Symbiotic Associations of Plants with Beneficial Microbes: Perspectives and Challenges for Agronomical Applications

A special issue of Agronomy (ISSN 2073-4395). This special issue belongs to the section "Soil and Plant Nutrition".

Deadline for manuscript submissions: closed (31 October 2019) | Viewed by 58542

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Guest Editor
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università di Torino, V.le Mattioli 25, Torino, Italy
Interests: plant–microbe interaction; arbuscular mycorrhizal fungi; symbiosis; rhizosphere microbiota; plant-growth promoting microorganisms
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Special Issue Information

Dear colleagues,

In the last years the “microbiota” concept has revolutionized our view of the interactions among microbes and the so called “higher organisms”.

Plants, as all the other eukaryotes, live and interact with complex microbial communities. Root symbioses, and more generally the interaction with soil beneficial microbes, have been showed to positively influence plant's health, productivity and tolerance to diverse stresses, both in wild and cultivated conditions.

It is thus not surprising that the interest has risen towards a science-driven use of plant beneficial microrganism as natural fertilizers.

Recent analytical advances such as high throughput genomics and meta -omics, metabolomics, plant phenotyping as well as the development of refined bioinformatic tools allow a better knowledge of beneficial plant microbe interactions in a systems biology perspective.

Despite all these technical progresses, we are still far from an exhaustive understanding of this topic, at the same time so promising and challenging.

The purpose of this Special Issue is to bring togethter the current knowledge on how plant symbioses can be managed to improve plant health. Papers are welcome that describe single case studies, technical advances as well as perspective views, to depict an up-to-date scenario of the potential to turn plant symbiotic interactions into agricultural practices.

Dr. Alessandra Salvioli di Fossalunga
Guest Editor

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Keywords

  • root symbioses
  • plant beneficial microbes
  • microbial inioculants
  • crop productivity
  • biotic stresses
  • abiotic stresses

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Published Papers (9 papers)

