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Biological Nitrogen Fixation
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Biological Nitrogen Fixation

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

Deadline for manuscript submissions: closed (30 April 2019) | Viewed by 37912

Special Issue Editor

Prof. Dr. Hari B. Krishnan

E-Mail Website
Guest Editor
Plant Genetics Research Unit, USDA-ARS, 108 Curtis Hall, University of Missouri, Columbia, MO 65211, USA
Interests: plant molecular biology; plant microbe interaction; soybean seed composition; biological nitrogen fixation; sulfur assimilation; plant biotechnology

Special Issue Information

Dear Colleagues,

Nitrogen is the most abundant element present in the Earth’s atmosphere and is essential for life. However, it occurs as chemically unreactive nitrogen gas (N2). This critical element is required for plant growth and productivity. It is a key component of proteins, nucleic acids, ATP and chlorophyll. Plants can only utilize reduced forms of nitrogen such as ammonia (NH3) or nitrate (NO3−). Some microorganisms, such as Rhizobia and Bradyrhizobia, have the unique ability to enter into a symbiotic relationship with legumes leading to the formation of nodules, where atmospheric nitrogen is reduced to ammonia. This reduced nitrogen is utilized by the plants for its growth and development, a process called biological nitrogen fixation (BNF). This sustainable process is beneficial for the environment since it can drastically reduce the use of polluting commercial fertilizers. Tremendous progress has been made during last few decades to understand the complex process of symbiotic nitrogen fixation that eventually could lead to the extension of BNF to non-leguminous crops. This Special Issue will cover a wide range of topics in the area of symbiotic nitrogen fixation. We invite investigators to submit original research articles that explore different topics on symbiotic nitrogen fixation including, but not limited to:

  • Regulation and genetics of nitrogen fixation
  • Carbon and nitrogen metabolism
  • Host-specificity in nodulation
  • R genes in the control of nodulation specificity
  • Rhizobial T3/T4 secretion systems and role of symbiotic effectors
  • Nodule-specific symbiotic peptides 
  • Extension of nitrogen fixation to other crops

Prof. Dr. Hari B. Krishnan
Guest Editor

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Keywords

  • Rhizobium-legume interaction
  • Nodulation
  • Effectors
  • T3/T4 secretion systems
  • Symbiosis
  • Nitrogen fixation
  • Host-specificity
  • R genes
  • Legumes

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Published Papers (8 papers)

