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Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: closed (31 July 2024) | Viewed by 25917

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Dr. Odair Alberton

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Postgraduate Program in Biotechnology Applied to Agriculture, Paranaense University, Umuarama 87502-210, PR, Brazil
Interests: plant growth promoting bacteria

Prof. Dr. Galdino Andrade

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Department of Microbiology, Biological Sciences Center, State University of Londrina, Londrina 86057-970, PR, Brazil
Interests: soil ecology; mycorrhiza; rhizophere; biological control
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Dear Colleagues,

We are faced with increasing demand for food from an ever-growing world population and over one-third of the world’s crop yields are lost due to pests, diseases, and environmental stresses. To promote agricultural production in a sustainable way, i.e., to reduce the negative impact of agrochemicals, it is very important to exploit the functions of plant-associated microbes, such as plant growth-promoting bacteria (PGPB) and Mycorrhizal fungi. The plant microbiome may increase the genetic potential of its host, triggers the plant’s immune system, improves nutrient acquisition capacity and root architecture, and enhances environmental stress tolerance. An important part of the plant microbiome includes plant growth-promoting bacteria (PGPB), which can reside in the rhizosphere and phyllosphere or can colonize the plant’s interior tissues (endophytic bacteria). PGPB may promote plant growth directly by facilitating nutrient acquisition or modulating hormone levels or indirectly by reducing the negative effects of pathogens on plant growth and development.

In plants, mycorrhizal fungi play a fundamental role in maintaining the optimal vegetative state and in limiting damage from both stress and parasites. Mycorrhizal fungi acting as a physical barrier against root pathogens, produce several organic compounds that are able to interfere with the pathogenicity of bacteria and fungi at the soil level and beyond. Additionally, mycorrhizal fungi have been shown to play an important role in containing the damage from pathogens and pests, albeit with different mechanisms and improve the nutrient acquisition capacity of the plants. This Special Issue of Plants will highlight the activity of PGPB and mycorrhizal fungi in the biological control of plant parasites (pathogens and pests) and as biostimulate, agents, aiming to find applications in agriculture and environmental sustainability

Dr. Odair Alberton
Prof. Dr. Galdino Andrade
Guest Editors

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Keywords

abiotic and biotic stresses
arbuscular mycorrhiza
biocontrol
bioinoculants
biological control
biostimulate agents
mycorrhizal symbiosis
PGPB
plant–microbe interactions

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Published Papers (10 papers)

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13 pages, 3720 KiB

Open AccessArticle

Isolation and Plant Growth Promotion Effect of Endophytic Siderophore-Producing Bacteria: A Study on Halophyte Sesuvium portulacastrum

by Xinyi Cen, Hua Li, Yanhua Zhang, Lingfeng Huang and Yuanrong Luo

Plants 2024, 13(19), 2703; https://doi.org/10.3390/plants13192703 - 27 Sep 2024

Cited by 4 | Viewed by 1480

Abstract

The objective of the present study was to isolate endophytes from the roots of the halophyte Sesuvium portulacastrum, which is applied for aquatic phytoremediation. From these endophytes, siderophore-producing bacteria were specifically isolated for their potential capacity to promote plant growth. The siderophore production capacity of the isolated bacteria was quantified, and a high-yield siderophore-producing strain was selected for further investigation. A total of 33 endophytic bacteria were successfully isolated and identified using a culturable approach. Of these, 10 siderophore-producing bacteria were identified using the selective agar assay, displaying siderophore unit (SU) values ranging from 11.90% to 80.39%. It is noteworthy that Erwinia sp. QZ-E9 exhibited the highest siderophore production capacity, achieving an SU of 80.39%. A microcosm co-cultivation experiment was conducted with the strain QZ-E9 in iron-deficient conditions (2 μmol/L Fe³⁺). The results demonstrated that strain QZ-E9 significantly enhanced the growth of S. portulacastrum, by increases in both fresh weight (1.41 g) and root length (18.7 cm). Furthermore, fluorescence in situ hybridization (FISH) was utilized to ascertain the colonization pattern of strain QZ-E9 within the plant roots. The analysis demonstrated that strain QZ-E9 exhibited extensive colonization of the epidermal and outer cortical cells of S. portulacastrum roots, as well as the intercellular spaces and vascular tissues. This colonization indicated that Erwinia sp. QZ-E9 plays a crucial role in promoting the growth of S. portulacastrum, presumably through its siderophore-mediated iron acquisition mechanism. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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19 pages, 2263 KiB