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Research

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10 pages, 1596 KiB  
Article
Screening, Identification, and Optimization of Fermentation Conditions of an Antagonistic Endophyte to Wheat Head Blight
by Peigen Zhang, Yongxing Zhu, Dongfang Ma, Wenjie Xu, Jingjing Zhou, Hanwen Yan, Lei Yang and Junliang Yin
Agronomy 2019, 9(9), 476; https://doi.org/10.3390/agronomy9090476 - 22 Aug 2019
Cited by 34 | Viewed by 4400
Abstract
Fusarium Head Blight (FHB, scab) is a destructive fungal disease that causes extensive yield and quality losses in wheat and other small cereals. Biological control of FHB is considered to be an alternative disease management strategy that is environmentally benign, durable, and compatible [...] Read more.
Fusarium Head Blight (FHB, scab) is a destructive fungal disease that causes extensive yield and quality losses in wheat and other small cereals. Biological control of FHB is considered to be an alternative disease management strategy that is environmentally benign, durable, and compatible with other control measures. In this study, to screen antagonistic bacteria with the potential to manage FHB, 113 endophytes were isolated from the stems, leaves, panicles, and roots of wheat. Among them, six strains appeared to effectively inhibit Fusarium graminearum growth and one isolate, XS-2, showed a highly antagonistic effect against FHB. An in vitro antagonistic test of XS-2 on wheat heads confirmed that XS-2 could suppress the disease severity of FHB. The 16S rDNA sequence analysis revealed that XS-2 is a strain of Bacillus amyloliquefaciens. Antagonistic spectrum analyses showed that XS-2 had antagonistic effects against two and four types of cotton and fruit tree pathogens, respectively. The fermentation condition assays showed that glucose and peptone are the most suitable nutrient sources for XS-2, and that the optimal pH value and temperature for fermentation were 7.4 and 28 °C, respectively. Our study indicates that XS-2 has a good antagonistic effect on FHB and lays a theoretical foundation for the application of the strain as a biological agent in the field to control FHB. Full article
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16 pages, 659 KiB  
Article
Biofertilizer Production for Agronomic Application and Evaluation of Its Symbiotic Effectiveness in Soybeans
by Aung Zaw Htwe, Seinn Moh Moh, Kyi Moe and Takeo Yamakawa
Agronomy 2019, 9(4), 162; https://doi.org/10.3390/agronomy9040162 - 27 Mar 2019
Cited by 17 | Viewed by 6758
Abstract
This study was conducted to evaluate the effects of Bradyrhizobium japonicum SAY3-7, Bradyrhizobium elkanii BLY3-8, and Streptomyces griseoflavus P4 on the symbiotic effectiveness of soybeans before biofertilizer production, to produce biofertilizer containing the studied three strains (SAY3-7, BLY3-8, and P4), to test the [...] Read more.
This study was conducted to evaluate the effects of Bradyrhizobium japonicum SAY3-7, Bradyrhizobium elkanii BLY3-8, and Streptomyces griseoflavus P4 on the symbiotic effectiveness of soybeans before biofertilizer production, to produce biofertilizer containing the studied three strains (SAY3-7, BLY3-8, and P4), to test the effectiveness of the biofertilizer on soybean varieties, and to assess the varietal effects and interaction effects between variety and biofertilizer on plant growth, nodulation, nitrogen fixation, nutrient absorption, and seed yield. Nitrogen fixation was measured using the acetylene reduction assay and ureide methods. Contents of nutrients (N, P, K, Ca, and Mg) were also measured to calculate their uptakes. In this study, synergistic effects of nitrogen fixation were induced by combined inoculation with SAY3-7, BLY3-8 and P4 in all tested soybean varieties. Therefore, we assumed that an effective biofertilizer could be produced using these effective bacteria (SAY3-7, BLY3-8, and P4). After making biofertilizer using these effective bacteria, packages were stored at 30 °C. The populations of the bacteria in the biofertilizer were maintained at a density of 1 × 108 colony forming units (cfu) g−1 for P4 and 7 × 109 cells g−1 for Bradyrhizobium. Diluting biofertilizer by 10−3 proved more effective for nodulation and nitrogen fixation than other dilution treatments. Moreover, this biofertilizer significantly promoted plant growth, nodulation, nitrogen fixation, nutrient uptakes, and seed yield in Yezin-3 and Yezin-6 soybean varieties. Yezin-6 is a more efficient variety than Yezin-3 for improved plant growth, nodulation, nitrogen fixation, nutrient absorption, and seed yield. Taken together, the application of an effective biofertilizer and the use of an efficient soybean variety can play important roles in promoting plant growth, nodulation, nitrogen fixation, and higher seed yield. Full article
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19 pages, 2338 KiB  
Article
Mycorrhizal Fungi Enhance Resistance to Herbivores in Tomato Plants with Reduced Jasmonic Acid Production
by Ludovico Formenti and Sergio Rasmann
Agronomy 2019, 9(3), 131; https://doi.org/10.3390/agronomy9030131 - 12 Mar 2019
