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Cited by 15Mycorrhizal Fungi and Plant InteractionsPlant-Microbe Interactions and ImmunityAgriculture, Plant Science, Crop Management

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Co-inoculation of arbuscular mycorrhizal fungi and Bacillus subtilis enhances morphological traits, growth, and nutrient uptake in maize under limited phosphorus availability

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Severo, Helane Cristina de Andrade Rodrigue, de Santana Arauco, Adriana Miranda, Nunes, Raimundo Wesley Fonseca, Monteiro, Gilnair Nunes, Duarte, Maria Helena Ferreira, da Silva, Allana Pereira Moura, de Castro Ferreira, Adriele, Luz, Milena Rodrigues, de Souza Miranda, Rafael, de Araújo, Ademir Sérgio Ferreira, da Costa, Elaine Martins·2025·Scientific Reports
DOI 10.1038/s41598-025-10038-6PMC PMC12260011
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Abstract

The use of beneficial microorganisms to enhance phosphate fertilizer use efficiency and solubilize residual phosphorus (P) is a promising strategy to improve soil P availability for plants. This study tested the hypothesis that inoculation with arbuscular mycorrhizal fungi, either alone or in combination with Bacillus subtilis, enhances maize growth and optimizes nutrient availability, particularly phosphorus. The experiment was conducted under greenhouse conditions with four replications, following an 8 × 3 factorial design. Treatments included individual inoculations with Bacillus subtilis (IPACC26), Rhizophagus clarus (RJN102A), Claroideoglomus etunicatum (SCT101A), and a commercial inoculant of Rhizophagus intraradices (Rootella BR ULTRA), as well as three co-inoculations (IPACC26 combined with each fungus) and a non-inoculated control. These treatments were combined with three levels of phosphate fertilization (0, 50, and 100% of the recommended P level). Mycorrhizal colonization improved root architecture and increased photosynthetic pigments and uptake of P and other nutrients, resulting in greater plant growth and biomass production. The most pronounced effects were observed in plants inoculated with R. clarus and C. etunicatum, either alone or in combination with B. subtilis, at the 0 and 50% P levels. At 0% P, inoculated plants accumulated significantly more biomass, with root and shoot dry mass up to 3,000% and 680% higher, respectively, than those of uninoculated plants; this effect was associated with a 1,700% increase in shoot P accumulation compared to the control. These findings highlight the potential of these inoculants as biofertilizers for more sustainable and efficient phosphorus management in maize cultivation.

