Plant Microbiome Augmentation and Stimulation: New Strategies to Grow Crops with Reduced Agrochemicals

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Plant Microbe Interactions".

Deadline for manuscript submissions: closed (30 June 2021) | Viewed by 48898

Special Issue Editors


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Guest Editor
Department of Plant Biology, Rutgers University, New Brunswick, NJ 08901, USA
Interests: microbial endophytes of plants; rhizophagy cycle; plant defensive symbioses; plant nutritional symbioses
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Biotechnological & Environmental Sciences Department, Universidad Autonoma de Guadalajara, Patria 1201, Lomas del Valle, Zapopan 45129, Jalisco, Mexico
Interests: abiotic and biotic stress; bio-inoculants; endophytic bacteria; microbiome modulation; nutrient-transfer symbiosis; reactive oxygen species

Special Issue Information

Dear Colleagues,

There is currently widespread interest in utilizing plant microbiomes in order to manage crops as safe alternatives or supplements to the use of chemical fertilizers and other agrochemicals. Plant microbiome augmentation and stimulation strategies include: (1) promotion of plant growth and health through the addition of microbes (including endophytes, epiphytes, rhizobacteria or mycorrhizae) to the plant microbiome; and (2) use of substances that stimulate microbial activities in plants or in association with plant roots. The use of plant microbiome augmentation and stimulation may allow agriculturists and horticulturists to more sustainably produce crops at a reduced cost with fewer agrochemicals and reduced environmental degradation. An industry is growing that is based on the use of plant microbes in agriculture, with many companies developing products that involve addition of microbes to plants, seeds, or soils around plants, or substances that stimulate the plant microbiome. There is limited understanding of how microbiome augmentation, or stimulation of the plant microbiome, functions to promote plant growth. This Special Issue is intended to increase our understanding of how plant microbiome augmentation and stimulation works and how technologies based on these strategies may be used to improve agricultural practice and production.

Prof. Dr. Miguel Beltran-Garcia
Prof. Dr. James White
Guest Editors

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Keywords

  • Bacillus
  • endophytes
  • epiphytes
  • endophytic fungi
  • mycorrhizae
  • Pseudomonas
  • rhizobacteria

Published Papers (11 papers)

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Editorial

Jump to: Research, Review

3 pages, 182 KiB  
Editorial
Introduction to Special Issue: Plant Microbiome Augmentation and Stimulation—New Strategies to Grow Crops with Reduced Agrochemicals
by Miguel J. Beltran-Garcia and James F. White
Microorganisms 2021, 9(9), 1887; https://doi.org/10.3390/microorganisms9091887 - 06 Sep 2021
Cited by 1 | Viewed by 1547
Abstract
Since the early work of Justus von Liebig on nutrient absorption in plants in the 1800s [...] Full article

