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18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions

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A special issue of Biology (ISSN 2079-7737). This special issue belongs to the section "Plant Science".

Deadline for manuscript submissions: closed (30 November 2023) | Viewed by 29309

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Prof. Dr. Manuel Becana

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Estación Experimental de Aula Dei, Consejo Superior de Investigaciones Científicas (CSIC), 50080 Zaragoza, Spain
Interests: legume nodules; legume-rhizobia symbiosis; nitric oxide; plant hemoglobins (phytoglobins); reactive nitrogen species; reactive oxygen species

Dr. Isabel V. Castro

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Instituto Nacional de Investigação Agrária e Veterinária, 2780-159 Oeiras, Portugal
Interests: rhizobia-legume symbiosis; rhizobia molecular characterization and diversity; biofertilization
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Prof. Dr. Jose Maria Vinardell

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Departamento de Microbiología, Facultad de Biología, Universidad de Sevilla, 41012 Sevilla, Spain
Interests: rhizobia-legume symbiosis; rhizobial molecular signals; regulatory circuits of rhizobial symbiotic genes
Special Issues, Collections and Topics in MDPI journals

Dr. Ana Rincón

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Departamento de Suelo, Planta y Calidad Ambiental, Instituto de Ciencias Agrarias, CSIC, 28080 Madrid, Spain
Interests: mycorrhizal symbiosis; PGPR; selection of inoculants; soil microbial ecology; global change

Special Issue Information

Dear Colleagues,

A wide range of microorganisms live in association with plants, including diazotrophic bacteria, mycorrhizal fungi, plant growth-promoting rhizobacteria (PGPR), and leaf and seed endophytes. These microorganisms, among other beneficial effects, provide the plant with nitrogen and phosphorus in assimilable form, facilitate water uptake, produce plant hormones, and enhance the tolerance of plants to abiotic and biotic stresses. Probably the most well-known beneficial association is the nitrogen-fixing symbiosis between soil rhizobia and legume roots because of its agronomical relevance and its potential to reduce the input of nitrogen fertilizers. However, other symbioses are also very relevant. Mycorrhizal fungi improve the nutrient status of their host plants and actinorhizal plants are used for timber and reclamation of degraded lands. Moreover, there is an upsurge of interest in the study of plant microbiomes and of mechanisms underlying the interactions of plants with fungal and bacterial endophytes because they enhance crop yield.

This Special Issue will comprise original research articles covering physiology, biochemistry, genetics, genomics, evolution and agricultural applications of beneficial microorganisms and of their host symbiotic partners.

Prof. Dr. Manuel Becana
Dr. Isabel Videira e Castro
Prof. Dr. Jose Maria Vinardell
Dr. Ana Rincón
Guest Editors

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Keywords

actinorhizal plants
legumes
microbiome
mycorrhizae
nitrogen fixation
PGPR
rhizobium
symbiosis

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Published Papers (10 papers)

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Research

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20 pages, 4055 KiB

Open AccessArticle

Diversity, Genomics and Symbiotic Characteristics of Sinorhizobia That Nodulate Desmanthus spp. in Northwest Argentina

by Nicolás Emilio Zuber, Laura Viviana Fornasero, Sofía Agostina Erdozain Bagolín, Mauricio Javier Lozano, Juan Sanjuán, María Florencia Del Papa and Antonio Lagares

