Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects

A special issue of Agronomy (ISSN 2073-4395). This special issue belongs to the section "Crop Breeding and Genetics".

Deadline for manuscript submissions: closed (1 May 2022) | Viewed by 21729

Special Issue Editors


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Guest Editor
Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Saint Petersburg 196608, Russia
Interests: cell biology of plant‒microbe interactions; legume‒rhizobial symbiosis; plant‒microbe interface
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Guest Editor
Department of Biotechnology, All-Russia Research Institute for Agricultural Microbiology, Saint Petersburg 196608, Russia
Interests: genetics and cell biology of plant‒microbe interactions; legume‒rhizobial symbiosis; legume‒mycorrhizal symbiosis
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

In recent years, sustainable agriculture has been actively developing all over the world, aimed at the production of high-grade, ecologically friendly, and health-improving agricultural products. The widespread use of legumes in sustainable agriculture will increase biological nitrogen fixation, reduce energy costs, improve the physical properties of soil, and increase its biodiversity. In addition, legumes are important food and forage crops, being the main crops in some regions. In recent years, significant progress has been achieved in deciphering the molecular and cellular mechanisms of the development of symbiotic nodules.

We invite you to please share your findings on the molecular and cellular mechanisms of symbiotic nitrogen fixation in crops in this Special Issue. Submissions on the following topics (but not limited to) are invited: (1) omics sciences in the crop symbiotic nitrogen fixation, (2) interactions of macro- and micro-symbionts during the development of the plant–microbe interface, (3) signal transduction during the formation and development of a symbiotic nodule, (4) plant cell reorganization during rhizobia accommodation, and (5) the participation of phytohormones and reactive oxygen species in the formation and development of a symbiotic nodule. Original research papers, methods, reviews, and short communications are also welcome.

Dr. Anna Tsyganova
Dr. Viktor E. Tsyganov
Guest Editors

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Keywords

  • Crop legume
  • Symbiotic nodule
  • Plant-microbe interface
  • Infection thread
  • Symbiosome
  • Nod factors and receptors
  • Signal transduction
  • Symbiotic genes
  • Transcriptomics
  • Proteomics
  • Metabolomics
  • Phytohormones
  • Reactive oxygen species
  • Symbiotic effectiveness

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Published Papers (8 papers)

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Editorial

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4 pages, 213 KiB  
Editorial
Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects
by Anna V. Tsyganova and Viktor E. Tsyganov
Agronomy 2022, 12(11), 2857; https://doi.org/10.3390/agronomy12112857 - 15 Nov 2022
Viewed by 1210
Abstract
The production of high-value, environmentally friendly and healthy food has been the major global focus of sustainable agriculture in recent years [...] Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)

