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Plant Rhizobium Interactions

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

Deadline for manuscript submissions: 16 June 2024 | Viewed by 5077

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Guest Editor
State Key Laboratory of Agriculture Microbiology, Hubei Hongshan Laboratory, Huazhong Agriculture University, Wuhan 430000, China
Interests: plant-microbe interactions; legume-rhizobial symbiosis; MAMP-trigged plant immunity
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Special Issue Information

Dear Colleagues,

The symbiotic interaction between legumes and rhizobia results in the formation of nodules, where nitrogen gas is reduced into ammonium for plant hosts. However, the rhizobium host range is largely limited to the family of leguminous plants (Fabaceae), and it would be a huge challenge to transfer this ability to nonlegumes. This Special Issue will highlight some of the key findings in the molecular basis of legume–rhizobial interaction, as well as review articles that covers rhizobial symbiosis. We also invite submissions of original research articles that provide novel insights into all areas of legume–rhizobial symbiosis.

Dr. Yangrong Cao
Guest Editor

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Published Papers (6 papers)

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Research

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12 pages, 2501 KiB  
Article
Overexpression of GmPAP4 Enhances Symbiotic Nitrogen Fixation and Seed Yield in Soybean under Phosphorus-Deficient Condition
by Xi Sun, Huantao Zhang, Zhanwu Yang, Xinzhu Xing, Zhao Fu, Xihuan Li, Youbin Kong, Wenlong Li, Hui Du and Caiying Zhang
Int. J. Mol. Sci. 2024, 25(7), 3649; https://doi.org/10.3390/ijms25073649 - 25 Mar 2024
Viewed by 526
Abstract
Legume crops establish symbiosis with nitrogen-fixing rhizobia for biological nitrogen fixation (BNF), a process that provides a prominent natural nitrogen source in agroecosystems; and efficient nodulation and nitrogen fixation processes require a large amount of phosphorus (P). Here, a role of GmPAP4, a [...] Read more.
Legume crops establish symbiosis with nitrogen-fixing rhizobia for biological nitrogen fixation (BNF), a process that provides a prominent natural nitrogen source in agroecosystems; and efficient nodulation and nitrogen fixation processes require a large amount of phosphorus (P). Here, a role of GmPAP4, a nodule-localized purple acid phosphatase, in BNF and seed yield was functionally characterized in whole transgenic soybean (Glycine max) plants under a P-limited condition. GmPAP4 was specifically expressed in the infection zones of soybean nodules and its expression was greatly induced in low P stress. Altered expression of GmPAP4 significantly affected soybean nodulation, BNF, and yield under the P-deficient condition. Nodule number, nodule fresh weight, nodule nitrogenase, APase activities, and nodule total P content were significantly increased in GmPAP4 overexpression (OE) lines. Structural characteristics revealed by toluidine blue staining showed that overexpression of GmPAP4 resulted in a larger infection area than wild-type (WT) control. Moreover, the plant biomass and N and P content of shoot and root in GmPAP4 OE lines were also greatly improved, resulting in increased soybean yield in the P-deficient condition. Taken together, our results demonstrated that GmPAP4, a purple acid phosphatase, increased P utilization efficiency in nodules under a P-deficient condition and, subsequently, enhanced symbiotic BNF and seed yield of soybean. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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20 pages, 4182 KiB  
Article
Effects of Elevated Temperature on Pisum sativum Nodule Development: I—Detailed Characteristic of Unusual Apical Senescence
by Tatiana A. Serova, Pyotr G. Kusakin, Anna B. Kitaeva, Elena V. Seliverstova, Artemii P. Gorshkov, Daria A. Romanyuk, Vladimir A. Zhukov, Anna V. Tsyganova and Viktor E. Tsyganov
Int. J. Mol. Sci. 2023, 24(24), 17144; https://doi.org/10.3390/ijms242417144 - 05 Dec 2023
Cited by 3 | Viewed by 798
Abstract
Despite global warming, the influence of heat on symbiotic nodules is scarcely studied. In this study, the effects of heat stress on the functioning of nodules formed by Rhizobium leguminosarum bv. viciae strain 3841 on pea (Pisum sativum) line SGE were [...] Read more.
Despite global warming, the influence of heat on symbiotic nodules is scarcely studied. In this study, the effects of heat stress on the functioning of nodules formed by Rhizobium leguminosarum bv. viciae strain 3841 on pea (Pisum sativum) line SGE were analyzed. The influence of elevated temperature was analyzed at histological, ultrastructural, and transcriptional levels. As a result, an unusual apical pattern of nodule senescence was revealed. After five days of exposure, a senescence zone with degraded symbiotic structures was formed in place of the distal nitrogen fixation zone. There was downregulation of various genes, including those associated with the assimilation of fixed nitrogen and leghemoglobin. After nine days, the complete destruction of the nodules was demonstrated. It was shown that nodule recovery was possible after exposure to elevated temperature for 3 days but not after 5 days (which coincides with heat wave duration). At the same time, the exposure of plants to optimal temperature during the night leveled the negative effects. Thus, the study of the effects of elevated temperature on symbiotic nodules using a well-studied pea genotype and Rhizobium strain led to the discovery of a novel positional response of the nodule to heat stress. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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18 pages, 34455 KiB  
Article
Effects of Elevated Temperature on Pisum sativum Nodule Development: II—Phytohormonal Responses
by Anna B. Kitaeva, Tatiana A. Serova, Pyotr G. Kusakin and Viktor E. Tsyganov
Int. J. Mol. Sci. 2023, 24(23), 17062; https://doi.org/10.3390/ijms242317062 - 02 Dec 2023
Cited by 1 | Viewed by 825
Abstract
