Development of the Legume Root Nodules

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

Deadline for manuscript submissions: closed (30 June 2023) | Viewed by 17048

Special Issue Editors


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Guest Editor
All-Russia Research Institute for Agricultural Microbiology, Podbelsky Chausse 3, Pushkin, 196608 St. Petersburg, Russia
Interests: legume-rhizobial symbiosis; receptors; signal transduction; plant transformation; protein expression

E-Mail Website
Guest Editor
Laboratory of Plant Microbe Environment Interactions (LIPME), Toulouse, France
Interests: root and nodule development similarities and specificities in legumes; effect of symbiotic molecules on root development

Special Issue Information

Dear Colleagues,

The formation of symbiotic nitrogen-fixing nodules represents a process in which the development of new organs substantially depends on the impact of exogenous and endogenous factors. This regulation can be achieved by means of a complex network of receptors, transcription factors and phytohormones. However, the exact mechanisms underlying such interactions to regulate nodulation remain unknown. The development of the legume root nodule raises many interesting questions concerning plant cell proliferation and differentiation, concerted alteration in the pattern of gene expression in plant and bacterial cells, signal regulation and phytohormonal control, as well as similarities with other development processes, such as lateral root formation. This Special Issue of Plants will highlight the latest data concerning developmental regulation of nodulation.

Dr. Elena Dolgikh
Dr. Sandra Bensmihen
Guest Editors

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Keywords

  • legume-rhizobial symbiosis
  • nodulation
  • transcription factors
  • phytohormones

Published Papers (6 papers)

