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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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Article
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Fungal community composition predicts forest carbon storage at a continental scale
Soil microbial diversity and composition is thought to play a major role in elemental cycling. Here, the authors analyse a large dataset of soil microbiome and carbon data from European forests and find that soil fungal community composition is a strong predictor of carbon storage.
- Mark A. Anthony
- , Leho Tedersoo
- & Colin Averill
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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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Phytophagy impacts the quality and quantity of plant carbon resources acquired by mutualistic arbuscular mycorrhizal fungi
Plant antagonists may disrupt the allocation of carbon resources from plants to mutualistic microorganisms. Here, the authors report how plants attacked by cyst nematodes and aphids maintain carbon transfer to arbuscular mycorrhizal fungi through fatty acid transfer whilst the limiting the loss of sugars.
- C. A. Bell
- , E. Magkourilou
- & K. J. Field
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Article
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Genome-resolved metatranscriptomics reveals conserved root colonization determinants in a synthetic microbiota
The identification of processes activated by specific microbes during microbiota colonization of plant roots is hampered by technical issues in metatranscriptomics. Here, Vannier et al. colonized germ-free plants with a defined root microbiota comprising over 100 microbial isolates, and addressed those issues in various ways to identify strain-specific processes as well as common gene sets activated by microbes during root colonization.
- Nathan Vannier
- , Fantin Mesny
- & Stéphane Hacquard
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Article
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Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning
The authors investigate microbiota properties for plant protection using synthetic communities and machine learning approaches. They identify strains that reduce pathogen colonization despite variation in microbiota composition.
- Barbara Emmenegger
- , Julien Massoni
- & Julia A. Vorholt
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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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Auxin-producing bacteria promote barley rhizosheath formation
The rhizosheath, or the soil layer closely attached to roots, can help plants tolerate drought. Here, the authors show that rhizosheath formation in barley is promoted by soil bacteria that produce indole-3-acetic acid, a common auxin.
- Feiyun Xu
- , Hanpeng Liao
- & Weifeng Xu
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Article
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Control of arbuscule development by a transcriptional negative feedback loop in Medicago
Zhang et al. report that Medicago AR2/ERF transcription regulators WRI5a-ERM1-ERF12 form a transcriptional negative feedback loop to coordinate arbuscular lipid supply, enabling the maintenance of a stable, reciprocally beneficial symbiosis.
- Qiang Zhang
- , Shuangshuang Wang
- & Yina Jiang
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Article
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A fungal sesquiterpene biosynthesis gene cluster critical for mutualist-pathogen transition in Colletotrichum tofieldiae
Plant-associated fungi range from pathogens to mutualists. Here the authors identify a gene cluster in a Colletotrichum tofieldiae strain that is required to allow the fungus to transition from a mutualist to a pathogen depending on the nutritional status of the host.
- Kei Hiruma
- , Seishiro Aoki
- & Yusuke Saijo
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Article
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Acidification suppresses the natural capacity of soil microbiome to fight pathogenic Fusarium infections
We have limited knowledge on how soil conditions affect microbiota and plant health. Here, the authors find that soil acidification impacts bacterial communities and reduces the capacity of soils to combat fungal pathogens such as Fusarium.
- Xiaogang Li
- , Dele Chen
- & Manuel Delgado-Baquerizo
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Article
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The NAC transcription factors SNAP1/2/3/4 are central regulators mediating high nitrogen responses in mature nodules of soybean
Symbiotic nitrogen fixation (SNF) in legumes is suppressed by the presence of soil inorganic. nitrogen (N). Here the authors characterize a transcriptional regulatory network underlying the N-inhibition of SNF in soybean nodules.
- Xin Wang
- , Zhimin Qiu
- & Yuefeng Guan
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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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A protein kinase coordinates cycles of autophagy and glutaminolysis in invasive hyphae of the fungus Magnaporthe oryzae within rice cells
The blast fungus Magnaporthe oryzae produces invasive hyphae in living rice cells during early infection. Here, the authors show that a fungal protein kinase promotes this biotrophic growth phase by coordinating cycles of autophagy and glutaminolysis in invasive hyphae.
