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Pea-Rhizobial and Pea-Mycorrhizal Symbioses

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Protection and Biotic Interactions".

Deadline for manuscript submissions: closed (1 April 2021) | Viewed by 45632

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Dr. Viktor E. Tsyganov

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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

Prof. Nicholas J. Brewin

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Guest Editor

John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK
Interests: legume-rhizobium symbiosis; plant cell wall remodeling; infection threads; legume root nodule morphogenesis

Special Issue Information

Dear Colleagues,

The pea (Pisum sativum L.) is one of the most important legume crops in the world. The most important aspect of pea biology is its ability to form endosymbioses as a result of interaction with rhizobia and endomycorrhizal fungi. The formation of these symbioses allows the pea to largely satisfy its needs for various nutrients, primarily nitrogen and phosphorus, through symbiotrophic nutrition.

Its natural variation in nodulation ability was first detected in pea genotypes from Afghanistan, which did not form nodules with European strains about 90 years ago. Since then, large collections of mutants with various abnormalities in the development of symbiotic nodules have been obtained for the pea. A study of these mutants revealed about 50 symbiotic loci involved in controlling the nodulation in the pea. Moreover, the study of mutants incapable of nodulation allowed the identification of symbiotic loci that control not only the development of nodules, but also endomycorrhizal symbiosis.

However, the large genome size and the lack of effective protocols for the stable genetic transformation of the pea made it difficult to identify the symbiotic pea genes. Nevertheless, over the past 15 years, based on advances in the genetics of model legumes, several symbiotic genes have been identified in the pea, and recent sequencing of the pea genome opens up new possibilities in identifying new pea genes involved in the formation of symbiotic nodules and endomycorrhiza.

It is necessary to note that pea endosymbioses are excellent models for studying the cellular and physiological mechanisms of plant-microbial interactions.

This special volume is aimed at summarizing the latest achievements in genetics, cell biology, and physiology of pea-Rhizobium and pea-endomycorrhizal fungi symbioses. Original research papers, methods, reviews, and short communications are also welcome.

Dr. Viktor E. Tsyganov
Prof. Nicholas J. Brewin
Guest Editors

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Keywords

nodule
arbuscular mycorrhiza
nod factor and receptors
plant-microbe interface
infection thread
symbiosome
symbiotic genes
transcriptomics
metabolomics
phytohormones
reactive oxygen species
cytoskeleton
senescence

Published Papers (12 papers)

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Research

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20 pages, 4596 KiB

Open AccessFeature PaperArticle

Metabolic Alterations in Pisum sativum Roots during Plant Growth and Arbuscular Mycorrhiza Development

by Oksana Shtark, Roman Puzanskiy, Galina Avdeeva, Vladislav Yemelyanov, Alexey Shavarda, Daria Romanyuk, Marina Kliukova, Anastasia Kirpichnikova, Igor Tikhonovich, Vladimir Zhukov and Maria Shishova

Plants 2021, 10(6), 1033; https://doi.org/10.3390/plants10061033 - 21 May 2021

Cited by 14 | Viewed by 2699

Abstract

Intensive exchange of nutrients is a crucial part of the complex interaction between a host plant and fungi within arbuscular mycorrhizal (AM) symbiosis. For the first time, the present study demonstrates how inoculation with AMF Rhizophagus irregularis affects the pea (Pisum sativum L.) root metabolism at key stages of plant development. These correspond to days 21 (vegetation), 42 (flowering initiation), and 56 (fruiting-green pod). Metabolome profiling was carried out by means of a state-of-the-art GC-MS technique. The content shifts revealed include lipophilic compounds, sugars, carboxylates, and amino acids. The metabolic alterations were principally dependent on the stage of plant development but were also affected by the development of AM fungi, a fact which highlights interaction between symbiotic partners. The comparison of the present data with the results of leaf metabolome profiling earlier obtained did not reveal common signatures of metabolic response to mycorrhization in leaves and roots. We supposed that the feedback for the development and symbiotic interaction on the part of the supraorganismic system (root + AM fungi) was the cause of the difference between the metabolic profile shift in leaf and root cells that our examination revealed. New investigations are required to expand our knowledge of metabolome plasticity of the whole organism and/or system of organisms, and such results might be put to use for the intensification of sustainable agriculture. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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15 pages, 1309 KiB