Open AccessArticle

Improving Beneficial Traits in Bacillus cabrialesii subsp. cabrialesii TE3^T through UV-Induced Genomic Changes

by Pamela Helué Morales Sandoval, María Edith Ortega Urquieta, Valeria Valenzuela Ruíz, Kevin Montañez Acosta, Kevin Alejandro Campos Castro, Fannie I. Parra Cota, Gustavo Santoyo and Sergio de los Santos Villalobos

Plants 2024, 13(18), 2578; https://doi.org/10.3390/plants13182578 - 14 Sep 2024

Cited by 3 | Viewed by 1803

Abstract

It is essential to hunt for new technologies that promote sustainable practices for agroecosystems; thus, the bioprospecting of beneficial microorganisms complementing with mutation induction techniques to improve their genomic, metabolic, and functional traits is a promising strategy for the development of sustainable microbial inoculants. Bacillus cabrialesii subsp. cabrialesii strain TE3^T, a previously recognized plant growth-promoting and biological control agent, was subjected to UV mutation induction to improve these agro-biotechnological traits. Dilutions were made which were spread on Petri dishes and placed under a 20 W UV lamp at 10-min intervals for 60 min. After the UV-induced mutation of this strain, 27 bacterial colonies showed morphological differences compared to the wild-type strain; however, only a strain named TE3^T-UV25 showed an improvement in 53.6% of the biocontrol against Bipolaris sorokiniana vs. the wild-type strain, by competition of nutrient and space (only detected in the mutant strain), as well as diffusible metabolites. Furthermore, the ability to promote wheat growth was evaluated by carrying out experiments under specific greenhouse conditions, considering un-inoculated, strain TE3^T, and strain TE3^T-UV25 treatments. Thus, after 120 days, biometric traits in seedlings were quantified and statistical analyses were performed, which showed that strain TE3^T-UV25 maintained its ability to promote wheat growth in comparison with the wild-type strain. On the other hand, using bioinformatics tools such as ANI, GGDC, and TYGS, the Overall Genome Relatedness Index (OGRI) and phylogenomic relationship of mutant strain TE3^T-UV25 were performed, confirming that it changed its taxonomic affiliation from B. cabrialesii subsp. cabrialesii to Bacillus subtilis. In addition, genome analysis showed that the mutant, wild-type, and B. subtilis strains shared 3654 orthologous genes; however, a higher number of shared genes (3954) was found between the TE3^T-UV25 mutant strain and B. subtilis 168, while the mutant strain shared 3703 genes with the wild-type strain. Genome mining was carried out using the AntiSMASH v7.0 web server and showed that mutant and wild-type strains shared six biosynthetic gene clusters associated with biocontrol but additionally, pulcherriminic acid cluster only was detected in the genome of the mutant strain and Rhizocticin A was exclusively detected in the genome of the wild-type strain. Finally, using the PlaBase tool, differences in the number of genes (17) associated with beneficial functions in agroecosystems were detected in the genome of the mutant vs. wild-type strain, such as biofertilization, bioremediation, colonizing plant system, competitive exclusion, phytohormone, plant immune response stimulation, putative functions, stress control, and biocontrol. Thus, the UV-induced mutation was a successful strategy to improve the bioactivity of B. cabrialesii subsp. cabrialesii TE3^T related to the agro-biotecnology applications. The obtained mutant strain, B. subtilis TE3^T-UV25, is a promising strain to be further studied as an active ingredient for the bioformulation of bacterial inoculants to migrate sustainable agriculture. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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15 pages, 1150 KiB

