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Symbiotic Nitrogen Fixation in Legume Nodules: Metabolism and Regulatory Mechanisms

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 (25 January 2014) | Viewed by 67974

Special Issue Editors

Institute for Genomics of Crop Abiotic Stress Tolerance (IGCAST), Texas Tech University, Lubbock, TX 79409, USA
Interests: plants; environmental stress; signaling molecules; transcription factors; gene identification and analysis; gene regulatory network; signal transduction
Special Issues, Collections and Topics in MDPI journals
Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, 230-0045, Japan
Interests: plant-microbe interactions; legumes; N2 fixation; abiotic stress; plant metabolism; plant adaptations; functional genomics

Special Issue Information

Dear Colleagues,

Symbiotic nitrogen fixation is important biological process in the development of sustainable agriculture by which the atmospheric nitrogen (N2) is converted to ammonia with the aid of a key enzyme called nitrogenase. It is achieved by bacteria inside the cells of de novo formed organs, the nodules, which usually develop on roots of various leguminous plants. This process is resulted from the complex interaction between the host plant and rhizobia (used as a colloquial reference to Rhizobium, Bradyrhizobium, Sinorhizobium and Mesorhizobium). This mutualistic relationship is beneficial for both symbiotic partners; the host plant provides the rhizobia with carbon and a source of energy for growth and functions while the rhizobia fix atmospheric N2 and provide the plant with a source of reduced nitrogen in the form of ammonium. To increase knowledge of this vital process of particular importance in sustainable agriculture, major emphasis should be laid on the nodule metabolism and various regulatory pathways. This special issue aims to cover, but not limited to, (i) identification and functional analyses of the genes responsible in rhizobia and legumes, (ii) the physiological and biochemical bases of legume-rhizobia communication, and (iii) the signal transduction pathways responsible for the finely orchestrated induction of the symbiosis-specific genes involved in nodule establishment, development and functioning. A highlighted awareness of such knowledge remains a key element in designing strategies to enhance the productivity of legume crops by genetic engineering for higher performance.

Dr. Lam-Son Phan Tran
Dr. Saad Sulieman
Guest Editors

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Keywords

  • nitrogen fixation
  • legume
  • symbiosis
  • nitrogenase
  • nodule
  • carbon metabolism
  • nitrogen metabolism
  • oxygen supply
  • translocation

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Published Papers (8 papers)

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Editorial

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626 KiB  
Editorial
Symbiotic Nitrogen Fixation in Legume Nodules: Metabolism and Regulatory Mechanisms
by Saad Sulieman and Lam-Son Phan Tran
Int. J. Mol. Sci. 2014, 15(11), 19389-19393; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms151119389 - 24 Oct 2014
Cited by 23 | Viewed by 6847
Abstract
The special issue “Symbiotic Nitrogen Fixation in Legume Nodules: Metabolism and Regulatory Mechanisms” aims to investigate the physiological and biochemical advances in the symbiotic process with an emphasis on nodule establishment, development and functioning. The original research articles included in this issue provide [...] Read more.
The special issue “Symbiotic Nitrogen Fixation in Legume Nodules: Metabolism and Regulatory Mechanisms” aims to investigate the physiological and biochemical advances in the symbiotic process with an emphasis on nodule establishment, development and functioning. The original research articles included in this issue provide important information regarding novel aspects of nodule metabolism and various regulatory pathways, which could have important future implications. This issue also included one review article that highlights the importance of using legume trees in the production of renewable biofuels. Full article

