MtCRE1‐dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in <i>Medicago truncatula</i>

Plet, Julie; Wasson, Anton; Ariel, Federico; Signor, Christine Le; Baker, David; Mathesius, Ulrike; Crespi, Martín; Frugier, Florian

doi:10.1111/j.1365-313x.2010.04447.x

Cited by 257 publications

(410 citation statements)

References 58 publications

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“…This regulatory network seems to be conserved in M. truncatula (Chen et al, 2009). In legumes, cytokinins are also necessary for the functioning of the nodule meristem, and cytokinin signaling genes are expressed preferentially in the meristematic region (Crespi and Frugier, 2008;Plet et al, 2011). Thus, with respect to this character, the SAM and nodule meristem are equivalent, in agreement with the hypothesis of Hirsch and Larue (1997) that suggests that nodules might have shoot characters.…”

Section: Discussionsupporting

confidence: 73%

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NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

et al. 2012

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During their symbiotic interaction with rhizobia, legume plants develop symbiosis-specific organs on their roots, called nodules, that house nitrogen-fixing bacteria. The molecular mechanisms governing the identity and maintenance of these organs are unknown. Using Medicago truncatula nodule root (noot) mutants and pea (Pisum sativum) cochleata (coch) mutants, which are characterized by the abnormal development of roots from the nodule, we identified the NOOT and COCH genes as being necessary for the robust maintenance of nodule identity throughout the nodule developmental program. NOOT and COCH are Arabidopsis thaliana BLADE-ON-PETIOLE orthologs, and we have shown that their functions in leaf and flower development are conserved in M. truncatula and pea. The identification of these two genes defines a clade in the BTB/POZ-ankyrin domain proteins that shares conserved functions in eudicot organ development and suggests that NOOT and COCH were recruited to repress root identity in the legume symbiotic organ.

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Section: Discussionsupporting

confidence: 73%

“…Real-time RT-PCR analyses were performed as described by Plet et al (2011). The reference genes used for M. truncatula qRT-PCR analysis were reported earlier by Gruber et al (2009).…”

Section: Gene Expression Analysesmentioning

confidence: 99%

NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

et al. 2012

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“…Type A ARR expression is one hallmark of the activation of CK pathways, and the upregulation of several type A ARRs has been observed following treatments with CK, rhizobium, and purified Nod factors (Op den Camp et al, 2011;Plet et al, 2011;Ariel et al, 2012). We observed the induction of several of these ARRs following inoculation with rhizobium, with most genes induced by 12 to 24 hpi, consistent with the up-regulation of IPT (and presumably de novo CK biosynthesis) at 12 hpi (Supplemental Fig.…”

Section: Nod Factors Affect the Transcriptional Regulation Of Hormonesupporting

confidence: 54%

“…In legumes CKs function to initiate nodule organogenesis (Gonzalez-Rizzo et al, 2006;Murray et al, 2007;Tirichine et al, 2007;Op den Camp et al, 2011;Plet et al, 2011) and autoregulation of nodulation (Sasaki et al, 2014). CKs are formed when an isopetenyl moiety is conjugated to adenine nucleotides via ISO-PENTENYLTRANSFERASES (IPTs).…”

Section: Et Regulates Multiple Hormone Biosynthetic Pathwaysmentioning

confidence: 99%

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

et al. 2015

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The legume-rhizobium symbiosis is initiated through the activation of the Nodulation (Nod) factor-signaling cascade, leading to a rapid reprogramming of host cell developmental pathways. In this work, we combine transcriptome sequencing with molecular genetics and network analysis to quantify and categorize the transcriptional changes occurring in roots of Medicago truncatula from minutes to days after inoculation with Sinorhizobium medicae. To identify the nature of the inductive and regulatory cues, we employed mutants with absent or decreased Nod factor sensitivities (i.e. Nodulation factor perception and Lysine motif domain-containing receptor-like kinase3, respectively) and an ethylene (ET)-insensitive, Nod factor-hypersensitive mutant (sickle). This unique data set encompasses nine time points, allowing observation of the symbiotic regulation of diverse biological processes with high temporal resolution. Among the many outputs of the study is the early Nod factorinduced, ET-regulated expression of ET signaling and biosynthesis genes. Coupled with the observation of massive transcriptional derepression in the ET-insensitive background, these results suggest that Nod factor signaling activates ET production to attenuate its own signal. Promoter:b-glucuronidase fusions report ET biosynthesis both in root hairs responding to rhizobium as well as in meristematic tissue during nodule organogenesis and growth, indicating that ET signaling functions at multiple developmental stages during symbiosis. In addition, we identified thousands of novel candidate genes undergoing Nod factor-dependent, ET-regulated expression. We leveraged the power of this large data set to model Nod factor-and ET-regulated signaling networks using MERLIN, a regulatory network inference algorithm. These analyses predict key nodes regulating the biological process impacted by Nod factor perception. We have made these results available to the research community through a searchable online resource.

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“…NODULE INCEPTION and NODULATION SIGNALING PATHWAY1 and 2 [Kaló et al, 2005;Smit et al, 2005] and MtCLV3/ESR-RELATED12 and 13 [MtCLE12 and 13; Mortier et al, 2010;Saur et al, 2011]). Nodulation is also positively and negatively controlled by complex, context-dependent interactions with various hormones and peptides (Penmetsa and Cook, 1997;Gonzalez-Rizzo et al, 2006;Penmetsa et al, 2008;Mortier et al, 2010;Plet et al, 2011;Saur et al, 2011;Mortier et al, 2012;Larrainzar et al, 2015;van Zeijl et al, 2015). Collectively, these signals, along with the NF/SYM pathway, determine how, when, and where nodules form, as well as the overall nodule number on the root system (Penmetsa and Cook, 1997;Oldroyd et al, 2011).…”

mentioning

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.

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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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MtCRE1‐dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula

Cited by 257 publications

References 58 publications

NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

NODULE ROOT and COCHLEATA Maintain Nodule Development and Are Legume Orthologs of Arabidopsis BLADE-ON-PETIOLE Genes

Deep Sequencing of the Medicago truncatula Root Transcriptome Reveals a Massive and Early Interaction between Nodulation Factor and Ethylene Signals

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

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