Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair

Fournier, Joëlle; Teillet, Alice; Chabaud, Mireille; Ivanov, Sergey; Genre, Andrea; Limpens, Erik; Carvalho-Niebel, Fernanda de; Barker, David G.

doi:10.1104/pp.114.253302

Cited by 127 publications

(137 citation statements)

References 59 publications

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“…A number of NF-regulated candidate genes that have potential to take part in these different processes were described in "Results." For example, numerous genes, coding for proteins involved in the cell wall and cytoskeleton structure or dynamics, as well as membrane or vesicular trafficking, were identified in line with the major subcellular remodeling associated with infection thread formation (Fournier et al, 2015). The strong NF up-regulation of MtLYK10, for which the expression is not detectable in control epidermal cells, probably also contributes to the preparation for infection, since the orthologous L. japonicus EPR3 gene encodes a receptor for Rhizobium spp.…”

Section: Discussionmentioning

confidence: 92%

“…This would be similar to NIN, which is required for symbiotic gene induction in the epidermis and cortex, as well as Rhizobium spp. infection and nodule initiation, while restricting ENOD11 expression on the one hand and nodulation on the other hand, via CLE peptides Soyano et al, 2013Soyano et al, , 2014Laloum et al, 2014;Yoro et al, 2014;Fournier et al, 2015;Vernié et al, 2015). Consequently, the impact of the pEPI:AtCKX3 construct might depend on the relative efficiency of different processes (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…NIN is required to initiate nodule formation in the cortex (Schauser et al, 1999) and to transcriptionally activate NF-YA1 (Soyano et al, 2013;Laloum et al, 2014), a transcription factor (TF) involved in various nodulation steps (Combier et al, 2006;Soyano et al, 2013;Laporte et al, 2014;Xiao et al, 2014). In the epidermis, NIN is necessary for the onset of rhizobium infection Fournier et al, 2015) but restricts the expression of EARLY NODULIN11 (ENOD11), a marker of the preinfection and infection steps Vernié et al, 2015). ENOD11 is up-regulated in response to NF by ETHYLENE RESPONSE FACTOR REQUIRED FOR NODULATION1 (ERN1; Andriankaja et al, 2007;Middleton et al, 2007) as well as NUCLEAR TRAN-SCRIPTION FACTOR Y (MtNF-YA1) and MtNF-YA2 (Laloum et al, 2014).…”

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confidence: 99%

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A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

et al. 2016

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Nod factors (NFs) are lipochitooligosaccharidic signal molecules produced by rhizobia, which play a key role in the rhizobiumlegume symbiotic interaction. In this study, we analyzed the gene expression reprogramming induced by purified NF (4 and 24 h of treatment) in the root epidermis of the model legume Medicago truncatula. Tissue-specific transcriptome analysis was achieved by laser-capture microdissection coupled to high-depth RNA sequencing. The expression of 17,191 genes was detected in the epidermis, among which 1,070 were found to be regulated by NF addition, including previously characterized NF-induced marker genes. Many genes exhibited strong levels of transcriptional activation, sometimes only transiently at 4 h, indicating highly dynamic regulation. Expression reprogramming affected a variety of cellular processes, including perception, signaling, regulation of gene expression, as well as cell wall, cytoskeleton, transport, metabolism, and defense, with numerous NF-induced genes never identified before. Strikingly, early epidermal activation of cytokinin (CK) pathways was indicated, based on the induction of CK metabolic and signaling genes, including the CRE1 receptor essential to promote nodulation. These transcriptional activations were independently validated using promoter:b-glucuronidase fusions with the MtCRE1 CK receptor gene and a CK response reporter (TWO COMPONENT SIGNALING SENSOR NEW). A CK pretreatment reduced the NF induction of the EARLY NODULIN11 (ENOD11) symbiotic marker, while a CK-degrading enzyme (CYTOKININ OXIDASE/DEHYDROGENASE3) ectopically expressed in the root epidermis led to increased NF induction of ENOD11 and nodulation. Therefore, CK may play both positive and negative roles in M. truncatula nodulation.

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

et al. 2016

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“…Infection thread and pocket formation was visualized using a GFP-labeled S. meliloti Sm1021 strain (Fournier et al, 2015) or a Methylene Blue staining for the S. meliloti WSM1022 strain (Vasse and Truchet, 1984). Methylene Blue staining was used both as an independent method for assessing infection thread and pocket formation and as the preferred method when transgenic roots expressing GFP were analyzed.…”

Section: Visualization and Quantification Of Infection Thread Formationmentioning

confidence: 99%

Different Pathways Act Downstream of the CEP Peptide Receptor CRA2 to Regulate Lateral Root and Nodule Development

Mohd‐Radzman

Laffont²,

Ivanovici³

et al. 2016

Plant Physiol.

