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1. Comparison of nodule endophyte composition, diversity, and gene content between Medicago truncatula genotypes

   https://doi.org/10.1094/PBIOMES-10-20-0077-R  

   Burns, Mannix; Epstein, Brendan; Burghardt, Liana (May 2021, Phytobiomes Journal)

   null (Ed.)

   Leguminous plants form symbiotic relationships with rhizobia. These nitrogen-fixing bacteria live in specialized root organs called nodules. While rhizobia form the most notable host relationship within root nodules, other bacterial endophytes also inhabit these root nodules and can influence host-rhizobia interactions as well as exert effects of their own, whether beneficial or detrimental. In this study, we investigate differences in nodule communities between genotypes (A17 and R108) of a single plant species, the model legume Medicago truncatula. While diversity of endophytes in nodules was similar across hosts, both nodule endophyte composition and gene functional groups differed. In contrast to the significant direct effect of host genotype, neither the presence nor identity of a host in the previous generation (either A17 or R108) had a significant effect on the nodule endophyte diversity or composition. However, whether or not a host was present altered gene functional groups. We conclude that genetic variation within a legume host species can play an important role in the establishment of nodule microbiomes. Further studies, including GWAS and functional assays, can open the door for engineering and optimizing nodule endophyte communities that promote growth or have other beneficial qualities. 

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2. Nitrogen enrichment alters selection on rhizobial genes

   https://doi.org/10.1101/2024.11.25.625319  

   Hill, Caleb A; McMullen, John G; Lennon, Jay T (November 2024, bioRxiv)

   1 Abstract Mutualisms evolve over time when individuals belonging to different species derive fitness benefits through the exchange of resources and services. Although prevalent in natural and managed ecosystems, mutualisms can be destabilized by environmental fluctuations that alter the costs and benefits of maintaining the symbiosis. In the rhizobia-legume mutualism, bacteria provide reduced nitrogen to the host plant in exchange for photosynthates that support bacterial metabolism. However, this relationship can be disrupted by the addition of external nitrogen sources to the soil, such as fertilizers. While the molecular mechanisms underpinning the rhizobia-legume symbiosis are well-characterized, the genome-wide fitness effects of nitrogen enrichment on symbiotic rhizobia are less clear. Here, we inoculated a randomly barcoded transposon-site sequencing (RB-TnSeq) library of the bacteriumEnsifer(Sinorhizobium)melilotiinto soils containing a host plant, alfalfa (Medicago sativa), under conditions of low and high nitrogen availability. Although plant performance remained robust to fertilization, nitrogen enrichment altered gene fitness for specific traits and functions in the rhizobial partner. Genes involved in carbohydrate metabolism showed increased fitness irrespective of soil nutrient content, whereas fitness gains in quorum-sensing genes were only observed in high-nitrogen environments. We also documented reductions in the fitness of nucleotide metabolism and cell-growth genes, while genes from oxidative phosphorylation and various amino-acid biosynthesis pathways were detrimental to fitness under elevated soil nitrogen, underscoring the complex trade-offs in rhizobial responses to nutrient enrichment. Our experimental functional genomics approach identified gene functions and pathways across allE. melilotireplicons that may be associated with the disruption of an agronomically important mutualism. 2ImportanceUnderstanding the evolutionary dynamics of the rhizobia-legume mutualism is important for elucidating how plant-soil-microbe interactions operate in natural and managed ecosystems. Legumes constitute a significant portion of global food production and generate 25% of all terrestrially fixed nitrogen. The application of chemical fertilizers can disrupt the mutualism by altering the selective pressures experienced by symbiotic rhizobia, potentially affecting gene fitness throughout the microbial genome and leading to the evolution of less productive or cooperative mutualists. To investigate how exogenous nitrogen inputs influence gene fitness during the complex rhizobial lifecycle, we used a barcoded genome-wide mutagenesis screen to quantify gene-level fitness across the rhizobial genome during symbiosis and identify metabolic functions affected by nitrogen enrichment. Our findings provide genomic insight into potential eco-evolutionary mechanisms by which symbioses are maintained or degraded over time in response to changing environmental conditions. 

