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Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms
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Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 18744

Special Issue Editors

Prof. Jose J. Pueyo

E-Mail Website
Guest Editor
Institute of Agricultural Sciences, ICA-CSIC, Madrid, Spain
Interests: plant-microbial interactions; symbiosis
Dr. Elena E. Fedorova

E-Mail Website
Guest Editor
K.A.Timiryazev Institute of Plant Physiology, Russian Academy of Science, Moscow, Russia
Interests: plant-microbial interactions; symbiosis

Special Issue Information

Dear Colleagues,

The symbiotic interactions of microorganisms with plants are extremely important in agriculture and the environment. In recent decades, the research in this area has mainly focused on the signaling mechanisms between microorganisms and plants. These studies revealed the pathways that enable the entrance of selected microorganisms into the apoplast and, to some extent, into the symplast of the host plant, while restricting colonization by all other microorganisms. The definition of “symbiosis”, if interpreted in a broader sense, may be mutually beneficial, partly parasitic, or neutral during the different stages of development. The analysis of existing similarities and differences between symbiotic and parasitic colonization, represents a new research direction in this area.

Recently, new tools, such as genomics, transcriptomics, microbiome and secretome analyses, have revealed the complexity of the mutual influence between partners, as well as the significant role of environmental conditions on the processes of interaction. However, the knowledge concerning the intracellular stage of symbiosis is still insufficient, despite the fact that the efficiency of symbiosis largely depends on the appropriate interaction of the microsymbiont and host cells after colonization.

We would like to invite our colleagues to share their ideas and results concerning the research on the molecular mechanisms of symbiosis, especially the intracellular stage of colonization, and to submit manuscripts to the Special Issue of IJMS entitled: “Microbial colonization of the host plant: cellular and molecular mechanisms of symbiosis”.

Prof. Jose J. Pueyo
Dr. Elena E. Fedorova
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • plant–microbial interactions
  • symbiosis
  • rhizobia
  • signaling
  • intracellular accommodation

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Published Papers (7 papers)

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Editorial

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5 pages, 203 KiB  
Editorial
Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms of Symbiosis
by Elena E. Fedorova and José J. Pueyo
Int. J. Mol. Sci. 2024, 25(1), 639; https://doi.org/10.3390/ijms25010639 - 4 Jan 2024
Viewed by 1166
Abstract
Nitrogen is an essential element for all plants, animals, and microorganisms in the Earth’s biosphere [...] Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)