Research

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1385 KiB  
Article
Identification of Cold-Responsive miRNAs and Their Target Genes in Nitrogen-Fixing Nodules of Soybean
by Senlei Zhang, Youning Wang, Kexue Li, Yanmin Zou, Liang Chen and Xia Li
Int. J. Mol. Sci. 2014, 15(8), 13596-13614; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms150813596 - 05 Aug 2014
Cited by 47 | Viewed by 8220
Abstract
As a warm climate species, soybean is highly sensitive to chilling temperatures. Exposure to chilling temperatures causes a significant reduction in the nitrogen fixation rate in soybean plants and subsequent yield loss. However, the molecular basis for the sensitivity of soybean to chilling [...] Read more.
As a warm climate species, soybean is highly sensitive to chilling temperatures. Exposure to chilling temperatures causes a significant reduction in the nitrogen fixation rate in soybean plants and subsequent yield loss. However, the molecular basis for the sensitivity of soybean to chilling is poorly understood. In this study, we identified cold-responsive miRNAs in nitrogen-fixing nodules of soybean. Upon chilling, the expression of gma-miR397a, gma-miR166u and gma-miR171p was greatly upregulated, whereas the expression of gma-miR169c, gma-miR159b, gma-miR319a/b and gma-miR5559 was significantly decreased. The target genes of these miRNAs were predicted and validated using 5' complementary DNA ends (5'-RACE) experiments, and qPCR analysis identified putative genes targeted by the cold-responsive miRNAs in response to chilling temperatures. Taken together, our results reveal that miRNAs may be involved in the protective mechanism against chilling injury in mature nodules of soybean. Full article
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348 KiB  
Article
The Activity of Nodules of the Supernodulating Mutant Mtsunn Is not Limited by Photosynthesis under Optimal Growth Conditions
by Ricardo A. Cabeza, Annika Lingner, Rebecca Liese, Saad Sulieman, Mehmet Senbayram, Merle Tränkner, Klaus Dittert and Joachim Schulze
Int. J. Mol. Sci. 2014, 15(4), 6031-6045; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms15046031 - 10 Apr 2014
Cited by 12 | Viewed by 8089
Abstract
Legumes match the nodule number to the N demand of the plant. When a mutation in the regulatory mechanism deprives the plant of that ability, an excessive number of nodules are formed. These mutants show low productivity in the fields, mainly due to [...] Read more.
Legumes match the nodule number to the N demand of the plant. When a mutation in the regulatory mechanism deprives the plant of that ability, an excessive number of nodules are formed. These mutants show low productivity in the fields, mainly due to the high carbon burden caused through the necessity to supply numerous nodules. The objective of this study was to clarify whether through optimal conditions for growth and CO2 assimilation a higher nodule activity of a supernodulating mutant of Medicago truncatula (M. truncatula) can be induced. Several experimental approaches reveal that under the conditions of our experiments, the nitrogen fixation of the supernodulating mutant, designated as sunn (super numeric nodules), was not limited by photosynthesis. Higher specific nitrogen fixation activity could not be induced through short- or long-term increases in CO2 assimilation around shoots. Furthermore, a whole plant P depletion induced a decline in nitrogen fixation, however this decline did not occur significantly earlier in sunn plants, nor was it more intense compared to the wild-type. However, a distinctly different pattern of nitrogen fixation during the day/night cycles of the experiment indicates that the control of N2 fixing activity of the large number of nodules is an additional problem for the productivity of supernodulating mutants. Full article
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1354 KiB  
Article
Effect of Nitrate on Nodule and Root Growth of Soybean (Glycine max (L.) Merr.)
by Akinori Saito, Sayuri Tanabata, Takanari Tanabata, Seiya Tajima, Manabu Ueno, Shinji Ishikawa, Norikuni Ohtake, Kuni Sueyoshi and Takuji Ohyama
Int. J. Mol. Sci. 2014, 15(3), 4464-4480; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms15034464 - 13 Mar 2014
Cited by 77 | Viewed by 8887
Abstract
The application of combined nitrogen, especially nitrate, to soybean plants is known to strongly inhibit nodule formation, growth and nitrogen fixation. In the present study, we measured the effects of supplying 5 mM nitrate on the growth of nodules, primary root, and lateral [...] Read more.
