Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc‐<scp>LCO</scp>s in <i>Medicago truncatula</i>

Camps, Céline; Jardinaud, Marie-Françoise; Rodrı́guez-Lázaro, David; Carrère, Sébastien; Hervé, Christine; Debelle, Frédéric; Gamas, Pascal; Bensmihen, Sandra; Gough, Clare

doi:10.1111/nph.13427

Cited by 56 publications

(56 citation statements)

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“…As DMI2 is part of the CSSP and PUB1 is induced by Myc-LCOs (Camps et al, 2015), PUB1 could be involved in the AM symbiosis through its interaction with DMI2. To examine this hypothesis we analyzed the spatial expression patterns of DMI2 and PUB1 during AM fungal colonization.…”

Section: Pub1 Is Expressed Throughout Am Fungal Colonizationmentioning

confidence: 99%

PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula

et al. 2016

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ORCID IDs: 0000-0003-1387-6370 (T.V.); 0000-0002-7723-7757 (M.M.); 0000-0002-3204-3537 (C.l.S.).PUB1, an E3 ubiquitin ligase, which interacts with and is phosphorylated by the LYK3 symbiotic receptor kinase, negatively regulates rhizobial infection and nodulation during the nitrogen-fixing root nodule symbiosis in Medicago truncatula. In this study, we show that PUB1 also interacts with and is phosphorylated by DOES NOT MAKE INFECTIONS 2, the key symbiotic receptor kinase of the common symbiosis signaling pathway, required for both the rhizobial and the arbuscular mycorrhizal (AM) endosymbioses. We also show here that PUB1 expression is activated during successive stages of root colonization by Rhizophagus irregularis that is compatible with its interaction with DOES NOT MAKE INFECTIONS 2. Through characterization of a mutant, pub1-1, affected by the E3 ubiquitin ligase activity of PUB1, we have shown that the ubiquitination activity of PUB1 is required to negatively modulate successive stages of infection and development of rhizobial and AM symbioses. In conclusion, PUB1 represents, to our knowledge, a novel common component of symbiotic signaling integrating signal perception through interaction with and phosphorylation by two key symbiotic receptor kinases, and downstream signaling via its ubiquitination activity to fine-tune both rhizobial and AM root endosymbioses.

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Section: Pub1 Is Expressed Throughout Am Fungal Colonizationmentioning

confidence: 99%

PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula

et al. 2016

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“…3). A total of 12 developmental stages of S. meliloti nodulation were investigated, ranging from the initial stages of interaction with the rhizobia (Larrainzar et al, 2015) to senescing nodule organs, as well as root tissue treated with sulfated and nonsulfated Myc-LCOs, representing a single early signaling step in mycorrhizal colonization (Camps et al, 2015).…”

Section: Symbiosismentioning

confidence: 99%

“…RNA-seq data covering early rhizobial infection events at nine time points between 0 and 48 h post inoculation (hpi) were obtained from Larrainzar et al (2015). RNA-seq data of roots inoculated with sulfated (blue) or nonsulfated (red) synthetic Myc-LCO molecules were obtained from Camps et al (2015). RNA-seq data covering nodule development from 4 to 28 d post inoculation (dpi) were generated in house.…”

Section: Macronutrient Deficienciesmentioning

confidence: 99%

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Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

et al. 2017

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Growing evidence indicates that small, secreted peptides (SSPs) play critical roles in legume growth and development, yet the annotation of SSP-coding genes is far from complete. Systematic reannotation of the Medicago truncatula genome identified 1,970 homologs of established SSP gene families and an additional 2,455 genes that are potentially novel SSPs, previously unreported in the literature. The expression patterns of known and putative SSP genes based on 144 RNA sequencing data sets covering various stages of macronutrient deficiencies and symbiotic interactions with rhizobia and mycorrhiza were investigated. Focusing on those known or suspected to act via receptor-mediated signaling, 240 nutrient-responsive and 365 nodulation-responsive Signaling-SSPs were identified, greatly expanding the number of SSP gene families potentially involved in acclimation to nutrient deficiencies and nodulation. Synthetic peptide applications were shown to alter root growth and nodulation phenotypes, revealing additional regulators of legume nutrient acquisition. Our results constitute a powerful resource enabling further investigations of specific SSP functions via peptide treatment and reverse genetics.