Cited by 29 | Viewed by 5428
Abstract
Arbuscular mycorrhizal (AM) fungi favor plant growth by improving nutrient acquisition, but also by increasing their resistance against abiotic and biotic stressors, including herbivory. Mechanisms of AM fungal mediated increased resistance include a direct effect of AM fungi on plant vigor, but also [...] Read more.
Arbuscular mycorrhizal (AM) fungi favor plant growth by improving nutrient acquisition, but also by increasing their resistance against abiotic and biotic stressors, including herbivory. Mechanisms of AM fungal mediated increased resistance include a direct effect of AM fungi on plant vigor, but also a manipulation of the hormonal cascades, such as the systemic activation of jasmonic acid (JA) dependent defenses. However, how AM fungal inoculation and variation in the endogenous JA production interact to produce increased resistance against insect herbivores remains to be further elucidated. To address this question, three genotypes of Solanum lycopersicum L., a JA-biosynthesis deficient mutant, a JA over-accumulating mutant, and their wild-type were either inoculated with AM fungi or left un-inoculated. Plant growth-related traits and resistance against Spodoptera littoralis (Boisduval) caterpillars, a major crop pest, were measured. Overall, we found that deficiency in JA production reduced plant development and were the least resistant against S. littoralis. Moreover, AM fungi increased plant resistance against S. littoralis, but such beneficial effect was more pronounced in JA-deficient plant than on JA over-accumulating plants. These results highlight that AM fungi-driven increased plant resistance is negatively affected by the ability of plants to produce JA and that AM fungi complement JA-mediated endogenous plant defenses in this system. Full article
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11 pages, 258 KiB  
Article
Monosporic Inoculation of Economically Important Horticultural Species with Native Endomycorrhizae under Greenhouse Conditions
by Flor S. Hernandez, Rosalinda M. Villarreal, Valentin R. Torres and Adrien Gallou
Agronomy 2019, 9(3), 130; https://doi.org/10.3390/agronomy9030130 - 12 Mar 2019
Viewed by 2600
Abstract
Research into the symbiotic relationship between plants and arbuscular mycorrhizal fungi (AMF) is key for sustainable agricultural intensification. The objective of the present study is to evaluate native AMF at the monosporic level in greenhouse-grown, economically important crops. Agricultural soil samples from three [...] Read more.
Research into the symbiotic relationship between plants and arbuscular mycorrhizal fungi (AMF) is key for sustainable agricultural intensification. The objective of the present study is to evaluate native AMF at the monosporic level in greenhouse-grown, economically important crops. Agricultural soil samples from three locations (Saltillo, Zaragoza, and Parras) were obtained by combining portions resulting from a zigzag sampling pattern. From these samples, 15 morphotypes were extracted according to a modified Gerdemann’s technique and monosporically inoculated on melon, cucumber, tomato, and onion, 30 days after their sowing. Under a completely random experimental design, 16 treatments with three repetitions were defined. Plant height, root length, stem diameter, total fresh weight, fresh root weight, dry root weight, bulb weight, fresh leaf weight, total dry weight, flower number, leaf number, fruit number, spore number, and percentage of colonization were all evaluated. The results were subjected to the analysis of variance (ANOVA) and the Tukey comparison test (p ≤ 0.05), which showed that the monosporic inoculation favors significantly the AMF and the host, while the T6 (Saltillo spore + Steiner modified with 20% of the normal phosphorus concentration) showed a greater response uniformity on onion and melon, which indicates its great potential as an inoculum. Full article
12 pages, 271 KiB  
Article
Effects of Biofertilizer Produced from Bradyrhizobium and Streptomyces griseoflavus on Plant Growth, Nodulation, Nitrogen Fixation, Nutrient Uptake, and Seed Yield of Mung Bean, Cowpea, and Soybean
by Aung Zaw Htwe, Seinn Moh Moh, Khin Myat Soe, Kyi Moe and Takeo Yamakawa
Agronomy 2019, 9(2), 77; https://doi.org/10.3390/agronomy9020077 - 11 Feb 2019
Cited by 95 | Viewed by 16765
Abstract
The use of biofertilizers is important for sustainable agriculture, and the use of nodule bacteria and endophytic actinomycetes is an attractive way to enhance plant growth and yield. This study tested the effects of a biofertilizer produced from Bradyrhizobium strains and Streptomyces griseoflavus [...] Read more.