The application of combined nitrogen, especially nitrate, to soybean plants is known to strongly inhibit nodule formation, growth and nitrogen fixation. In the present study, we measured the effects of supplying 5 mM nitrate on the growth of nodules, primary root, and lateral roots under light at 28 °C or dark at 18 °C conditions. Photographs of the nodulated roots were periodically taken by a digital camera at 1-h intervals, and the size of the nodules was measured with newly developed computer software. Nodule growth was depressed approximately 7 h after the addition of nitrate under light conditions. The nodule growth rate under dark conditions was almost half that under light conditions, and nodule growth was further suppressed by the addition of 5 mM nitrate. Similar results were observed for the extending growth rate of the primary root as those for nodule growth supplied with 5 mM nitrate under light/dark conditions. In contrast, the growth of lateral roots was promoted by the addition of 5 mM nitrate. The 2D-PAGE profiles of nodule protein showed similar patterns between the 0 and 5 mM nitrate treatments, which suggested that metabolic integrity may be maintained with the 5 mM nitrate treatment. Further studies are required to confirm whether light or temperature condition may give the primary effect on the growth of nodules and roots. Full article
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547 KiB  
Communication
A Proteomic Approach of Bradyrhizobium/Aeschynomene Root and Stem Symbioses Reveals the Importance of the fixA Locus for Symbiosis
by Nathanael Delmotte, Samuel Mondy, Benoit Alunni, Joel Fardoux, Clémence Chaintreuil, Julia A. Vorholt, Eric Giraud and Benjamin Gourion
Int. J. Mol. Sci. 2014, 15(3), 3660-3670; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms15033660 - 28 Feb 2014
Cited by 13 | Viewed by 7794
Abstract
Rhizobia are soil bacteria that are able to form symbiosis with plant hosts of the legume family. These associations result in the formation of organs, called nodules in which bacteria fix atmospheric nitrogen to the benefit of the plant. Most of our knowledge [...] Read more.
Rhizobia are soil bacteria that are able to form symbiosis with plant hosts of the legume family. These associations result in the formation of organs, called nodules in which bacteria fix atmospheric nitrogen to the benefit of the plant. Most of our knowledge on the metabolism and the physiology of the bacteria during symbiosis derives from studying roots nodules of terrestrial plants. Here we used a proteomics approach to investigate the bacterial physiology of photosynthetic Bradyrhizobium sp. ORS278 during the symbiotic process with the semi aquatical plant Aeschynomene indica that forms root and stem nodules. We analyzed the proteomes of bacteria extracted from each type of nodule. First, we analyzed the bacteroid proteome at two different time points and found only minor variation between the bacterial proteomes of 2-week- and 3-week-old nodules. High conservation of the bacteroid proteome was also found when comparing stem nodules and root nodules. Among the stem nodule specific proteins were those related to the phototrophic ability of Bradyrhizobium sp. ORS278. Furthermore, we compared our data with those obtained during an extensive genetic screen previously published. The symbiotic role of four candidate genes which corresponding proteins were found massively produced in the nodules but not identified during this screening was examined. Mutant analysis suggested that in addition to the EtfAB system, the fixA locus is required for symbiotic efficiency. Full article
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360 KiB  
Article
Plant Dependence on Rhizobia for Nitrogen Influences Induced Plant Defenses and Herbivore Performance
by Jennifer M. Dean, Mark C. Mescher and Consuelo M. De Moraes
Int. J. Mol. Sci. 2014, 15(1), 1466-1480; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms15011466 - 21 Jan 2014
Cited by 42 | Viewed by 7498
Abstract
Symbiotic rhizobia induce many changes in legumes that could affect aboveground interactions with herbivores. We explored how changing the intensity of Bradyrhizobium japonicum, as modulated by soil nitrogen (N) levels, influenced the interaction between soybean (Glycine max) and herbivores of [...] Read more.