Open AccessArticle

Growth and Phytochemistry of Cymbopogon citratus Stapf Inoculated with Plant Growth-Promoting Bacteria under Different Lead Levels

by Rayane Monique Sete da Cruz, Henrique Ferreira, Jonas Marcelo Jaski, Marcelo Coelho Esperança Vieira, Mariana Moraes Pinc, Silvia Graciele Hülse de Souza and Odair Alberton

Plants 2024, 13(7), 944; https://doi.org/10.3390/plants13070944 - 25 Mar 2024

Cited by 2 | Viewed by 2066

Abstract

This study aimed to investigate the phytochemistry of lemongrass (Cymbopogon citratus) inoculated with Azospirillum brasilense and grown in lead (Pb)-contaminated soil to assess its responses to inoculation under different Pb levels. The experimental design was completely randomized in a 2 × 5 factorial scheme: two levels of A. brasilense (absence or presence) and five Pb levels. After four months of treatment, the following were analyzed: total and reducing sugars, total phenolic content, flavonoids, antioxidant activity, antioxidant enzymes, proline, and essential oil (EO) content and composition. Soil Pb levels and A. brasilense inoculation affected phytochemicals in lemongrass plants. Azospirillum inoculation reduced total sugars in the roots at all soil Pb levels, while increasing Pb levels favored a rise in sugar contents. There was an increase in flavonoid content in treatments associated with Pb and inoculated with A. brasilense. Antioxidant capacity was lower at lower Pb levels, regardless of bacterial inoculation. Enzymatic response was mainly affected by Pb concentrations between 50 and 100 mg kg⁻¹ soil. EO content was influenced by soil Pb levels, with higher EO production at 500 mg Pb kg⁻¹ soil and without A. brasilense inoculation. Overall, lemongrass cultivation in Pb-contaminated areas can be an alternative to phytoremediation and EO production for the industry. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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17 pages, 3938 KiB

Open AccessArticle

Characterization of Rhizosphere Microbial Diversity and Selection of Plant-Growth-Promoting Bacteria at the Flowering and Fruiting Stages of Rapeseed

by Mengjiao Wang, Haiyan Sun and Zhimin Xu

Plants 2024, 13(2), 329; https://doi.org/10.3390/plants13020329 - 22 Jan 2024

Cited by 2 | Viewed by 2786

Abstract

Plant rhizosphere microorganisms play an important role in modulating plant growth and productivity. This study aimed to elucidate the diversity of rhizosphere microorganisms at the flowering and fruiting stages of rapeseed (Brassica napus). Microbial communities in rhizosphere soils were analyzed via high-throughput sequencing of 16S rRNA for bacteria and internal transcribed spacer (ITS) DNA regions for fungi. A total of 401 species of bacteria and 49 species of fungi in the rhizosphere soil samples were found in three different samples. The composition and diversity of rhizosphere microbial communities were significantly different at different stages of rapeseed growth. Plant-growth-promoting rhizobacteria (PGPRs) have been widely applied to improve plant growth, health, and production. Thirty-four and thirty-one PGPR strains were isolated from the rhizosphere soil samples collected at the flowering and fruiting stages of rapeseed, respectively. Different inorganic phosphorus- and silicate-solubilizing and auxin-producing capabilities were found in different strains, in addition to different heavy-metal resistances. This study deepens the understanding of the microbial diversity in the rapeseed rhizosphere and provides a microbial perspective of sustainable rapeseed cultivation. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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14 pages, 10683 KiB

Open AccessArticle

Employing a Plant Probiotic Actinomycete for Growth Promotion of Lettuce (Lactuca sativa L. var. longifolia) Cultivated in a Hydroponic System under Nutrient Limitation

by Benyapa Kitwetch, Pharada Rangseekaew, Yupa Chromkaew, Wasu Pathom-Aree and Sirasit Srinuanpan

