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Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms

Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms | Microbiology | Scoop.it

Symbiosis between rhizobia soil bacteria and legume plants results in the formation of root nodules where plant cells are fully packed with nitrogen fixing bacteria. In the host cells, the bacteria adapt to the intracellular environment and gain the ability for nitrogen fixation. Depending on the host plants, the symbiotic fate of bacteria can be either reversible or irreversible. In Medicago and related legume species, the bacteria undergo a host-directed multistep differentiation process culminating in the formation of elongated and branched polyploid bacteria with definitive loss of cell division ability. The plant factors are nodule-specific symbiotic peptides. Approximately 600 of them are nodule-specific cysteine-rich (NCR) peptides produced in the rhizobium-infected plant cells. NCRs are targeted to the endosymbionts, and concerted action of different sets of peptides governs different stages of endosymbiont maturation, whereas the symbiotic function of individual NCRs is unknown. This study focused on NCR247, a cationic peptide exhibiting in vitro antimicrobial activities. We show that NCR247 acts in those nodule cells where bacterial cell division is arrested and cell elongation begins. NCR247 penetrates the bacteria and forms complexes with many bacterial proteins. Interaction with FtsZ required for septum formation is one of the host interventions for inhibiting bacterial cell division. Complex formation with the ribosomal proteins affects translation and contributes to altered proteome and physiology of the endosymbiont. Binding to the chaperone GroEL amplifies the NCR247-modulated biological processes. We show that GroEL1 ofSinorhizobium meliloti is required for efficient infection, terminal differentiation, and nitrogen fixation.


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The symbiotic transcription factor MtEFD and cytokinins are positively acting in the Medicago truncatula and Ralstonia solanacearum pathogenic interaction.

A plant-microbe dual biological system was set up involving the model legume Medicago truncatula and two bacteria, the soil-borne root pathogen Ralstonia solanacearum and the beneficial symbiont Sinorhizobium meliloti. Comparison of transcriptomes under symbiotic and pathogenic conditions highlighted the transcription factor MtEFD (Ethylene response Factor required for nodule Differentiation) as being upregulated in both interactions, together with a set of cytokinin-related transcripts involved in metabolism, signaling and response. MtRR4 (Response Regulator), a cytokinin primary response gene negatively regulating cytokinin signaling and known as a target of MtEFD in nodulation processes, was retrieved in this set of transcripts. Refined studies of MtEFD and MtRR4 expression during M. truncatula and R. solanacearum interaction indicated differential kinetics of induction and requirement of central regulators of bacterial pathogenicity, HrpG and HrpB. Similar to MtRR4, MtEFD upregulation during the pathogenic interaction was dependent on cytokinin perception mediated by the MtCRE1 (Cytokinin REsponse 1) receptor. The use of M. truncatula efd-1 and cre1-1 mutants evidenced MtEFD and cytokinin perception as positive factors for bacterial wilt development. These factors therefore play an important role in both root nodulation and root disease development.

 

Moreau S, Fromentin J, Vailleau F, Vernié T, Huguet S, Balzergue S, Frugier F, Gamas P, Jardinaud MF. (2013). 

New Phytol. 2013 Dec 11.. [Epub ahead of print] 


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An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser capture microdissection coupled to RNA-seq

An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser capture microdissection coupled to RNA-seq | Microbiology | Scoop.it

Rhizobium-induced root nodules are organs specialized for symbiotic nitrogen fixation. Indeterminate-type nodules are formed from an apical meristem and exhibit a spatial zonation which corresponds to successive developmental stages. To get a dynamic and integrated view of plant and bacterial gene expression associated with nodule development, we set up a sensitive and comprehensive approach based upon oriented high depth RNA-seq coupled to laser micro-dissection of nodule regions. This study, focused on the association between the model legume Medicago truncatula and its symbiont Sinorhizobium meliloti, led to the production of 942 million sequencing read pairs that were unambiguously mapped on plant and bacterial genomes. Bioinformatic and statistical analyses enabled in-depth comparison, at a whole genome level, of gene expression in specific nodule zones. Previously characterized symbiotic genes displayed the expected spatial pattern of expression, thus validating the robustness of the approach. We illustrate the interest of this resource by examining gene expression associated with three essential elements of nodule development, namely meristem activity, cell differentiation and selected signaling processes related to bacterial Nod factors and to the redox status. We found that transcription factor genes essential for the control of the root apical meristem were also expressed in the nodule meristem, while plant mRNAs most enriched in nodules compared to roots were mostly associated with zones comprising both plant and bacterial partners. The data, accessible on a dedicated web site, represent a rich resource for microbiologists and plant biologists to address a variety of questions of both fundamental and applied interest.