Symbiotic rhizobia induce many changes in legumes that could affect aboveground interactions with herbivores. We explored how changing the intensity of Bradyrhizobium japonicum, as modulated by soil nitrogen (N) levels, influenced the interaction between soybean (Glycine max) and herbivores of different feeding guilds. When we employed a range of fertilizer applications to manipulate soil N, plants primarily dependent on rhizobia for N exhibited increased root nodulation and higher levels of foliar ureides than plants given N fertilizer; yet all treatments maintained similar total N levels. Soybean podworm (Helicoverpa zea) larvae grew best on plants with the highest levels of rhizobia but, somewhat surprisingly, preferred to feed on high-N-fertilized plants when given a choice. Induction of the defense signaling compound jasmonic acid (JA) by H. zea feeding damage was highest in plants primarily dependent on rhizobia. Differences in rhizobial dependency on soybean did not appear to affect interactions with the phloem-feeding soybean aphid (Aphis glycines). Overall, our results suggest that rhizobia association can affect plant nutritional quality and the induction of defense signaling pathways and that these effects may influence herbivore feeding preferences and performance—though such effects may vary considerably for different classes of herbivores. Full article
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917 KiB  
Article
Mutation in the pssA Gene Involved in Exopolysaccharide Synthesis Leads to Several Physiological and Symbiotic Defects in Rhizobium leguminosarum bv. trifolii
by Monika Janczarek and Kamila Rachwał
Int. J. Mol. Sci. 2013, 14(12), 23711-23735; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms141223711 - 05 Dec 2013
Cited by 22 | Viewed by 7407
Abstract
The symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum bv. trifolii 24.2 secretes large amounts of acidic exopolysaccharide (EPS), which plays a crucial role in establishment of effective symbiosis with clover. The biosynthesis of this heteropolymer is conducted by a multi-enzymatic complex located in the bacterial [...] Read more.
The symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum bv. trifolii 24.2 secretes large amounts of acidic exopolysaccharide (EPS), which plays a crucial role in establishment of effective symbiosis with clover. The biosynthesis of this heteropolymer is conducted by a multi-enzymatic complex located in the bacterial inner membrane. PssA protein, responsible for the addition of glucose-1-phosphate to a polyprenyl phosphate carrier, is involved in the first step of EPS synthesis. In this work, we characterize R. leguminosarum bv. trifolii strain Rt270 containing a mini-Tn5 transposon insertion located in the 3'-end of the pssA gene. It has been established that a mutation in this gene causes a pleiotropic effect in rhizobial cells. This is confirmed by the phenotype of the mutant strain Rt270, which exhibits several physiological and symbiotic defects such as a deficiency in EPS synthesis, decreased motility and utilization of some nutrients, decreased sensitivity to several antibiotics, an altered extracellular protein profile, and failed host plant infection. The data of this study indicate that the protein product of the pssA gene is not only involved in EPS synthesis, but also required for proper functioning of Rhizobium leguminosarum bv. trifolii cells. Full article
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Review

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1171 KiB  
Review
The Role of Symbiotic Nitrogen Fixation in Sustainable Production of Biofuels
by Bandana Biswas and Peter M. Gresshoff
Int. J. Mol. Sci. 2014, 15(5), 7380-7397; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms15057380 - 29 Apr 2014
Cited by 61 | Viewed by 11976
Abstract
With the ever-increasing population of the world (expected to reach 9.6 billion by 2050), and altered life style, comes an increased demand for food, fuel and fiber. However, scarcity of land, water and energy accompanied by climate change means that to produce enough [...] Read more.
With the ever-increasing population of the world (expected to reach 9.6 billion by 2050), and altered life style, comes an increased demand for food, fuel and fiber. However, scarcity of land, water and energy accompanied by climate change means that to produce enough to meet the demands is getting increasingly challenging. Today we must use every avenue from science and technology available to address these challenges. The natural process of symbiotic nitrogen fixation, whereby plants such as legumes fix atmospheric nitrogen gas to ammonia, usable by plants can have a substantial impact as it is found in nature, has low environmental and economic costs and is broadly established. Here we look at the importance of symbiotic nitrogen fixation in the production of biofuel feedstocks; how this process can address major challenges, how improving nitrogen fixation is essential, and what we can do about it. Full article
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