Dataset Information

Molecular Basis of Root Nodule Symbiosis between Bradyrhizobium and 'Crack-Entry' Legume Groundnut (Arachis hypogaea L.).

ABSTRACT: Nitrogen is one of the essential plant nutrients and a major factor limiting crop productivity. To meet the requirements of sustainable agriculture, there is a need to maximize biological nitrogen fixation in different crop species. Legumes are able to establish root nodule symbiosis (RNS) with nitrogen-fixing soil bacteria which are collectively called rhizobia. This mutualistic association is highly specific, and each rhizobia species/strain interacts with only a specific group of legumes, and vice versa. Nodulation involves multiple phases of interactions ranging from initial bacterial attachment and infection establishment to late nodule development, characterized by a complex molecular signalling between plants and rhizobia. Characteristically, legumes like groundnut display a bacterial invasion strategy popularly known as "crack-entry'' mechanism, which is reported approximately in 25% of all legumes. This article accommodates critical discussions on the bacterial infection mode, dynamics of nodulation, components of symbiotic signalling pathway, and also the effects of abiotic stresses and phytohormone homeostasis related to the root nodule symbiosis of groundnut and Bradyrhizobium. These parameters can help to understand how groundnut RNS is programmed to recognize and establish symbiotic relationships with rhizobia, adjusting gene expression in response to various regulations. This review further attempts to emphasize the current understanding of advancements regarding RNS research in the groundnut and speculates on prospective improvement possibilities in addition to ways for expanding it to other crops towards achieving sustainable agriculture and overcoming environmental challenges.

SUBMITTER: Sharma V

PROVIDER: S-EPMC7076665 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Molecular Basis of Root Nodule Symbiosis between <i>Bradyrhizobium</i> and 'Crack-Entry' Legume Groundnut (<i>Arachis hypogaea</i> L.).

Sharma Vinay V Bhattacharyya Samrat S Kumar Rakesh R Kumar Ashish A Ibañez Fernando F Wang Jianping J Guo Baozhu B Sudini Hari K HK Gopalakrishnan Subramaniam S DasGupta Maitrayee M Varshney Rajeev K RK Pandey Manish K MK

Plants (Basel, Switzerland) 20200220 2

Nitrogen is one of the essential plant nutrients and a major factor limiting crop productivity. To meet the requirements of sustainable agriculture, there is a need to maximize biological nitrogen fixation in different crop species. Legumes are able to establish root nodule symbiosis (RNS) with nitrogen-fixing soil bacteria which are collectively called rhizobia. This mutualistic association is highly specific, and each rhizobia species/strain interacts with only a specific group of legumes, and ...[more]

PMID: 32093403

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Project description:Bradyrhizobium arachidis strain CCBAU 051107 could differentiate into swollen and nonswollen bacteroids in determinate root nodules of peanut (Arachis hypogaea) and indeterminate nodules of Sophora flavescens, respectively, with different N2 fixation efficiencies. To reveal the mechanism of bacteroid differentiation and symbiosis efficiency in association with different hosts, morphologies, transcriptomes, and nitrogen fixation efficiencies of the root nodules induced by strain CCBAU 051107 on these two plants were compared. Our results indicated that the nitrogenase activity of peanut nodules was 3 times higher than that of S. flavescens nodules, demonstrating the effects of rhizobium-host interaction on symbiotic effectiveness. With transcriptome comparisons, genes involved in biological nitrogen fixation (BNF) and energy metabolism were upregulated, while those involved in DNA replication, bacterial chemotaxis, and flagellar assembly were significantly downregulated in both types of bacteroids compared with those in free-living cells. However, expression levels of genes involved in BNF, the tricarboxylic acid (TCA) cycle, the pentose phosphate pathway, hydrogenase synthesis, poly-β-hydroxybutyrate (PHB) degradation, and peptidoglycan biosynthesis were significantly greater in the swollen bacteroids of peanut than those in the nonswollen bacteroids of S. flavescens, while contrasting situations were found in expression of genes involved in urea degradation, PHB synthesis, and nitrogen assimilation. Especially higher expression of ureABEF and aspB genes in bacteroids of S. flavescens might imply that the BNF product and nitrogen transport pathway were different from those in peanut. Our study revealed the first differences in bacteroid differentiation and metabolism of these two hosts and will be helpful for us to explore higher-efficiency symbiosis between rhizobia and legumes. IMPORTANCE Rhizobial differentiation into bacteroids in leguminous nodules attracts scientists to investigate its different aspects. The development of bacteroids in the nodule of the important oil crop peanut was first investigated and compared to the status in the nodule of the extremely promiscuous medicinal legume Sophora flavescens by using just a single rhizobial strain of Bradyrhizobium arachidis, CCBAU 051107. This strain differentiates into swollen bacteroids in peanut nodules and nonswollen bacteroids in S. flavescens nodules. The N2-fixing efficiency of the peanut nodules is three times higher than that of S. flavescens. By comparing the transcriptomes of their bacteroids, we found that they have similar gene expression spectra, such as nitrogen fixation and motivity, but different spectra in terms of urease activity and peptidoglycan biosynthesis. Those altered levels of gene expression might be related to their functions and differentiation in respective nodules. Our studies provided novel insight into the rhizobial differentiation and metabolic alteration in different hosts.