 

Roux B, Rodde N, Jardinaud MF, Timmers T, Sauviac L, Cottret L, Carrère S, Sallet E, Courcelle E, Moreau S, Debellé F, Capela D, de Carvalho-Niebel F,Gouzy J, Bruand C, Gamas P. (2014). Plant J. Jan 31.: [Epub ahead of print]


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Host plant peptides elicit a transcriptional response to control the S. meliloti cell cycle during symbiosis

Host plant peptides elicit a transcriptional response to control the S. meliloti cell cycle during symbiosis | Microbiology | Scoop.it

The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called "nodule-specific cysteine-rich" (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.

 

Penterman J1, Abo RP, De Nisco NJ, Arnold MF, Longhi R, Zanda M, Walker GC. (2014). Proc Natl Acad Sci U S A. Mar 4;111(9):3561-6. 

 


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ExpR coordinates the expression of symbiotically important, bundle-forming Flp pili with quorum sensing in Sinorhizobium meliloti

Type IVb pili in enteropathogenic bacteria function as a host-colonization factor by mediating tight adherence to host cells, but their role in bacteria-plant symbiosis is currently unknown. The genome of the symbiotic soil bacteriumSinorhizobium meliloti contains two clusters encoding proteins for Type IVb pili of the Flp (fimbrial low-molecular-weight protein) subfamily. To establish the role of Flp pili in the symbiotic interaction of S. meliloti and its host Medicago sativa, we deleted pilA1 that encodes the putative pilin subunit in the chromosomal flp1 cluster and conducted competitive nodulation assays. ThepilA1 deletion strain formed 27% fewer nodules than wild type. Transmission electron microscopy revealed the presence of bundle-forming pili protruding from the polar and lateral region of S. meliloti wild-type cells. The putative pilus assembly ATPase, CpaE1, fused to mCherry showed a predominantly unilateral localization. Transcriptional reporter gene assays demonstrated that expression of pilA1 peaks in early stationary phase and is repressed by the quorum sensing regulator ExpR, which also controls production of exopolysaccharides and motility. Binding of acyl homoserine lactone-activated ExpR to the pilA1 promoter was confirmed with electrophoretic mobility shift assays. A 17-bp consensus sequence for ExpR binding was identified within the 28-bp protected region by DNase I detected by footprinting analyses. Our results show that Flp pili are important for efficient symbiosis of S. meliloti with its plant host. The temporal inverse regulation of exopolysaccharides and pili by ExpR enables S. meliloti to achieve a coordinated expression of cellular processes during early stages of host interaction.

 Zatakia HM, Nelson CE, Syed UJ, Scharf BE. (2014). Appl Environ Microbiol. Feb 7. [Epub ahead of print]


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Nature's microbiome: introduction - Molecular Ecology Special Issue

Nature's microbiome: introduction - Molecular Ecology Special Issue | Microbiology | Scoop.it

In this special issue of Molecular Ecology, we present 28 articles incorporating molecular and bioinformatics tools to dissect the intimate and prolonged associations that define symbioses. We have organized these studies into three sections, focused on (i) the composition of symbiotic communities and how this varies across hosts, tissues and development, and in response to environmental change (‘The Dynamic Microbiome’); (ii) the roles that microbes play for their hosts and the underlying mechanisms behind these functions (‘Microbiome Function’); and (iii) the nature and mechanisms of interactions between hosts and symbionts and between the co-inhabiting symbionts themselves (‘The Interactive Microbiome’). These articles highlight the state-of-the-art in microbiome research, with novel discoveries for well-developed models and for other budding systems beyond the human realm.


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Biochemical characterization of a nitrogen-type phosphotransferase system reveals enzyme EINtr integrates carbon and nitrogen signaling in Sinorhizobium meliloti

Biochemical characterization of a nitrogen-type phosphotransferase system reveals enzyme EINtr integrates carbon and nitrogen signaling in Sinorhizobium meliloti | Microbiology | Scoop.it

