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1. Phosphorus deprivation affects composition and spatial distribution of membrane lipids in legume nodules.

   https://doi.org/doi.org/10.1093/plphys/kiaa115  

   Dokwal, D; Romsdahl, TB; Kunz, DA; Alonso, AP; Dickstein, R (January 2021, Plant physiology)

   null (Ed.)

   In legumes, symbiotic nitrogen (N) fixation (SNF) occurs in specialized organs called nodules after successful interactions between legume hosts and rhizobia. In a nodule, N-fixing rhizobia are surrounded by symbiosome membranes, through which the exchange of nutrients and ammonium occurs between bacteria and the host legume. Phosphorus (P) is an essential macronutrient, and N2-fixing legumes have a higher requirement for P than legumes grown on mineral N. As in the previous studies, in P deficiency, barrel medic (Medicago truncatula) plants had impaired SNF activity, reduced growth, and accumulated less phosphate in leaves, roots, and nodules compared with the plants grown in P sufficient conditions. Membrane lipids in M. truncatula tissues were assessed using electrospray ionization–mass spectrometry. Galactolipids were found to increase in P deficiency, with declines in phospholipids (PL), especially in leaves. Lower PL losses were found in roots and nodules. Subsequently, matrix-assisted laser desorption/ionization–mass spectrometry imaging was used to spatially map the distribution of the positively charged phosphatidylcholine (PC) species in nodules in both P-replete and P-deficient conditions. Our results reveal heterogeneous distribution of several PC species in nodules, with homogeneous distribution of other PC classes. In P poor conditions, some PC species distributions were observed to change. The results suggest that specific PC species may be differentially important in diverse nodule zones and cell types, and that membrane lipid remodeling during P stress is not uniform across the nodule. 

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2. The Impacts of Domestication and Breeding on Nitrogen Fixation Symbiosis in Legumes

   https://doi.org/10.3389/fgene.2020.00973  

   Liu, J; Yu, X; Qin, Q; Dinkins, Randy D; Zhu, H. (July 2020, Frontiers in genetics)

   Legumes are the second most important family of crop plants. One defining feature of legumes is their unique ability to establish a nitrogen-fixing root nodule symbiosis with soil bacteria known as rhizobia. Since domestication from their wild relatives, crop legumes have been under intensive breeding to improve yield and other agronomic traits but with little attention paid to the belowground symbiosis traits. Theoretical models predict that domestication and breeding processes, coupled with high‐input agricultural practices, might have reduced the capacity of crop legumes to achieve their full potential of nitrogen fixation symbiosis. Testing this prediction requires characterizing symbiosis traits in wild and breeding populations under both natural and cultivated environments using genetic, genomic, and ecological approaches. However, very few experimental studies have been dedicated to this area of research. Here, we review how legumes regulate their interactions with soil rhizobia and how domestication, breeding and agricultural practices might have affected nodulation capacity, nitrogen fixation efficiency, and the composition and function of rhizobial community. We also provide a perspective on how to improve legume-rhizobial symbiosis in sustainable agricultural systems. 

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3. Pangenome Evolution Reconciles Robustness and Instability of Rhizobial Symbiosis

   https://doi.org/10.1128/mbio.00074-22  

   Weisberg, Alexandra J.; Rahman, Arafat; Backus, Dakota; Tyavanagimatt, Parinita; Chang, Jeff H.; Sachs, Joel L. (June 2022, mBio)

   Cooper, Vaughn S. (Ed.)

   ABSTRACT Root nodulating rhizobia are nearly ubiquitous in soils and provide the critical service of nitrogen fixation to thousands of legume species, including staple crops. However, the magnitude of fixed nitrogen provided to hosts varies markedly among rhizobia strains, despite host legumes having mechanisms to selectively reward beneficial strains and to punish ones that do not fix sufficient nitrogen. Variation in the services of microbial mutualists is considered paradoxical given host mechanisms to select beneficial genotypes. Moreover, the recurrent evolution of non-fixing symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. Here, we deconstructed hundreds of genome sequences from genotypically and phenotypically diverse Bradyrhizobium strains and revealed mechanisms that generate variation in symbiotic nitrogen fixation. We show that this trait is conferred by a modular system consisting of many extremely large integrative conjugative elements and few conjugative plasmids. Their transmissibility and propensity to reshuffle genes generate new combinations that lead to uncooperative genotypes and make individual partnerships unstable. We also demonstrate that these same properties extend beneficial associations to diverse host species and transfer symbiotic capacity among diverse strains. Hence, symbiotic nitrogen fixation is underpinned by modularity, which engenders flexibility, a feature that reconciles evolutionary robustness and instability. These results provide new insights into mechanisms driving the evolution of mobile genetic elements. Moreover, they yield a new predictive model on the evolution of rhizobial symbioses, one that informs on the health of organisms and ecosystems that are hosts to symbionts and that helps resolve the long-standing paradox. IMPORTANCE Genetic variation is fundamental to evolution yet is paradoxical in symbiosis. Symbionts exhibit extensive variation in the magnitude of services they provide despite hosts having mechanisms to select and increase the abundance of beneficial genotypes. Additionally, evolution of uncooperative symbiont genotypes is predicted to destabilize symbiosis, but breakdown has rarely been observed. We analyzed genome sequences of Bradyrhizobium, bacteria that in symbioses with legume hosts, fix nitrogen, a nutrient essential for ecosystems. We show that genes for symbiotic nitrogen fixation are within elements that can move between bacteria and reshuffle gene combinations that change host range and quality of symbiosis services. Consequently, nitrogen fixation is evolutionarily unstable for individual partnerships, but is evolutionarily stable for legume- Bradyrhizobium symbioses in general. We developed a holistic model of symbiosis evolution that reconciles robustness and instability of symbiosis and informs on applications of rhizobia in agricultural settings. 

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4. The role of microRNAs in the legume–Rhizobium nitrogen-fixing symbiosis

   https://doi.org/10.1093/jxb/eraa018  

   Hoang, Nhung T; Tóth, Katalin; Stacey, Gary; Mittler, Ron (March 2020, Journal of Experimental Botany)

   Abstract Under nitrogen starvation, most legume plants form a nitrogen-fixing symbiosis with Rhizobium bacteria. The bacteria induce the formation of a novel organ called the nodule in which rhizobia reside as intracellular symbionts and convert atmospheric nitrogen into ammonia. During this symbiosis, miRNAs are essential for coordinating the various plant processes required for nodule formation and function. miRNAs are non-coding, endogenous RNA molecules, typically 20–24 nucleotides long, that negatively regulate the expression of their target mRNAs. Some miRNAs can move systemically within plant tissues through the vascular system, which mediates, for example, communication between the stem/leaf tissues and the roots. In this review, we summarize the growing number of miRNAs that function during legume nodulation focusing on two model legumes, Lotus japonicus and Medicago truncatula, and two important legume crops, soybean (Glycine max) and common bean (Phaseolus vulgaris). This regulation impacts a variety of physiological processes including hormone signaling and spatial regulation of gene expression. The role of mobile miRNAs in regulating legume nodule number is also highlighted. 

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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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