Project description:BACKGROUND:Specialized interactions help structure communities, but persistence of specialized organisms is puzzling because a generalist can occupy more environments and partake in more beneficial interactions. The "Jack-of-all-trades is a master of none" hypothesis asserts that specialists persist because the fitness of a generalist utilizing a particular habitat is lower than that of a specialist adapted to that habitat. Yet, there are many reasons to expect that mutualists will generalize on partners.Plant-soil feedbacks help to structure plant and microbial communities, but how frequently are soil-based symbiotic mutualistic interactions sufficiently specialized to influence species distributions and community composition? To address this question, we quantified realized partner richness and phylogenetic breadth of four wild-grown native legumes (Lupinus bicolor, L. arboreus, Acmispon strigosus and A. heermannii) and performed inoculation trials to test the ability of two hosts (L. bicolor and A. strigosus) to nodulate (fundamental partner richness), benefit from (response specificity), and provide benefit to (effect specificity) 31 Bradyrhizobium genotypes. RESULTS:In the wild, each Lupinus species hosted a broader genetic range of Bradyrhizobium than did either Acmispon species, suggesting that Acmispon species are more specialized. In the greenhouse, however, L. bicolor and A. strigosus did not differ in fundamental association specificity: all inoculated genotypes nodulated both hosts. Nevertheless, A. strigosus exhibited more specificity, i.e., greater variation in its response to, and effect on, Bradyrhizobium genotypes. Lupinus bicolor benefited from a broader range of genotypes but averaged less benefit from each. Both hosts obtained more fitness benefit from symbionts isolated from conspecific hosts; those symbionts in turn gained greater fitness benefit from hosts of the same species from which they were isolated. CONCLUSIONS:This study affirmed two important tenets of evolutionary theory. First, as predicted by the Jack-of-all-trades is a master of none hypothesis, specialist A. strigosus obtained greater benefit from its beneficial symbionts than did generalist L. bicolor. Second, as predicted by coevolutionary theory, each test species performed better with partner genotypes isolated from conspecifics. Finally, positive fitness feedback between the tested hosts and symbionts suggests that positive plant-soil feedback could contribute to their patchy distributions in this system.

Project description:Legume plants have colonized almost all terrestrial biotopes. Their ecological success is partly due to the selective advantage provided by their symbiotic association with nitrogen-fixing bacteria called rhizobia, which allow legumes to thrive on marginal lands and nitrogen depleted soils where non-symbiotic plants cannot grow. Additionally, their symbiotic capacities result in a high protein content in their aerial parts and seeds. This interesting nutritional value has led to the domestication and agricultural exploitation of several legumes grown for seeds and/or fodder for human and domestic animal consumption. Several cultivated legume species are thus grown far beyond their natural geographic range. Other legume species have become invasives, spreading into new habitats. The cultivation and establishment of legume species outside of their original range requires either that they are introduced or cultivated along with their original symbiotic partner or that they find an efficient symbiotic partner in their introduced habitat. The peanut, Arachis hypogaea, a native of South America, is now cultivated throughout the world. This species forms root nodules with Bradyrhizobium, but it is unclear whether these came with the seeds from their native range or were acquired locally. Here we propose to investigate the phylogeography of Bradyrhizobium spp. associated with a number of different wild and cultivated legume species from a range of geographical areas, including numerous strains isolated from peanut roots across the areas of peanut cultivation. This will allow us to address the question of whether introduced/cultivated peanuts associate with bacteria from their original geographic range, i.e., were introduced together with their original bacterial symbionts, or whether they acquired their current associations de novo from the bacterial community within the area of introduction. We will base the phylogenetic analysis on sequence data from both housekeeping and core genes and a symbiotic gene (nif). Differences between the phylogenetic signal of symbiotic and non-symbiotic genes could result from horizontal transfer of symbiosis capacity. Thus this study will also allow us to elucidate the processes by which this symbiotic association has evolved within this group of Bradyrhizobium spp.

Dataset Information

Molecular Basis of Root Nodule Symbiosis between Bradyrhizobium and 'Crack-Entry' Legume Groundnut (Arachis hypogaea L.).

Publications

Molecular Basis of Root Nodule Symbiosis between <i>Bradyrhizobium</i> and 'Crack-Entry' Legume Groundnut (<i>Arachis hypogaea</i> L.).

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