Research

Jump to: Editorial

20 pages, 4547 KiB  
Article
Molecular Phylogenetic Analysis of Salt-Tolerance-Related Genes in Root-Nodule Bacteria Species Sinorhizobium meliloti
by Victoria Spartakovna Muntyan and Marina Lvovna Roumiantseva
Agronomy 2022, 12(8), 1968; https://doi.org/10.3390/agronomy12081968 - 20 Aug 2022
Cited by 4 | Viewed by 2267
Abstract
A molecular phylogenetic analysis of salt-tolerance-related genes was carried out using complete genome sequencing data available for 26 Sinorhizobium meliloti strains and for 25 bacterial strains belonging to 17 genera. It was revealed that the genes of the first and the second stages [...] Read more.
A molecular phylogenetic analysis of salt-tolerance-related genes was carried out using complete genome sequencing data available for 26 Sinorhizobium meliloti strains and for 25 bacterial strains belonging to 17 genera. It was revealed that the genes of the first and the second stages of the response to salt stress (aqpZ, trkH, and trkA, and betICBA) have copies of many of the above- indicated genes on pSymA. Data obtained can provide evidence that this replicon, known to be essential for nitrogen fixation rhizobia activity, also has a significant role in the formation of a stress-related gene pool. The closest putative phylogenetic relatives were identified for all 14 tested genes and these are the first insights into the evolutionary pathways for the formation of a stress-related gene pool in root nodule nitrogen-fixing bacteria. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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33 pages, 3160 KiB  
Article
Ensifer meliloti L6-AK89, an Effective Inoculant of Medicago lupulina Varieties: Phenotypic and Deep-Genome Screening
by Marina L. Roumiantseva, Maria E. Vladimirova, Alla S. Saksaganskaia, Victoria S. Muntyan, Alexandra P. Kozlova, Alexey M. Afonin, Olga A. Baturina and Boris V. Simarov
Agronomy 2022, 12(4), 766; https://doi.org/10.3390/agronomy12040766 - 22 Mar 2022
Cited by 9 | Viewed by 3217
Abstract
This paper presents a deep analysis of the accessory genome of an economically promising strain of Ensifer (Sinorhizobium) meliloti, L6-AK89, obtained as a result of next-generation high-throughput sequencing (MiSeq, MinIon). Strain L6-AK89 is a StrR mutant of the native [...] Read more.
This paper presents a deep analysis of the accessory genome of an economically promising strain of Ensifer (Sinorhizobium) meliloti, L6-AK89, obtained as a result of next-generation high-throughput sequencing (MiSeq, MinIon). Strain L6-AK89 is a StrR mutant of the native strain CIAM1775, a symbiont of Medicago lupulina that adapted to a saline and arid habitat in NW Kazakhstan. CIAM1775 is an effective inoculant of M. lupulina cv. Mira (fodder type standard), cultivated on moderately acid soils in the NW agricultural region of Russia. Strain L6-AK89 makes it possible to obtain the expected high (>150%) increases in dry mass of the same plant variety in plant tests. The L6-AK89 genome has an increased proportion of sequences related to the accessory elements relative to reference strain Rm1021, 7.4% versus 4.8%. A set of 53 nod/noe/nol/nif/fdx/fix genes and 32 genes involved in stress tolerance together with 16S rRNA and recAatpDglnIIgyrBdnaJ were evaluated. The high symbiotic efficiency of L6-АК89 with hop clover is most likely due to unique features of its genome, in combination with structural differences in its nod and stress-related genes, as well as unique clusters of quorum-sensing genes and osmoprotector synthesis. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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16 pages, 9209 KiB  
Article
Glycyrrhiza uralensis Nodules: Histological and Ultrastructural Organization and Tubulin Cytoskeleton Dynamics
by Anna V. Tsyganova, Anna B. Kitaeva, Artemii P. Gorshkov, Pyotr G. Kusakin, Alexandra R. Sadovskaya, Yaroslav G. Borisov and Viktor E. Tsyganov
Agronomy 2021, 11(12), 2508; https://doi.org/10.3390/agronomy11122508 - 10 Dec 2021
Cited by 5 | Viewed by 2642
Abstract
Chinese liquorice (Glycyrrhiza uralensis Fisch. ex DC.) is widely used in the food industry and as a medicine. Like other legumes, G. uralensis forms symbiotic nodules. However, the structural organization of G. uralensis nodules is poorly understood. In this study, we analyzed [...] Read more.