- Gang Li
- , Ziwen Gong
- & Richard A. Wilson
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Article
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Symbiont-host interactome mapping reveals effector-targeted modulation of hormone networks and activation of growth promotion
Pathogens secrete effectors to promote disease, symbionts might use them to confer benefits. Here, the authors identify 106 candidate effectors from the symbiont Serendipita indica, characterise their interactions, and reveal their roles in regulating phytohormone signalling and promoting growth.
- Rory Osborne
- , Laura Rehneke
- & Patrick Schäfer
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Article
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Seasonal activities of the phyllosphere microbiome of perennial crops
Understanding the interactions between plants and microorganisms can inform microbiome management to enhance crop productivity and resilience to stress. Here, Howe et al. use metagenomics and metatranscriptomics to study changes in the leaf microbiome of perennial crops over two growing seasons.
- Adina Howe
- , Nejc Stopnisek
- & Ashley Shade
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Article
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Stabilization of membrane topologies by proteinaceous remorin scaffolds
In plants, plasma membrane topologies are predominantly driven by the cell wall. In this study, the authors demonstrate that remorin proteins can take over these functions at specialized, unwalled plasma membranes such as infection droplets associated with symbiotic infection threads.
- Chao Su
- , Marta Rodriguez-Franco
- & Thomas Ott
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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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Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2
Lipochitooligosaccharide (LCO) perception by legumes is required to establish symbiotic relationships with nitrogen fixing bacteria. Here the authors show that nutrient starvation can activate LCO perception in cereals to promote symbiotic association with arbuscular mycorrhizal fungi.
- Xin-Ran Li
- , Jongho Sun
- & Giles E. D. Oldroyd
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Article
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The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5
Plant-parasitic nematodes are a threat to crop production. Combining bioinformatics, genetic and biochemical approaches, the authors show that the plant pathogen beet cyst nematode possesses an incomplete vitamin B5 synthesis pathway, of potential prokaryotic origin, complemented by its plant host.
- Shahid Siddique
- , Zoran S. Radakovic
- & Sebastian Eves-van den Akker
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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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Distinct ankyrin repeat subdomains control VAPYRIN locations and intracellular accommodation functions during arbuscular mycorrhizal symbiosis
VAPYRIN is a plant protein required for symbiosis with arbuscular mycorrhizal fungi. Here the authors identify VAPYRIN domains that control subcellular targeting and protein-protein interactions and propose that VAPYRIN acts in the nucleus and cytoplasm to coordinate signaling and intracellular arbuscule accommodation.
- Penelope L. Lindsay
- , Sergey Ivanov
- & Maria J. Harrison
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Article
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An ancestral function of strigolactones as symbiotic rhizosphere signals
Strigolactones (SLs) regulate angiosperm development and promote symbiosis with arbuscular mycorrhizae. Here the authors show that bryosymbiol, an SL present in bryophytes and angiosperms, promotes AM symbiosis in Marchantia paleacea suggesting an ancestral function of SLs as rhizosphere signals.
- Kyoichi Kodama
- , Mélanie K. Rich
- & Junko Kyozuka
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Article
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Nitrogen represses haustoria formation through abscisic acid in the parasitic plant Phtheirospermum japonicum
Parasitic plants obtain nutrients from their hosts. Here the authors show that nitrogen sufficiency suppresses parasitism in the root parasite Phtheirospermum japonicum by increasing levels of the phytohormone ABA suggesting that the degree of parasitism is regulated by nutrient availability.
- Anna Kokla
- , Martina Leso
- & Charles W. Melnyk
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Article
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PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis
Arbuscular mycorrhiza support plant phosphate uptake. Here Das et al. show that PHR transcription factors permit arbuscular mycorrhiza symbiosis by promoting gene expression related to symbiosis development and maintenance.
- Debatosh Das
- , Michael Paries
- & Caroline Gutjahr
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Article
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Shared features and reciprocal complementation of the Chlamydomonas and Arabidopsis microbiota
Plants and algae associate with microbial communities that affect their growth and development. Here, the authors characterize the microbiota associated with a unicellular alga in soil, revealing extensive taxonomic and functional overlap with the root microbiota of land plants.
