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Nitrogen and Nod factor signaling determine Lotus japonicus root exudate composition and bacterial assembly
Nod factor signaling, and nitrate distinctly affect Lotus japonicus root exudate, microbiome composition and connectivity, emphasizing the role of signaling between plant and distinct members of soil microbiota in shaping the overall assemblies.
- Ke Tao
- , Ib T. Jensen
- & Simona Radutoiu
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Review Article
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Choreographing root architecture and rhizosphere interactions through synthetic biology
Engineering the form and function of root systems and their associated microbiota could provide a means to mitigate adverse climate-driven effects. Here, the authors review the recent developments in plant and rhizobacterial synthetic biology and highlight engineering targets for applications in root systems and rhizosphere.
- Carin J. Ragland
- , Kevin Y. Shih
- & José R. Dinneny
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Article
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IMA peptides regulate root nodulation and nitrogen homeostasis by providing iron according to internal nitrogen status
The authors show IRON MAN peptides have an essential role in symbiotic nitrogen fixation during legume-rhizobium symbiosis. The peptides additionally function to regulate nitrogen homeostasis by controlling nitrogen-iron balance.
- Momoyo Ito
- , Yuri Tajima
- & Takuya Suzaki
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Article
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Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
Engineering ammonium excretion diazotrophs suffers from severe penalties to the bacteria. Here, the authors utilize a thermo-sensitive glutamine synthetase-based regulatory switch that permits diurnal changes in diazotrophic lifestyle, coincident with seasonal temperatures for cereal cultivation.
- Yuqian Tang
- , Debin Qin
- & Yi-Ping Wang
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Article
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Single-cell analysis identifies genes facilitating rhizobium infection in Lotus japonicus
The authors use single-cell analysis to identify genes specifically expressed in plant root cells that respond to infection by nitrogen-fixing rhizobia. They show that one of these genes, SYMRKL1, is required for normal progression of infection.
- Manuel Frank
- , Lavinia Ioana Fechete
- & Stig Uggerhøj Andersen
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Article
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A signal peptide peptidase is required for ER-symbiosome proximal association and protein secretion
During nitrogen fixing symbiosis, rhizobia enter legume nodule cells to form the symbiosome. Here the authors report that a nodule-specific signal peptide peptidase is essential for the molecular communication between host cells and the symbiont.
- Jian Yang
- , Niu Zhai
- & Huairong Pan
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Article
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The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation
Cytokinin is essential for regulation of nodulation. Here, the authors identified a B-type response regulator GmRR11d that governs a transcriptional program associated with nodulation and cytokinin activation essential for systemic regulation of nodulation.
- Jiahuan Chen
- , Zhijuan Wang
- & Xia Li
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Article
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Enzymes and cellular interplay required for flux of fixed nitrogen to ureides in bean nodules
Tropical legumes export fixed nitrogen from nodules as ureides. Here, the authors describe how ureides are produced by several biosynthetic enzymes in different nodule cell types and provide explanations for metabolic compartmentation.
- Luisa Voß
- , Katharina J. Heinemann
- & Claus-Peter Witte
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Article
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Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus
Nodule development in legumes is a cytokinin dependent process. Here the authors show that high nitrate supply, which limits nodulation, suppresses cytokinin biosynthesis in Lotus japonicus which contrasts with the positive effect of nitrate on cytokinin biosynthesis in non-legumes
- Jieshun Lin
- , Yuda Purwana Roswanjaya
- & Dugald Reid
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Article
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Rapid evolution of bacterial mutualism in the plant rhizosphere
Beneficial plant-microbe interactions are common in nature, but direct evidence for the evolution of mutualism is scarce. Here, Li et al. experimentally evolve a rhizospheric bacterium and find that it can evolve into a mutualist on a relatively short timescale.
- Erqin Li
- , Ronnie de Jonge
- & Alexandre Jousset
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Article
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Genetics of nodulation in Aeschynomene evenia uncovers mechanisms of the rhizobium–legume symbiosis
The establishment of symbiotic interaction between Aeschynomene evenia and photosynthetic bradyrhizobia doesn’t involve the canonical Nod factors and infection threads. Here, the authors assemble the draft genome of A. evenia and identify a receptor-like kinase in mediating the symbiotic interaction.
- Johan Quilbé
- , Léo Lamy
- & Jean-François Arrighi
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Article
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MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus
In legumes, shoot-derived signals regulate rhizobial symbiosis to balance the benefits of N2 fixation with the energy costs of nodule production. Here Okuma et al. show that Lotus miR2111 is produced in the leaves from the MIR2111-5 locus and is a graft-transmissable signal that enhances nodulation in the roots.
- Nao Okuma
- , Takashi Soyano
- & Masayoshi Kawaguchi
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Article
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The NIN transcription factor coordinates CEP and CLE signaling peptides that regulate nodulation antagonistically
CLE and CEP peptides regulate rhizobial symbiosis in legumes to balance the benefits of nitrogen fixation with the metabolic costs of nodule production. Here Laffont et al. show that cytokinin and bacterial Nod factors induce Medicago CEP7 which acts antagonistically to CLE13 to fine-tune nodulation.