Research

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21 pages, 8912 KiB  
Article
Sinorhizobium meliloti DnaJ Is Required for Surface Motility, Stress Tolerance, and for Efficient Nodulation and Symbiotic Nitrogen Fixation
by Paula Brito-Santana, Julián J. Duque-Pedraza, Lydia M. Bernabéu-Roda, Cristina Carvia-Hermoso, Virginia Cuéllar, Francisco Fuentes-Romero, Sebastián Acosta-Jurado, José-María Vinardell and María J. Soto
Int. J. Mol. Sci. 2023, 24(6), 5848; https://doi.org/10.3390/ijms24065848 - 19 Mar 2023
Cited by 4 | Viewed by 2295
Abstract
Bacterial surface motility is a complex microbial trait that contributes to host colonization. However, the knowledge about regulatory mechanisms that control surface translocation in rhizobia and their role in the establishment of symbiosis with legumes is still limited. Recently, 2-tridecanone (2-TDC) was identified [...] Read more.
Bacterial surface motility is a complex microbial trait that contributes to host colonization. However, the knowledge about regulatory mechanisms that control surface translocation in rhizobia and their role in the establishment of symbiosis with legumes is still limited. Recently, 2-tridecanone (2-TDC) was identified as an infochemical in bacteria that hampers microbial colonization of plants. In the alfalfa symbiont Sinorhizobium meliloti, 2-TDC promotes a mode of surface motility that is mostly independent of flagella. To understand the mechanism of action of 2-TDC in S. meliloti and unveil genes putatively involved in plant colonization, Tn5 transposants derived from a flagellaless strain that were impaired in 2-TDC-induced surface spreading were isolated and genetically characterized. In one of the mutants, the gene coding for the chaperone DnaJ was inactivated. Characterization of this transposant and newly obtained flagella-minus and flagella-plus dnaJ deletion mutants revealed that DnaJ is essential for surface translocation, while it plays a minor role in swimming motility. DnaJ loss-of-function reduces salt and oxidative stress tolerance in S. meliloti and hinders the establishment of efficient symbiosis by affecting nodule formation efficiency, cellular infection, and nitrogen fixation. Intriguingly, the lack of DnaJ causes more severe defects in a flagellaless background. This work highlights the role of DnaJ in the free-living and symbiotic lifestyles of S. meliloti. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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21 pages, 4232 KiB  
Article
Sodium Accumulation in Infected Cells and Ion Transporters Mistargeting in Nodules of Medicago truncatula: Two Ugly Items That Hinder Coping with Salt Stress Effects
by Natalia A. Trifonova, Roman Kamyshinsky, Teodoro Coba de la Peña, Maria I. Koroleva, Olga Kulikova, Victoria Lara-Dampier, Pavel Pashkovskiy, Mikhail Presniakov, José J. Pueyo, M. Mercedes Lucas and Elena E. Fedorova
Int. J. Mol. Sci. 2022, 23(18), 10618; https://doi.org/10.3390/ijms231810618 - 13 Sep 2022
Cited by 3 | Viewed by 2298
Abstract
The maintenance of intracellular nitrogen-fixing bacteria causes changes in proteins’ location and in gene expression that may be detrimental to the host cell fitness. We hypothesized that the nodule’s high vulnerability toward salt stress might be due to alterations in mechanisms involved in [...] Read more.
The maintenance of intracellular nitrogen-fixing bacteria causes changes in proteins’ location and in gene expression that may be detrimental to the host cell fitness. We hypothesized that the nodule’s high vulnerability toward salt stress might be due to alterations in mechanisms involved in the exclusion of Na+ from the host cytoplasm. Confocal and electron microscopy immunolocalization analyses of Na+/K+ exchangers in the root nodule showed the plasma membrane (MtNHX7) and endosome/tonoplast (MtNHX6) signal in non-infected cells; however, in mature infected cells the proteins were depleted from their target membranes and expelled to vacuoles. This mistargeting suggests partial loss of the exchanger’s functionality in these cells. In the mature part of the nodule 7 of the 20 genes encoding ion transporters, channels, and Na+/K+ exchangers were either not expressed or substantially downregulated. In nodules from plants subjected to salt treatments, low temperature-scanning electron microscopy and X-ray microanalysis revealed the accumulation of 5–6 times more Na+ per infected cell versus non-infected one. Hence, the infected cells’ inability to withstand the salt may be the integral result of preexisting defects in the localization of proteins involved in Na+ exclusion and the reduced expression of key genes of ion homeostasis, resulting in premature senescence and termination of symbiosis. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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Review

