Proteomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Strodtman, Kent N.; Frank, Sooyoung; Stevenson, Severin E.; Thelen, Jay J.; Emerich, David W.

doi:10.3390/ijms19123947

Cited by 10 publications

(7 citation statements)

References 46 publications

(76 reference statements)

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“…They also synthesize appendages [13], and the protein [10] and RNA levels (Figure 1C) remain constant. Strodtman et al have shown that post-symbiotic bacteria remain metabolically active up to 119 days after planting [24]. The retention of transcriptional, translational [24], and metabolic [24] activities of the bacteria as the plant cells dies is behavior reminiscent of a hemibiotroph [25,26].…”

Section: Discussionmentioning

confidence: 99%

“…Strodtman et al have shown that post-symbiotic bacteria remain metabolically active up to 119 days after planting [24]. The retention of transcriptional, translational [24], and metabolic [24] activities of the bacteria as the plant cells dies is behavior reminiscent of a hemibiotroph [25,26]. A hemibiotroph is an organism that is saprophytic or parasitic in living tissue while the plant is alive and upon plant death consumes the dead tissue [25,26].…”

Section: Discussionmentioning

confidence: 99%

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Transcriptomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Franck

Strodtman

Qiu

et al. 2018

IJMS

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Transcriptomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Franck

Strodtman

Qiu

et al. 2018

IJMS

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“…The content of PHB in bacteroids is dependent on the relative rates of synthesis and degradation during active nitrogen fixation (Lodwig & Poole, 2003). High accumulation of PHB in bacteroids is a feature of senescing nodules in different legumes (Hernández‐López et al., 2018; Li et al., 2015; Strodtman et al., 2018), which could be due to a variety of causes, including a shift in the redox state of the cell, shifts in the nitrogen–carbon balance, or disruption in the ability to degrade and utilize PHB. Lastly, the higher number of nodules produced in gmuox1 roots (Figure 1c) is consistent with previous reports on Fix − mutants in legumes (Bourcy et al., 2013; Wang et al., 2016; Xi et al., 2013), which was suggested to compensate for the fixation deficiency in the mutant roots.…”

Section: Discussionmentioning

confidence: 99%

Critical role for uricase and xanthine dehydrogenase in soybean nitrogen fixation and nodule development

et al. 2021

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De novo purine biosynthesis is required for the incorporation of fixed nitrogen in ureide exporting nodules, as formed on soybean [Glycine max (L.) Merr.] roots. However, in many cases, the enzymes involved in this pathway have been deduced strictly from genome annotations with little direct genetic evidence, such as mutant studies, to confirm their biochemical function or importance to nodule development. While efforts to develop large mutant collections of soybean are underway, research on this plant is still hampered by the inability to obtain mutations in any specific gene of interest. Using a forward genetic approach, as well as CRISPR/Cas9 gene editing via Agrobacterium rhizogenes‐mediated hairy root transformation, we identified and characterized the role of GmUOX (Uricase) and GmXDH (Xanthine Dehydrogenase) in nitrogen fixation and nodule development in soybean. The gmuox knockout soybean mutants displayed nitrogen deficiency chlorosis and early nodule senescence, as exemplified by the reduced nitrogenase (acetylene reduction) activity in nodules, the internal greenish‐white internal appearance of nodules, and diminished leghemoglobin production. In addition, gmuox1 nodules showed collapsed infected cells with degraded cytoplasm, aggregated bacteroids with no discernable symbiosome membranes, and increased formation of poly‐β‐hydroxybutyrate granules. Similarly, knockout gmxdh mutant nodules, generated with the CRISPR/Cas9 system, also exhibited early nodule senescence. These genetic studies confirm the critical role of the de novo purine metabolisms pathway not only in the incorporation of fixed nitrogen but also in the successful development of a functional, nitrogen‐fixing nodule. Furthermore, these studies demonstrate the great utility of the CRISPR/Cas9 system for studying root‐associated gene traits when coupled with hairy root transformation.