- Carole Laffont
- , Ariel Ivanovici
- & Florian Frugier
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Article
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Genome-scale metabolic reconstruction of the symbiosis between a leguminous plant and a nitrogen-fixing bacterium
The association between leguminous plants and rhizobial bacteria is a paradigmatic example of a symbiosis driven by metabolic exchanges. Here, diCenzo et al. report the reconstruction and modelling of a genome-scale metabolic network of the plant Medicago truncatula nodulated by the bacterium Sinorhizobium meliloti.
- George C. diCenzo
- , Michelangelo Tesi
- & Marco Fondi
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Article
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Glycerol-3-phosphate mediates rhizobia-induced systemic signaling in soybean
Movement of glycerol-3-phosphate (G3P) promotes systemic resistance following local pathogen infections. Here the authors show that rootward movement of shoot-synthesized G3P occurs in response to root-recognition of incompatible rhizobia and promotes exclusion of non-desirable bacteria in roots.
- M. B. Shine
- , Qing-ming Gao
- & Aardra Kachroo
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Article
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Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations
CASTOR is a Lotus japonicus ion channel required for nuclear Ca2+ spiking and establishing rhizobial and mycorrhizal symbioses. Here, via structural and functional analysis, Kim et al. show that CASTOR is a Ca2+-selective channel activated via Ca2+ binding to a soluble gating ring consisting of tandem RCK domains.
- Sunghoon Kim
- , Weizhong Zeng
- & Youxing Jiang
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Article
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A protein complex required for polar growth of rhizobial infection threads
Many legumes accommodate rhizobial symbionts via transcellular infection threads. Here the authors show that in Medicago root hairs, polar growth of the infection thread requires a tip-localized protein complex consisting of VPY and VPY-like proteins that are stabilized by the E3 ligase LIN, as well as an exocyst complex subunit.
- Cheng-Wu Liu
- , Andrew Breakspear
- & Jeremy D. Murray
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Article
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Variation in bradyrhizobial NopP effector determines symbiotic incompatibility with Rj2-soybeans via effector-triggered immunity
The soybean Rj2 gene encodes a TIR-NBS-LRR protein that confers resistance to nodulation by certain rhizobial strains. Here, the authors show that T3SS effector NopP is an avirulence protein that is necessary for Bradyrhizobium diazoefficiens USDA 122 to trigger Rj2-dependent incompatibility.
- Masayuki Sugawara
- , Satoko Takahashi
- & Kiwamu Minamisawa
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Article
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A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus
Leguminous plants host nitrogen-fixing bacteria in root nodules, but cease symbiosis when sufficient nitrogen is available. Here, the authors show that the Lotus japonicus transcription factor NRSYM1 activates the production of CLE-RS2 in nitrogen-sufficient conditions to prevent nodulation
- Hanna Nishida
- , Sachiko Tanaka
- & Takuya Suzaki
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Article
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Symbiosis limits establishment of legumes outside their native range at a global scale
Symbiosis with nitrogen-fixing bacteria (rhizobia) aids the growth of many legume species, but may also restrict their ability to colonize new regions lacking suitable rhizobia. Here, the authors show that symbiotic legumes are indeed less likely to become established in new regions than their non-symbiotic relatives.
- Anna K. Simonsen
- , Russell Dinnage
- & Peter H. Thrall
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Article
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Differential regulation of the Epr3 receptor coordinates membrane-restricted rhizobial colonization of root nodule primordia
TheLotus japonicus LysM receptor kinase EPR3 perceives rhizobial exopolysaccharides to initiate infection of the root epidermis. Here the authors show that EPR3 also mediates infection thread progression in the root cortex and show that key transcription factors that regulate symbiosis specify the expression of Epr3.
- Yasuyuki Kawaharada
- , Mette W. Nielsen
- & Jens Stougaard
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Article
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DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection
Bacterial Nod Factors (NF) regulate the formation of nitrogen fixing symbiotic nodules on legume roots. Here, the authors show that gibberellins act via DELLA proteins to regulate nodulation and propose that DELLA acts with NSP2 and NF-YA1 as a transcriptional co-activator of ERN1-dependent NF signalling.
- Camille Fonouni-Farde
- , Sovanna Tan
- & Anouck Diet
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Article
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DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways
Symbiotic associations between legumes and nitrogen-fixing bacteria are regulated by a CCaMK-IPD3 protein complex which promotes nodule initiation. Here, Jin et al. propose that DELLA proteins positively regulate nodulation by enhancing phosphorylation of IPD3 and acting as a positive regulator of transcription.
- Yue Jin
- , Huan Liu
- & Ertao Wang
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Covalently linked hopanoid-lipid A improves outer-membrane resistance of a Bradyrhizobium symbiont of legumes
Lipopolysaccharides (LPSs) in the outer membrane of Gram-negative bacteria play key roles in the microbial interactions with animals and plants. Here the authors identify a unique LPS with a covalently-attached hopanoid moiety that contributes to membrane stability in a bacterial symbiont of legumes.
- Alba Silipo
- , Giuseppe Vitiello
- & Antonio Molinaro
RinRK1 enhances NF receptors accumulation in nanodomain-like structures at root-hair tip