High temperature is one of the most important factors limiting legume productivity. We have previously shown the induction of senescence in the apical part of nodules of the pea SGE line, formed by Rhizobium leguminosarum bv. viciae strain 3841, when they were exposed [...] Read more.
High temperature is one of the most important factors limiting legume productivity. We have previously shown the induction of senescence in the apical part of nodules of the pea SGE line, formed by Rhizobium leguminosarum bv. viciae strain 3841, when they were exposed to elevated temperature (28 °C). In this study, we analyzed the potential involvement of abscisic acid (ABA), ethylene, and gibberellins in apical senescence in pea nodules under elevated temperature. Immunolocalization revealed an increase in ABA and 1-aminocyclopropane-1-carboxylic acid (ACC, the precursor of ethylene biosynthesis) levels in cells of the nitrogen fixation zone in heat-stressed nodules in 1 day of exposure compared to heat-unstressed nodules. Both ABA and ethylene appear to be involved in the earliest responses of nodules to heat stress. A decrease in the gibberellic acid (GA3) level in heat-stressed nodules was observed. Exogenous GA3 treatment induced a delay in the degradation of the nitrogen fixation zone in heat-stressed nodules. At the same time, a decrease in the expression level of many genes associated with nodule senescence, heat shock, and defense responses in pea nodules treated with GA3 at an elevated temperature was detected. Therefore, apical senescence in heat-stressed nodules is regulated by phytohormones in a manner similar to natural senescence. Gibberellins can be considered as negative regulators, while ABA and ethylene can be considered positive regulators. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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22 pages, 6112 KiB  
Article
Dual RNA-Seq Analysis Pinpoints a Balanced Regulation between Symbiosis and Immunity in Medicago truncatula-Sinorhizobium meliloti Symbiotic Nodules
by Dandan Zhang, Qiujin Wu, Yanwen Zhao, Ziang Yan, Aifang Xiao, Haixiang Yu and Yangrong Cao
Int. J. Mol. Sci. 2023, 24(22), 16178; https://doi.org/10.3390/ijms242216178 - 10 Nov 2023
Cited by 1 | Viewed by 890
Abstract
Legume–rhizobial symbiosis initiates the formation of root nodules, within which rhizobia reside and differentiate into bacteroids to convert nitrogen into ammonium, facilitating plant growth. This process raises a fundamental question: how is plant immunity modulated within nodules when exposed to a substantial number [...] Read more.
Legume–rhizobial symbiosis initiates the formation of root nodules, within which rhizobia reside and differentiate into bacteroids to convert nitrogen into ammonium, facilitating plant growth. This process raises a fundamental question: how is plant immunity modulated within nodules when exposed to a substantial number of foreign bacteria? In Medicago truncatula, a mutation in the NAD1 (Nodules with Activated Defense 1) gene exclusively results in the formation of necrotic nodules combined with activated immunity, underscoring the critical role of NAD1 in suppressing immunity within nodules. In this study, we employed a dual RNA-seq transcriptomic technology to comprehensively analyze gene expression from both hosts and symbionts in the nad1-1 mutant nodules at different developmental stages (6 dpi and 10 dpi). We identified 89 differentially expressed genes (DEGs) related to symbiotic nitrogen fixation and 89 DEGs from M. truncatula associated with immunity in the nad1-1 nodules. Concurrently, we identified 27 rhizobial DEGs in the fix and nif genes of Sinorhizobium meliloti. Furthermore, we identified 56 DEGs from S. meliloti that are related to stress responses to ROS and NO. Our analyses of nitrogen fixation-defective plant nad1-1 mutants with overactivated defenses suggest that the host employs plant immunity to regulate the substantial bacterial colonization in nodules. These findings shed light on the role of NAD1 in inhibiting the plant’s immune response to maintain numerous rhizobial endosymbiosis in nodules. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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29 pages, 13019 KiB  
Article
Comparison of the Formation of Plant–Microbial Interface in Pisum sativum L. and Medicago truncatula Gaertn. Nitrogen-Fixing Nodules
by Anna V. Tsyganova, Elena V. Seliverstova and Viktor E. Tsyganov
Int. J. Mol. Sci. 2023, 24(18), 13850; https://doi.org/10.3390/ijms241813850 - 08 Sep 2023
Cited by 1 | Viewed by 810
Abstract
Different components of the symbiotic interface play an important role in providing positional information during rhizobial infection and nodule development: successive changes in cell morphology correspond to subsequent changes in the molecular architecture of the apoplast and the associated surface structures. The localisation [...] Read more.
Different components of the symbiotic interface play an important role in providing positional information during rhizobial infection and nodule development: successive changes in cell morphology correspond to subsequent changes in the molecular architecture of the apoplast and the associated surface structures. The localisation and distribution of pectins, xyloglucans, and cell wall proteins in symbiotic nodules of Pisum sativum and Medicago truncatula were studied using immunofluorescence and immunogold analysis in wild-type and ineffective mutant nodules. As a result, the ontogenetic changes in the symbiotic interface in the nodules of both species were described. Some differences in the patterns of distribution of cell wall polysaccharides and proteins between wild-type and mutant nodules can be explained by the activation of defence reaction or premature senescence in mutants. The absence of fucosylated xyloglucan in the cell walls in the P. sativum nodules, as well as its predominant accumulation in the cell walls of uninfected cells in the M. truncatula nodules, and the presence of the rhamnogalacturonan I (unbranched) backbone in meristematic cells in P. sativum can be attributed to the most striking species-specific features of the symbiotic interface. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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Review