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Research

20 pages, 3467 KiB  
Article
Biochemical and Anatomical Investigation of Sesbania herbacea (Mill.) McVaugh Nodules Grown under Flooded and Non-Flooded Conditions
by Hari B. Krishnan, Nathan W. Oehrle, Alaa A. Alaswad, William (Gene) Stevens, K. M. Maria John, Devanand L. Luthria and Savithiry S. Natarajan
Int. J. Mol. Sci. 2019, 20(8), 1824; https://doi.org/10.3390/ijms20081824 - 12 Apr 2019
Cited by 7 | Viewed by 5234
Abstract
Sesbania herbacea, a native North American fast-growing legume, thrives in wet and waterlogged conditions. This legume enters into symbiotic association with rhizobia, resulting in the formation of nitrogen-fixing nodules on the roots. A flooding-induced anaerobic environment imposes a challenge for the survival [...] Read more.
Sesbania herbacea, a native North American fast-growing legume, thrives in wet and waterlogged conditions. This legume enters into symbiotic association with rhizobia, resulting in the formation of nitrogen-fixing nodules on the roots. A flooding-induced anaerobic environment imposes a challenge for the survival of rhizobia and negatively impacts nodulation. Very little information is available on how S. herbacea is able to thrive and efficiently fix N2 in flooded conditions. In this study, we found that Sesbania plants grown under flooded conditions were significantly taller, produced more biomass, and formed more nodules when compared to plants grown on dry land. Transmission electron microscopy of Sesbania nodules revealed bacteroids from flooded nodules contained prominent polyhydroxybutyrate crystals, which were absent in non-flooded nodules. Gas and ion chromatography mass spectrometry analysis of nodule metabolites revealed a marked decrease in asparagine and an increase in the levels of gamma aminobutyric acid in flooded nodules. 2-D gel electrophoresis of nodule bacteroid proteins revealed flooding-induced changes in their protein profiles. Several of the bacteroid proteins that were prominent in flooded nodules were identified by mass spectrometry to be members of the ABC transporter family. The activities of several key enzymes involved in nitrogen metabolism was altered in Sesbania flooded nodules. Aspartate aminotransferase (AspAT), an enzyme with a vital role in the assimilation of reduced nitrogen, was dramatically elevated in flooded nodules. The results of our study highlight the potential of S. herbacea as a green manure and sheds light on the morphological, structural, and biochemical adaptations that enable S. herbacea to thrive and efficiently fix N2 in flooded conditions. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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20 pages, 3535 KiB  
Article
Structural Variations in LysM Domains of LysM-RLK PsK1 May Result in a Different Effect on Pea–Rhizobial Symbiosis Development
by Anna N. Kirienko, Nadezhda A. Vishnevskaya, Anna B. Kitaeva, Oksana Yu. Shtark, Polina Yu. Kozyulina, Richard Thompson, Marion Dalmais, Abdelhafid Bendahmane, Igor A. Tikhonovich and Elena A. Dolgikh
Int. J. Mol. Sci. 2019, 20(7), 1624; https://doi.org/10.3390/ijms20071624 - 1 Apr 2019
Cited by 10 | Viewed by 4166
Abstract
Lysin-motif receptor-like kinase PsK1 is involved in symbiosis initiation and the maintenance of infection thread (IT) growth and bacterial release in pea. We verified PsK1 specificity in relation to the Nod factor structure using k1 and rhizobial mutants. Inoculation with nodO [...] Read more.
Lysin-motif receptor-like kinase PsK1 is involved in symbiosis initiation and the maintenance of infection thread (IT) growth and bacterial release in pea. We verified PsK1 specificity in relation to the Nod factor structure using k1 and rhizobial mutants. Inoculation with nodO and nodE nodO mutants significantly reduced root hair deformations, curling, and the number of ITs in k1-1 and k1-2 mutants. These results indicated that PsK1 function may depend on Nod factor structures. PsK1 with replacement in kinase domain and PsSYM10 co-production in Nicotiana benthamiana leaves did not induce a hypersensitive response (HR) because of the impossibility of signal transduction into the cell. Replacement of P169S in LysM3 domain of PsK1 disturbed the extracellular domain (ECD) interaction with PsSYM10′s ECD in Y2H system and reduced HR during the co-production of full-length PsK1 and PsSYM0 in N. benthamiana. Lastly, we explored the role of PsK1 in symbiosis with arbuscular mycorrhizal (AM) fungi; no significant differences between wild-type plants and k1 mutants were found, suggesting a specific role of PsK1 in legume–rhizobial symbiosis. However, increased sensitivity to a highly aggressive Fusarium culmorum strain was found in k1 mutants compared with the wild type, which requires the further study of the role of PsK1 in immune response regulation. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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20 pages, 14086 KiB  
Article
Classical Soybean (Glycine max (L.) Merr) Symbionts, Sinorhizobium fredii USDA191 and Bradyrhizobium diazoefficiens USDA110, Reveal Contrasting Symbiotic Phenotype on Pigeon Pea (Cajanus cajan (L.) Millsp)
by Alaa A. Alaswad, Nathan W. Oehrle and Hari B. Krishnan
Int. J. Mol. Sci. 2019, 20(5), 1091; https://doi.org/10.3390/ijms20051091 - 3 Mar 2019
Cited by 7 | Viewed by 5673
Abstract
Pigeon pea (Cajanus cajan (L.) Millspaugh) is cultivated widely in semiarid agricultural regions in over 90 countries around the world. This important legume can enter into symbiotic associations with a wide range of rhizobia including Bradyrhizobium and fast-growing rhizobia. In comparison with [...] Read more.