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3. Insight into the control of nodule immunity and senescence during Medicago truncatula symbiosis

   https://doi.org/10.1093/plphys/kiac505  

   Berrabah, Fathi; Bernal, Gautier; Elhosseyn, Ait-Salem; El Kassis, Cyrille; L’Horset, Roxane; Benaceur, Farouk; Wen, Jiangqi; Mysore, Kirankumar S.; Garmier, Marie; Gourion, Benjamin; et al (October 2022, Plant Physiology)

   Abstract Medicago (Medicago truncatula) establishes a symbiosis with the rhizobia Sinorhizobium sp, resulting in the formation of nodules where the bacteria fix atmospheric nitrogen. The loss of immunity repression or early senescence activation compromises symbiont survival and leads to the formation of nonfunctional nodules (fix−). Despite many studies exploring an overlap between immunity and senescence responses outside the nodule context, the relationship between these processes in the nodule remains poorly understood. To investigate this phenomenon, we selected and characterized three Medicago mutants developing fix− nodules and showing senescence responses. Analysis of specific defense (PATHOGENESIS-RELATED PROTEIN) or senescence (CYSTEINE PROTEASE) marker expression demonstrated that senescence and immunity seem to be antagonistic in fix− nodules. The growth of senescence mutants on non-sterile (sand/perlite) substrate instead of sterile in vitro conditions decreased nodule senescence and enhanced defense, indicating that environment can affect the immunity/senescence balance. The application of wounding stress on wild-type (WT) fix+ nodules led to the death of intracellular rhizobia and associated with co-stimulation of defense and senescence markers, indicating that in fix+ nodules the relationship between the two processes switches from opposite to synergistic to control symbiont survival during response to the stress. Our data show that the immune response in stressed WT nodules is linked to the repression of DEFECTIVE IN NITROGEN FIXATION 2 (DNF2), Symbiotic CYSTEINE-RICH RECEPTOR-LIKE KINASE (SymCRK), and REGULATOR OF SYMBIOSOME DIFFERENTIATION (RSD), key genes involved in symbiotic immunity suppression. This study provides insight to understand the links between senescence and immunity in Medicago nodules. 

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4. A microbiome engineering framework to evaluate rhizobial symbionts of legumes

   https://doi.org/10.1007/s11104-021-04892-2  

   Quides, Kenjiro W.; Atamian, Hagop S. (June 2021, Plant and Soil)

   null (Ed.)

   Abstract Background For well over a century, rhizobia have been recognized as effective biofertilizer options for legume crops. This has led to the widespread use of rhizobial inoculants in agricultural systems, but a recurring issue has emerged: applied rhizobia struggle to provide growth benefits to legume crops. This has largely been attributed to the presence of soil rhizobia and has been termed the ‘rhizobial competition problem.’ Scope Microbiome engineering has emerged as a methodology to circumvent the rhizobial competition problem by creating legume microbiomes that do not require exogenous rhizobia. However, we highlight an alternative implementation of microbiome engineering that focuses on untangling the complexities of the symbiosis that contribute to the rhizobial competition problem. We outline three approaches that use different starting inocula to test hypotheses to overcome the rhizobial competition problem. Conclusions The approaches we suggest are targeted at various stages of the legume-rhizobium symbiosis and will help us uncover underlying molecular mechanisms that contribute to the rhizobial competition problem. We conclude with an integrative perspective of these different approaches and suggest a path forward for future research on legumes and their complex microbiome. 

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5. Host-imposed control mechanisms in legume–rhizobia symbiosis

   https://doi.org/10.1038/s41564-024-01762-2  

   Porter, Stephanie S; Dupin, Simon E; Denison, R Ford; Kiers, E Toby; Sachs, Joel L (August 2024, Nature Microbiology)

   Legumes are ecologically and economically important plants that contribute to nutrient cycling and agricultural sustainability, features tied to their intimate symbiosis with nitrogen-fixing rhizobia. However, rhizobia vary dramatically in quality, ranging from highly growth- promoting to nonbeneficial. Therefore, optimizing plant benefits from this symbiosis requires host mechanisms that select for beneficial rhizobia and limit losses to nonbeneficial strains. Here, we examine the considerable scientific progress made in decoding host control over rhizobia, empirically demonstrating both molecular and cellular mechanisms and their effects on symbiotic benefits. Pre-infection control requires plant production and detection of precise molecular signals to attract and select compatible rhizobia strains. Post-infection mechanisms leverage nodule- and cell-level compartmentalization of symbionts to enable host control over rhizobia development and proliferation in planta. These layers of host preferential allocation act as a series of sieves, each of which contributes to legume fitness by directing host resources to a narrowing subset of more-beneficial rhizobia. 

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