RESEARCH PAPER
Research area: Sustainable Agriculture, Plant-Microbe Interactions
Plant growth-promoting rhizobacteria enhance root and shoot growth and biomass production in chrysanthemum: Evidence from pot and field experiments
A. N. M. Shahriar Zawad1, Tanim Jabid Hossain1.2*, Md. Mahfuz Ahmed1, Nadia Islam1, Imteaj Uddin Chowdhury1, Mohammad Razuanul Hoque1
1 Department of Biochemistry and Molecular Biology, University of Chittagong, Chattogram, Bangladesh
2 Laboratory for Health, Omics and Pathway Exploration (HOPE Lab), Chattogram, Bangladesh
*Corresponding author: Tanim Jabid Hossain, Email: tanim.bmb@gmail.com
Plant growth-promoting rhizobacteria (PGPR) enhance plant growth, biomass production, and environmental adaptability, offering a sustainable, eco-friendly solution to boost crop productivity and agricultural sustainability. This study evaluated the impact of six PGPR isolates – Bacillus cereus PGPR-13, Acinetobacter oleivorans PGPR-14, Staphylococcus epidermidis PGPR-15, Pantoea dispersa PGPR-24, Serratia nematodiphila PGPR-27, and Pantoea anthophila PGPR-34 – and their consortium, on Chrysanthemum growth under pot and field conditions. The PGPR strains, previously isolated from chrysanthemum rhizosphere and confirmed for in vitro plant growth-promoting activities, significantly enhanced key growth parameters, including stem length, root length, stem diameter, and biomass accumulation. Among individual treatments, A. oleivorans (PGPR-14) achieved a remarkable 114% increase in stem length during pot trials, while the consortium exhibited the highest stem diameter (1.09 cm) and dry biomass (33.03 g). Field trials confirmed these findings, with consortium-treated plants attaining superior growth metrics, including a stem length of 75.33 cm, root length of 31.73 cm, fresh biomass of 512 g, and dry biomass of 284.33 g, outperforming most individual strains. S. epidermidis (PGPR-15) and S. nematodiphila (PGPR-27) also demonstrated notable biomass enhancements, with mean fresh weights exceeding 390 g in field trials. These results highlight the synergistic effects of the PGPR consortium and the exceptional growth-promoting potential of individual strains such as A. oleivorans, S. epidermidis, and P. dispersa. The study underscores the promise of PGPR as sustainable biofertilizers to enhance chrysanthemum growth, offering an effective and ecofriendly solution to reduce dependence on chemical inputs. Future research should focus on optimizing microbial consortia, elucidating their functional mechanisms, and expanding their applications to enhance crop productivity and sustainability across diverse agricultural systems.
Plant growth-promoting rhizobacteria, PGPR field trials, root and shoot growth, biomass accumulation, sustainable plant growth, PGPR consortium, biofertilizer, pot experiments.
● PGPR significantly enhanced root, shoot growth, and biomass in chrysanthemum plant
● Synergistic microbial consortia proved highly effective for boosting plant growth
● A. oleivorans, S. epidermidis, and P. dispersa show strong growth-promoting effects
● Pot and field experiments validate PGPR as effective tool for chrysanthemum farming
● Study highlights the synergy and sustainability of PGPR consortia in agriculture
The use of Plant Growth-Promoting Rhizobacteria (PGPR) is an innovative and ecologically sustainable approach for enhancing plant growth, health, and productivity [1]. These beneficial microorganisms colonize plant roots and employ a diverse array of mechanisms to support growth, health, and productivity [2]. Key mechanisms of PGPR include improving nutrient availability through phosphate solubilization, nitrogen fixation, and mineral mobilization; synthesizing phytohormones like auxins and gibberellins; and suppressing phytopathogens through the production of antimicrobial compounds [3, 4]. Integrating PGPR into agricultural practices is essential for promoting sustainable agriculture, which aims to reduce dependence on synthetic fertilizers and pesticides while ensuring soil health and productivity [5]. Sustainable agriculture is crucial for achieving the United Nations’ Sustainable Development Goals (SDGs), particularly SDG 2, which focuses on eradicating hunger, achieving food security, improving nutrition, and promoting sustainable agricultural practices [6].