- Paloma Durán
- , José Flores-Uribe
- & Ruben Garrido-Oter
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Article
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Genetic determinants of endophytism in the Arabidopsis root mycobiome
Plant roots host diverse fungal communities that affect plant health. Here, Mesny et al. use comparative genomics and transcriptomics of fungal isolates from the Arabidopsis thaliana root mycobiota, together with root colonization assays, to identify genetic determinants of endophytism.
- Fantin Mesny
- , Shingo Miyauchi
- & Stéphane Hacquard
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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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Structural signatures in EPR3 define a unique class of plant carbohydrate receptors
Exopolysaccharides (EPS) are perceived by legumes and regulate symbiosis with rhizobia. Here the authors describe the structure of the Lotus EPS receptor, EPR3 and show that it has atypical βαββ and βαβ folds that represent a structural signature for a unique class of EPS receptors in the plant kingdom.
- Jaslyn E. M. M. Wong
- , Kira Gysel
- & Kasper R. Andersen
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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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The negative regulator SMAX1 controls mycorrhizal symbiosis and strigolactone biosynthesis in rice
Signaling via the D14L karrikin receptor conditions rice roots for association with arbuscular mycorrhizal fungi. Here, Choi et al. show that SMAX1, a rice homolog of an Arabidopsis repressor of karrikin signaling, acts downstream of D14L to suppress mycorrhizal symbiosis and strigolactone biosynthesis.
- Jeongmin Choi
- , Tak Lee
- & Uta. Paszkowski
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Article
| Open Access
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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A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula
Polysaccharide molecules chitooligosaccharides (COs) and peptidoglycan not only activate plant immunity but also trigger plant symbiosis signalling. Here the authors show that a combination of COs and lipochitooligosaccharides (LCOs) act synergistically to suppress immunity and promote symbiosis to facilitate beneficial fungal associations.
- Feng Feng
- , Jongho Sun
- & Giles E. D. Oldroyd
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Article
| Open Access
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
| Open Access
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
| Open Access
A rice Serine/Threonine receptor-like kinase regulates arbuscular mycorrhizal symbiosis at the peri-arbuscular membrane
The peri-arbuscular membrane (PAM) mediates mutually-beneficial nutrient exchange between plants and arbuscular mycorrhizal (AM) fungi. Here the authors identify ARK1, a PAM-specific receptor-like kinase from rice that sustains AM symbiosis post-arbuscule development.
- Ronelle Roth
- , Marco Chiapello
- & Uta Paszkowski
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Article
| Open Access
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
| Open Access
The Gastrodia elata genome provides insights into plant adaptation to heterotrophy
Gastrodia elata is an obligate mycoheterotrophic plant with highly reduced leaves and bracts in scape. Here, Yuan et al sequence and analyze its 1.06 Gb genome which provides insights in adaptation to a lifestyle of heterotrophy.
- Yuan Yuan
- , Xiaohua Jin
- & Luqi Huang
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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
| Open Access
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
| Open Access
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
| Open Access
Carbon translocation from a plant to an insect-pathogenic endophytic fungus
The endophytic fungusMetarhizium robertsiiis also an insect pathogen and can facilitate transfer of insect-derived nitrogen to host plants. Here, the authors show that carbon is transferred from plant to fungus suggesting a tripartite interaction where nitrogen is exchanged for photosynthate.
- Scott W. Behie
- , Camila C. Moreira
- & Michael J. Bidochka
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Article
| Open Access
Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum
The ascomycete Cenococcum geophilum is a beneficial mycorrhizal symbiont found frequently on tree roots. Here the authors use comparative genomics and transcriptomics to define genomic signatures that differentiate the beneficial C. geophilumfrom its saprotrophic and pathogenic relatives.
- Martina Peter
- , Annegret Kohler
- & Francis M. Martin
RinRK1 enhances NF receptors accumulation in nanodomain-like structures at root-hair tip