Research

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17 pages, 1255 KiB  
Article
Oak (Quercus robur) Associated Endophytic Paenibacillus sp. Promotes Poplar (Populus spp.) Root Growth In Vitro
by Dorotėja Vaitiekūnaitė, Sigutė Kuusienė and Emilija Beniušytė
Microorganisms 2021, 9(6), 1151; https://doi.org/10.3390/microorganisms9061151 - 27 May 2021
Cited by 15 | Viewed by 3568
Abstract
Soil fertilization is necessary for high-demand crop production in agriculture and forestry. Our current dependence on chemical fertilizers has significant harmful side effects. Biofertilization using microorganisms is a sustainable way to limit the need for chemical fertilizers in various enterprises. Most plant endophytic [...] Read more.
Soil fertilization is necessary for high-demand crop production in agriculture and forestry. Our current dependence on chemical fertilizers has significant harmful side effects. Biofertilization using microorganisms is a sustainable way to limit the need for chemical fertilizers in various enterprises. Most plant endophytic bacteria have thus far been unstudied for their plant growth promoting potential and hence present a novel niche for new biofertilizer strains. We isolated English oak (Quercus robur) endophytic bacteria and tested them for plant growth promoting traits (PGPTs) such as nitrogen fixation, phosphate mineralization/solubilization, siderophore and indole-3-acetic acid (IAA) production. We also investigated the effect the selected isolate had on poplar (Populus spp.) microshoot vegetative growth parameters in vitro. In total 48 bacterial strains were isolated, attributed to Bacillus, Delftia, Paenibacillus, Pantoea and Pseudomonas genera. All the isolates displayed at least three PGPTs, with 39.6% of the isolates displaying all five (all were Pseudomonas spp.) and 18.75% displaying four. Based on relative abundance, Paenibacillus sp. isolate was selected for the poplar microshoot inoculation study. The isolate had a significant positive effect on poplar microshoot root growth and development. Two tested poplar genotypes both had increased lateral root number and density, fresh and dry root biomass. Furthermore, one genotype had increased length and number of adventitious roots as well as a decrease in fresh aboveground biomass. The root enhancement was attributed to IAA production. We propose this isolate for further studies as a potential biofertilizer. Full article
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22 pages, 7778 KiB  
Article
Chemical Interactions at the Interface of Plant Root Hair Cells and Intracellular Bacteria
by Xiaoqian Chang, Kathryn L. Kingsley and James F. White
Microorganisms 2021, 9(5), 1041; https://doi.org/10.3390/microorganisms9051041 - 12 May 2021
Cited by 23 | Viewed by 9272
Abstract
In this research, we conducted histochemical, inhibitor and other experiments to evaluate the chemical interactions between intracellular bacteria and plant cells. As a result of these experiments, we hypothesize two chemical interactions between bacteria and plant cells. The first chemical interaction between endophyte [...] Read more.
In this research, we conducted histochemical, inhibitor and other experiments to evaluate the chemical interactions between intracellular bacteria and plant cells. As a result of these experiments, we hypothesize two chemical interactions between bacteria and plant cells. The first chemical interaction between endophyte and plant is initiated by microbe-produced ethylene that triggers plant cells to grow, release nutrients and produce superoxide. The superoxide combines with ethylene to form products hydrogen peroxide and carbon dioxide. In the second interaction between microbe and plant the microbe responds to plant-produced superoxide by secretion of nitric oxide to neutralize superoxide. Nitric oxide and superoxide combine to form peroxynitrite that is catalyzed by carbon dioxide to form nitrate. The two chemical interactions underlie hypothesized nutrient exchanges in which plant cells provide intracellular bacteria with fixed carbon, and bacteria provide plant cells with fixed nitrogen. As a consequence of these two interactions between endophytes and plants, plants grow and acquire nutrients from endophytes, and plants acquire enhanced oxidative stress tolerance, becoming more tolerant to abiotic and biotic stresses. Full article
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16 pages, 1437 KiB  
Article
Native Vineyard Non-Saccharomyces Yeasts Used for Biological Control of Botrytis cinerea in Stored Table Grape
by Antonio Domenico Marsico, Matteo Velenosi, Rocco Perniola, Carlo Bergamini, Scott Sinonin, Vanessa David-Vaizant, Flavia Angela Maria Maggiolini, Alexandre Hervè, Maria Francesca Cardone and Mario Ventura
Microorganisms 2021, 9(2), 457; https://doi.org/10.3390/microorganisms9020457 - 22 Feb 2021
Cited by 14 | Viewed by 2721
Abstract
Postharvest spoilage fungi, such as Botrytis cinerea, are considered the main cause of losses of fresh fruit quality and vegetables during storage, distribution, and consumption. The current control strategy is the use of SO2 generator pads whose application is now largely [...] Read more.