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“…5,6 The gene expression changes that underlie symbiotic development have been documented through detailed transcript profiling 7,8 and some transcriptional regulators have been identified, some of which are downstream components of the symbiosis signaling pathway. 4,[9][10][11] Development of AM symbiosis is also influenced by plant hormones and treatment of roots with gibberellic acid (GA) leads either to alterations in fungal entry into the root or abolishes arbuscule development.…”

Section: Introductionmentioning

confidence: 99%

DELLA proteins regulate expression of a subset of AM symbiosis-induced genes inMedicago truncatula

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Lévesque-Tremblay

Park

et al. 2016

Plant Signaling & Behavior

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The majority of the vascular flowering plants form symbiotic associations with fungi from the phylum Glomeromycota through which both partners gain access to nutrients, either mineral nutrients in the case of the plant, or carbon, in the case of the fungus. 1 The association develops in the roots and requires substantial remodeling of the root cortical cells where branched fungal hyphae, called arbuscules, are housed in a new membrane-bound apoplastic compartment.2 Nutrient exchange between the symbionts occurs over this interface and its development and maintenance is critical for symbiosis. Previously, we showed that DELLA proteins, which are well known as repressors of gibberellic acid signaling, also regulate development of AM symbiosis and are necessary to enable arbuscule development.3 Furthermore, constitutive overexpression of a dominant DELLA protein (della1-D18) is sufficient to induce transcripts of several AM symbiosis-induced genes, even in the absence of the fungal symbiont. 4 Here we further extend this approach and identify AM symbiosis genes that respond transcriptionally to constitutive expression of a dominant DELLA protein and also genes that do respond to this treatment. Additionally, we demonstrate that DELLAs interact with REQUIRED FOR ARBUSCULE DEVELOPMENT 1 (RAD1) which further extends our knowledge of GRAS factor complexes that have the potential to regulate gene expression during AM symbiosis. Development of arbuscular mycorrhizal (AM) symbiosis involves signal exchange between the symbionts and a highly conserved plant symbiosis signaling pathway plays a central role in controlling fungal growth into the root and the development of the symbiotic interface in the cortical cells. 5,6 The gene expression changes that underlie symbiotic development have been documented through detailed transcript profiling 7,8 and some transcriptional regulators have been identified, some of which are downstream components of the symbiosis signaling pathway. 4,[9][10][11] Development of AM symbiosis is also influenced by plant hormones and treatment of roots with gibberellic acid (GA) leads either to alterations in fungal entry into the root or abolishes arbuscule development. The precise outcome depends on the concentration of GA applied.12 Genes encoding enzymes of GA biosynthesis and metabolism are differentially regulated during symbiosis 7,13-17 and associated with the colonized regions of the cortex.18 Furthermore, both bioactive and inactive GAs are present in mycorrhizal roots. All of these data suggest a role for GAs in regulating aspects of symbiotic development. 18,19 DELLA proteins are members of a specific sub-group of the GRAS family of transcriptional regulators that possess a unique domain, the DELLA domain, located toward the N-terminal end of the protein.20 DELLAs function as repressors of GA signaling and their mechanism of action has been elucidated through extensive studies in Arabidopsis. Briefly, in the presence of GA, the GA receptor (GID) interacts with the DELLAs through ...

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Combined genetic and transcriptomic analysis reveals three major signalling pathways activated by Myc‐LCOs in Medicago truncatula

Cited by 56 publications

References 123 publications

PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula

PUB1 Interacts with the Receptor Kinase DMI2 and Negatively Regulates Rhizobial and Arbuscular Mycorrhizal Symbioses through Its Ubiquitination Activity in Medicago truncatula

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

DELLA proteins regulate expression of a subset of AM symbiosis-induced genes inMedicago truncatula

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