Biology 2023, 12(7), 958; https://doi.org/10.3390/biology12070958 - 4 Jul 2023

Viewed by 1646

Abstract

Desmanthus spp. are legumes with the ability to associate with diverse α-proteobacteria—a microsymbiont—in order to establish nitrogen-fixing root nodules. A previous investigation from our laboratory revealed that the main bacteria associated with Desmanthus paspalaceus in symbiosis in central Argentina (Province of Santa Fe) were quite diverse and belonged to the genera Rhizobium and Mesorhizobium. To achieve a more extensive view of the local microsymbionts associated with Desmanthus spp., we sampled three different sites in Jujuy and Salta, in northwest Argentina. Matrix-assisted Laser-Desorption-Ionization Time-of-Flight mass spectrometry (MALDI-TOF) typing, 16S-rDNA analysis, and genome sequencing demonstrated that the dominant root-nodule microsymbionts belonged to the genus Sinorhizobium, with some sequenced genomes related to Sinorhizobium mexicanum, Sinorhizobium chiapanecum, and Sinorhizobium psoraleae. An analysis of nodA and nodC markers indicated that, in some of the isolates, horizontal gene transfer appeared to be responsible for the lack of congruence between the phylogenies of the chromosome and of the symbiotic region. These results revealed diverse evolutionary strategies for reaching the current Desmanthus-microsymbiont diversity. What is remarkable beside their observed genetic diversity is that the tolerance profiles of these isolates to abiotic stresses (temperature, salt concentration, pH) were quite coincident with the separation of the sinorhizobia according to place of origin, suggesting possible ecoedaphic adaptations. This observation, together with the higher aerial dry-weight matter that some isolates generated in Desmanthus virgatus cv. Marc when compared to the biomass generated by the commercial strain Sinorhizobium terangae CB3126, distinguish the collected sinorhizobia as constituting valuable germplasm for evaluation in local fields to select for more efficient symbiotic pairs. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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20 pages, 3329 KiB

Open AccessArticle

Physiological and Genetic Modifications Induced by Plant-Growth-Promoting Rhizobacteria (PGPR) in Tomato Plants under Moderate Water Stress

by Jose Antonio Lucas, Ana Garcia-Villaraco, Maria Belen Montero-Palmero, Blanca Montalban, Beatriz Ramos Solano and Francisco Javier Gutierrez-Mañero

Biology 2023, 12(7), 901; https://doi.org/10.3390/biology12070901 - 23 Jun 2023

Cited by 13 | Viewed by 2807

Abstract

Physiological, metabolic, and genetic changes produced by two plant growth promoting rhizobacteria (PGPR) Pseudomonas sp. (internal code of the laboratory: N 5.12 and N 21.24) inoculated in tomato plants subjected to moderate water stress (10% polyethylene glycol-6000; PEG) were studied. Photosynthesis efficiency, photosynthetic pigments, compatible osmolytes, reactive oxygen species (ROS) scavenging enzymes activities, oxidative stress level and expression of genes related to abscisic acid synthesis (ABA; 9-cis-epoxycarotenoid dioxygenase NCDE1 gene), proline synthesis (Pyrroline-5-carboxylate synthase P5CS gene), and plasma membrane ATPase (PM ATPase gene) were measured. Photosynthetic efficiency was compromised by PEG, but bacterial-inoculated plants reversed the effects: while N5.12 increased carbon fixation (37.5%) maintaining transpiration, N21.24 increased both (14.2% and 31%), negatively affecting stomatal closure, despite the enhanced expression of NCDE1 and plasma membrane ATPase genes, evidencing the activation of different adaptive mechanisms. Among all parameters evaluated, photosynthetic pigments and antioxidant enzymes guaiacol peroxidase (GPX) and ascorbate peroxidase (APX) responded differently to both strains. N 5.12 increased photosynthetic pigments (70% chlorophyll a, 69% chlorophyll b, and 65% carotenoids), proline (33%), glycine betaine (4.3%), and phenolic compounds (21.5%) to a greater extent, thereby decreasing oxidative stress (12.5% in Malondialdehyde, MDA). Both bacteria have highly beneficial effects on tomato plants subjected to moderate water stress, improving their physiological state. The use of these bacteria in agricultural production systems could reduce the amount of water for agricultural irrigation without having a negative impact on food production. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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19 pages, 4078 KiB

Open AccessArticle

The T6SS-Dependent Effector Re78 of Rhizobium etli Mim1 Benefits Bacterial Competition

by Bruna Fernanda Silva De Sousa, Lucía Domingo-Serrano, Alvaro Salinero-Lanzarote, José Manuel Palacios and Luis Rey

Biology 2023, 12(5), 678; https://doi.org/10.3390/biology12050678 - 4 May 2023

Cited by 6 | Viewed by 3724

Abstract

The genes of the type VI secretion system (T6SS) from Rhizobium etli Mim1 (ReMim1) that contain possible effectors can be divided into three modules. The mutants in them indicated that they are not required for effective nodulation with beans. To analyze T6SS expression, a putative promoter region between the tssA and tssH genes was fused in both orientations to a reporter gene. Both fusions are expressed more in free living than in symbiosis. When the module-specific genes were studied using RT-qPCR, a low expression was observed in free living and in symbiosis, which was clearly lower than the structural genes. The secretion of Re78 protein from the T6SS gene cluster was dependent on the presence of an active T6SS. Furthermore, the expression of Re78 and Re79 proteins in E. coli without the ReMim1 nanosyringe revealed that these proteins behave as a toxic effector/immunity protein pair (E/I). The harmful action of Re78, whose mechanism is still unknown, would take place in the periplasmic space of the target cell. The deletion of this ReMim1 E/I pair resulted in reduced competitiveness for bean nodule occupancy and in lower survival in the presence of the wild-type strain. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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13 pages, 1708 KiB