In Sinorhizobium meliloti, catabolite repression is influenced by a non-canonical nitrogen-type phosphotransferase system (PTSNtr). In this PTSNtrthe protein HPr is phosphorylated on histidine-22 by the enzyme EINtr and the flux of phosphate through this residue onto downstream proteins leads to an increase in succinate-mediated catabolite repression (SMCR). In order to explore the molecular determinants of HPr phosphorylation by EINtrboth proteins were purified and the activity of EINtr was measured. Experimentally determined kinetic parameters of EINtr activity were significantly slower than those determined for the carbohydrate-type EI in Escherichia coli. Enzymatic assays showed that glutamine, a signal of nitrogen availability in many Gram-negative bacteria, strongly inhibits EINtr. Binding experiments using the isolated GAF domain of EINtr showed that it is the domain responsible for detection of glutamine. EINtr activity was not affected by α-ketoglutarate and no binding between the EIGAF and α-ketoglutarate could be detected. These data suggest that in S. melilloti, EINtr phosphorylation of HPr is regulated by signals from both carbon metabolism (PEP) and nitrogen metabolism (glutamine).

 

Goodwin R1, Gage DJ (2014). J Bacteriol. Mar 14. [Epub ahead of print]


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Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms

Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms | Microbiology | Scoop.it

Symbiosis between rhizobia soil bacteria and legume plants results in the formation of root nodules where plant cells are fully packed with nitrogen fixing bacteria. In the host cells, the bacteria adapt to the intracellular environment and gain the ability for nitrogen fixation. Depending on the host plants, the symbiotic fate of bacteria can be either reversible or irreversible. In Medicago and related legume species, the bacteria undergo a host-directed multistep differentiation process culminating in the formation of elongated and branched polyploid bacteria with definitive loss of cell division ability. The plant factors are nodule-specific symbiotic peptides. Approximately 600 of them are nodule-specific cysteine-rich (NCR) peptides produced in the rhizobium-infected plant cells. NCRs are targeted to the endosymbionts, and concerted action of different sets of peptides governs different stages of endosymbiont maturation, whereas the symbiotic function of individual NCRs is unknown. This study focused on NCR247, a cationic peptide exhibiting in vitro antimicrobial activities. We show that NCR247 acts in those nodule cells where bacterial cell division is arrested and cell elongation begins. NCR247 penetrates the bacteria and forms complexes with many bacterial proteins. Interaction with FtsZ required for septum formation is one of the host interventions for inhibiting bacterial cell division. Complex formation with the ribosomal proteins affects translation and contributes to altered proteome and physiology of the endosymbiont. Binding to the chaperone GroEL amplifies the NCR247-modulated biological processes. We show that GroEL1 ofSinorhizobium meliloti is required for efficient infection, terminal differentiation, and nitrogen fixation.


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Cell Host & Microbe: CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development (2014)

Cell Host & Microbe: CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development (2014) | Microbiology | Scoop.it

Nuclear calcium oscillations are a hallmark of symbiotically stimulated plant root cells. Activation of the central nuclear decoder, calcium- and calmodulin-dependent kinase (CCaMK), triggers the entire symbiotic program including root nodule organogenesis, but the mechanism of signal transduction by CCaMK was unknown. We show that CYCLOPS, a direct phosphorylation substrate of CCaMK, is a DNA-binding transcriptional activator. Two phosphorylated serine residues within the N-terminal negative regulatory domain of CYCLOPS are necessary for its activity. CYCLOPS binds DNA in a sequence-specific and phosphorylation-dependent manner and transactivates the NODULE INCEPTION (NIN) gene. A phosphomimetic version of CYCLOPS was sufficient to trigger root nodule organogenesis in the absence of rhizobia and CCaMK. CYCLOPS thus induces a transcriptional activation cascade, in which NIN and a heterotrimeric NF-Y complex act in hierarchical succession to initiate symbiotic root nodule development


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Single acquisition of protelomerase gave rise to speciation of a large and diverse clade within the Agrobacterium/Rhizobium supercluster characterized by the presence of a linear chromid

Single acquisition of protelomerase gave rise to speciation of a large and diverse clade within the Agrobacterium/Rhizobium supercluster characterized by the presence of a linear chromid | Microbiology | Scoop.it