Postharvest spoilage fungi, such as Botrytis cinerea, are considered the main cause of losses of fresh fruit quality and vegetables during storage, distribution, and consumption. The current control strategy is the use of SO2 generator pads whose application is now largely under observation. A high quantity of SO2 can be deleterious for fresh fruits and vegetables and it is not allowed in organic agriculture. For this reason, great attention has been recently focused on identifying Biological Control Agents (BCA) to implement biological approaches devoid of chemicals. In this direction, we carried out our study in isolating five different non-Saccharomyces yeast strains from local vineyards in the South of Italy as possible BCA. We performed both in vitro and in vivo assays in semi-commercial conditions on detached grape berries stored at 0 °C, simulating the temperature normally used during cold storage, and obtained relevant results. We isolated three M. pulcherrima strains and one L. thermotolerans strain able to largely antagonize the development of the B. cinerea, at both in vitro and in vivo conditions. In particular, we detected the ability of the three isolates of M. pulcherrima strains Ale4, N20/006, and Pr7 and the L. thermotolerans strain N10 to completely inhibit (100% in reduction) the mycelial growth of B. cinerea by producing fungistatic compounds. We found, using an extracellular lytic enzymes activity assay, that such activity could be related to lipid hydrolyzation, β-1,3-glucanase and pectinase activity, and pectinase and protease activity, depending on the yeasts used. Results from our in vitro assays allowed us to hypothesize for M. pulcherrima strains Ale4 and N20/006 a possible combination of both the production of soluble metabolites and volatile organic compounds to antagonize against B. cinerea growth. Moreover, in semi-commercial conditions, the M. pulcherrima strain N20/006 and L. thermotolerans strain N10 showed relevant antagonistic effect also at low concentrations (with a significantly reduction of ‘slip skin’ incidence of 86.4% and 72.7%, respectively), thus highlighting a peculiar property to use in commercial development for organic agriculture and the handling process. Full article
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18 pages, 3105 KiB  
Article
A Gnotobiotic Model to Examine Plant and Microbiome Contributions to Survival under Arsenic Stress
by María del Carmen Molina, James F. White, Sara García-Salgado, M. Ángeles Quijano and Natalia González-Benítez
Microorganisms 2021, 9(1), 45; https://doi.org/10.3390/microorganisms9010045 - 26 Dec 2020
Cited by 8 | Viewed by 2556
Abstract
So far, the relative importance of the plant and its microbiome in the development of early stages of plant seedling growth under arsenic stress has not been studied. To test the role of endophytic bacteria in increasing plant success under arsenic stress, gnotobiotic [...] Read more.
So far, the relative importance of the plant and its microbiome in the development of early stages of plant seedling growth under arsenic stress has not been studied. To test the role of endophytic bacteria in increasing plant success under arsenic stress, gnotobiotic seeds of J. montana were inoculated with two endophytic bacteria: Pantoea conspicua MC-K1 (PGPB and As resistant bacteria) and Arthrobacter sp. MC-D3A (non-helper and non-As resistant bacteria) and an endobacteria mixture. In holobiotic seedlings (with seed-vectored microbes intact), neither the capacity of germination nor development of roots and lateral hairs was affected at 125 μM As(V). However, in gnotobiotic seedlings, the plants are negatively impacted by absence of a microbiome and presence of arsenic, resulting in reduced growth of roots and root hairs. The inoculation of a single PGPB (P. conspicua-MCK1) shows a tendency to the recovery of the plant, both in arsenic enriched and arsenic-free media, while the inoculation with Arthrobacter sp. does not help in the recovery of the plants. Inoculation with a bacterial mixture allows recovery of plants in arsenic free media; however, plants did not recover under arsenic stress, probably because of a bacterial interaction in the mixture. Full article
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15 pages, 2615 KiB  
Article
Plant Health and Rhizosphere Microbiome: Effects of the Bionematicide Aphanocladium album in Tomato Plants Infested by Meloidogyne javanica
by Claudia Leoni, Elisabetta Piancone, Nicola Sasanelli, Giovanni Luigi Bruno, Caterina Manzari, Graziano Pesole, Luigi R. Ceci and Mariateresa Volpicella
Microorganisms 2020, 8(12), 1922; https://doi.org/10.3390/microorganisms8121922 - 03 Dec 2020
Cited by 15 | Viewed by 2754
Abstract
The artificial introduction in the soil of antagonistic microorganisms can be a successful strategy, alternative to agrochemicals, for the control of the root-knot nematodes (Meloidogyne spp.) and for preserving plant health. On the other hand, plant roots and the associated rhizosphere constitute [...] Read more.