Plants 2023, 12(22), 3793; https://doi.org/10.3390/plants12223793 - 7 Nov 2023

Cited by 8 | Viewed by 3424

Abstract

The consumption of lettuce is associated with an increased risk of ingesting nitrate, a naturally occurring and potentially harmful compound that can have adverse effects on human health. Hydroponic cultivation systems serve as effective tools for regulating nutrient solutions and nitrogen availability, which are essential for controlling nitrate levels. However, the techniques for reducing nutrient levels need to be appropriately calibrated based on lettuce growth responses and their interactions with the environment and growing conditions. Previous studies have demonstrated that plant probiotic actinomycetes can alleviate nutritional stress in various crops. However, there is a noticeable gap in research concerning the effects of actinomycetes on hydroponically grown lettuce, particularly under nutrient-limiting conditions. This study aimed to evaluate the effectiveness of the actinomycete Streptomyces thermocarboxydus S3 in enhancing lettuce growth in a nutrient-restricted hydroponic system. The results indicated that the detrimental effects of nutrient stress on lettuce were mitigated by the inoculation of lettuce with S. thermocarboxydus S3. This mitigation was evident in various growth parameters, including leaf count, shoot length, and the fresh and dry weights of both shoots and roots. In the presence of nutritional stress, S. thermocarboxydus S3 likely mitigated the negative effects on lettuce by reducing hydrogen peroxide levels, presumably through the synthesis of H₂O₂-scavenging enzymes. Furthermore, S. thermocarboxydus S3 successfully survived and colonized lettuce roots. Therefore, the inoculation of lettuce with S. thermocarboxydus S3 offers significant advantages for promoting lettuce growth in nutrient-limited hydroponic systems. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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12 pages, 1057 KiB

Open AccessArticle

Impact Assessment of Lead-Tolerant Rhizobacteria to Improve Soil Health Using Indian Mustard (Brassica juncea) as an Indicator Plant

by Zain Mushtaq, Adnan Akhter, Hafiz Azhar Ali Khan, Waheed Anwar, Abeer Hashem, Graciela Dolores Avila-Quezada and Elsayed Fathi Abd_Allah

Plants 2023, 12(16), 3005; https://doi.org/10.3390/plants12163005 - 21 Aug 2023

Cited by 3 | Viewed by 2076

Abstract

Due to ongoing human activities, heavy metals are heavily accumulated in the soil. This leads to an increase in the discharge and the quick spread of heavy metal pollution in human settlements and natural habitats, having a disastrous effect on agricultural products. The current experiment was planned to evaluate the effect of lead-tolerant-plant-growth-promoting rhizobacteria (LTPGPR) on growth, yield, antioxidant activities, physiology, and lead uptake in the root, shoot, and seed of Indian mustard (Brassica juncea) in lead-amended soil. Three pre-isolated well-characterized lead-tolerant rhizobacterial strains—S10, S5, and S2—were used to inoculate seeds of Indian mustard grown at three different levels of lead (300 mg kg⁻¹, 600 mg kg⁻¹, 900 mg kg⁻¹) contaminated soil. The experiment was designed following a completely randomized design (CRD) under factorial arrangements. Lead nitrate was used as a source of lead contamination. At harvesting, data regarding growth, physiology, yield per plant, antioxidant activities, malondialdehyde and proline content, and lead uptake in the root, shoot, and seed of Indian mustard were recorded. Results demonstrated that lead contamination at all levels significantly reduced the plant growth, yield, and physiological processes. Plants inoculated with lead-tolerant rhizobacteria showed a significant improvement in plant growth, yield, antioxidant activities, and physiological attributes and cause a valuable reduction in the malondialdehyde contents of Indian mustard in lead-contaminated soil. Moreover, plants inoculated with lead-tolerant rhizobacteria also showed an increment in lead uptake in the vegetative parts and a significant reduction of lead contents in the seed of Indian mustard. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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11 pages, 2310 KiB