Chrysanthemum is one of the most economically and culturally significant floricultural crops worldwide, renowned for its ornamental appeal and therapeutic properties. Widely cultivated for cut flowers, garlands, and landscaping, chrysanthemums are also valued for their bioactive compounds, which exhibit antimicrobial, anti-inflammatory, and neuroprotective effects [7, 8]. However, chrysanthemum cultivation typically involves intensive use of synthetic agrochemicals to enhance growth and yield. Such practices pose significant environmental challenges, including soil degradation, pollution of water resources, disruption of soil microbial communities, and increased vulnerability to pests and diseases [9]. These issues underscore the urgent need for sustainable alternatives to conventional agricultural practices.
To address these pressing issues, this study builds on our previous work with PGPR strains isolated from the rhizosphere of chrysanthemum plants. In earlier research, 34 isolates were screened for their plant growth-promoting traits, including auxin production, phosphate solubilization, nitrogen fixation, and ammonia production. Among these, seven promising strains were selected based on their superior traits and identified as belonging to the genera Acinetobacter, Bacillus, Pantoea, Serratia, and Staphylococcus. These strains also exhibited robust abiotic stress tolerance, demonstrating their adaptability to diverse environmental conditions [10]. These findings positioned these strains as potential candidates for biofertilizer development aimed at enhancing plant growth under practical agricultural settings.
The current study focuses on evaluating the efficacy of these selected PGPR strains in pot and field trials using chrysanthemum seedlings. The primary objective is to assess their impact on chrysanthemum growth and development, thereby reducing the reliance on synthetic fertilizers and contributing to sustainable agricultural practices. By bridging the gap between laboratory research and field application, this study aims to provide valuable insights into the practical utility of PGPR as biofertilizers in chrysanthemum cultivation. Furthermore, this research seeks to establish a framework for integrating environmentally friendly and efficient plant growth-promoting agents into sustainable agricultural systems, advancing the adoption of PGPR for floriculture and beyond.
Six rhizobacterial strains were used for field and pot trials in this study including Bacillus cereus PGPR-13, Acinetobacter oleivorans PGPR-14, Staphylococcus epidermidis PGPR-15, Pantoea dispersa PGPR-24, Serratia nematodiphila PGPR-27, and Pantoea anthophila PGPR-34. Their isolation, identification and in vitro plant growth promoting activities have been previously reported [10]. Root associated soil from chrysanthemum plants was suspended in sterile distilled water, serially diluted and plated on LB and TSB media. Distinct bacterial colonies were purified through repeated streaking and preserved in glycerol stocks. The isolates were identified by amplifying and sequencing their 16S rRNA genes using primers 27F and 1492R. Sequence analysis was conducted with NCBI BLAST and EzBioCloud, and taxonomy was assigned based on sequence similarity, % identity, and alignment with type strains.
Chrysanthemum plants of uniform age and size were used for field and pot studies. Fourteen-day-old seedlings with stem length of approximately 2.5 inches, were obtained from a local nursery and prepared for the experiments.
Soil preparation
Loamy soil was collected from arable land adjacent to the Faculty of Biological Sciences (22º28´3´´N, 91º46´49´´E), University of Chittagong. The soil was crushed, ground, and sieved through a metal mesh, then mixed with compost (ACI Limited, Bangladesh) in a 3:2 ratio. The soil-compost mixture was sterilized [11, 12] and distributed into 12×12 inch pots in a laminar airflow chamber. The pots were covered with sterile aluminum foil to prevent contamination.
Preparation and application of bacterial inocula
The six rhizobacterial strains and Escherichia coli ATCC 25922, used as a reference strain for comparison, were cultured in nutrient broth at 30ºC with continuous shaking at 150 rpm for 12-14 hours. A consortium of the six bacteria was also prepared. The optical density of the cultures was adjusted to 0.7 - 0.9 at 600 nm [13–15]. For each pot, 30 mL of bacterial culture was evenly mixed with approximately 7.3 Kg of the sterile soil-compost mixture, and a single chrysanthemum seedling was planted in each pot [13]. A negative control without bacterial inoculation was included. The pots were maintained under natural environmental conditions for further observation [11, 16].
