfection or microbiolization), and the second factor to different osmotic potentials (0.0, -0.2, -0.4, -0.6 and - 0.8 MPa). Water deficit was induced using solutions containing polyethylene glycol 6000 (PEG 6000), prepared in accordance with Villela et al. (1991). The 0.0 MPa potential corresponded to the control, in which the substrate was moistened only with distilled water.
The bacteria were isolated from the internal tissues and rhizosphere of banana plants in northern Minas Gerais and Bahia states. The isolates were previously characterized and showed potential for the production of indole-3-acetic acid (IAA), gibberellin, siderophores, and lytic enzymes, as well as phosphate solubilization, nitrogen fixation and ACC-deaminase activity (Souza et al., 2013; Andrade et al., 2014; Souza et al., 2017; Silva, 2018).
The experiment was conducted in a completely randomized design, with four replications of 50 seeds per treatment, totaling 120 experimental units.
The bacterial suspensions were adjusted using a spectrophotometer to an optical density of 1 absorbance unit at a wavelength (λ) of 540 nm, for subsequent seed microbiolization. The seeds were disinfected according to the methodology of Martins et al. (2018) and air-dried in a laminar flow hood for 8 hours. The seeds were microbiolized with bacterial suspension. The bacteria-free treatment underwent disinfection and microbiolization using a saline solution (NaOH 0.85%) without adding bacteria, and the absolute control was neither disinfected nor microbiolized.
For the germination test, seeds were sown on Germitest® paper moistened with PEG 6000 solutions or distilled water (bacteria-free control) at 2.5 times its dry weight and placed in plastic germination boxes (Gerbox®). The boxes were placed in a digital germinator set to 25 °C and evaluated four days after sowing (DAS) to count the number of normal seedlings, with results expressed in percentage. Normal seedlings were those that exhibited fully developed, proportional, and healthy essential structures (root system and shoot) (Brasil, 2009).
After 96 hours, radicle protrusion was evaluated by counting the seeds with a visible radicle at least two millimeters long, with the results expressed in percentage.
Additionally, the first germination count consisted of the number of normal seedlings obtained at 5 DAS, with the results expressed in percentage (Brasil, 2009).
The germination seed index (GSI) was determined through daily assessments of the number of seeds showing radicle protrusion until normal seedling formation. At the end of the test, the data from the daily assessments were used to calculate the GSI via the formula proposed by Maguire (1962).
Fresh weight was obtained by weighing normal seedlings from each treatment/replication on an analytical balance (0.0001 g), with the results expressed in g.seedling-1.
Shoot and root length were measured with a graduated ruler at the end of germination testing and the results expressed in cm.seedling-1.
The results were submitted to analysis of variance (ANOVA), means compared by the Scott-Knottt test at 1% probability, and the means of PEG 6000 concentrations to regression analysis. Regression models were selected based on the significance of the coefficients, considering the model that best explained the biological phenomenon. The variables were analyzed using the Sisvar program (Ferreira, 2011).
RESULTS AND DISCUSSION
A statistically significant interaction (p ≤ 0.01) was observed between the bacterial strains and PEG 6000-induced osmotic potentials for the variables germination, radicle protrusion, FGC, GSI, seedling fresh weight, and shoot and root length. These results indicate that tomato seed microbiolization with ACC deaminase-producing bacteria positively influenced seed germination capacity and seedling development under water deficit.
In seed treatments with ACC deaminase-producing bacteria, germination percentage declined progressively with decreasing osmotic potential, indicating a consistent linear trend. This behavior was consistent across all the treatments (Table 1), demonstrating that an increase in water deficit induced by negative PEG 6000 potentials had an adverse effect on germination potential as observed by Catão et al. (2024).
Regression equations for germination speed index (GSI), radicle protrusion, and first count in tomato seeds microbiolized with ACC deaminase-producing bacteria under PEG 6000-induced water deficit.
GSI declined in all treatments as osmotic potential decreased, indicating that greater osmotic stress caused by negative PEG 6000 potentials had a negative effect on tomato seed germination, even when seeds were microbiolized with ACC deaminase-synthesizing bacteria known for mitigating the effects of stress (Table 1).
Radicle protrusion and FGC, also known indicators of plant vigor, showed similar behavior among the bacterial strains as a function of osmotic concentrations (Table 1). These parameters exhibited linear declines with increasingly negative PEG 6000 concentrations, suggesting a uniform response by vigor assessment variables to the osmotic concentrations tested.