Open AccessArticle

Mycorrhizal Fungal Effects on Plant Growth, Osmolytes, and CsHsp70s and CsPIPs Expression in Leaves of Cucumber under a Short-Term Heat Stress

by Xin-Ran Liu, Zi-Yi Rong, Xiao Tian, Abeer Hashem, Elsayed Fathi Abd_Allah, Ying-Ning Zou and Qiang-Sheng Wu

Plants 2023, 12(16), 2917; https://doi.org/10.3390/plants12162917 - 11 Aug 2023

Cited by 10 | Viewed by 2557

Abstract

Arbuscular mycorrhizal (AM) fungi enhance plant stress tolerance, but it is unclear whether AM fungi affect heat tolerance in cucumbers. This study aimed to analyze how an AM fungus, Diversispora versiformis, affected growth, chlorophyll, five osmolytes, and plasma membrane intrinsic proteins (PIPs) and heat shock protein 70 (Hsp70) gene expression in cucumber leaves after a short-term (80 h) heat stress. Heat treatment significantly reduced root AM fungal colonization rate (0.26 folds). Heat treatment also distinctly suppressed plant height, stem diameter, and biomass, whereas AM fungal inoculation improved these growth variables as well as the chlorophyll index, with the benefit being more obvious under heat than under no-heat stress conditions. Heat treatment triggered differential changes in osmolytes (sucrose, fructose, and betaine) of inoculated and uninoculated cucumbers, whereas inoculation with AM fungus significantly raised leaf sucrose, fructose, glucose, betaine, and proline levels when compared to non-AM fungal inoculation. Heat treatment increased the expression of two (CsPIP1;6 and CsPIP2;1) of eight CsPIPs in inoculated and uninoculated plants, whereas AM fungal inoculation up-regulated the expression of CsPIP1;6, CsPIP2;1, and CsPIP2;6 under heat stress conditions. Hsp70s expressed differently in inoculated and uninoculated plants under heat versus no-heat stress, with 6 of 11 CsHsp70s down-regulated in inoculated plants. Under heat stress conditions, AM fungus only up-regulated CsHsp70-8 expression in 11 Hsp70s, while another eight CsHsp70s were down-regulated. Heat treatment and AM fungal inoculation both increased the expression of CsHsp70-8 and CsPIP1;6. It was concluded that AM fungus-inoculated cucumbers have high levels of growth, chlorophyll, and osmolytes under heat stress and do not require high CsPIPs and CsHsp70s expression to tolerate a short-term heat treatment. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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15 pages, 7187 KiB

Open AccessArticle

Characterization of Antagonistic Bacteria Paenibacillus polymyxa ZYPP18 and the Effects on Plant Growth

by Xiangying Li, Sujing Ma, Yuan Meng, Wei Wei, Chen Peng, Chunli Ling, Susu Fan and Zhenyu Liu

Plants 2023, 12(13), 2504; https://doi.org/10.3390/plants12132504 - 30 Jun 2023

Cited by 9 | Viewed by 3075

Abstract

Paenibacillus polymyxa is a plant growth–promoting rhizobacteria (PGPR) that has significant biocontrol properties. Wheat sheath blight caused by Rhizoctonia cerealis is a significant soil–borne disease of wheat that causes significant losses in wheat production, and the biological control against the disease has received extensive attention. P. polymyxa ZYPP18 was identified using morphological and molecular characterization. An antagonistic activity experiment verified that ZYPP18 inhibits the growth of R. cerealis on artificial growth media. A detached leaf assay verified that ZYPP18 inhibits the expansion of wheat sheath blight on the detached leaf. ZYPP18 has been found to possess plant growth–promoting properties, as well as the ability to solubilize phosphate and generate indole–3–acetic acid. Results from hydroponic experiments showed that wheat seedlings treated with ZYPP18 grew faster. Additionally, pot experiments and field experiments demonstrated that ZYPP18 effectively controls the occurrence of wheat sheath blight. ZYPP18 reduced the incidence of wheat sheath blight in wheat seedlings by 37.37% and 37.90%, respectively. The control effect of ZYPP18 on wheat sheath blight was 56.30% and 65.57%, respectively. These findings provide evidence that P. polymyxa ZYPP18 is an effective biological factor that can control disease and promote plant growth. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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13 pages, 1452 KiB

