Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling

Mortier, Virginie; Wever, Eva De; Vuylsteke, Marnik; Holsters, Marcelle; Goormachtig, Sofie

doi:10.1111/j.1365-313x.2011.04881.x

Cited by 119 publications

(107 citation statements)

References 64 publications

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“…The induction of CLE genes and NIN in response to cytokinin was diminished in loss-of-function mutants (hit1) of the LHK1 cytokinin receptor. The findings indicate that CLE-RS1 and CLE-RS2 expression is mediated by cytokinin signaling, and that NIN expression is a prerequisite for infection and cytokinin-induced CLE expression, consistent with previous observations on the expression of MtCLE12 and MtCLE13 (22).…”

Section: Resultssupporting

confidence: 80%

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Soyano

Hirakawa

Sato

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

189

200

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Autoregulatory negative-feedback loops play important roles in finebalancing tissue and organ development. Such loops are composed of short-range intercellular signaling pathways via cell-cell communications. On the other hand, leguminous plants use a long-distance negative-feedback system involving root-shoot communication to control the number of root nodules, root lateral organs that harbor symbiotic nitrogen-fixing bacteria known as rhizobia. This feedback system, known as autoregulation of nodulation (AON), consists of two long-distance mobile signals: root-derived and shoot-derived signals. Two Lotus japonicus CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE)-related small peptides, CLE ROOT SIGNAL1 (CLE-RS1) and CLE-RS2, function as root-derived signals and are perceived by a shoot-acting AON factor, the HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor protein, an ortholog of Arabidopsis CLAVATA1, which is responsible for shoot apical meristem homeostasis. This peptide-receptor interaction is necessary for systemic suppression of nodulation. How the onset of nodulation activates AON and how optimal nodule numbers are maintained remain unknown, however. Here we show that an RWP-RK-containing transcription factor, NODULE INCEPTION (NIN), which induces nodule-like structures without rhizobial infection when expressed ectopically, directly targets CLE-RS1 and CLE-RS2. Roots constitutively expressing NIN systemically repress activation of endogenous NIN expression in untransformed roots of the same plant in a HAR1-dependent manner, leading to systemic suppression of nodulation and down-regulation of CLE expression. Our findings provide, to our knowledge, the first molecular evidence of a long-distance autoregulatory negative-feedback loop that homeostatically regulates nodule organ formation.L ong-distance organ-to-organ communications are generally critical for coordinating development and environmental adaptation in multicellular organisms, particularly plants that continuously produce postembryonic organs in various environmental conditions (1, 2). Autoregulatory negative-feedback loops play important roles in fine-balancing tissue and organ development. Such feedback loops include short-range intercellular signaling via cell-cell communication. In Arabidopsis, shoot apical meristem (SAM) regulation involves a well-characterized short-range negative-feedback loop that maintains the homeostasis of plant organ development (3-6). The molecular substance of long-distance negative-feedback loops that homeostatically regulate organ production and development remains largely unknown, however.Leguminous plants use long-distance autoregulatory negativefeedback systems involving root-shoot communications to control the number of root nodules, symbiotic root lateral organs formed as consequence of successful interaction with nitrogenfixing bacteria, collectively known as rhizobia. This nodule symbiosis is beneficial to host plants, because rhizobia accommodated in nodules convert atmospheric nitrogen to ammonium, a ...

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Section: Resultssupporting

confidence: 80%

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Soyano

Hirakawa

Sato

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

189

200

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“…CLE-RS2 is also strongly upregulated in the roots of plants grown under high nitrate conditions that are known to abolish nodulation. Conversely, knockdown of Medicago truncatula MtCLE12 and MtCLE13 resulted in a significant increase in nodule number 17 . Functionally similar CLE genes have also been identified in other leguminous species [18][19][20][21] .…”

mentioning

confidence: 99%

Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase

et al. 2013

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Leguminous plants establish a symbiosis with rhizobia to enable nitrogen fixation in root nodules under the control of the presumed root-to-shoot-to-root negative feedback called autoregulation of nodulation. In Lotus japonicus, autoregulation is mediated by CLE-RS genes that are specifically expressed in the root, and the receptor kinase HAR1 that functions in the shoot. However, the mature functional structures of CLE-RS gene products and the molecular nature of CLE-RS/HAR1 signalling governed by these spatially distant components remain elusive. Here we show that CLE-RS2 is a post-translationally arabinosylated glycopeptide derived from the CLE domain. Chemically synthesized CLE-RS glycopeptides cause significant suppression of nodulation and directly bind to HAR1 in an arabinose-chain and sequencedependent manner. In addition, CLE-RS2 glycopeptide specifically produced in the root is found in xylem sap collected from the shoot. We propose that CLE-RS glycopeptides are the long sought mobile signals responsible for the initial step of autoregulation of nodulation.

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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.

111

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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Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling

Cited by 119 publications

References 64 publications

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase

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

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