A cultivable plot measuring 16×12 feet (22º28´N, 91º46´49´´E) near the Faculty of Biological Sciences, University of Chittagong, was selected and prepared for the field experiments following a randomized complete block design [17, 18]. During field preparation, 25 grams of urea, muriate of potash, and triple superphosphate along with 5 kilograms of compost, were applied in the soil. Rectangle-shaped beds measuring 5×2.5 feet were prepared. Trenches approximately 10 inches wide were created around each bed, with adequate spacing of the same measurement between the beds [17]. Before planting, the roots of the chrysanthemum seedling were soaked in the bacterial inocula [18, 19], and small craters where the seedlings were planted were inoculated with 30 mL of the bacterial suspension.
Chrysanthemum plants were harvested, and growth measurements were recorded based on several parameters, including stem length and diameter, root length, leaf size, and fresh and dry weights of the plants [14, 17–20]. Fresh weight was measured immediately after harvesting, while dry weight was recorded after sun-drying the samples to a constant weight. Harvesting and data collection were conducted 115 days after the initiation of each experimental method.
The obtained data were analyzed for mean and standard deviation. Statistical analyses included one-way Analysis of Variance (ANOVA) using GraphPad Prism 10. Dunnett’s test was performed to determine significant differences, with a p-value ≤ 0.05 considered statistically significant.
Impact of PGPR on chrysanthemum growth in pot experiments
The effect of PGPR isolates, including Bacillus cereus PGPR-13, Acinetobacter oleivorans PGPR-14, Staphylococcus epidermidis PGPR-15, Pantoea dispersa PGPR-24, Serratia nematodiphila PGPR-27, and Pantoea anthophila PGPR-34, as well as a consortium of these isolates, on chrysanthemum plant growth was evaluated. Both individual strains and the consortium significantly improved plant growth, with PGPR-14 and the consortium showing the most pronounced effects on stem length, root length, total plant height, biomass accumulation, and morphological traits.
Figure 1. Effect of Plant Growth-Promoting Rhizobacteria (PGPR) on chrysanthemum growth in pot experiments. Plant growth parameters, including root length, stem length, total plant height, stem diameter, leaf length, leaf width, fresh weight, and dry weight, were evaluated following treatments with Bacillus cereus (PGPR-13), Acinetobacter oleivorans (PGPR-14), Staphylococcus epidermidis (PGPR-15), Pantoea dispersa (PGPR-24), Serratia nematodiphila (PGPR-27), Pantoea anthophila (PGPR-34), and their consortium. A. oleivorans and the consortium achieved the most significant increases in growth and biomass compared to untreated controls. Data are expressed as mean ± standard error (n = 3 replicates), with ** indicating statistically significant differences (Dunnett’s test, P ≤ 0.05).
PGPR-mediated enhancement of stem, root and overall plant growth
The application of PGPR isolates significantly influenced the growth of chrysanthemum plants. Stem length was notably enhanced in plants treated with PGPR-14, which achieved 71.17 cm - a 114% increase compared to the control (33.2 cm, p < 0.05). The consortium also demonstrated notable improvement (57.07 cm), whereas PGPR-27 and PGPR-34 showed moderate effects, with lengths of 41.17 cm and 36.1 cm, respectively. Similarly, root growth exhibited a positive trend across most PGPR-treated groups, although the differences observed between treatments and the control were not highly significant. PGPR-14 treatment led to the longest roots (26.1 cm), followed by the consortium (24.2 cm). The untreated control displayed a root length of 18.5 cm, indicating limited growth compared to treated plants. Total plant height, calculated from the root and stem length, was most enhanced in PGPR-14-treated plants (97.27 cm), representing an 88% increase over the control (51.7 cm, p < 0.05). The consortium treatment also performed significantly well, with a total plant height of 81.27 cm, also exceeding other treatments.