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14 pages, 1742 KiB  
Review
Autophagy and Symbiosis: Membranes, ER, and Speculations
by Maria G. Semenova, Alekandra N. Petina and Elena E. Fedorova
Int. J. Mol. Sci. 2024, 25(5), 2918; https://doi.org/10.3390/ijms25052918 - 02 Mar 2024
Viewed by 618
Abstract
The interaction of plants and soil bacteria rhizobia leads to the formation of root nodule symbiosis. The intracellular form of rhizobia, the symbiosomes, are able to perform the nitrogen fixation by converting atmospheric dinitrogen into ammonia, which is available for plants. The symbiosis [...] Read more.
The interaction of plants and soil bacteria rhizobia leads to the formation of root nodule symbiosis. The intracellular form of rhizobia, the symbiosomes, are able to perform the nitrogen fixation by converting atmospheric dinitrogen into ammonia, which is available for plants. The symbiosis involves the resource sharing between two partners, but this exchange does not include equivalence, which can lead to resource scarcity and stress responses of one of the partners. In this review, we analyze the possible involvement of the autophagy pathway in the process of the maintenance of the nitrogen-fixing bacteria intracellular colony and the changes in the endomembrane system of the host cell. According to in silico expression analysis, ATG genes of all groups were expressed in the root nodule, and the expression was developmental zone dependent. The analysis of expression of genes involved in the response to carbon or nitrogen deficiency has shown a suboptimal access to sugars and nitrogen in the nodule tissue. The upregulation of several ER stress genes was also detected. Hence, the root nodule cells are under heavy bacterial infection, carbon deprivation, and insufficient nitrogen supply, making nodule cells prone to autophagy. We speculate that the membrane formation around the intracellular rhizobia may be quite similar to the phagophore formation, and the induction of autophagy and ER stress are essential to the success of this process. Full article
(This article belongs to the Special Issue Plant Rhizobium Interactions)
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