The artificial introduction in the soil of antagonistic microorganisms can be a successful strategy, alternative to agrochemicals, for the control of the root-knot nematodes (Meloidogyne spp.) and for preserving plant health. On the other hand, plant roots and the associated rhizosphere constitute a complex system in which the contribution of microbial community is fundamental to plant health and development, since microbes may convert organic and inorganic substances into available plant nutrients. In the present study, the potential nematicidal activity of the biopesticide Aphanocladium album (A. album strain MX-95) against the root-knot nematode Meloidogyne javanica in infected tomato plants was investigated. Specifically, the effect of the A. album treatment on plant fitness was evaluated observing the plant morphological traits and also considering the nematode propagation parameters, the A. album MX-95 vitality and population density. In addition, the treatment effects on the rhizosphere microbiome were analysed by a metabarcoding procedure. Treatments with A. album isolate MX-95 significantly decreased root gall severity index and soil nematode population. The treatment also resulted in increased rhizosphere microbial populations. A. album MX-95 can be favourably considered as a new bionematicide to control M. javanica infestation. Full article
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14 pages, 1420 KiB  
Article
Microbiome Management by Biological and Chemical Treatments in Maize Is Linked to Plant Health
by Peter Kusstatscher, Wisnu Adi Wicaksono, Dhivya P. Thenappan, Eveline Adam, Henry Müller and Gabriele Berg
Microorganisms 2020, 8(10), 1506; https://doi.org/10.3390/microorganisms8101506 - 30 Sep 2020
Cited by 15 | Viewed by 3587
Abstract
The targeted application of plant growth-promoting rhizobacteria (PGPR) provides the key for a future sustainable agriculture with reduced pesticide application. PGPR interaction with the indigenous microbiota is poorly understood, but essential to develop reliable applications. Therefore, Stenotrophomonas rhizophila SPA-P69 was applied as a [...] Read more.
The targeted application of plant growth-promoting rhizobacteria (PGPR) provides the key for a future sustainable agriculture with reduced pesticide application. PGPR interaction with the indigenous microbiota is poorly understood, but essential to develop reliable applications. Therefore, Stenotrophomonas rhizophila SPA-P69 was applied as a seed coating and in combination with a fungicide based on the active ingredients fludioxonil, metalaxyl-M, captan and ziram. The plant performances and rhizosphere compositions of treated and non-treated maize plants of two field trials were analyzed. Plant health was significantly increased by treatment; however, overall corn yield was not changed. By applying high-throughput amplicon sequencing of the 16S rRNA and the ITS genes, the bacterial and fungal changes in the rhizosphere due to different treatments were determined. Despite the fact that treatments had a significant impact on the rhizosphere microbiota (9–12%), the field site was identified as the main driver (27–37%). The soil microbiota composition from each site was significantly different, which explains the site-specific effects. In this study we were able to show the first indications how PGPR treatments increase plant health via microbiome shifts in a site-specific manner. This way, first steps towards a detailed understanding of PGPRs and developments of consistently efficient applications in diverse environments are made. Full article
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21 pages, 14566 KiB  
Article
Biological Control of Verticillium Wilt on Olive Trees by the Salt-Tolerant Strain Bacillus velezensis XT1
by David Castro, Marta Torres, Inmaculada Sampedro, Fernando Martínez-Checa, Borja Torres and Victoria Béjar
Microorganisms 2020, 8(7), 1080; https://doi.org/10.3390/microorganisms8071080 - 20 Jul 2020
Cited by 20 | Viewed by 5236
Abstract
Verticillium wilt, caused by the pathogen Verticillium dahliae, is extremely devastating to olive trees (Olea europea). Currently, no successful control measure is available against it. The objective of this work was to evaluate the antifungal activity of Bacillus velezensis XT1, [...] Read more.