Linear chromosomes are atypical in bacteria and likely a secondary trait derived from ancestral circular molecules. Within the Rhizobiaceae family, whose genome contains at least two chromosomes, a particularity of Agrobacterium fabrum (formerly A. tumefaciens) secondary chromosome (chromid) is to be linear and hairpin-ended thanks to the TelA protelomerase. Linear topology and telA distributions within this bacterial family was screened by pulse field gel electrophoresis and PCR. In A. rubi, A. larrymoorei, Rhizobium skierniewicense, A. viscosum, Agrobacterium sp. NCPPB 1650, and every genomospecies of the biovar 1/A. tumefaciens species complex (including R. pusense, A. radiobacter, A. fabrum, R. nepotum plus seven other unnamed genomospecies), linear chromid topologies were retrieved concomitantly with telA presence, whereas the remote species A. vitis, Allorhizobium undicola, Rhizobium rhizogenes and Ensifer meliloti harbored a circular chromid as well as no telA gene. Moreover, the telA phylogeny is congruent with that of recA used as a marker gene of the Agrobacterium phylogeny. Collectively, these findings strongly suggest that single acquisition of telA by an ancestor was the founding event of a large and diverse clade characterized by the presence of a linear chromid. This clade, characterized by unusual genome architecture, appears to be a relevant candidate to serve as a basis for a possible redefinition of the controversial Agrobacterium genus. In this respect, investigating telA in sequenced genomes allows to both ascertain the place of concerned strains into Agrobacterium spp. and their actual assignation to species/genomospecies in this genus.

 Ramírez-Bahena MH, Vial L, Lassalle F, Diel B, Chapulliot D, Daubin V, Nesme X, Muller D. (2014). Mol Phylogenet Evol. Jan 17.  [Epub ahead of print] 


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Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti

Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti | Microbiology | Scoop.it

In α-proteobacteria, strict regulation of cell cycle progression is necessary for the specific cellular differentiation required for adaptation to diverse environmental niches. The symbiotic lifestyle of Sinorhizobium meliloti requires a drastic cellular differentiation that includes genome amplification. To achieve polyploidy, the S. meliloti cell cycle program must be altered to uncouple DNA replication from cell division. In the α-proteobacterium Caulobacter crescentus, cell cycle-regulated transcription plays an important role in the control of cell cycle progression but this has not been demonstrated in other α-proteobacteria. Here we describe a robust method for synchronizing cell growth that enabled global analysis of S. meliloti cell cycle-regulated gene expression. This analysis identified 462 genes with cell cycle-regulated transcripts, including several key cell cycle regulators, and genes involved in motility, attachment, and cell division. Only 28% of the 462 S. meliloti cell cycle-regulated genes were also transcriptionally cell cycle-regulated in C. crescentus. Furthermore, CtrA- and DnaA-binding motif analysis revealed little overlap between the cell cycle-dependent regulons of CtrA and DnaA in S. meliloti and C. crescentus. The predicted S. meliloti cell cycle regulon of CtrA, but not that of DnaA, was strongly conserved in more closely related α-proteobacteria with similar ecological niches as S. meliloti, suggesting that the CtrA cell cycle regulatory network may control functions of central importance to the specific lifestyles of α-proteobacteria.

 

De Nisco NJ1, Abo RP, Wu CM, Penterman J, Walker GC. (2014). Proc Natl Acad Sci U S A. Mar 4;111(9):3217-

 


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The genome, proteome and phylogenetic analysis of Sinorhizobium meliloti phage ΦM12, the founder of a new group of T4-superfamily phages

The genome, proteome and phylogenetic analysis of Sinorhizobium meliloti phage ΦM12, the founder of a new group of T4-superfamily phages | Microbiology | Scoop.it

Phage ΦM12 is an important transducing phage of the nitrogen-fixing rhizobial bacterium Sinorhizobium meliloti. Here we report the genome, phylogenetic analysis, and proteome of ΦM12, the first report of the genome and proteome of a rhizobium-infecting T4-superfamily phage. The structural genes of ΦM12 are most similar to T4-superfamily phages of cyanobacteria. ΦM12 is the first reported T4-superfamily phage to lack genes encoding class I ribonucleotide reductase (RNR) and exonuclease dexA, and to possess a class II coenzyme B12-dependent RNR. ΦM12's novel collection of genes establishes it as the founder of a new group of T4-superfamily phages, fusing features of cyanophages and phages of enteric bacteria.