Open AccessArticle

Co-Inoculation of Mesorhizobium ciceri with Either Bacillus sp. or Enterobacter aerogenes on Chickpea Improves Growth and Productivity in Phosphate-Deficient Soils in Dry Areas of a Mediterranean Region

by Imane Benjelloun, Imane Thami Alami, Mohamed El Khadir, Allal Douira and Sripada M. Udupa

Plants 2021, 10(3), 571; https://doi.org/10.3390/plants10030571 - 17 Mar 2021

Cited by 18 | Viewed by 3369

Abstract

Biological nitrogen fixation requires a large amount of phosphorus (P). However, most of the soils are P-deficient and the extensive use of P- chemical fertilizers constitute a serious threat to the environment. In this context, two field experiments were carried out to investigate the effect of co-inoculation of Mesorhizobium ciceri with phosphate solubilizing bacteria (PSB), Bacillus sp., and Enterobacter aerogenes, on chickpea as an alternative to chemical nitrogen (N) and phosphorous fertilizers in P-deficient soils in dry areas of Morocco. The results revealed that combined inoculation of chickpea with rhizobia and PSB showed a significant enhancement of chickpea nodulation, biomass production, yields and N, P, and protein content in grains as compared to single inoculation or single application of N or P. A significantly higher increase was obtained by inoculating chickpea with Mesorhizobium sp. MA72 combined with E. aerogenes P1S6. This combination allowed an enhancement of more than 270% in nodulation, 192% in shoot dry weight and 242% in grain yield. The effect of this combination was equivalent to the effect of combined application of N and P fertilizers. Formulation of biofertilizers based on tasted strains could be used for chickpea co-inoculation in P-deficient soils for an eco-friendly sustainable production of chickpea. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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21 pages, 5932 KiB

Open AccessArticle

Assessment of Genetic Diversity and Symbiotic Efficiency of Selected Rhizobia Strains Nodulating Lentil (Lens culinaris Medik.)

by Badreddine Sijilmassi, Abdelkarim Filali-Maltouf, Hassan Boulahyaoui, Aymane Kricha, Kenza Boubekri, Sripada Udupa, Shiv Kumar and Ahmed Amri

Plants 2021, 10(1), 15; https://doi.org/10.3390/plants10010015 - 24 Dec 2020

Cited by 14 | Viewed by 3218

Abstract

A total of 14 Rhizobium strains were isolated from lentil accessions grown at the ICARDA experimental research station at Marchouch in Morocco and used for molecular characterization and symbiotic efficiency assessment. Individual phylogenetic analysis using the 16S rRNA gene, house-keeping genes rpoB, recA, and gyrB, and symbiotic genes nodD and nodA along with Multilocus Sequence Analysis (MLSA) of the concatenated genes (16S rRNA-rpoB-recA-gyrB) was carried out for the identification and clustering of the isolates. The symbiotic efficiency of the strains was assessed on three Moroccan lentil cultivars (Bakria, Chakkouf, and Zaria) based on the number of nodules, plant height, plant dry weight, and total nitrogen content in leaves. The results showed that the individual phylogenetic analysis clustered all the strains into Rhizobium laguerreae and Rhizobium leguminosarum with sequence similarity ranging from 94 to 100%, except one strain which clustered with Mesorhizobium huakuii with sequence similarity of 100%. The MLSA of the concatenated genes and the related percentages of similarity clustered these strains into two groups of Rhizobium species, with one strain as a new genospecies when applying the threshold of 96%. For symbiotic efficiency, the Bakria variety showed the best association with 10 strains compared to its non-inoculated control (p-value ≤ 0.05), followed by Chakkouf and Zaria. The present study concluded that the genetic diversity and the symbiotic efficiency of Rhizobium strains appeared to be mainly under the control of the lentil genotypes. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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13 pages, 4685 KiB