Verticillium wilt, caused by the pathogen Verticillium dahliae, is extremely devastating to olive trees (Olea europea). Currently, no successful control measure is available against it. The objective of this work was to evaluate the antifungal activity of Bacillus velezensis XT1, a well-characterized salt-tolerant biocontrol strain, against the highly virulent defoliating V. dahliae V024. In vitro, strain XT1 showed to reduce fungal mycelium from 34 to 100%, depending on if the assay was conducted with the supernatant, volatile compounds, lipopeptides or whole bacterial culture. In preventive treatments, when applied directly on young olive trees, it reduced Verticillium incidence rate and percentage of severity by 54 and ~80%, respectively. It increased polyphenol oxidase (PPO) activity by 395%, indicating an enhancement of disease resistance in plant tissues, and it decreased by 20.2% the number of fungal microsclerotia in soil. In adult infected trees, palliative inoculation of strain XT1 in the soil resulted in a reduction in Verticillium symptom severity by ~63%. Strain XT1 is biosafe, stable in soil and able to colonize olive roots endophytically. All the traits described above make B. velezensis XT1 a promising alternative to be used in agriculture for the management of Verticillium wilt. Full article
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17 pages, 3780 KiB  
Article
Crop Protection against Botrytis cinerea by Rhizhosphere Biological Control Agent Bacillus velezensis XT1
by Laura Toral, Miguel Rodríguez, Victoria Béjar and Inmaculada Sampedro
Microorganisms 2020, 8(7), 992; https://doi.org/10.3390/microorganisms8070992 - 03 Jul 2020
Cited by 33 | Viewed by 5239
Abstract
This study aims to evaluate the use of Bacillus velezensis strain XT1 as a plant growth-promoting rhizobacterium (PGPR) and biocontrol agent against B. cinerea in tomato and strawberry plants. Foliar and radicular applications of strain XT1 increased plant total biomass as compared to [...] Read more.
This study aims to evaluate the use of Bacillus velezensis strain XT1 as a plant growth-promoting rhizobacterium (PGPR) and biocontrol agent against B. cinerea in tomato and strawberry plants. Foliar and radicular applications of strain XT1 increased plant total biomass as compared to the control and B. cinerea-infected plants, with root applications being, on the whole, the most effective mode of treatment. Applications of the bacterium were found to reduce infection parameters such as disease incidence and severity by 50% and 60%, respectively. We analyzed stress parameters and phytohormone content in order to evaluate the capacity of XT1 to activate the defense system through phytohormonal regulation. Overall, the application of XT1 reduced oxidative damage, while the H2O2 and malondialdehyde (MDA) content was lower in XT1-treated and B. cinerea-infected plants as compared to non-XT1-treated plants. Moreover, treatment with XT1 induced callose deposition, thus boosting the response to pathogenic infection. The results of this study suggest that the signaling and activation pathways involved in defense mechanisms are mediated by jasmonic acid (JA) and ethylene hormones, which are induced by preventive treatment with XT1. The study also highlights the potential of preventive applications of strain XT1 to activate defense mechanisms in strawberry and tomato plants through hormone regulation. Full article
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21 pages, 4442 KiB  
Article
Plant Growth Enhancement using Rhizospheric Halotolerant Phosphate Solubilizing Bacterium Bacillus licheniformis QA1 and Enterobacter asburiae QF11 Isolated from Chenopodium quinoa Willd
by Ismail Mahdi, Nidal Fahsi, Mohamed Hafidi, Abdelmounaaim Allaoui and Latefa Biskri
Microorganisms 2020, 8(6), 948; https://doi.org/10.3390/microorganisms8060948 - 24 Jun 2020
Cited by 65 | Viewed by 5961
Abstract
Plant growth-promoting rhizobacteria represent a promising solution to enhancing agricultural productivity. Here, we screened phosphate solubilizing bacteria from the rhizospheric soil of Chenopodium quinoa Willd and assessed their plant-growth promoting rhizobacteria (PGPR) properties including production of indole-3-acetic acid (IAA), siderophores, hydrogen cyanide (HCN), [...] Read more.
Plant growth-promoting rhizobacteria represent a promising solution to enhancing agricultural productivity. Here, we screened phosphate solubilizing bacteria from the rhizospheric soil of Chenopodium quinoa Willd and assessed their plant-growth promoting rhizobacteria (PGPR) properties including production of indole-3-acetic acid (IAA), siderophores, hydrogen cyanide (HCN), ammonia and extracellular enzymes. We also investigated their tolerance to salt stress and their capacity to form biofilms. Two isolated strains, named QA1 and QF11, solubilized phosphate up to 346 mg/L, produced IAA up to 795.31 µg/mL, and tolerated up to 2 M NaCl in vitro. 16S rRNA and Cpn60 gene sequencing revealed that QA1 and QF11 belong to the genus Bacillus licheniformis and Enterobacter asburiae, respectively. In vivo, early plant growth potential showed that quinoa seeds inoculated either with QA1 or QF11 displayed higher germination rates and increased seedling growth. Under saline irrigation conditions, QA1 enhanced plant development/growth. Inoculation with QA1 increased leaf chlorophyll content index, enhanced P and K+ uptake and decreased plant Na+ uptake. Likewise, plants inoculated with QF11 strain accumulated more K+ and had reduced Na+ content. Collectively, our findings support the use of QA1 and QF11 as potential biofertilizers. Full article
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Review