Open AccessArticle

Aromatic Plants and Their Associated Arbuscular Mycorrhizal Fungi Outcompete Tuber melanosporum in Compatibility Assays with Truffle-Oaks

by Vasiliki Barou, Ana Rincón, Cinta Calvet, Amelia Camprubí and Javier Parladé

Biology 2023, 12(4), 628; https://doi.org/10.3390/biology12040628 - 20 Apr 2023

Cited by 2 | Viewed by 2731

Abstract

The high value of black truffle recompenses the slow growth of the fungus when established in the field. Adding a secondary crop, such as medicinal and aromatic plants (MAPs), could further enhance the sustainability of truffle production agro-forest systems. The dual cultures of ectomycorrhizal truffle-oak seedlings and MAPs (lavender, thyme, and sage) previously inoculated and non-inoculated with native arbuscular mycorrhizal fungi (AMF), were established to evaluate plant–fungi relationships. After 12 months in a shadehouse, plants’ growth, mycorrhizal colonization, and extraradical soil mycelium (both of Tuber melanosporum and AMF) were measured. Overall, truffle-oaks’ growth was negatively affected by the presence of MAPs, especially when inoculated with AMF. In turn, the presence of truffle-oaks barely affected the co-cultured MAPs, and only lavenders showed a significant growth reduction. All AMF-inoculated MAPs showed higher shoot and root biomass than non-inoculated ones. Compared to truffle-oaks growing alone, the presence of co-cultured MAPs, especially when they were AMF-inoculated, significantly decreased both the ectomycorrhizas and soil mycelium of T. melanosporum. These results reveal the strong competition between AMF and T. melanosporum and warn about the need for the protection of intercropping plants and their associated symbiotic fungi to avoid reciprocal counterproductive effects in mixed truffle-oak–AMF–MAP plantations. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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18 pages, 3346 KiB

Open AccessArticle

Competitiveness and Phylogenetic Relationship of Rhizobial Strains with Different Symbiotic Efficiency in Trifolium repens: Conversion of Parasitic into Non-Parasitic Rhizobia by Natural Symbiotic Gene Transfer

by María A. Morel Revetria, Andrés Berais-Rubio, Matías Giménez, Juan Sanjuán, Santiago Signorelli and Jorge Monza

Biology 2023, 12(2), 243; https://doi.org/10.3390/biology12020243 - 3 Feb 2023

Cited by 1 | Viewed by 2329

Abstract

In Uruguayan soils, populations of native and naturalized rhizobia nodulate white clover. These populations include efficient rhizobia but also parasitic strains, which compete for nodule occupancy and hinder optimal nitrogen fixation by the grassland. Nodulation competitiveness assays using gusA-tagged strains proved a high nodule occupancy by the inoculant strain U204, but this was lower than the strains with intermediate efficiencies, U268 and U1116. Clover biomass production only decreased when the parasitic strain UP3 was in a 99:1 ratio with U204, but not when UP3 was at equal or lower numbers than U204. Based on phylogenetic analyses, strains with different efficiencies did not cluster together, and U1116 grouped with the parasitic strains. Our results suggest symbiotic gene transfer from an effective strain to U1116, thereby improving its symbiotic efficiency. Genome sequencing of U268 and U204 strains allowed us to assign them to species Rhizobium redzepovicii, the first report of this species nodulating clover, and Rhizobium leguminosarun, respectively. We also report the presence of hrrP- and sapA-like genes in the genomes of WSM597, U204, and U268 strains, which are related to symbiotic efficiency in rhizobia. Interestingly, we report here chromosomally located hrrP-like genes. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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22 pages, 3455 KiB