 

Brewer TE, Elizabeth Stroupe M, Jones KM (2014). Virology. Feb;450-451:84-97


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The Sinorhizobium meliloti EmrR Regulator Is Required for Efficient Colonization of Medicago sativa Root Nodules

The nitrogen-fixing bacterium Sinorhizobium meliloti must adapt to diverse conditions encountered during its symbiosis with leguminous plants. We characterized a new symbiotically relevant gene, emrR (SMc03169), whose product belongs to the TetR family of repressors and is divergently transcribed from emrAB genes encoding a putative major facilitator superfamily-type efflux pump. An emrR deletion mutant produced more succinoglycan, displayed increased cell-wall permeability, and exhibited higher tolerance to heat shock. It also showed lower tolerance to acidic conditions, a reduced production of siderophores, and lower motility and biofilm formation. The simultaneous deletion of emrA and emrR genes restored the mentioned traits to the wild-type phenotype, except for survival under heat shock, which was lower than that displayed by the wild-type strain. Furthermore, the ΔemrR mutant as well as the double ΔemrAR mutant was impaired in symbiosis with Medicago sativa; it formed fewer nodules and competed poorly with the wild-type strain for nodule colonization. Expression profiling of the ΔemrR mutant showed decreased expression of genes involved in Nod-factor and rhizobactin biosynthesis and in stress responses. Expression of genes directing the biosynthesis of succinoglycan and other polysaccharides were increased. EmrR may therefore be involved in a regulatory network targeting membrane and cell wall modifications in preparation for colonization of root hairs during symbiosis.

 

Santos MR, Marques AT, Becker JD, Moreira LM. (2014). Mol Plant Microbe Interact. Apr;27(4):388-99.


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The Sinorhizobium meliloti EmrR Regulator Is Required for Efficient Colonization of Medicago sativa Root Nodules

The nitrogen-fixing bacterium Sinorhizobium meliloti must adapt to diverse conditions encountered during its symbiosis with leguminous plants. We characterized a new symbiotically relevant gene, emrR (SMc03169), whose product belongs to the TetR family of repressors and is divergently transcribed from emrAB genes encoding a putative major facilitator superfamily-type efflux pump. An emrR deletion mutant produced more succinoglycan, displayed increased cell-wall permeability, and exhibited higher tolerance to heat shock. It also showed lower tolerance to acidic conditions, a reduced production of siderophores, and lower motility and biofilm formation. The simultaneous deletion of emrA and emrR genes restored the mentioned traits to the wild-type phenotype, except for survival under heat shock, which was lower than that displayed by the wild-type strain. Furthermore, the ΔemrR mutant as well as the double ΔemrAR mutant was impaired in symbiosis with Medicago sativa; it formed fewer nodules and competed poorly with the wild-type strain for nodule colonization. Expression profiling of the ΔemrR mutant showed decreased expression of genes involved in Nod-factor and rhizobactin biosynthesis and in stress responses. Expression of genes directing the biosynthesis of succinoglycan and other polysaccharides were increased. EmrR may therefore be involved in a regulatory network targeting membrane and cell wall modifications in preparation for colonization of root hairs during symbiosis.

 

Santos MR, Marques AT, Becker JD, Moreira LM. (2014). Mol Plant Microbe Interact. Apr;27(4):388-99.


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Legume nodulation

Legume nodulation | Microbiology | Scoop.it

For reasons that are unclear, no eukaryotic enzymes can break the triple bond of N2. The reduction of N2 to NH3 (nitrogen fixation) is limited to prokaryotes and is catalysed by nitrogenase. Since most of the nitrogen entering the biosphere (around 100 million metric tonnes of N2 per annum) does so through nitrogenase activity (lightning contributes about 10%), those plants that associate with nitrogen-fixing bacteria have a significant selective advantage under conditions of limiting nitrogen

 

J. Allan Downie (2014). Current Biology Volume 24, Issue 5, 3 March 2014, Pages R184–R19

 


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Cell Host & Microbe: CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development (2014)

Cell Host & Microbe: CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development (2014) | Microbiology | Scoop.it

Nuclear calcium oscillations are a hallmark of symbiotically stimulated plant root cells. Activation of the central nuclear decoder, calcium- and calmodulin-dependent kinase (CCaMK), triggers the entire symbiotic program including root nodule organogenesis, but the mechanism of signal transduction by CCaMK was unknown. We show that CYCLOPS, a direct phosphorylation substrate of CCaMK, is a DNA-binding transcriptional activator. Two phosphorylated serine residues within the N-terminal negative regulatory domain of CYCLOPS are necessary for its activity. CYCLOPS binds DNA in a sequence-specific and phosphorylation-dependent manner and transactivates the NODULE INCEPTION (NIN) gene. A phosphomimetic version of CYCLOPS was sufficient to trigger root nodule organogenesis in the absence of rhizobia and CCaMK. CYCLOPS thus induces a transcriptional activation cascade, in which NIN and a heterotrimeric NF-Y complex act in hierarchical succession to initiate symbiotic root nodule development


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