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“…Additionally, their presence can reduce the proliferation and multiplication of free-living rhizobia in the soil, delaying or inhibiting nodule formation [186][187][188][189]. Nitrogen fertilizer application also leads to premature nodule senescence and feedback inhibition of nitrogenase activity [190][191][192][193][194][195][196]. The inhibitory effects of nitrogen fertilizers on nodulation are likely plant-mediated, and different strains of rhizobia exhibit varying degrees of tolerance to these effects [197,198].…”

Section: Effect Of N Fertilizer On Root-hair Curling Infection Thread...mentioning

confidence: 99%

Enhancing Rhizobium–Legume Symbiosis and Reducing Nitrogen Fertilizer Use Are Potential Options for Mitigating Climate Change

Abd-Alla,

Al-Amri,

El-Enany

2023

Agriculture

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This review article explores the impact of nitrogen fertilizers on the symbiotic relationship between Rhizobium bacteria and legume plants. Nitrogen fixation has the potential to address the global protein shortage by increasing nitrogen supply in agriculture. However, the excessive use of synthetic fertilizers has led to environmental consequences and high energy consumption. To promote sustainable agriculture, alternative approaches such as biofertilizers that utilize biological nitrogen fixation have been introduced to minimize ecological impact. Understanding the process of biological nitrogen fixation, where certain bacteria convert atmospheric nitrogen into ammonia, is crucial for sustainable agriculture. This knowledge helps reduce reliance on synthetic fertilizers and maintain soil fertility. The symbiotic relationship between Rhizobium bacteria and leguminous plants plays a vital role in sustainable agriculture by facilitating access to atmospheric nitrogen, improving soil fertility, and reducing the need for chemical fertilizers. To achieve optimal nitrogen fixation and plant growth, it is important to effectively manage nitrogen availability, soil conditions, and environmental stressors. Excessive nitrogen fertilization can negatively affect the symbiotic association between plants and rhizobia, resulting in reduced soil health, altered mutualistic relationships, and environmental concerns. Various techniques can be employed to enhance symbiotic efficiency by manipulating chemotaxis, which is the ability of rhizobia to move towards plant roots. Plant-specific metabolites called (iso)flavonoids play a crucial role in signaling and communication between legume plants and rhizobia bacteria, initiating the symbiotic relationship and enhancing nitrogen fixation and plant growth. Excessive nitrogen fertilizer application can disrupt the communication between rhizobia and legumes, impacting chemotaxis, root exudation patterns, nodulation, and the symbiotic relationship. High levels of nitrogen fertilizers can inhibit nitrogenase, a critical enzyme for plant growth, leading to reduced nitrogenase activity. Additionally, excessive nitrogen can compromise the energy demands of nitrogen fixation, resulting in decreased nitrogenase activity. This review discusses the disadvantages of using nitrogenous fertilizers and the role of symbiotic biological nitrogen fixation in reducing the need for these fertilizers. By using effective rhizobial strains with compatible legume cultivars, not only can the amounts of nitrogenous fertilizers be reduced, but also the energy inputs and greenhouse gas emissions associated with their manufacturing and application. This approach offers benefits in terms of reducing greenhouse gas emissions and saving energy. In conclusion, this paper provides a comprehensive overview of the current understanding of the impact of nitrogen fertilizers on the symbiotic relationship between Rhizobium and legume plants. It also discusses potential strategies for sustainable agricultural practices. By managing nitrogen fertilizers carefully and improving our understanding of the symbiotic relationship, we can contribute to sustainable agriculture and minimize environmental impact.

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Proteomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Cited by 10 publications

References 46 publications

Transcriptomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Transcriptomic Characterization of Bradyrhizobium diazoefficiens Bacteroids Reveals a Post-Symbiotic, Hemibiotrophic-Like Lifestyle of the Bacteria within Senescing Soybean Nodules

Critical role for uricase and xanthine dehydrogenase in soybean nitrogen fixation and nodule development

Enhancing Rhizobium–Legume Symbiosis and Reducing Nitrogen Fertilizer Use Are Potential Options for Mitigating Climate Change

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