Open AccessArticle

Plant-Mediated Effects of Beneficial Microbes and a Plant Strengthener against Spider Mites in Tomato

by Konstantinos Samaras, Soultana Mourtiadou, Theodoros Arampatzis, Myrsini Kakagianni, Maria Feka, Felix Wäckers, Kalliope K. Papadopoulou, George D. Broufas and Maria L. Pappas

Plants 2023, 12(4), 938; https://doi.org/10.3390/plants12040938 - 18 Feb 2023

Cited by 5 | Viewed by 2579

Abstract

The two-spotted spider mite Tetranychus urticae is a polyphagous herbivore with a worldwide distribution, and is a serious pest in tomato and other crops. As an alternative to chemical pesticides, biological control with the release of natural enemies such as predatory mites represent an efficient method to control T. urticae in many crops, but not in tomato. Other biological control agents, such as beneficial microbes, as well as chemical compounds, which can act as plant defense elicitors that confer plant resistance against pests and pathogens, may prove promising biological solutions for the suppression of spider mite populations in tomato. Here, we assessed this hypothesis by recording the effects of a series of fungal and bacterial strains and the plant strengthener acibenzolar-s-methyl for their plant-mediated effects on T. urticae performance in two tomato cultivars. We found significant negative effects on the survival, egg production and spider mite feeding damage on plants inoculated with microbes or treated with the plant strengthener as compared to the control plants. Our results highlight the potential of beneficial microbes and plant strengtheners in spider mite suppression in addition to plant disease control. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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Review

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20 pages, 1182 KiB

Open AccessReview

Microbial Fertilizers: A Study on the Current Scenario of Brazilian Inoculants and Future Perspectives

by Matheus F. L. Andreata, Leandro Afonso, Erika T. G. Niekawa, Julio M. Salomão, Kawany Roque Basso, Maria Clara D. Silva, Leonardo Cruz Alves, Stefani F. Alarcon, Maria Eugenia A. Parra, Kathlen Giovana Grzegorczyk, Andreas Lazaros Chryssafidis and Galdino Andrade

Plants 2024, 13(16), 2246; https://doi.org/10.3390/plants13162246 - 13 Aug 2024

Cited by 2 | Viewed by 2530

Abstract

The increasing need for sustainable agricultural practices, combined with the demand for enhanced crop productivity, has led to a growing interest in utilizing microorganisms for biocontrol of diseases and pests, as well as for growth promotion. In Brazilian agriculture, the use of plant growth-promoting rhizobacteria (PGPR) and plant growth-promoting fungi (PGPF) has become increasingly prevalent, with a corresponding rise in the number of registered microbial inoculants each year. PGPR and PGPF occupy diverse niches within the rhizosphere, playing a crucial role in soil nutrient cycling and influencing a wide range of plant physiological processes. This review examines the primary mechanisms employed by these microbial agents to promote growth, as well as the strategy of co-inoculation to enhance product efficacy. Furthermore, we provide a comprehensive analysis of the microbial inoculants currently available in Brazil, detailing the microorganisms accessible for major crops, and discuss the market’s prospects for the research and development of novel products in light of current challenges faced in the coming years. Full article

(This article belongs to the Special Issue Plant Growth Promoting Bacteria and Mycorrhizas as Biocontrol and Biostimulants Agents)

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