Chinese liquorice (Glycyrrhiza uralensis Fisch. ex DC.) is widely used in the food industry and as a medicine. Like other legumes, G. uralensis forms symbiotic nodules. However, the structural organization of G. uralensis nodules is poorly understood. In this study, we analyzed the histological and ultrastructural organization and dynamics of the tubulin cytoskeleton in various cells from different histological zones of indeterminate nodules formed by two strains of Mesorhizobium sp. The unusual walls of infection threads and formation of multiple symbiosomes with several swollen bacteroids were observed. A large amount of poly-β-hydroxybutyrate accumulated in the bacteroids, while the vacuoles of meristematic and uninfected cells contained drop-shaped osmiophilic inclusions. Immunolocalization of the tubulin cytoskeleton and quantitative analysis of cytoskeletal elements revealed patterns of cortical microtubules in meristematic, infected and uninfected cells, and of endoplasmic microtubules associated with infection structures, typical of indeterminate nodules. The intermediate pattern of endoplasmic microtubules in infected cells was correlated with disordered arrangement of symbiosomes. Thus, analysis of the structural organization of G. uralensis nodules revealed some ancestral features more characteristic of determinate nodules, demonstrating the evolutionary closeness of G. uralensis nodulation to more ancient members of the legume family. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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18 pages, 5261 KiB  
Article
Laser Microdissection of Pisum sativum L. Nodules Followed by RNA-Seq Analysis Revealed Crucial Transcriptomic Changes during Infected Cell Differentiation
by Pyotr G. Kusakin, Tatiana A. Serova, Natalia E. Gogoleva, Yuri V. Gogolev and Viktor E. Tsyganov
Agronomy 2021, 11(12), 2504; https://doi.org/10.3390/agronomy11122504 - 9 Dec 2021
Cited by 10 | Viewed by 3104
Abstract
Garden pea (Pisum sativum L.) is a globally important legume crop. Like other legumes, it forms beneficial symbiotic interactions with the soil bacteria rhizobia, gaining the ability to fix atmospheric nitrogen. In pea nodules, the meristem is long-lasting and results in the [...] Read more.
Garden pea (Pisum sativum L.) is a globally important legume crop. Like other legumes, it forms beneficial symbiotic interactions with the soil bacteria rhizobia, gaining the ability to fix atmospheric nitrogen. In pea nodules, the meristem is long-lasting and results in the formation of several histological zones that implicate a notable differentiation of infected host cells. However, the fine transcriptional changes that accompany differentiation are still unknown. In this study, using laser microdissection followed by RNA-seq analysis, we performed transcriptomic profiling in the early infection zone, late infection zone, and nitrogen fixation zone of 11-day-old nodules of pea wild-type line SGE. As a result, a list of functional groups of differentially expressed genes (DEGs) in different nodule histological zones and a list of genes with the most prominent expression changes during nodule development were obtained. Their analyses demonstrated that the highest amount of DEGs was associated with the nitrogen fixation zone. Among well-known genes controlling nodule development, we revealed genes that can be novel players throughout nodule formation. The characterized genes in pea were compared with those previously described in other legumes and their possible functions in nodule development are discussed. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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23 pages, 10438 KiB  
Article
Association Study of Symbiotic Genes in Pea (Pisum sativum L.) Cultivars Grown in Symbiotic Conditions
by Vladimir A. Zhukov, Aleksandr I. Zhernakov, Anton S. Sulima, Olga A. Kulaeva, Marina S. Kliukova, Alexey M. Afonin, Oksana Y. Shtark and Igor A. Tikhonovich
Agronomy 2021, 11(11), 2368; https://doi.org/10.3390/agronomy11112368 - 22 Nov 2021
Cited by 6 | Viewed by 2779
Abstract
In garden pea (Pisum sativum L.), several symbiotic genes are known to control the development of mutualistic symbioses with nodule bacteria (NB) and arbuscular mycorrhizal fungi (AMF). Here, we studied whether the allelic state of the symbiotic genes was associated with the [...] Read more.
In garden pea (Pisum sativum L.), several symbiotic genes are known to control the development of mutualistic symbioses with nodule bacteria (NB) and arbuscular mycorrhizal fungi (AMF). Here, we studied whether the allelic state of the symbiotic genes was associated with the growth parameters of pea plants under single inoculation with NB and under double inoculation with NB + AMF. Using different statistical methods, we analyzed the dataset obtained from a pot experiment that involved 99 pea cultivars, 10 of which were characterized as having shortened internodes due to the presence of the natural mutation p.A229T in the developmental gene Le. The plant’s habitus strongly influenced most of the studied growth and yield parameters and the effectiveness of the symbiotic interactions under NB and NB + AMF inoculation. Double inoculation had different effects on Le+ (normal) and le (dwarf) plants with regard to nitrogen and phosphorus content in seeds. Regardless of the Le-status of plants, allelic states of the symbiotic gene LykX encoding the putative receptor of Nod factors (bacterial signal molecules) were shown to be associated with seed number, thousand-seed weight, and pod number at the level of FDR < 0.001, whereas associations of allelic states of the other studied symbiotic genes were less significant. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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22 pages, 1414 KiB  