Effect of PGPR on plant morphological traits
Stem diameter was significantly influenced by PGPR application. Plants treated with the consortium exhibited the largest stem diameter (1.09 cm), nearly twice that of the control (0.61 cm; p < 0.0001). PGPR-14 also induced a notable increase in stem diameter, reaching 0.85 cm. Other treatments, including PGPR-23 and PGPR-34, also showed improvements in stem diameter, though these differences were relatively less pronounced. Leaf length and width showed minimal variation among the treatments. While plants treated with PGPR isolates displayed slightly longer and wider leaves compared to the control, these differences were not statistically significant. Nevertheless, PGPR-14 resulted in the longest leaves (9.62 cm), while the consortium-treated plants showed moderately enhanced lengths (8.36 cm). Leaf width was greatest in plants treated with PGPR-13 (6.69 cm) and the consortium (6.11 cm), compared to the control (4.76 cm).
Effect of PGPR on plant biomass
Both fresh and dry plant weights exhibited noticeable variation across treatments. The PGPR-24 -treated plants recorded the highest fresh weight (88.25 g), followed by consortium (87.75 g) and PGPR-14 (68.38 g). In contrast, the control plants showed a significantly lower fresh weight (47.91 g). Dry weights followed a similar trend, with the highest dry weight observed in consortium-treated plants (33.03 g), significantly exceeding the control (11.61 g). PGPR-24 and PGPR-14 also showed substantial improvement, with weights of 27.08 g and 20.84 g, respectively, indicating a potential enhancement in biomass accumulation due to PGPR application.
PGPR effects on chrysanthemum growth in field trial
The field trial corroborated the findings of the pot experiment, demonstrating significant improvements in chrysanthemum plant growth following inoculation with PGPR isolates and their consortium. The evaluated growth parameters - stem length, root length, total plant growth, stem diameter, leaf size, and plant weight - highlighted the positive effects of specific bacterial treatments compared to the control and E. coli-treated plants.
Figure 2. Impact of Plant Growth-Promoting Rhizobacteria (PGPR) isolates and consortium on chrysanthemum growth in field trials. Field trial treatments included Bacillus cereus (PGPR-13), Acinetobacter oleivorans (PGPR-14), Staphylococcus epidermidis (PGPR-15), Pantoea dispersa (PGPR-24), Serratia nematodiphila (PGPR-27), Pantoea anthophila (PGPR-34), and their consortium. Key growth metrics, including stem length, root length, total plant height, stem diameter, leaf length and width, fresh weight, and dry weight, were assessed. The consortium treatment consistently achieved the greatest improvements in growth and biomass accumulation, outperforming individual PGPR isolates across most parameters. Data are presented as mean ± standard error (n = 3 replicates), with *, **, and **** indicating significant differences (Dunnett’s test, P ≤ 0.05).
PGPR on stem, root and overall growth of chrysanthemum plants in field trials
The consortium-treated plants exhibited the most pronounced increase in stem length, with an average of 75.33 cm, representing a substantial improvement over the control (39.67 cm) and E. coli-treated plants. Among the individual strains, PGPR-27 (50.7 cm), PGPR-14 (49 cm), PGPR-15 (45.7 cm), and PGPR-24 (45.7 cm) also promoted stem growth significantly compared to the control. Similar trends were observed in root length, where the consortium-treated plants achieved the highest root elongation (31.73 cm), followed by PGPR-14 (30.33 cm) and PGPR-15 (29.83 cm), compared to the control (25.73 cm). Total plant growth, measured as the sum of stem and root lengths, was most notable in the consortium-treated group (107.07 cm), which exhibited a substantial increase over the control (65.40 cm). Among individual treatments, PGPR-27 (80.33 cm), PGPR-14 (79.33 cm), and PGPR-15 (75.50 cm) demonstrated enhanced growth, further validating their plant growth-promoting potential.
PGPR effects on stem diameter and leaf size
Stem diameter was significantly influenced by the treatments. The consortium-treated plants exhibited the largest stem diameter (1.37 cm), comparable to PGPR-14 (1.37 cm) and PGPR-15 (1.50 cm), which were significantly greater than the control (0.96 cm) and E. coli-treated plants (0.97 cm). No significant variations in leaf length or width were observed among the treatments. All PGPR-treated plants showed comparable leaf sizes to the control, indicating that leaf dimensions may be less responsive to PGPR application compared to other growth parameters.
