A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis

Tirichine, Leïla; Sandal, Niels; Madsen, Lene Heegaard; Radutoiu, Simona; Albrektsen, Anita S.; Sato, Shusei; Asamizu, Erika; Tabata, Satoshi; Stougaard, Jens

doi:10.1126/science.1132397

Cited by 480 publications

(509 citation statements)

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“…It appears that this cytokinin receptor has an important role in initiating cortical cell division, as a constitutively active mutant of L. japonicus LHK1 induces spontaneous initiation of cell division in the absence of infecting bacteria 60 .…”

Section: Targeting Infection Threadsmentioning

confidence: 99%

“…DMI3 encodes a Ca 2+ -calmodulin-dependent protein kinase that is required for the induction of cell division in the root cortex and for the transcriptional changes required for the establishment of the symbiosis. Two GRAS family transcriptional regulators, nodulation signalling pathway 1 (NSP1) and NSP2, are also required [58][59][60] ) are required for infection threads to extend to the base of the root hair cell. c | MtCRE1 (REFS [58][59][60] ), MtBIT1/ERN 44 , MtRIT1 (REF.…”

Section: Future Perspectivesmentioning

confidence: 99%

“…Two GRAS family transcriptional regulators, nodulation signalling pathway 1 (NSP1) and NSP2, are also required [58][59][60] ) are required for infection threads to extend to the base of the root hair cell. c | MtCRE1 (REFS [58][59][60] ), MtBIT1/ERN 44 , MtRIT1 (REF. 62 ) and MtSLI 64 are required for infection thread penetration into the underlying cell layers.…”

Section: Future Perspectivesmentioning

confidence: 99%

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How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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Nitrogen-fixing rhizobial bacteria and leguminous plants have evolved complex signal exchange mechanisms that allow a specific bacterial species to induce its host plant to form invasion structures through which the bacteria can enter the plant root. Once the bacteria have been endocytosed within a host-membrane-bound compartment by root cells, the bacteria differentiate into a new form that can convert atmospheric nitrogen into ammonia. Bacterial differentiation and nitrogen fixation are dependent on the microaerobic environment and other support factors provided by the plant. In return, the plant receives nitrogen from the bacteria, which allows it to grow in the absence of an external nitrogen source. Here, we review recent discoveries about the mutual recognition process that allows the model rhizobial symbiont Sinorhizobium meliloti to invade and differentiate inside its host plant alfalfa (Medicago sativa) and the model host plant barrel medic (Medicago truncatula).The recent completion of the Sinorhizobium meliloti genome sequence, and the progress towards the completion of the Medicago truncatula genome sequence, have led to a surge in the molecular characterization of the determinants that are involved in the development of the symbiosis between rhizobial bacteria and leguminous plants. Aromatic compounds from legumes called flavonoids first signal the rhizobial bacteria to produce lipochitooligosaccharide compounds called Nod factors 1 . Nod factors that are secreted by the bacteria activate multiple responses in the host plant that prepare the plant to receive the invading bacteria. Nod factors and symbiotic exopolysaccharides induce the plant to form infection threads, which are thin tubules filled with bacteria that penetrate into the plant cortical tissue and deliver the bacteria to their target cells. Plant cells in the inner cortex internalize the invading bacteria in host-membrane-bound compartments that mature into structures known Correspondence to G.C.W. gwalker@mit.edu. Competing interests statementThe authors declare no competing financial interests. DATABASES Invasion of plant rootsAlthough plant roots are exposed to various micro-organisms in the soil, their cell walls form a strong protective barrier against most harmful species. The early steps in the invasion of barrel medic (M. truncatula) and alfalfa (Medicago sativa) roots by S. meliloti are characterized by the reciprocal exchange of signals that allow the bacteria to use the plant root hair cells as a means of entry. Initial signal exchangeFlavonoid compounds (2-phenyl-1,4-benzopyrone derivatives) produced by leguminous plants are the first signals to be exchanged by host-rhizobial symbiont pairs 1 (FIG. 1). Flavonoids bind bacterial NodD proteins, which are members of the LysR family of transcriptional regulators, and activate these proteins to induce the transcription of rhizobial genes 1,2 . For example, the M. sativa-derived flavonoid luteolin stimulates binding of an active form of NodD1 to an S. meliloti 'nod-box' p...