Article
Ensifer aridi LMR001T Symbiosis and Tolerance to Stress Do Not Require the Alternative Sigma Factor RpoE2
by Meryem Belfquih, Ilham Sakrouhi, Hassan Ait-Benhassou, Emeric Dubois, Dany Severac, Abdelkarim Filali-Maltouf and Antoine Le Quere
Agronomy 2021, 11(9), 1787; https://doi.org/10.3390/agronomy11091787 - 7 Sep 2021
Cited by 5 | Viewed by 2438
Abstract
The recently proposed species Ensifer aridi represents an interesting model to study adaptive mechanisms explaining its maintenance under stressful pedo-climatic conditions. To get insights into functions associated with hyperosmotic stress adaptation in E. aridi, we first performed RNAseq profiling of cells grown [...] Read more.
The recently proposed species Ensifer aridi represents an interesting model to study adaptive mechanisms explaining its maintenance under stressful pedo-climatic conditions. To get insights into functions associated with hyperosmotic stress adaptation in E. aridi, we first performed RNAseq profiling of cells grown under sub-lethal stresses applied by permeating (NaCl) and non-permeating (PEG8000) solutes that were compared to a transcriptome from unstressed bacteria. Then an a priori approach, consisting of targeted mutagenesis of the gene encoding alternative sigma factor (rpoE2), involved in the General Stress Response combined with phenotyping and promoter gfp fusion-based reporter assays of selected genes was carried out to examine the involvement of rpoE2 in symbiosis and stress response. The majority of motility and chemotaxis genes were repressed by both stresses. Results also suggest accumulation of compatible solute trehalose under stress and other metabolisms such as inositol catabolism or the methionine cycling-generating S-adenosyl methionine appears strongly induced notably under salt stress. Interestingly, many functions regulated by salt were shown to favor competitiveness for nodulation in other rhizobia, supporting a role of stress genes for proper symbiosis’ development and functioning. However, despite activation of the general stress response and identification of several genes possibly under its control, our data suggest that rpoE2 was not essential for stress tolerance and symbiosis’ development, indicating that E. aridi possesses alternative regulatory mechanisms to adapt and respond to stressful environments. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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17 pages, 3033 KiB  
Article
Increasing the Legume–Rhizobia Symbiotic Efficiency Due to the Synergy between Commercial Strains and Strains Isolated from Relict Symbiotic Systems
by Vera Safronova, Anna Sazanova, Irina Kuznetsova, Andrey Belimov, Polina Guro, Denis Karlov, Oleg Yuzikhin, Elizaveta Chirak, Alla Verkhozina, Alexey Afonin, Evgeny Andronov and Igor Tikhonovich
Agronomy 2021, 11(7), 1398; https://doi.org/10.3390/agronomy11071398 - 12 Jul 2021
Cited by 3 | Viewed by 2820
Abstract
The phenomenon of rhizobial synergy was investigated to increase the efficiency of nitrogen-fixing symbiosis of alfalfa (Medicago varia Martyn), common vetch (Vicia sativa L.) or red clover (Trifolium pratense L.). These plants were co-inoculated with the respective commercial strains Sinorhizobium [...] Read more.
The phenomenon of rhizobial synergy was investigated to increase the efficiency of nitrogen-fixing symbiosis of alfalfa (Medicago varia Martyn), common vetch (Vicia sativa L.) or red clover (Trifolium pratense L.). These plants were co-inoculated with the respective commercial strains Sinorhizobium meliloti RCAM1750, Rhizobium leguminosarum RCAM0626 or R. leguminosarum RCAM1365 and with the strains Mesorhizobium japonicum Opo-235, M. japonicum Opo-242, Bradyrhizobium sp. Opo-243 or M. kowhaii Ach-343 isolated from the relict legumes Oxytropis popoviana Peschkova and Astragalus chorinensis Bunge. The isolates mentioned above had additional symbiotic genes (fix, nif, nodnoe and nol) as well as the genes promoting plant growth and symbiosis formation (acdRS, genes associated with the biosynthesis of gibberellins and auxins, genes of T3SS, T4SS and T6SS secretion systems) compared to the commercial strains. Nodulation assays showed that in some variants of co-inoculation the symbiotic parameters of plants such as nodule number, plant biomass or acetylene reduction activity were increased. We assume that the study of microbial synergy using rhizobia of relict legumes will make it possible to carry out targeted selection of co-microsymbionts to increase the efficiency of agricultural legume–rhizobia systems. Full article
(This article belongs to the Special Issue Rhizobial Symbiosis in Crop Legumes: Molecular and Cellular Aspects)
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