The use of biofertilizers is important for sustainable agriculture, and the use of nodule bacteria and endophytic actinomycetes is an attractive way to enhance plant growth and yield. This study tested the effects of a biofertilizer produced from Bradyrhizobium strains and Streptomyces griseoflavus on leguminous, cereal, and vegetable crops. Nitrogen fixation was measured using the acetylene reduction assay. Under N-limited or N-supplemented conditions, the biofertilizer significantly promoted the shoot and root growth of mung bean, cowpea, and soybean compared with the control. Therefore, the biofertilizer used in this study was effective in mung bean, cowpea, and soybean regardless of N application. In this study, significant increments in plant growth, nodulation, nitrogen fixation, nitrogen, phosphorus, and potassium (NPK) uptake, and seed yield were found in mung beans and soybeans. Therefore, Bradyrhizobium japonicum SAY3-7 plus Bradyrhizobium elkanii BLY3-8 and Streptomyces griseoflavus are effective bacteria that can be used together as biofertilizer for the production of economically important leguminous crops, especially soybean and mung bean. The biofertilizer produced from Bradyrhizobium and S. griseoflavus P4 will be useful for both soybean and mung bean production. Full article
15 pages, 3204 KiB  
Article
Didymella pinodes Affects N and P Uptakes and Their Efficiencies in a Tripartite Mutualism of Pea
by Getinet Desalegn, Reinhard Turetschek, Stefanie Wienkoop and Hans-Peter Kaul
Agronomy 2019, 9(2), 52; https://doi.org/10.3390/agronomy9020052 - 26 Jan 2019
Cited by 2 | Viewed by 3084
Abstract
In pea (Pisum sativum L.) production, Didymella pinodes (Berk. & A. Bloxam) Petr. is the most damaging aerial pathogen globally. In two completely randomized pot experiments with four replicates, we studied the effects of D. pinodes infection interaction with three symbiotic treatments [...] Read more.
In pea (Pisum sativum L.) production, Didymella pinodes (Berk. & A. Bloxam) Petr. is the most damaging aerial pathogen globally. In two completely randomized pot experiments with four replicates, we studied the effects of D. pinodes infection interaction with three symbiotic treatments (Rhizobium leguminosarum biovar viciae, arbuscular mycorrhizal fungi (AMF) and co-inoculation of both) and a non-symbiotic control on one or two pea cultivars. Grain yield and yield components of pea, uptakes and physiological efficiencies of N and P and nitrogen fixation were recorded. The results show that there were significant interaction effects among treatments. Therefore, productivity of crops and their uptakes and efficiencies of N and P are dependent on plant health conditions, effectiveness of microbial symbionts and response of pea genotypes. For cv. Protecta inoculated with both symbionts, pathogen infection compared to healthy plants significantly enhanced P acquisition. Overall, plants inoculated with rhizobia alone had higher grain yield by 20–30% and nitrogen fixation by 20–25% than in dual symbiosis independent of plant health conditions. In conclusion, aerial pathogen, pea genotypes and microbial symbionts interactions modified N and P uptake and their efficiencies, which can lead to improving final grain yield quantity and quality in a sustainable farming system. Full article
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11 pages, 624 KiB  
Article
Delivery of Inoculum of Rhizophagus irregularis via Seed Coating in Combination with Pseudomonas libanensis for Cowpea Production
by Ying Ma, Aleš Látr, Inês Rocha, Helena Freitas, Miroslav Vosátka and Rui S. Oliveira
Agronomy 2019, 9(1), 33; https://doi.org/10.3390/agronomy9010033 - 15 Jan 2019
Cited by 35 | Viewed by 6755
Abstract
Cowpea (Vigna unguiculata L. Walp) is an important legume grown primarily in semi-arid area. Its production is generally inhibited by various abiotic and biotic stresses. The use of beneficial microorganisms (e.g., plant growth promoting bacteria (PGPB) and arbuscular mycorrhizal fungi (AMF)) can [...] Read more.
Cowpea (Vigna unguiculata L. Walp) is an important legume grown primarily in semi-arid area. Its production is generally inhibited by various abiotic and biotic stresses. The use of beneficial microorganisms (e.g., plant growth promoting bacteria (PGPB) and arbuscular mycorrhizal fungi (AMF)) can enhance agricultural production, as these microorganisms can improve soil fertility and plant tolerance to environmental stresses, thus enhancing crop yield in an eco-friendly manner. Application of PGPB and AMF in large scale agriculture needs to be improved. Thus, the use of seed coating could be an efficient mechanism for placement of inocula into soils. The aim of this study was to evaluate the effects of the AMF Rhizophagus irregularis BEG140 and the PGPB Pseudomonas libanensis TR1 alone or in combination on the biomass and physiological traits of cowpea. Four treatments were set: (i) non-inoculated control; (ii) PGPB; (iii) AMF applied via seed coating; and (iv) PGPB + AMF applied via seed coating. Cowpea plants inoculated via seed coating with R. irregularis and those inoculated with R. irregularis + P. libanensis showed root mycorrhizal colonization of 21.7% and 24.2%, respectively. PGPB P. libanensis was efficient in enhancing plant biomass and seed yield. There was no benefit of single (AMF) or dual (PGPB + AMF) inoculation on plant growth or seed yield. The application of beneficial soil microorganisms can be a viable approach for sustainable cowpea production in precision agriculture scenarios. Full article
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Review