Under ideal osmotic conditions (0.0 MPa), there was no significant difference between treatments, with higher germination percentages than those stipulated by the Brazilian Ministry of Agriculture, Livestock and Supply (MAPA) for certified tomato seeds (Brasil, 2012). Cabra-Cendales et al. (2017) studied the effect of inoculation with the GIBI 200 Bacillus subtilis strain on germination in cherry tomato seeds and found no statistically significant difference between germination percentages in inoculated and non-inoculated seeds. In the present study, the highest germination percentages were recorded at -0.2 MPa in treatments with B. thuringiensis E-24 and the absolute control, differing statistically from the remaining treatments. However, bacteria-free treatments and those with Bacillus sp. E37 did not reach the minimum germination percentage (75%) established by MAPA. As water deficit increased, B. pumilus RZ-1 promoted the highest germination at -0.4 MPa, with no significant difference between treatments at osmotic potentials of -0.6 and -0.8 MPa (Table 2).
Studies have shown reduced germination in tomato seeds under water deficit (Florido et al., 2018; Carvalho et al., 2021). This is because water deficit during seed imbibition can decrease the tissue hydration rate and oxygen diffusion, which also delays the onset of enzymatic activity, ultimately leading to reduced meristematic growth and compromising cell elongation, cell wall synthesis, and radicle emission (Marcos-Filho, 2015; Obroucheva et al., 2017).
Research on treating rice, canola and wheat seeds with ACC deaminase-producing bacteria has shown a decline in ethylene concentration and an increase in germination rate and vigor (Siddiqui et al., 2015; Safari et al., 2018; Sarkar et al., 2018; Zhou et al., 2022).
With respect to the behavior of the bacterial strains at each osmotic potential, at 0.0 MPa, E-24, E-154 and the bacteria-free treatment obtained the highest GSI values, differing statistically from the remaining treatments (Table 3). These high GSI values indicate faster initial seed development even under stress conditions caused by low water availability.
The absolute control was statistically superior at -0.2 MPa, differing from the bacteria-free and E-37 treatments. At -0.4 MPa, seeds microbiolized with RZ-1 obtained the highest average GSI, showing statistical superiority to the other treatments. There was no significant difference between the treatments tested at osmotic potentials of -0.6 and -0.8 MPa (Table 3).
The results demonstrated that at the lowest osmotic potential where germination occurred (-0.4 MPa), the RZ-1 isolate was the most efficient at mitigating the effects of water deficit. This can be attributed to the ability of the B. pumilus RZ-1 strain to induce seed tolerance to water stress by reducing excess endogenous ethylene levels, which typically increase due to the harmful effects of stress. This behavior is consistent with Glick et al. (2007), who confirmed the ability of ACC deaminase-active isolates to reduce ethylene levels, demonstrating that bacteria producing higher ACC deaminase levels are more efficient.
Statistical analysis revealed different responses among the bacterial strains at each osmotic potential for radicle protrusion and FGC. B. thuringiensis E-24 and B. pumilus E-154 obtained higher mean radicle protrusion values at 0.0 MP, differing from the remaining treatments (Table 4).
For FGC, E-24 also stood out at the highest osmotic potential, along with the bacteria-free treatment. These strains were statistically superior to RZ-1 and E-154 (Table 5).
Treatments involving disinfection/microbiolization (E-24; E-154; E-37; RZ-1; no bacteria) did not yield positive results for radicle protrusion and FGC at -0.2 MPa, with the absolute control exhibiting superior performance. It should be noted that both these variables were assessed within the first five days of experiment onset. Based on this information, and considering treatment responses at the end of the experiment, we can infer that the bacteria investigated require a longer interaction period with tomato seeds under water deficit conditions to balance endogenous ethylene levels and alter the hormone’s effect from suppressing to promoting germination. Glick et al. (1998) presented a model demonstrating that bacterial access to ACC is governed by a concentration gradient, and that plants must exude a larger amount of ACC to maintain a balance between internal and external ACC levels. However, bacterial interaction with the rhizosphere depends on different organic compounds that serve as bacterial attractants, ensuring robust colonization of rhizosphere and rhizoplane regions.
The production and endogenous signaling of ethylene are essential for the rapid adaptative response of plants to salinity, enabling physiological adjustments that favor survival. However, excessive synthesis of this hormone under continuous stress can have a harmful effect on plant growth and development, potentially leading to plant death in extreme cases. Thus, strict control of ethylene homeostasis is a key factor in plant survival under stress, and the resumption of growth in subsequent stages. Various positive and negative feedback mechanisms regulate ethylene biosynthesis and signaling, as reviewed by Vandenbussche et al. (2012). In experiments with rice seedlings, exogenous ethylene application increased salinity sensitivity, whereas treatment with 1-MCP, an ethylene perception inhibitor, promoted greater stress tolerance. Additionally, the activity of the genes MHZ7/OsEIN2, MHZ6/OsEIL1 and OsEIL2, related to the ethylene signaling pathway, has been associated with lower tolerance to different stressors (Yang et al., 2015).