Open AccessArticle

Identification of BELL Transcription Factors Involved in Nodule Initiation and Development in the Legumes Pisum sativum and Medicago truncatula

by Alexandra V. Dolgikh, Elizaveta S. Rudaya and Elena A. Dolgikh

Plants 2020, 9(12), 1808; https://doi.org/10.3390/plants9121808 - 20 Dec 2020

Cited by 9 | Viewed by 2751

Abstract

Single three-amino acid loop extension (TALE) homeodomain proteins, including the KNOTTED-like (KNOX) and BEL-like (BELL) families in plants, usually work as heterodimeric transcription factor complexes to regulate different developmental processes, often via effects on phytohormonal pathways. Nitrogen-fixing nodule formation in legumes is regulated by different families of homeodomain transcription factors. Whereas the role of KNOX transcription factors in the control of symbiosis was studied early, BELL transcription factors have received less attention. Here, we report the identification and expression analysis of BELL genes in the legume plants Medicago truncatula and Pisum sativum, which are involved in regulating symbiosis initiation and development. A more precise analysis was performed for the most significantly upregulated PsBELL1-2 gene in pea. We found that the PsBELL1-2 transcription factor could be a potential partner of PsKNOX9. In addition, we showed that PsBELL1-2 can interact with the PsDELLA1 (LA) protein-regulator of the gibberellin pathway, which has a previously demonstrated important role in symbiosis development. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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25 pages, 4427 KiB

Open AccessArticle

The Role of Symbiotic Microorganisms, Nutrient Uptake and Rhizosphere Bacterial Community in Response of Pea (Pisum sativum L.) Genotypes to Elevated Al Concentrations in Soil

by Andrey A. Belimov, Alexander I. Shaposhnikov, Darya S. Syrova, Arina A. Kichko, Polina V. Guro, Oleg S. Yuzikhin, Tatiana S. Azarova, Anna L. Sazanova, Edgar A. Sekste, Vladimir A. Litvinskiy, Vladimir V. Nosikov, Aleksey A. Zavalin, Evgeny E. Andronov and Vera I. Safronova

Plants 2020, 9(12), 1801; https://doi.org/10.3390/plants9121801 - 18 Dec 2020

Cited by 12 | Viewed by 2958

Abstract

Aluminium being one of the most abundant elements is very toxic for plants causing inhibition of nutrient uptake and productivity. The aim of this study was to evaluate the potential of microbial consortium consisting of arbuscular mycorrhizal fungus (AMF), rhizobia and PGPR for counteracting negative effects of Al toxicity on four pea genotypes differing in Al tolerance. Pea plants were grown in acid soil supplemented with AlCl₃ (pH_KCl = 4.5) or neutralized with CaCO₃ (pH_KCl = 6.2). Inoculation increased shoot and/or seed biomass of plants grown in Al-supplemented soil. Nodule number and biomass were about twice on roots of Al-treated genotypes after inoculation. Inoculation decreased concentrations of water-soluble Al in the rhizosphere of all genotypes grown in Al-supplemented soil by about 30%, improved N₂ fixation and uptake of fertilizer ¹⁵N and nutrients from soil, and increased concentrations of water-soluble nutrients in the rhizosphere. The structure of rhizospheric microbial communities varied to a greater extent depending on the plant genotype, as compared to soil conditions and inoculation. Thus, this study highlights the important role of symbiotic microorganisms and the plant genotype in complex interactions between the components of the soil-microorganism-plant continuum subjected to Al toxicity. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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16 pages, 2227 KiB

Open AccessFeature PaperArticle

Analysis of the Interaction between Pisum sativum L. and Rhizobium laguerreae Strains Nodulating This Legume in Northwest Spain

by José David Flores-Félix, Lorena Carro, Eugenia Cerda-Castillo, Andrea Squartini, Raúl Rivas and Encarna Velázquez