PGPR role in plant biomass enhancement
In terms of biomass accumulation, the consortium-treated plants exhibited the highest fresh and dry weights, with mean values of 512 g and 284.33 g, respectively. Among the individual treatments, PGPR-15 and PGPR-27 significantly enhanced biomass production, with fresh and dry weights of 392.33 g and 166.33 g for PGPR-15, and 390.67 g and 175.67 g for PGPR-27. PGPR-14 also demonstrated notable efficacy, with fresh and dry weights of 388.33 g and 236.67 g, respectively. In contrast, the control plants showed the lowest biomass, with fresh and dry weights of 301 g and 167.67 g, respectively.
This study evaluated the effects of PGPR strains and their consortium on chrysanthemum plants under pot and field conditions. The findings demonstrated significant enhancements in stem growth, biomass accumulation, and root development, particularly with specific strains such as PGPR-14 (A. oleivorans), PGPR-15 (S. epidermidis), PGPR-27 (S. nematodiphila), and the bacterial consortium.
PGPR-influence on growth and structural development
Notable increases in stem length and root length were observed, particularly in plants treated with PGPR-14 and the consortium. These findings align with previous studies attributing the growth-promoting effects of PGPR to traits such as auxin production, phosphate solubilization, and stress tolerance. PGPR-14 (A. oleivorans) consistently exhibited the highest improvements across multiple growth parameters, including root and shoot elongation and biomass accumulation, both in pot and field trials. Species from the genus Acinetobacter are well-documented for their nutrient mobilization and stress mitigation mechanisms, enhancing shoot and root biomass effectively [21–23]. Stem diameter, a key structural growth parameter, was also significantly influenced by PGPR treatments, with the consortium and PGPR-15 (S. epidermidis) demonstrating the most pronounced effects. Enhanced stem thickness could result from improved nutrient uptake and hormonal signaling induced by PGPR [24]. This aligns with reports where PGPR strains, including Bacillus cereus, enhanced stem girth and shoot development in crops such as chili pepper, watermelon, cucumber, and eggplant [25]. Additionally, biomass accumulation, both fresh and dry weight, was significantly improved by PGPR treatments, with the consortium outperforming most single-strain treatments except for PGPR-14. The synergistic effects of multiple bacterial strains in the consortium likely contributed to this improvement by promoting nutrient solubilization, stress resilience, and metabolic efficiency [26, 27]. Leaf size parameters (length and width), however, showed minimal variation across treatments. This corroborates previous studies that reported limited effects of PGPR on leaf dimensions but significant impacts on root elongation, shoot growth, and yield-related traits [28].
Superior growth effect of A. oleivorans and the consortium
A. oleivorans (PGPR-14) consistently demonstrated significant plant growth-promoting effects across experimental conditions. Known for efficient phosphate solubilization, auxin production, and stress tolerance, Acinetobacter species have been shown to enhance root and shoot growth in crops such as wheat, mung bean, and fenugreek [29]. The bacterial consortium also demonstrated remarkable growth-promoting effect, particularly under field conditions. This can be due to the complementary PGP traits of its constituent strains, collectively enhancing plant growth [27].
Interestingly, the consortium, despite including PGPR-14, sometimes displayed slightly lower effects compared to PGPR-14 alone, potentially due to factors such as microbial competition, resource limitations, or inhibitory metabolites produced during co-inoculation. Certain microbes within the consortium may exhibit antimicrobial activity [30, 31], which may have also played a role, potentially reducing overall plant growth-promoting efficiency of the consortium compared to PGPR-14 alone. Similar observations have been reported in studies involving Bacillus subtilis, where interactions with other strains occasionally reduced its PGP efficiency [32]. Further investigation into the synergistic and antagonistic interactions within PGPR consortia, guided by functional genomic and metagenomic analyses [33, 34], could uncover mechanisms of synergism or competition within microbial communities [35], providing deeper insights into their dynamics and optimizing their application in agricultural systems.