Pigeon pea (Cajanus cajan (L.) Millspaugh) is cultivated widely in semiarid agricultural regions in over 90 countries around the world. This important legume can enter into symbiotic associations with a wide range of rhizobia including Bradyrhizobium and fast-growing rhizobia. In comparison with other major legumes such as soybean and common bean, only limited information is available on the symbiotic interaction of pigeon pea with rhizobia. In this study, we investigated the ability of two classical soybean symbionts—S. fredii USDA191 and B. diazoefficiens USDA110—and their type 3 secretion system (T3SS) mutants, to nodulate pigeon pea. Both S. fredii USDA191 and a T3SS mutant S. fredii RCB26 formed nitrogen-fixing nodules on pigeon pea. Inoculation of pigeon pea roots with B. diazoefficiens USDA110 and B. diazoefficiens Δ136 (a T3SS mutant) resulted in the formation of Fix− and Fix+ nodules, respectively. Light and transmission electron microscopy of Fix- nodules initiated by B. diazoefficiens USDA110 revealed the complete absence of rhizobia within these nodules. In contrast, Fix+ nodules formed by B. diazoefficiens Δ136 revealed a central region that was completely filled with rhizobia. Ultrastructural investigation revealed the presence of numerous bacteroids surrounded by peribacteroid membranes in the infected cells. Analysis of nodule proteins by one- and two-dimensional gel electrophoresis revealed that leghemoglobin was absent in B. diazoefficiens USDA110 nodules, while it was abundantly present in B. diazoefficiens Δ136 nodules. Results of competitive nodulation assays indicated that B. diazoefficiens Δ136 had greater competitiveness for nodulation on pigeon pea than did the wild type strain. Our results suggest that this T3SS mutant of B. diazoefficiens, due to its greater competitiveness and ability to form Fix+ nodules, could be exploited as a potential inoculant to boost pigeon pea productivity. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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16 pages, 3159 KiB  
Article
Sinorhizobium fredii HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean
by Juan Carlos Crespo-Rivas, Pilar Navarro-Gómez, Cynthia Alias-Villegas, Jie Shi, Tao Zhen, Yanbo Niu, Virginia Cuéllar, Javier Moreno, Teresa Cubo, José María Vinardell, José Enrique Ruiz-Sainz, Sebastián Acosta-Jurado and María José Soto
Int. J. Mol. Sci. 2019, 20(3), 787; https://doi.org/10.3390/ijms20030787 - 12 Feb 2019
Cited by 16 | Viewed by 4949
Abstract
Members of Rhizobiaceae contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In Rhizobium leguminosarum and Sinorhizobium meliloti, [...] Read more.
Members of Rhizobiaceae contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In Rhizobium leguminosarum and Sinorhizobium meliloti, mutations in rirA do not impair symbiotic nitrogen fixation. In this study, a rirA mutant of broad host range S. fredii HH103 has been constructed (SVQ780) and its free-living and symbiotic phenotypes evaluated. No production of siderophores could be detected in either the wild-type or SVQ780. The rirA mutant exhibited a growth advantage under iron-deficient conditions and hypersensitivity to hydrogen peroxide in iron-rich medium. Transcription of rirA in HH103 is subject to autoregulation and inactivation of the gene upregulates fbpA, a gene putatively involved in iron transport. The S. fredii rirA mutant was able to nodulate soybean plants, but symbiotic nitrogen fixation was impaired. Nodules induced by the mutant were poorly infected compared to those induced by the wild-type. Genetic complementation reversed the mutant’s hypersensitivity to H2O2, expression of fbpA, and symbiotic deficiency in soybean plants. This is the first report that demonstrates a role for RirA in the Rhizobium-legume symbiosis. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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22 pages, 10002 KiB  
Article
Expression Analysis of PIN Genes in Root Tips and Nodules of Lotus japonicus
by Izabela Sańko-Sawczenko, Dominika Dmitruk, Barbara Łotocka, Elżbieta Różańska and Weronika Czarnocka
Int. J. Mol. Sci. 2019, 20(2), 235; https://doi.org/10.3390/ijms20020235 - 9 Jan 2019
Cited by 11 | Viewed by 4992
Abstract
Auxins are postulated to be one of the pivotal factors in nodulation. However, their transporters in Lotus japonicus, the model species for the study of the development of determinate-type root nodules, have been scarcely described so far, and thus their role in [...] Read more.
Auxins are postulated to be one of the pivotal factors in nodulation. However, their transporters in Lotus japonicus, the model species for the study of the development of determinate-type root nodules, have been scarcely described so far, and thus their role in nodulation has remained unknown. Our research is the first focusing on polar auxin transporters in L. japonicus. We analyzed and compared expression of PINs in 20 days post rhizobial inoculation (dpi) and 54 dpi root nodules of L. japonicus by real-time quantitative polymerase chain reaction (qPCR) along with the histochemical β-glucuronidase (GUS) reporter gene assay in transgenic hairy roots. The results indicate that LjPINs are essential during root nodule development since they are predominantly expressed in the primordia and young, developing nodules. However, along with differentiation, expression levels of several PINs decreased and occurred particularly in the nodule vascular bundles, especially in connection with the root’s stele. Moreover, our study demonstrated the importance of both polar auxin transport and auxin intracellular homeostasis during L. japonicus root nodule development and differentiation. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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16 pages, 1993 KiB  