Plants 2020, 9(12), 1755; https://doi.org/10.3390/plants9121755 - 11 Dec 2020

Cited by 7 | Viewed by 3335

Abstract

Pisum sativum L. (pea) is one of the most cultivated grain legumes in European countries due to the high protein content of its seeds. Nevertheless, the rhizobial microsymbionts of this legume have been scarcely studied in these countries. In this work, we analyzed the rhizobial strains nodulating the pea in a region from Northwestern Spain, where this legume is widely cultivated. The isolated strains were genetically diverse, and the phylogenetic analysis of core and symbiotic genes showed that these strains belong to different clusters related to R. laguerreae sv. viciae. Representative strains of these clusters were able to produce cellulose and cellulases, which are two key molecules in the legume infection process. They formed biofilms and produced acyl-homoserine lactones (AHLs), which are involved in the quorum sensing regulation process. They also exhibited several plant growth promotion mechanisms, including phosphate solubilization, siderophore, and indole acetic acid production and symbiotic atmospheric nitrogen fixation. All strains showed high symbiotic efficiency on pea plants, indicating that strains of R. laguerreae sv. viciae are promising candidates for the biofertilization of this legume worldwide. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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16 pages, 4376 KiB

Open AccessArticle

Transcriptome Analysis of Alternative Splicing Events Induced by Arbuscular Mycorrhizal Fungi (Rhizophagus irregularis) in Pea (Pisum sativum L.) Roots

by Evgeny A. Zorin, Alexey M. Afonin, Olga A. Kulaeva, Emma S. Gribchenko, Oksana Y. Shtark and Vladimir A. Zhukov

Plants 2020, 9(12), 1700; https://doi.org/10.3390/plants9121700 - 03 Dec 2020

Cited by 8 | Viewed by 2814

Abstract

Alternative splicing (AS), a process that enables formation of different mRNA isoforms due to alternative ways of pre-mRNA processing, is one of the mechanisms for fine-tuning gene expression. Currently, the role of AS in symbioses formed by plants with soil microorganisms is not fully understood. In this work, a comprehensive analysis of the transcriptome of garden pea (Pisum sativum L.) roots in symbiosis with arbuscular mycorrhiza was performed using RNAseq and following bioinformatic analysis. AS profiles of mycorrhizal and control roots were highly similar, intron retention accounting for a large proportion of the observed AS types (67%). Using three different tools (SUPPA2, DRIMSeq and IsoformSwitchAnalyzeR), eight genes with AS events specific for mycorrhizal roots of pea were identified, among which four were annotated as encoding an apoptosis inhibitor protein, a serine/threonine-protein kinase, a dehydrodolichyl diphosphate synthase, and a pre-mRNA-splicing factor ATP-dependent RNA helicase DEAH1. In pea mycorrhizal roots, the isoforms of these four genes with preliminary stop codons leading to a truncated ORFs were up-regulated. Interestingly, two of these four genes demonstrating mycorrhiza-specific AS are related to the process of splicing, thus forming parts of the feedback loops involved in fine-tuning of gene expression during mycorrhization. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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12 pages, 2702 KiB

Open AccessCommunication

Shoot Extracts from Two Low Nodulation Mutants Significantly Reduce Nodule Number in Pea

by Christian A. Huynh and Frédérique C. Guinel

Plants 2020, 9(11), 1505; https://doi.org/10.3390/plants9111505 - 06 Nov 2020

Cited by 2 | Viewed by 2072

Abstract

E107 and E132 are pea mutants that nodulate poorly. Because they have a shoot-controlled nodulation phenotype, we asked if their mutated genes were implicated in the autoregulation of nodulation (AON), a mechanism which consists of two systemic circuits, the positive CEP/CRA2 and the negative CLE/SUNN, coordinated via NIN and miR2111. We further characterized the mutants’ phenotype by studying nodule distribution and nodulation efficiency. E107 was similar to wild-type (WT) in its nodule distribution, but E132 had an extended nodulation zone with nodules forming distally on its lateral roots. Moreover, we tested whether their shoots produced a compound inhibitory to nodulation. We made ethyl-acetate extracts of roots and shoots of both mutants and WT, which we applied to rhizobia-inoculated WT seedlings and to pure rhizobial cultures. Whereas free-living bacteria were unaffected by any of the extracts, WT treated with shoot extracts from either inoculated mutant had fewer nodules than that of control. E107 and E132 shoot extracts led to a 50% and a 35% reduction in nodule number, respectively. We propose that E107 and E132 belong to a new sub-class of AON mutants, i.e., hypo-nodulators, and that their respective gene products are acting in the AON descending branch, upstream of TML signaling. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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22 pages, 11156 KiB