Open AccessArticle

Non-Ionic Osmotic Stress Induces the Biosynthesis of Nodulation Factors and Affects Other Symbiotic Traits in Sinorhizobium fredii HH103

by Francisco Fuentes-Romero, Isamar Moyano-Bravo, Paula Ayala-García, Miguel Ángel Rodríguez-Carvajal, Francisco Pérez-Montaño, Sebastián Acosta-Jurado, Francisco Javier Ollero and José-María Vinardell

Biology 2023, 12(2), 148; https://doi.org/10.3390/biology12020148 - 18 Jan 2023

Cited by 6 | Viewed by 2499

Abstract

(1) Background: Some rhizobia, such as Rhizobium tropici CIAT 899, activate nodulation genes when grown under osmotic stress. This work aims to determine whether this phenomenon also takes place in Sinorhizobium fredii HH103. (2) Methods: HH103 was grown with and without 400 mM mannitol. β-galactosidase assays, nodulation factor extraction, purification and identification by mass spectrometry, transcriptomics by RNA sequencing, motility assays, analysis of acyl-homoserine lactones, and indole acetic acid quantification were performed. (3) Results: Non-ionic osmotic stress induced the production of nodulation factors. Forty-two different factors were detected, compared to 14 found in the absence of mannitol. Transcriptomics indicated that hundreds of genes were either activated or repressed upon non-ionic osmotic stress. The presence of 400 mM mannitol induced the production of indole acetic acid and acyl homoserine lactones, abolished swimming, and promoted surface motility. (4) Conclusions: In this work, we show that non-ionic stress in S. fredii HH103, caused by growth in the presence of 400 mM mannitol, provokes notable changes not only in gene expression but also in various bacterial traits, including the production of nodulation factors and other symbiotic signals. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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21 pages, 1451 KiB

Open AccessArticle

Impact of c-di-GMP on the Extracellular Proteome of Rhizobium etli

by María J. Lorite, Ariana Casas-Román, Lourdes Girard, Sergio Encarnación, Natalia Díaz-Garrido, Josefa Badía, Laura Baldomá, Daniel Pérez-Mendoza and Juan Sanjuán

Biology 2023, 12(1), 44; https://doi.org/10.3390/biology12010044 - 26 Dec 2022

Cited by 6 | Viewed by 3043

Abstract

Extracellular matrix components of bacterial biofilms include biopolymers such as polysaccharides, nucleic acids and proteins. Similar to polysaccharides, the secretion of adhesins and other matrix proteins can be regulated by the second messenger cyclic diguanylate (cdG). We have performed quantitative proteomics to determine the extracellular protein contents of a Rhizobium etli strain expressing high cdG intracellular levels. cdG promoted the exportation of proteins that likely participate in adhesion and biofilm formation: the rhizobial adhesion protein RapA and two previously undescribed likely adhesins, along with flagellins. Unexpectedly, cdG also promoted the selective exportation of cytoplasmic proteins. Nearly 50% of these cytoplasmic proteins have been previously described as moonlighting or candidate moonlighting proteins in other organisms, often found extracellularly. Western blot assays confirmed cdG-promoted export of two of these cytoplasmic proteins, the translation elongation factor (EF-Tu) and glyceraldehyde 3-phosphate dehydrogenase (Gap). Transmission Electron Microscopy immunolabeling located the Gap protein in the cytoplasm but was also associated with cell membranes and extracellularly, indicative of an active process of exportation that would be enhanced by cdG. We also obtained evidence that cdG increases the number of extracellular Gap proteoforms, suggesting a link between cdG, the post-translational modification and the export of cytoplasmic proteins. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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29 pages, 4568 KiB

Open AccessArticle

Geographically Disperse, Culturable Seed-Associated Microbiota in Forage Plants of Alfalfa (Medicago sativa L.) and Pitch Clover (Bituminaria bituminosa L.): Characterization of Beneficial Inherited Strains as Plant Stress-Tolerance Enhancers

by Marla Niza-Costa, Ana Sofía Rodríguez-dos Santos, Inês Rebelo-Romão, María Victoria Ferrer, Cristina Sequero López and Juan Ignacio Vílchez

Biology 2022, 11(12), 1838; https://doi.org/10.3390/biology11121838 - 16 Dec 2022