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18 pages, 1875 KiB  
Review
Lupin, a Unique Legume That Is Nodulated by Multiple Microsymbionts: The Role of Horizontal Gene Transfer
by Abdelhakim Msaddak, Mohamed Mars, Miguel A. Quiñones, M. Mercedes Lucas and José J. Pueyo
Int. J. Mol. Sci. 2023, 24(7), 6496; https://doi.org/10.3390/ijms24076496 - 30 Mar 2023
Cited by 6 | Viewed by 2107
Abstract
Lupin is a high-protein legume crop that grows in a wide range of edaphoclimatic conditions where other crops are not viable. Its unique seed nutrient profile can promote health benefits, and it has been proposed as a phytoremediation plant. Most rhizobia nodulating Lupinus [...] Read more.
Lupin is a high-protein legume crop that grows in a wide range of edaphoclimatic conditions where other crops are not viable. Its unique seed nutrient profile can promote health benefits, and it has been proposed as a phytoremediation plant. Most rhizobia nodulating Lupinus species belong to the genus Bradyrhizobium, comprising strains that are phylogenetically related to B. cytisi, B. hipponenese, B. rifense, B. iriomotense/B. stylosanthis, B. diazoefficiens, B. japonicum, B. canariense/B. lupini, and B. retamae/B. valentinum. Lupins are also nodulated by fast-growing bacteria within the genera Microvirga, Ochrobactrum, Devosia, Phyllobacterium, Agrobacterium, Rhizobium, and Neorhizobium. Phylogenetic analyses of the nod and nif genes, involved in microbial colonization and symbiotic nitrogen fixation, respectively, suggest that fast-growing lupin-nodulating bacteria have acquired their symbiotic genes from rhizobial genera other than Bradyrhizobium. Horizontal transfer represents a key mechanism allowing lupin to form symbioses with bacteria that were previously considered as non-symbiotic or unable to nodulate lupin, which might favor lupin’s adaptation to specific habitats. The characterization of yet-unstudied Lupinus species, including microsymbiont whole genome analyses, will most likely expand and modify the current lupin microsymbiont taxonomy, and provide additional knowledge that might help to further increase lupin’s adaptability to marginal soils and climates. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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13 pages, 3446 KiB  
Review
Rapid Changes to Endomembrane System of Infected Root Nodule Cells to Adapt to Unusual Lifestyle
by Elena E. Fedorova
Int. J. Mol. Sci. 2023, 24(5), 4647; https://doi.org/10.3390/ijms24054647 - 28 Feb 2023
Cited by 3 | Viewed by 2203
Abstract
Symbiosis between leguminous plants and soil bacteria rhizobia is a refined type of plant–microbial interaction that has a great importance to the global balance of nitrogen. The reduction of atmospheric nitrogen takes place in infected cells of a root nodule that serves as [...] Read more.
Symbiosis between leguminous plants and soil bacteria rhizobia is a refined type of plant–microbial interaction that has a great importance to the global balance of nitrogen. The reduction of atmospheric nitrogen takes place in infected cells of a root nodule that serves as a temporary shelter for thousands of living bacteria, which, per se, is an unusual state of a eukaryotic cell. One of the most striking features of an infected cell is the drastic changes in the endomembrane system that occur after the entrance of bacteria to the host cell symplast. Mechanisms for maintaining intracellular bacterial colony represent an important part of symbiosis that have still not been sufficiently clarified. This review focuses on the changes that occur in an endomembrane system of infected cells and on the putative mechanisms of infected cell adaptation to its unusual lifestyle. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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23 pages, 2572 KiB  
Review
Legumes Regulate Symbiosis with Rhizobia via Their Innate Immune System
by Estelle B. Grundy, Peter M. Gresshoff, Huanan Su and Brett J. Ferguson
Int. J. Mol. Sci. 2023, 24(3), 2800; https://doi.org/10.3390/ijms24032800 - 1 Feb 2023
Cited by 8 | Viewed by 4505
Abstract
Plant roots are constantly exposed to a diverse microbiota of pathogens and mutualistic partners. The host’s immune system is an essential component for its survival, enabling it to monitor nearby microbes for potential threats and respond with a defence response when required. Current [...] Read more.
Plant roots are constantly exposed to a diverse microbiota of pathogens and mutualistic partners. The host’s immune system is an essential component for its survival, enabling it to monitor nearby microbes for potential threats and respond with a defence response when required. Current research suggests that the plant immune system has also been employed in the legume-rhizobia symbiosis as a means of monitoring different rhizobia strains and that successful rhizobia have evolved to overcome this system to infect the roots and initiate nodulation. With clear implications for host-specificity, the immune system has the potential to be an important target for engineering versatile crops for effective nodulation in the field. However, current knowledge of the interacting components governing this pathway is limited, and further research is required to build on what is currently known to improve our understanding. This review provides a general overview of the plant immune system’s role in nodulation. With a focus on the cycles of microbe-associated molecular pattern-triggered immunity (MTI) and effector-triggered immunity (ETI), we highlight key molecular players and recent findings while addressing the current knowledge gaps in this area. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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26 pages, 785 KiB  
Review
The Rhizobial Type 3 Secretion System: The Dr. Jekyll and Mr. Hyde in the Rhizobium–Legume Symbiosis
by Irene Jiménez-Guerrero, Carlos Medina, José María Vinardell, Francisco Javier Ollero and Francisco Javier López-Baena
Int. J. Mol. Sci. 2022, 23(19), 11089; https://doi.org/10.3390/ijms231911089 - 21 Sep 2022
Cited by 23 | Viewed by 3184
Abstract
Rhizobia are soil bacteria that can establish a symbiotic association with legumes. As a result, plant nodules are formed on the roots of the host plants where rhizobia differentiate to bacteroids capable of fixing atmospheric nitrogen into ammonia. This ammonia is transferred to [...] Read more.
Rhizobia are soil bacteria that can establish a symbiotic association with legumes. As a result, plant nodules are formed on the roots of the host plants where rhizobia differentiate to bacteroids capable of fixing atmospheric nitrogen into ammonia. This ammonia is transferred to the plant in exchange of a carbon source and an appropriate environment for bacterial survival. This process is subjected to a tight regulation with several checkpoints to allow the progression of the infection or its restriction. The type 3 secretion system (T3SS) is a secretory system that injects proteins, called effectors (T3E), directly into the cytoplasm of the host cell, altering host pathways or suppressing host defense responses. This secretion system is not present in all rhizobia but its role in symbiosis is crucial for some symbiotic associations, showing two possible faces as Dr. Jekyll and Mr. Hyde: it can be completely necessary for the formation of nodules, or it can block nodulation in different legume species/cultivars. In this review, we compile all the information currently available about the effects of different rhizobial effectors on plant symbiotic phenotypes. These phenotypes are diverse and highlight the importance of the T3SS in certain rhizobium–legume symbioses. Full article
(This article belongs to the Special Issue Microbial Colonization of the Host Plant: Cellular and Molecular Mechanisms)
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