Open AccessArticle

The Fungicide Tetramethylthiuram Disulfide Negatively Affects Plant Cell Walls, Infection Thread Walls, and Symbiosomes in Pea (Pisum sativum L.) Symbiotic Nodules

by Artemii P. Gorshkov, Anna V. Tsyganova, Maxim G. Vorobiev and Viktor E. Tsyganov

Plants 2020, 9(11), 1488; https://doi.org/10.3390/plants9111488 - 04 Nov 2020

Cited by 14 | Viewed by 3361

Abstract

In Russia, tetramethylthiuram disulfide (TMTD) is a fungicide widely used in the cultivation of legumes, including the pea (Pisum sativum). Application of TMTD can negatively affect nodulation; nevertheless, its effect on the histological and ultrastructural organization of nodules has not previously been investigated. In this study, the effect of TMTD at three concentrations (0.4, 4, and 8 g/kg) on nodule development in three pea genotypes (laboratory lines Sprint-2 and SGE, and cultivar ‘Finale’) was examined. In SGE, TMTD at 0.4 g/kg reduced the nodule number and shoot and root fresh weights. Treatment with TMTD at 8 g/kg changed the nodule color from pink to green, indicative of nodule senescence. Light and transmission electron microscopy analyses revealed negative effects of TMTD on nodule structure in each genotype. ‘Finale’ was the most sensitive cultivar to TMTD and Sprint-2 was the most tolerant. The negative effects of TMTD on nodules included the appearance of a senescence zone, starch accumulation, swelling of cell walls accompanied by a loss of electron density, thickening of the infection thread walls, symbiosome fusion, and bacteroid degradation. These results demonstrate how TMTD adversely affects nodules in the pea and will be useful for developing strategies to optimize fungicide use on legume crops. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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21 pages, 1996 KiB

Open AccessArticle

Microbial Consortium of PGPR, Rhizobia and Arbuscular Mycorrhizal Fungus Makes Pea Mutant SGECd^t Comparable with Indian Mustard in Cadmium Tolerance and Accumulation

by Andrey A. Belimov, Alexander I. Shaposhnikov, Tatiana S. Azarova, Natalia M. Makarova, Vera I. Safronova, Vladimir A. Litvinskiy, Vladimir V. Nosikov, Aleksey A. Zavalin and Igor A. Tikhonovich

Plants 2020, 9(8), 975; https://doi.org/10.3390/plants9080975 - 31 Jul 2020

Cited by 25 | Viewed by 3121

Abstract

Cadmium (Cd) is one of the most widespread and toxic soil pollutants that inhibits plant growth and microbial activity. Polluted soils can be remediated using plants that either accumulate metals (phytoextraction) or convert them to biologically inaccessible forms (phytostabilization). The phytoremediation potential of a symbiotic system comprising the Cd-tolerant pea (Pisum sativum L.) mutant SGECd^t and selected Cd-tolerant microorganisms, such as plant growth-promoting rhizobacterium Variovorax paradoxus 5C-2, nodule bacterium Rhizobium leguminosarum bv. viciae RCAM1066, and arbuscular mycorrhizal fungus Glomus sp. 1Fo, was evaluated in comparison with wild-type pea SGE and the Cd-accumulating plant Indian mustard (Brassica juncea L. Czern.) VIR263. Plants were grown in pots in sterilized uncontaminated or Cd-supplemented (15 mg Cd kg⁻¹) soil and inoculated or not with the microbial consortium. Cadmium significantly inhibited growth of uninoculated and particularly inoculated SGE plants, but had no effect on SGECd^t and decreased shoot biomass of B. juncea. Inoculation with the microbial consortium more than doubled pea biomass (both genotypes) irrespective of Cd contamination, but had little effect on B. juncea biomass. Cadmium decreased nodule number and acetylene reduction activity of SGE by 5.6 and 10.8 times, whereas this decrease in SGECd^t was 2.1 and 2.8 times only, and the frequency of mycorrhizal structures decreased only in SGE roots. Inoculation decreased shoot Cd concentration and increased seed Cd concentration of both pea genotypes, but had little effect on Cd concentration of B. juncea. Inoculation also significantly increased concentration and/or accumulation of nutrients (Ca, Fe, K, Mg, Mn, N, P, S, and Zn) by Cd-treated pea plants, particularly by the SGECd^t mutant. Shoot Cd concentration of SGECd^t was twice that of SGE, and the inoculated SGECd^t had approximately similar Cd accumulation capacity as compared with B. juncea. Thus, plant–microbe systems based on Cd-tolerant micro-symbionts and plant genotypes offer considerable opportunities to increase plant HM tolerance and accumulation. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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Review