104

116

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C-TERMINALLY ENCODED PEPTIDEs (CEPs) control root system architecture in a non-cell-autonomous manner. In Medicago truncatula, MtCEP1 affects root development by increasing nodule formation and inhibiting lateral root emergence by unknown pathways. Here, we show that the MtCEP1 peptide-dependent increase in nodulation requires the symbiotic signaling pathway and ETHYLENE INSENSITIVE2 (EIN2)/SICKLE (SKL), but acts independently of SUPER NUMERIC NODULES. MtCEP1-dependent inhibition of lateral root development acts through an EIN2-independent mechanism. MtCEP1 increases nodulation by promoting rhizobial infections, the developmental competency of roots for nodulation, the formation of fused nodules, and an increase in frequency of nodule development that initiates at proto-phloem poles. These phenotypes are similar to those of the ein2/skl mutant and support that MtCEP1 modulates EIN2-dependent symbiotic responses. Accordingly, MtCEP1 counteracts the reduction in nodulation induced by increasing ethylene precursor concentrations, and an ethylene synthesis inhibitor treatment antagonizes MtCEP1 root phenotypes. MtCEP1 also inhibits the development of EIN2-dependent pseudonodule formation. Finally, mutants affecting the COMPACT ROOT ARCHITECTURE2 (CRA2) receptor, which is closely related to the Arabidopsis CEP Receptor1, are unresponsive to MtCEP1 effects on lateral root and nodule formation, suggesting that CRA2 is a CEP peptide receptor mediating both organogenesis programs. In addition, an ethylene inhibitor treatment counteracts the cra2 nodulation phenotype. These results indicate that MtCEP1 and its likely receptor, CRA2, mediate nodulation and lateral root development through different pathways.

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“…This allows entry of rhizobia into the plant cell via a tubular invagination of the plasma membrane and cell wall called the infection thread (IT). IT initiation occurs about 10 to 20 h after root hair curling is complete (Fournier et al, 2015). The IT then grows toward the base of the root hair cell and guides the bacteria to the root cortex (Fournier et al, 2008;Murray, 2011;Oldroyd et al, 2011).…”

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confidence: 99%

A Medicago truncatula Cystathionine-β-Synthase-like Domain-Containing Protein Is Required for Rhizobial Infection and Symbiotic Nitrogen Fixation

et al. 2016

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The symbiosis between leguminous plants and soil rhizobia culminates in the formation of nitrogen-fixing organs called nodules that support plant growth. Two Medicago truncatula Tnt1-insertion mutants were identified that produced small nodules, which were unable to fix nitrogen effectively due to ineffective rhizobial colonization. The gene underlying this phenotype was found to encode a protein containing a putative membrane-localized domain of unknown function (DUF21) and a cystathionine-b-synthase domain. The cbs1 mutants had defective infection threads that were sometimes devoid of rhizobia and formed small nodules with greatly reduced numbers of symbiosomes. We studied the expression of the gene, designated M. truncatula Cystathionine-b-Synthase-like1 (MtCBS1), using a promoter-b-glucuronidase gene fusion, which revealed expression in infected root hair cells, developing nodules, and in the invasion zone of mature nodules. An MtCBS1-GFP fusion protein localized itself to the infection thread and symbiosomes. Nodulation factor-induced Ca 2+ responses were observed in the cbs1 mutant, indicating that MtCBS1 acts downstream of nodulation factor signaling. MtCBS1 expression occurred exclusively during Medicago-rhizobium symbiosis. Induction of MtCBS1 expression during symbiosis was found to be dependent on Nodule Inception (NIN), a key transcription factor that controls both rhizobial infection and nodule organogenesis. Interestingly, the closest homolog of MtCBS1, MtCBS2, was specifically induced in mycorrhizal roots, suggesting common infection mechanisms in nodulation and mycorrhization. Related proteins in Arabidopsis have been implicated in cell wall maturation, suggesting a potential role for CBS1 in the formation of the infection thread wall.

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Remodeling of the Infection Chamber before Infection Thread Formation Reveals a Two-Step Mechanism for Rhizobial Entry into the Host Legume Root Hair

Cited by 127 publications

References 59 publications

A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

A Laser Dissection-RNAseq Analysis Highlights the Activation of Cytokinin Pathways by Nod Factors in the Medicago truncatula Root Epidermis

Different Pathways Act Downstream of the CEP Peptide Receptor CRA2 to Regulate Lateral Root and Nodule Development

A Medicago truncatula Cystathionine-β-Synthase-like Domain-Containing Protein Is Required for Rhizobial Infection and Symbiotic Nitrogen Fixation

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