Article
Proteomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules
by Kent N. Strodtman, Sooyoung Frank, Severin Stevenson, Jay J. Thelen and David W. Emerich
Int. J. Mol. Sci. 2018, 19(12), 3947; https://doi.org/10.3390/ijms19123947 - 8 Dec 2018
Cited by 7 | Viewed by 3797
Abstract
The form and physiology of Bradyrhizobium diazoefficiens after the decline of symbiotic nitrogen fixation has been characterized. Proteomic analyses showed that post-symbiotic B. diazoefficiens underwent metabolic remodeling as well-defined groups of proteins declined, increased or remained unchanged from 56 to 119 days after [...] Read more.
The form and physiology of Bradyrhizobium diazoefficiens after the decline of symbiotic nitrogen fixation has been characterized. Proteomic analyses showed that post-symbiotic B. diazoefficiens underwent metabolic remodeling as well-defined groups of proteins declined, increased or remained unchanged from 56 to 119 days after planting, suggesting a transition to a hemibiotrophic-like lifestyle. Enzymatic analysis showed distinct patterns in both the cytoplasm and the periplasm. Similar to the bacteroid, the post-symbiotic bacteria rely on a non-citric acid cycle supply of succinate and, although viable, they did not demonstrate the ability to grow within the senescent nodule. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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17 pages, 3361 KiB  
Article
Transcriptomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules
by Sooyoung Franck, Kent N. Strodtman, Jing Qiu and David W. Emerich
Int. J. Mol. Sci. 2018, 19(12), 3918; https://doi.org/10.3390/ijms19123918 - 7 Dec 2018
Cited by 6 | Viewed by 3495
Abstract
The transcriptional activity of Bradyrhizobium diazoefficens isolated from soybean nodules was monitored over the period from symbiosis to late plant nodule senescence. The bacteria retained a near constant level of RNA throughout this period, and the variation in genes demonstrating increased, decreased, and/or [...] Read more.
The transcriptional activity of Bradyrhizobium diazoefficens isolated from soybean nodules was monitored over the period from symbiosis to late plant nodule senescence. The bacteria retained a near constant level of RNA throughout this period, and the variation in genes demonstrating increased, decreased, and/or patterned transcriptional activity indicates that the bacteria are responding to the changing environment within the nodule as the plant cells progress from an organized cellular structure to an unorganized state of internal decay. The transcriptional variation and persistence of the bacteria suggest that the bacteria are adapting to their environment and acting similar to hemibiotrophs, which survive both as saprophytes on live plant tissues and then as necrophytes on decaying plant tissues. The host plant restrictions of symbiosis make B. diazoefficiens a highly specialized, restricted hemibiotroph. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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15 pages, 1342 KiB  
Article
Identification of Soybean Genes Whose Expression is Affected by the Ensifer fredii HH103 Effector Protein NopP
by Jinhui Wang, Jieqi Wang, Chunyan Liu, Chao Ma, Changyu Li, Yongqian Zhang, Zhaoming Qi, Rongsheng Zhu, Yan Shi, Jianan Zou, Qingying Li, Jingyi Zhu, Yingnan Wen, Zhijun Sun, Hanxi Liu, Hongwei Jiang, Zhengong Yin, Zhenbang Hu, Qingshan Chen, Xiaoxia Wu and Dawei Xinadd Show full author list remove Hide full author list
Int. J. Mol. Sci. 2018, 19(11), 3438; https://doi.org/10.3390/ijms19113438 - 2 Nov 2018
Cited by 18 | Viewed by 4355
Abstract
In some legume–rhizobium symbioses, host specificity is influenced by rhizobial nodulation outer proteins (Nops). However, the genes encoding host proteins that interact with Nops remain unknown. We generated an Ensifer fredii HH103 NopP mutant (HH103ΩNopP), and analyzed the nodule number (NN) and nodule [...] Read more.
In some legume–rhizobium symbioses, host specificity is influenced by rhizobial nodulation outer proteins (Nops). However, the genes encoding host proteins that interact with Nops remain unknown. We generated an Ensifer fredii HH103 NopP mutant (HH103ΩNopP), and analyzed the nodule number (NN) and nodule dry weight (NDW) of 10 soybean germplasms inoculated with the wild-type E. fredii HH103 or the mutant strain. An analysis of recombinant inbred lines (RILs) revealed the quantitative trait loci (QTLs) associated with NopP interactions. A soybean genomic region containing two overlapping QTLs was analyzed in greater detail. A transcriptome analysis and qRT-PCR assay were used to identify candidate genes encoding proteins that interact with NopP. In some germplasms, NopP positively and negatively affected the NN and NDW, while NopP had different effects on NN and NDW in other germplasms. The QTL region in chromosome 12 was further analyzed. The expression patterns of candidate genes Glyma.12g031200 and Glyma.12g073000 were determined by qRT-PCR, and were confirmed to be influenced by NopP. Full article
(This article belongs to the Special Issue Biological Nitrogen Fixation)
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