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29 pages, 3822 KiB

Open AccessReview

Symbiotic Regulatory Genes Controlling Nodule Development in Pisum sativum L.

by Viktor E. Tsyganov and Anna V. Tsyganova

Plants 2020, 9(12), 1741; https://doi.org/10.3390/plants9121741 - 09 Dec 2020

Cited by 20 | Viewed by 3165

Abstract

Analyses of natural variation and the use of mutagenesis and molecular-biological approaches have revealed 50 symbiotic regulatory genes in pea (Pisum sativum L.). Studies of genomic synteny using model legumes, such as Medicago truncatula Gaertn. and Lotus japonicus (Regel) K. Larsen, have identified the sequences of 15 symbiotic regulatory genes in pea. These genes encode receptor kinases, an ion channel, a calcium/calmodulin-dependent protein kinase, transcription factors, a metal transporter, and an enzyme. This review summarizes and describes mutant alleles, their phenotypic manifestations, and the functions of all identified symbiotic regulatory genes in pea. Some examples of gene interactions are also given. In the review, all mutant alleles in genes with identified sequences are designated and still-unidentified symbiotic regulatory genes of great interest are considered. The identification of these genes will help elucidate additional components involved in infection thread growth, nodule primordium development, bacteroid differentiation and maintenance, and the autoregulation of nodulation. The significance of symbiotic mutants of pea as extremely fruitful genetic models for studying nodule development and for comparative cell biology studies of legume nodules is clearly demonstrated. Finally, it is noted that many more sequences of symbiotic regulatory genes remain to be identified. Transcriptomics approaches and genome-wide sequencing could help address this challenge. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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25 pages, 959 KiB

Open AccessEditor’s ChoiceReview

Significance of Plant Growth Promoting Rhizobacteria in Grain Legumes: Growth Promotion and Crop Production

by Karivaradharajan Swarnalakshmi, Vandana Yadav, Deepti Tyagi, Dolly Wattal Dhar, Annapurna Kannepalli and Shiv Kumar

Plants 2020, 9(11), 1596; https://doi.org/10.3390/plants9111596 - 17 Nov 2020

Cited by 87 | Viewed by 10988

Abstract

Grain legumes are an important component of sustainable agri-food systems. They establish symbiotic association with rhizobia and arbuscular mycorrhizal fungi, thus reducing the use of chemical fertilizers. Several other free-living microbial communities (PGPR—plant growth promoting rhizobacteria) residing in the soil-root interface are also known to influence biogeochemical cycles and improve legume productivity. The growth and function of these microorganisms are affected by root exudate molecules secreted in the rhizosphere region. PGPRs produce the chemicals which stimulate growth and functions of leguminous crops at different growth stages. They promote plant growth by nitrogen fixation, solubilization as well as mineralization of phosphorus, and production of phytohormone(s). The co-inoculation of PGPRs along with rhizobia has shown to enhance nodulation and symbiotic interaction. The recent molecular tools are helpful to understand and predict the establishment and function of PGPRs and plant response. In this review, we provide an overview of various growth promoting mechanisms of PGPR inoculations in the production of leguminous crops. Full article

(This article belongs to the Special Issue Pea-Rhizobial and Pea-Mycorrhizal Symbioses)

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