Cited by 6 | Viewed by 3183

Abstract

Agricultural production is being affected by increasingly harsh conditions caused by climate change. The vast majority of crops suffer growth and yield declines due to a lack of water or intense heat. Hence, commercial legume crops suffer intense losses of production (20–80%). This situation is even more noticeable in plants used as fodder for animals, such as alfalfa and pitch trefoil, since their productivity is linked not only to the number of seeds produced, but also to the vegetative growth of the plant itself. Thus, we decided to study the microbiota associated with their seeds in different locations on the Iberian Peninsula, with the aim of identifying culturable bacteria strains that have adapted to harsh environments and that can be used as biotreatments to improve plant growth and resistance to stress. As potentially inherited microbiota, they may also represent a treatment with medium- and long-term adaptative effects. Hence, isolated strains showed no clear relationship with their geographical sampling location, but had about 50% internal similarity with their model plants. Moreover, out of the 51 strains isolated, about 80% were capable of producing biofilms; around 50% produced mid/high concentrations of auxins and grew notably in ACC medium; only 15% were characterized as xerotolerant, while more than 75% were able to sporulate; and finally, 65% produced siderophores and more than 40% produced compounds to solubilize phosphates. Thus, Paenibacillus amylolyticus BB B2-A, Paenibacillus xylanexedens MS M1-C, Paenibacillus pabuli BB Oeiras A, Stenotrophomonas maltophilia MS M1-B and Enterobacter hormaechei BB B2-C strains were tested as plant bioinoculants in lentil plants (Lens culinaris Medik.), showing promising results as future treatments to improve plant growth under stressful conditions. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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20 pages, 2481 KiB

Open AccessArticle

The Role of Two Linear β-Glucans Activated by c-di-GMP in Rhizobium etli CFN42

by Daniel Pérez-Mendoza, Lorena Romero-Jiménez, Miguel Ángel Rodríguez-Carvajal, María J. Lorite, Socorro Muñoz, Adela Olmedilla and Juan Sanjuán

Biology 2022, 11(9), 1364; https://doi.org/10.3390/biology11091364 - 17 Sep 2022

Cited by 8 | Viewed by 2527

Abstract

Bacterial exopolysaccharides (EPS) have been implicated in a variety of functions that assist in bacterial survival, colonization, and host–microbe interactions. Among them, bacterial linear β-glucans are polysaccharides formed by D-glucose units linked by β-glycosidic bonds, which include curdlan, cellulose, and the new described Mixed Linkage β-Glucan (MLG). Bis-(3′,5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) is a universal bacterial second messenger that usually promote EPS production. Here, we report Rhizobium etli as the first bacterium capable of producing cellulose and MLG. Significant amounts of these two β-glucans are not produced under free-living laboratory conditions, but their production is triggered upon elevation of intracellular c-di-GMP levels, both contributing to Congo red (CR⁺) and Calcofluor (CF⁺) phenotypes. Cellulose turned out to be more relevant for free-living phenotypes promoting flocculation and biofilm formation under high c-di-GMP conditions. None of these two EPS are essential for attachment to roots of Phaseolus vulgaris, neither for nodulation nor for symbiotic nitrogen fixation. However, both β-glucans separately contribute to the fitness of interaction between R. etli and its host. Overproduction of these β-glucans, particularly cellulose, appears detrimental for symbiosis. This indicates that their activation by c-di-GMP must be strictly regulated in time and space and should be controlled by different, yet unknown, regulatory pathways. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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15 pages, 3055 KiB

Open AccessEditor’s ChoiceReview

Iron Homeostasis in Azotobacter vinelandii

by Elena Rosa-Núñez, Carlos Echavarri-Erasun, Alejandro M. Armas, Viviana Escudero, César Poza-Carrión, Luis M. Rubio and Manuel González-Guerrero

Biology 2023, 12(11), 1423; https://doi.org/10.3390/biology12111423 - 12 Nov 2023

Cited by 1 | Viewed by 2467

Abstract

Iron is an essential nutrient for all life forms. Specialized mechanisms exist in bacteria to ensure iron uptake and its delivery to key enzymes within the cell, while preventing toxicity. Iron uptake and exchange networks must adapt to the different environmental conditions, particularly those that require the biosynthesis of multiple iron proteins, such as nitrogen fixation. In this review, we outline the mechanisms that the model diazotrophic bacterium Azotobacter vinelandii uses to ensure iron nutrition and how it adapts Fe metabolism to diazotrophic growth. Full article

(This article belongs to the Special Issue 18th SEFIN Meeting and 1st Spanish-Portuguese Congress on Beneficial Plant-Microorganism Interactions)

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