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17 pages, 1430 KiB  
Review
Probiotic Endophytes for More Sustainable Banana Production
by Miguel J. Beltran-Garcia, America Martinez-Rodriguez, Ileana Olmos-Arriaga, Benjamin Valdez-Salas, Yur Y. Chavez-Castrillon, Paolo Di Mascio and James F. White
Microorganisms 2021, 9(9), 1805; https://doi.org/10.3390/microorganisms9091805 - 25 Aug 2021
Cited by 10 | Viewed by 5160
Abstract
Climatic factors and pathogenic fungi threaten global banana production. Moreover, bananas are being cultivated using excessive amendments of nitrogen and pesticides, which shift the microbial diversity in plants and soil. Advances in high-throughput sequencing (HTS) technologies and culture-dependent methods have provided valuable information [...] Read more.
Climatic factors and pathogenic fungi threaten global banana production. Moreover, bananas are being cultivated using excessive amendments of nitrogen and pesticides, which shift the microbial diversity in plants and soil. Advances in high-throughput sequencing (HTS) technologies and culture-dependent methods have provided valuable information about microbial diversity and functionality of plant-associated endophytic communities. Under stressful (biotic or abiotic) conditions, plants can recruit sets of microorganisms to alleviate specific potentially detrimental effects, a phenomenon known as “cry for help”. This mechanism is likely initiated in banana plants infected by Fusarium wilt pathogen. Recently, reports demonstrated the synergistic and cumulative effects of synthetic microbial communities (SynComs) on naturally occurring plant microbiomes. Indeed, probiotic SynComs have been shown to increase plant resilience against biotic and abiotic stresses and promote growth. This review focuses on endophytic bacterial diversity and keystone taxa of banana plants. We also discuss the prospects of creating SynComs composed of endophytic bacteria that could enhance the production and sustainability of Cavendish bananas (Musa acuminata AAA), the fourth most important crop for maintaining global food security. Full article
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