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Fig. 1 Mycorrhizal colonization (A), colonization by hyphae (B), colonization by arbuscules (C), and colonization by vesicles (D) observed in roots of maize plants with different inoculations (Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, Bacillus subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 1 Mycorrhizal colonization (A), colonization by hyphae (B), colonization by arbuscules (C), and colonization by vesicles (D) observed in roots of maize plants with different inoculations (Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, Bacillus subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 2 Soil protein related to easily extractable glomalin (SPRG-EE) from maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 2 Soil protein related to easily extractable glomalin (SPRG-EE) from maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 3 Root length (A), Mean root diameter (B), average number of branches (C), root surface area (D), and root dry mass (E) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 3 Root length (A), Mean root diameter (B), average number of branches (C), root surface area (D), and root dry mass (E) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 4 Plant length (A), number of leaves (B) and basal stem diameter (C), and shoot dry mass (SDM) (D) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis, C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 4 Plant length (A), number of leaves (B) and basal stem diameter (C), and shoot dry mass (SDM) (D) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis, C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 5 Chlorophyll a (A), chlorophyll b (B), total chlorophyll (C), and carotenoid (D) contents, and leaf temperature (E) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 5 Chlorophyll a (A), chlorophyll b (B), total chlorophyll (C), and carotenoid (D) contents, and leaf temperature (E) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 6 Phosphorus accumulation in the shoots (A), in the root (B), and total (C), and phosphorus use efficiency (D) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis, C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.
Fig. 6 Phosphorus accumulation in the shoots (A), in the root (B), and total (C), and phosphorus use efficiency (D) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis, C. etunicatum, and non-inoculated control) and phosphorus levels (0, 50, and 100%). Uppercase letters compare inoculations within each phosphorus level, and lowercase letters compare levels within each inoculation. Means followed by the same letters do not differ significantly by the Scott-Knott test at 5%. ANOVA F values: ** = significant at 5%; ns = not significant.CC BY-NC-ND · PubMed Central
Fig. 7 Principal component analysis (PCA) (A) and cluster dendrogram (B) for variables total phosphorus (P total), phosphorus in shoots (P in shoots), phosphorus in roots (P in roots), shoot dry mass (SDM), plant length (PL), root dry mass (RDM), root length (RL), mean root diameter (MRD), average number of root branches (ANB), specific root surface area (SRA), basal stem diameter (BSD), chlorophyll a, chlorophyll b, total chlorophyll, carotenoids, leaf temperature (LT), and soil protein related to easily extractable glomalin (SPRG-EE) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated treatment) and phosphorus levels (0, 50, and 100%).
Fig. 7 Principal component analysis (PCA) (A) and cluster dendrogram (B) for variables total phosphorus (P total), phosphorus in shoots (P in shoots), phosphorus in roots (P in roots), shoot dry mass (SDM), plant length (PL), root dry mass (RDM), root length (RL), mean root diameter (MRD), average number of root branches (ANB), specific root surface area (SRA), basal stem diameter (BSD), chlorophyll a, chlorophyll b, total chlorophyll, carotenoids, leaf temperature (LT), and soil protein related to easily extractable glomalin (SPRG-EE) of maize plants with different inoculations (Bacillus subtilis, Rootella BR ULTRA, Rhizophagus clarus, Claroideoglomus etunicatum, B. subtilis + Rootella BR ULTRA, B. subtilis + R. clarus, B. subtilis + C. etunicatum, and non-inoculated treatment) and phosphorus levels (0, 50, and 100%).CC BY-NC-ND · PubMed Central

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Metadata

Authors
Severo, H. C. D. A. R., de Santana Arauco, A. M., Nunes, R. W. F., Monteiro, G. N., Duarte, M. H. F., da Silva, A. P. M., de Castro Ferreira, A., Luz, M. R., de Souza Miranda, R., de Araújo, A. S. F., & da Costa, E. M.
Affiliations
Universidade Federal do Piauí (BR)
Corresponding author
da Costa, Elaine Martins
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2025-07-15
Volume
15
Issue
1
Pages
25448-25448
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-025-10038-6
PMC
PMC12260011
OpenAlex
W4412402560
Cited by
15
References
1
Citations by year
2026: 12 · 2025: 3
FWCI
8.11
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycorrhizal Fungi and Plant Interactions
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Agriculture, Plant Science, Crop Management
Keywords
arbuscular mycorrhizal fungi, Bacillus subtilis, co-inoculation, maize, phosphorus limitation, phosphate solubilization, biofertilizers, Rhizophagus clarus, Claroideoglomus etunicatum, Glomus intraradices, mycorrhizal colonization, root architecture, photosynthetic pigments, phosphorus uptake, biomass production
MeSH terms
Nutrients, Bacillus subtilis, Zea mays, Fertilizers, Phosphorus, Soil, Plant Roots, Biomass, Mycorrhizae

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CoChat. (2026). Citation check: Co-inoculation of arbuscular mycorrhizal fungi and Bacillus subtilis enhances morphological traits, growth, and nutrient uptake in maize under limited phosphorus availability. https://app.cochat.ai/papers/10.1038/s41598-025-10038-6
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Severo, H. C. D. A. R., de Santana Arauco, A. M., Nunes, R. W. F., Monteiro, G. N., Duarte, M. H. F., da Silva, A. P. M., de Castro Ferreira, A., Luz, M. R., de Souza Miranda, R., de Araújo, A. S. F., & da Costa, E. M. (2025). Co-inoculation of arbuscular mycorrhizal fungi and Bacillus subtilis enhances morphological traits, growth, and nutrient uptake in maize under limited phosphorus availability. Scientific Reports. https://doi.org/10.1038/s41598-025-10038-6