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Research

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18 pages, 3310 KiB  
Article
Exogenously Applied Cytokinin Altered the Bacterial Release and Subsequent Stages of Nodule Development in Pea Ipd3/Cyclops Mutant
by Elizaveta S. Kantsurova (Rudaya), Alexandra N. Ivanova, Polina Y. Kozyulina and Elena A. Dolgikh
Plants 2023, 12(3), 657; https://0-doi-org.brum.beds.ac.uk/10.3390/plants12030657 - 2 Feb 2023
Cited by 1 | Viewed by 1494
Abstract
Regulation of plant hormonal status is one of the major targets of symbiotic signaling during nodule formation in legume plants. However, the genetic and hormonal networks that regulate transition to differentiation of nodules are not well-characterized in legume plants. Analysis of plant mutants [...] Read more.
Regulation of plant hormonal status is one of the major targets of symbiotic signaling during nodule formation in legume plants. However, the genetic and hormonal networks that regulate transition to differentiation of nodules are not well-characterized in legume plants. Analysis of plant mutants forming nodules impaired in rhizobial infection allowed us to identify some regulators involved in the control of the later stages of nodule development. In the current work, we extend our earlier studies on the influence of exogenously applied cytokinin on the later stages of nodule morphogenesis using pea sym33 (ipd3/cyclops) mutants impaired in the gene encoding IPD3/CYCLOPS transcription factor. One of the noticeable effects of the influence of exogenously applied cytokinin on nodules in the sym33-3 mutant was an increasing size of these structures. Cytokinin treatment was shown to stimulate bacterial release and increase the percentage of infected cells in nodules. To explore the role of possible regulators of nodule differentiation, we performed searching in pea transcriptome. The transcriptome study in pea P. sativum revealed the importance of the CCS52 regulator, EFD transcription factor, SYMREM regulator, RSD, the MADS-domain/AGL, and SHORT INTERNODE/STYLISH gene families encoding transcription factors in the control of nodule differentiation. Analysis of the expression patterns was verified by real-time PCR in response to exogenously applied cytokinin treatment. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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13 pages, 2231 KiB  
Article
High-Throughput Root Imaging Analysis Reveals Wide Variation in Root Morphology of Wild Adzuki bean (Vigna angularis) Accessions
by Rupesh Tayade, Seong-Hoon Kim, Pooja Tripathi, Yi-Dam Choi, Jung-Beom Yoon and Yoon-Ha Kim
Plants 2022, 11(3), 405; https://0-doi-org.brum.beds.ac.uk/10.3390/plants11030405 - 1 Feb 2022
Cited by 8 | Viewed by 2434
Abstract
Root system architecture and morphological diversification in wild accessions are important for crop improvement and productivity in adzuki beans. In this study, via analysis using 2-dimensional (2D) root imaging and WinRHIZO Pro software, we described the root traits of 61 adzuki bean accessions [...] Read more.
Root system architecture and morphological diversification in wild accessions are important for crop improvement and productivity in adzuki beans. In this study, via analysis using 2-dimensional (2D) root imaging and WinRHIZO Pro software, we described the root traits of 61 adzuki bean accessions in their early vegetative growth stage. These accessions were chosen for study because they are used in Korea’s crop improvement programs; however, their root traits have not been sufficiently investigated. Analysis of variance revealed a significant difference between the accessions of all measured root traits. Distribution analysis demonstrated that most of the root traits followed normal distribution. The accessions showed up to a 17-fold increase in the values in contrasting accessions for the root traits. For total root length (TRL), the values ranged from 82.43 to 1435 cm, and for surface area (SA), they ranged from 12.30 to 208.39 cm2. The values for average diameter (AD) ranged from 0.23 to 0.56 mm. Significant differences were observed for other traits. Overall, the results showed that the accession IT 305544 had the highest TRL, SA, and number of tips (NT), whereas IT 262477 and IT 262492 showed the lowest values for TRL, SA, and AD. Principal component analysis showed an 89% variance for PC1 and PC2. K-mean clustering explained 77.4% of the variance in the data and grouped the accessions into three clusters. All six root traits had greater coefficients of variation (≥15%) among the tested accessions. Furthermore, to determine which root traits best distinguished different accessions, the correlation within our set of accessions provided trait-based ranking depending on their contribution. The identified accessions may be advantageous for the development of new crossing combinations to improve root features in adzuki beans during the early growth stage. The root traits assessed in this study could be attributes for future adzuki bean crop selection and improvement. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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19 pages, 2724 KiB  
Article
Regulation of the Later Stages of Nodulation Stimulated by IPD3/CYCLOPS Transcription Factor and Cytokinin in Pea Pisum sativum L.
by Elizaveta S. Rudaya, Polina Yu. Kozyulina, Olga A. Pavlova, Alexandra V. Dolgikh, Alexandra N. Ivanova and Elena A. Dolgikh
Plants 2022, 11(1), 56; https://0-doi-org.brum.beds.ac.uk/10.3390/plants11010056 - 25 Dec 2021
Cited by 5 | Viewed by 3320
Abstract
The IPD3/CYCLOPS transcription factor was shown to be involved in the regulation of nodule primordia development and subsequent stages of nodule differentiation. In contrast to early stages, the stages related to nodule differentiation remain less studied. Recently, we have shown that the accumulation [...] Read more.
The IPD3/CYCLOPS transcription factor was shown to be involved in the regulation of nodule primordia development and subsequent stages of nodule differentiation. In contrast to early stages, the stages related to nodule differentiation remain less studied. Recently, we have shown that the accumulation of cytokinin at later stages may significantly impact nodule development. This conclusion was based on a comparative analysis of cytokinin localization between pea wild type and ipd3/cyclops mutants. However, the role of cytokinin at these later stages of nodulation is still far from understood. To determine a set of genes involved in the regulation of later stages of nodule development connected with infection progress, intracellular accommodation, as well as plant tissue and bacteroid differentiation, the RNA-seq analysis of pea mutant SGEFix--2 (sym33) nodules impaired in these processes compared to wild type SGE nodules was performed. To verify cytokinin’s influence on late nodule development stages, the comparative RNA-seq analysis of SGEFix--2 (sym33) mutant plants treated with cytokinin was also conducted. Findings suggest a significant role of cytokinin in the regulation of later stages of nodule development. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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Review