Carvalho et al. (2021) observed reduced vigor in tomato seeds during the first germination count under negative osmotic potentials, with the percentage of normal seedlings declining to 9% at -0.3 MPa. The authors attributed this to the loss of protoplasmic turgidity, which disrupts cell physiology and damages biomembrane systems (Bruni and Leopold, 1992). Silva-Junior et al. (2014) reported that an osmotic potential of -0.2 MPa can cause significant vigor loss in tomato seeds.
In the treatments studied, the growth characteristics analyzed indicated a highly significant linear effect (P<0.01) in seedlings subjected to osmotic concentrations, with reduced shoot and root length and seedling fresh weight observed as osmotic potential declined (Table 6). This phenomenon demonstrates that the increased water deficit negatively affected tomato seedling growth, potentially due to low reserve translocation to the embryo, which compromised seedling development as a result of possible structural and physiological damage (Fonseca et al., 2022). Reduced seedling length due to a progressive decline in osmotic potential has been reported in previous studies (Carvalho et al., 2021; Dutra et al., 2022; Fonseca et al., 2022).
Regression equations for shoot length (SL), root length (RL), and seedling fresh weight (SFW) of tomato seeds microbiolized with ACC deaminase-producing bacteria under PEG 6000-induced water deficit.
Similar behavior was observed across treatments for shoot and root length, with greater seedling growth gains associated with E-154 microbiolization in the absence of PEG 6000. The highest average shoot lengths at -0.2 MPa were 3.85 and 3.60 cm, recorded in the E- 154 and E-24 treatments, respectively (Table 7).
These strains also promoted root length increases, with respective mean values of 2.60 and 2.65 cm (Table 8). There was a substantial decline in shoot length at -0.3 MPa, consistent with the findings of Carvalho et al. (2021).
Microbioliztion with strains E-37 and RZ-1 did not increase root length, showing behavior similar to that of the bacteria-free treatment and absolute control. Sá et al. (2019) also observed inferior responses compared to the control in bean seeds microbiolized with Bacillus sp. species. Previous studies have reported conflicting results regarding microbiolization with certain microorganisms (Amaral et al., 2014; Junges et al., 2015; Junges et al., 2017; Romagna et al., 2019).
The first measurable effect of water deficit is undoubtedly reduced growth, largely due to decreased cell expansion, which depends on adequate turgor pressure (Taiz et al., 2017). In this context, the decline in shoot length in plants under water deficit can be considered a survival strategy to prevent water loss through transpiration (Correia and Nogueira, 2004).
Root length followed a trend similar to that observed for shoot length. At -0.4 MPa, the only treatments that promoted growth gains in tomato seedlings were those involving microbiolization with Bacillus RZ-1 and E-37 (Table 8).
Seedling fresh weight reinforced the responses observed in the growth variables; however, at -0.4 MPa, E- 37 and RZ-1 showed superior performance, differing significantly from the other treatments (Table 9).
Phytostimulation is considered one of the most important mechanisms by which rhizobacteria promote plant growth, mainly by stimulating cell division and root elongation (Martínez-Viveiros, 2010). Among the plant hormones involved, cytokinins play a key role in cell division and primary root growth. It should be noted that the genus Bacillus, widely used in the present study, is capable of producing these substances (Glick, 2014). Furthermore, Glick and Nascimento (2021) emphasize that ACC deaminase-producing bacteria can modulate ACC concentrations in the rhizosphere and phyllosphere by consuming ACC exuded by the plant or within plant tissues, directly limiting ACC availability and consequently reducing ethylene production.
The use of ACC deaminase-producing bacteria in agricultural crops has shown promising results for promoting plant growth under stress conditions. Niu et al. (2018) reported that ACC deaminase-producing bacteria associated with pearl millet can mitigate water deficit in plants, as evidence by improved seed germination and seedling development.
Further experiments will be conducted in a greenhouse under water deficit conditions, using tomato, bean and banana plants to evaluate the efficiency of bacterial strains in promoting plant development.
CONCLUSIONS
Increasingly negative osmotic concentrations resulted in a progressive decline in the germination percentage and germination speed index of tomato seeds.
Isolate RZ-1 proved effective under a water deficit of -0.4 MPa, maintaining higher germination rates when compared to non-inoculated treatments.
ACKNOWLEDGMENTS
The authors thank the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES; Financial Code 001) for granting of scholarships.
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Publication Dates
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Publication in this collection
06 June 2025 -
Date of issue
2025
History
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Received
07 Dec 2024 -
Accepted
23 Apr 2025