PGPR-24 (P. dispersa) demonstrated better outcomes than PGPR-34 (P. anthophila), highlighting variability in growth-promoting traits within the same genus. The genus Pantoea is known for its versatile PGP traits, including auxin production, phosphate solubilization, and stress adaptation, which aid in nutrient mobilization and root colonization [4]. However, P. dispersa’s superior field performance suggests an adaptive advantage in complex microbial communities, emphasizing the importance of studying PGPR diversity and niche specificity. Other effective strains, such as PGPR-27 (S. nematodiphila) and PGPR-15 (S. epidermidis), also significantly promoted plant growth. Both Serratia and Staphylococcus species are recognized for producing indole acetic acid (IAA), ammonia, and siderophores, which enhance root elongation, nutrient acquisition, and stress tolerance [36, 37].
Comparison between pot and field trials
The field trial outcomes largely validated the findings from pot experiments, with significant growth improvements achieved in both settings. However, the magnitude of growth promotion was generally higher in the field trial, particularly in the consortium-treated plants. This difference is likely due to the natural soil environment in field conditions, which may support better root establishment, microbial adaptation, and nutrient exchange. Similar results have been reported in studies involving chickpea and wheat, where PGPR effects were more pronounced under field conditions [38, 39]. The results also highlight the resilience of PGPR treatments under varying environmental conditions. Despite environmental challenges during the pot experiments, such as storm events, PGPR-treated plants demonstrated significant improvements over the control. This demonstrates the efficacy of PGPR strains in promoting plant growth under suboptimal conditions, emphasizing their potential application in practical agricultural settings.
Study limitations and practical implications
Despite efforts to maintain uniformity in nursery seedlings, slight variability among them cannot be entirely ruled out. Additionally, environmental factors, such as unexpected storms during the pot experiments, may have influenced the observed plant growth outcomes. Conducting trials in controlled greenhouse environments could help minimize these external variables. Nevertheless, the validation of PGPR effects in natural field conditions, as demonstrated in this study, remains essential for their practical agricultural application. The observed improvements in growth, biomass, and resilience emphasize PGPR’s potential as sustainable alternatives to chemical fertilizers. By improving nutrient availability and promoting stress tolerance, PGPR offer a promising, eco-friendly approach to increasing crop productivity while simultaneously reducing the environmental impact of conventional farming practices.
Conclusion and future perspectives
This study highlights the effectiveness of PGPR isolates, particularly A. oleivorans PGPR-14, S. nematodiphila PGPR-27, and S. epidermidis PGPR-15, in enhancing chrysanthemum growth. The consortium demonstrated synergistic effects, further enhancing plant growth and biomass accumulation. Future studies should focus on optimizing PGPR consortia to minimize microbial competition and maximize synergistic effects. Investigating the molecular mechanisms underlying PGPR-mediated growth promotion, along with their impact on diverse plant species, will provide deeper insights into their potential for sustainable agriculture.
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The authors thank the members of the Laboratory for Health, Omics and Pathway Exploration (HOPE Lab) and the Laboratory of Public Health and Environmental Research for their various support in this study.
This study was supported by a grant from the University of Chittagong to TJH.
The authors have no competing interests to declare.
TJH planned, designed and supervised this study. ANMSZ, MMA, NI, and IUC performed experiments. MRH provided administrative support, and co-supervised the study. ANMSZ carried out data analysis. TJH wrote the manuscript with assistance from ANMSZ. All authors approved the submitted manuscript.
This research investigates the role of plant growth-promoting rhizobacteria (PGPR) in enhancing chrysanthemum growth and biomass production. The study evaluates the effects of PGPR strains such as Acinetobacter oleivorans, Staphylococcus epidermidis, Pantoea dispersa, Bacillus cereus, Serratia nematodiphila, and Pantoea anthophila, individually and as a consortium, on root elongation, shoot growth, total plant height, stem diameter, and overall biomass accumulation. Pot and field trials demonstrate the potential of PGPR as sustainable biofertilizers to boost chrysanthemum cultivation. The findings highlight the significance of PGPR in improving agricultural productivity through environmentally friendly methods, promoting root and shoot development, enhancing plant morphological traits, and increasing fresh and dry weights. This work underscores the importance of biological stimulants in sustainable agriculture and floriculture.
Research keywords: PGPR, chrysanthemum growth, biomass production, plant growth-promoting bacteria, biofertilizers, root and shoot development, sustainable agriculture, floriculture, pot and field trials, microbial consortium.