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14 pages, 1852 KiB  
Review
The Effect of Arbuscular Mycorrhizal Fungi on Photosystem II of the Host Plant Under Salt Stress: A Meta-Analysis
by Yingnan Wang, Jinghong Wang, Xiufeng Yan, Shengnan Sun and Jixiang Lin
Agronomy 2019, 9(12), 806; https://doi.org/10.3390/agronomy9120806 - 26 Nov 2019
Cited by 18 | Viewed by 3636
Abstract
As important components of the photosynthetic apparatus, photosystems I (PS I) and II (PS II) are sensitive to salinity. Salt stress can destroy the PS II reaction center, disrupt electron transport from PS II to PS I, and ultimately lead to a decrease [...] Read more.
As important components of the photosynthetic apparatus, photosystems I (PS I) and II (PS II) are sensitive to salinity. Salt stress can destroy the PS II reaction center, disrupt electron transport from PS II to PS I, and ultimately lead to a decrease in the photosynthetic capacity of the plant. Arbuscular mycorrhizal fungi (AMF) can enhance the photosynthetic capacity of a host plant under salinity stress. However, this specific effect of AMF is not always predictable. Here, we conducted a meta-analysis including 436 independent observations to compare chlorophyll fluorescence parameters in response to AMF inoculation under salt stress. The results showed that AMF inoculation had a positive total impact on photosynthesis in the host plant. Subgroup analysis showed that annual host plants had better performance in terms of photosynthesis after inoculation. The mitigating effects of AMF on the photosynthetic rate (Pn), actual quantum yield of photochemical energy conversion in PS II (ɸPS II), and electron transfer rate (ETR) in C4 species were higher than those in C3 species. Moreover, the photosynthesis performance of monocotyledon species was better than that of dicotyledon species after AMF inoculation. The woody host plants had higher energy utilization by way of an enhanced electron transfer rate to reduce energy dissipation after AMF inoculation. Finally, the mitigating effect of AMF on plants under moderate salinity was stronger than that under high salinity. Among AMF species, Funneliformis mosseae was found to be the most effective in enhancing the photosynthesis performance of plants. For the analyzed dataset, AMF inoculation alleviated the detrimental effects of salinity on photosystem II of the host plant by improving the utilization of photons and photosynthetic electron transport, and also by reducing the susceptibility of photosystem II to photoinhibition. Full article
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21 pages, 1501 KiB  
Review
Deciphering the Symbiotic Plant Microbiome: Translating the Most Recent Discoveries on Rhizobia for the Improvement of Agricultural Practices in Metal-Contaminated and High Saline Lands
by Agnese Bellabarba, Camilla Fagorzi, George C. diCenzo, Francesco Pini, Carlo Viti and Alice Checcucci
Agronomy 2019, 9(9), 529; https://doi.org/10.3390/agronomy9090529 - 10 Sep 2019
Cited by 36 | Viewed by 8151
Abstract
Rhizosphere and plant-associated microorganisms have been intensely studied for their beneficial effects on plant growth and health. These mainly include nitrogen-fixing bacteria (NFB) and plant-growth promoting rhizobacteria (PGPR). This beneficial fraction is involved in major functions such as plant nutrition and plant resistance [...] Read more.
Rhizosphere and plant-associated microorganisms have been intensely studied for their beneficial effects on plant growth and health. These mainly include nitrogen-fixing bacteria (NFB) and plant-growth promoting rhizobacteria (PGPR). This beneficial fraction is involved in major functions such as plant nutrition and plant resistance to biotic and abiotic stresses, which include water deficiency and heavy-metal contamination. Consequently, crop yield emerges as the net result of the interactions between the plant genome and its associated microbiome. Here, we provide a review covering recent studies on PGP rhizobia as effective inoculants for agricultural practices in harsh soil, and we propose models for inoculant combinations and genomic manipulation strategies to improve crop yield. Full article
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