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Section: Targeting Infection Threadsmentioning

confidence: 99%

Section: Future Perspectivesmentioning

confidence: 99%

Section: Future Perspectivesmentioning

confidence: 99%

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How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

et al. 2007

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“…Cytokinins are essential for nodule development because L. japonicus knockout mutants for the cytokinin receptor gene, LHK1, or M. truncatula transgenic plants with suppressed expression of the ortholog, CRE1, were defective in nodule primordia formation (Gonzalez-Rizzo et al, 2006;Murray et al, 2007). Additionally, a L. japonicus gain-of-function mutant for the LHK1 receptor provoked spontaneous nodules, indicating that cytokinin signaling is both necessary and sufficient for nodule formation (Tirichine et al, 2007).…”

mentioning

confidence: 99%

“…Decoding of this Ca 2+ signature by a Ca 2+ calmodulin-binding protein (DMI3) results in the activation of the transcription factors Nodulation Signaling Pathway1 (NSP1), NSP2, Ethylene-Responsive Binding Domain Factor Required for Nodulation1 (ERN1), and Nodule Inception (NIN; Schauser et al, 1999;Catoira et al, 2000;Borisov et al, 2003;Oldroyd and Long, 2003;Gleason et al, 2006;Andriankaja et al, 2007;Marsh et al, 2007;Middleton et al, 2007;Oldroyd and Downie, 2008). NSP2, ERN1, and NIN also play a role downstream of the cytokinin signaling to trigger cortical cell division (Tirichine et al, 2007;Frugier et al, 2008).…”

mentioning

confidence: 99%

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Mortier

Herder²,

Whitford³

et al. 2010

Plant Physiology

294

409

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The CLAVATA3/embryo-surrounding region (CLE) peptides control the fine balance between proliferation and differentiation in plant development. We studied the role of CLE peptides during indeterminate nodule development and identified 25 MtCLE peptide genes in the Medicago truncatula genome, of which two genes, MtCLE12 and MtCLE13, had nodulation-related expression patterns that were linked to proliferation and differentiation. MtCLE13 expression was up-regulated early in nodule development. A high-to-low expression gradient radiated from the inner toward the outer cortical cell layers in a region defining the incipient nodule. At later stages, MtCLE12 and MtCLE13 were expressed in differentiating nodules and in the apical part of mature, elongated nodules. Functional analysis revealed a putative role for MtCLE12 and MtCLE13 in autoregulation of nodulation, a mechanism that controls the number of nodules and involves systemic signals mediated by a leucine-rich repeat receptor-like kinase, SUNN, which is active in the shoot. When MtCLE12 and MtCLE13 were ectopically expressed in transgenic roots, nodulation was abolished at the level of the nodulation factor signal transduction, and this inhibition involved long-distance signaling. In addition, composite plants with roots ectopically expressing MtCLE12 or MtCLE13 had elongated petioles. This systemic effect was not observed in transgenic roots ectopically expressing MtCLE12 and MtCLE13 in a sunn-1 mutant background, although nodulation was still strongly reduced. These results suggest multiple roles for CLE signaling in nodulation.

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Root‐nodule Symbiosis: Molecular Basis of Nodule Formation

Oldroyd

2007

Encyclopedia of Life Sciences

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Nutrient availability is a major limitation to plant growth. Legumes have entered into a symbiotic interaction with nitrogen‐fixing rhizobial bacteria that provide the plant with a source of nitrogen. The legume/rhizobial symbiosis is globally important for introducing nitrogen into biological systems. Legume crops are used in sustainable agricultural processes to naturally enrich the soil for nitrogen. Our understanding of the molecular mechanisms that underlie this interaction is expanding and we are beginning to understand the means by which the molecular dialogue occurs between the plant and the bacteria. The signalling pathway in the plant, that is responsible for the recognition of the bacterial signal Nod factor, appears to have evolved in part from a pre‐existing signalling pathway necessary for the establishment of the mycorrhizal symbiosis. Further research in this field may help to apply this symbiosis more broadly in agriculture.

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A Gain-of-Function Mutation in a Cytokinin Receptor Triggers Spontaneous Root Nodule Organogenesis

Cited by 480 publications

References 26 publications

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Root‐nodule Symbiosis: Molecular Basis of Nodule Formation

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