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33 pages, 1140 KiB  
Review
Arbuscular Mycorrhizal Symbiosis: A Strategy for Mitigating the Impacts of Climate Change on Tropical Legume Crops
by Wan Teng Loo, Kah-Ooi Chua, Purabi Mazumdar, Acga Cheng, Normaniza Osman and Jennifer Ann Harikrishna
Plants 2022, 11(21), 2875; https://0-doi-org.brum.beds.ac.uk/10.3390/plants11212875 - 27 Oct 2022
Cited by 14 | Viewed by 2919
Abstract
Climate change is likely to have severe impacts on food security in the topics as these regions of the world have both the highest human populations and narrower climatic niches, which reduce the diversity of suitable crops. Legume crops are of particular importance [...] Read more.
Climate change is likely to have severe impacts on food security in the topics as these regions of the world have both the highest human populations and narrower climatic niches, which reduce the diversity of suitable crops. Legume crops are of particular importance to food security, supplying dietary protein for humans both directly and in their use for feed and forage. Other than the rhizobia associated with legumes, soil microbes, in particular arbuscular mycorrhizal fungi (AMF), can mitigate the effects of biotic and abiotic stresses, offering an important complementary measure to protect crop yields. This review presents current knowledge on AMF, highlights their beneficial role, and explores the potential for application of AMF in mitigating abiotic and biotic challenges for tropical legumes. Due to the relatively little study on tropical legume species compared to their temperate growing counterparts, much further research is needed to determine how similar AMF–plant interactions are in tropical legumes, which AMF species are optimal for agricultural deployment and especially to identify anaerobic AMF species that could be used to mitigate flood stress in tropical legume crop farming. These opportunities for research also require international cooperation and support, to realize the promise of tropical legume crops to contribute to future food security. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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22 pages, 563 KiB  
Review
At the Root of Nodule Organogenesis: Conserved Regulatory Pathways Recruited by Rhizobia
by Maria Lebedeva, Mahboobeh Azarakhsh, Darina Sadikova and Lyudmila Lutova
Plants 2021, 10(12), 2654; https://0-doi-org.brum.beds.ac.uk/10.3390/plants10122654 - 2 Dec 2021
Cited by 7 | Viewed by 3450
Abstract
The interaction between legume plants and soil bacteria rhizobia results in the formation of new organs on the plant roots, symbiotic nodules, where rhizobia fix atmospheric nitrogen. Symbiotic nodules represent a perfect model to trace how the pre-existing regulatory pathways have been recruited [...] Read more.
The interaction between legume plants and soil bacteria rhizobia results in the formation of new organs on the plant roots, symbiotic nodules, where rhizobia fix atmospheric nitrogen. Symbiotic nodules represent a perfect model to trace how the pre-existing regulatory pathways have been recruited and modified to control the development of evolutionary “new” organs. In particular, genes involved in the early stages of lateral root development have been co-opted to regulate nodule development. Other regulatory pathways, including the players of the KNOX-cytokinin module, the homologues of the miR172-AP2 module, and the players of the systemic response to nutrient availability, have also been recruited to a unique regulatory program effectively governing symbiotic nodule development. The role of the NIN transcription factor in the recruitment of such regulatory modules to nodulation is discussed in more details. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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Other

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11 pages, 3617 KiB  
Protocol
Development of High-Quality Nuclei Isolation to Study Plant Root–Microbe Interaction for Single-Nuclei Transcriptomic Sequencing in Soybean
by Leonidas W. D’Agostino, Lenin Yong-Villalobos, Luis Herrera-Estrella and Gunvant B. Patil
Plants 2023, 12(13), 2466; https://0-doi-org.brum.beds.ac.uk/10.3390/plants12132466 - 28 Jun 2023
Viewed by 2122
Abstract
Single-nucleus RNA sequencing (sNucRNA-seq) is an emerging technology that has been rapidly adopted and demonstrated to be a powerful tool for detailed characterization of each cell- and sub cell-types in complex tissues of higher eukaryotes. sNucRNA-seq has also been used to dissect cell-type-specific [...] Read more.
Single-nucleus RNA sequencing (sNucRNA-seq) is an emerging technology that has been rapidly adopted and demonstrated to be a powerful tool for detailed characterization of each cell- and sub cell-types in complex tissues of higher eukaryotes. sNucRNA-seq has also been used to dissect cell-type-specific transcriptional responses to environmental or developmental signals. In plants, this technology is being utilized to identify cell-type-specific trajectories for the study of several tissue types and important traits, including the single-cell dissection of the genetic determinants regulating plant–microbe interactions. The isolation of high-quality nuclei is one of the prerequisite steps to obtain high-quality sNucRNA-seq results. Although nuclei isolation from several plant tissues is well established, this process is highly troublesome when plant tissues are associated with beneficial or pathogenic microbes. For example, root tissues colonized with rhizobium bacteria (nodules), leaf tissue infected with bacterial or fungal pathogens, or roots infected with nematodes pose critical challenges to the isolation of high-quality nuclei and use for downstream application. Therefore, isolation of microbe-free, high-quality nuclei from plant tissues are necessary to avoid clogging or interference with the microfluidic channel (e.g., 10× Genomics) or particle-templated emulsion that are used in sNucRNA-seq platforms. Here, we developed a simple, effective, and efficient method to isolate high-quality nuclei from soybean roots and root nodules, followed by washing out bacterial contamination. This protocol has been designed to be easily implemented into any lab environment, and it can also be scaled up for use with multiple samples and applicable to a variety of samples with the presence of microbes. We validated this protocol by successfully generating a barcoded library using the 10× Genomics microfluidic platform from tissue subjected to this procedure. This workflow was developed to provide an accessible alternative to instrument-based approaches (e.g., fluorescent cell sorting) and will expand the ability of researchers to perform experiments such as sNucRNA-seq and sNucATAC-seq on inherently heterogeneous plant tissue samples. Full article
(This article belongs to the Special Issue Development of the Legume Root Nodules)
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