Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation

Li, Dongxue; Kinkema, Mark; Gresshoff, Peter M.

doi:10.1016/j.jplph.2009.03.004

Cited by 47 publications

(53 citation statements)

References 93 publications

(126 reference statements)

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“…Experiments have shown that it might control the production/transportation of a root-derived signal that is sent to the shoot at the onset of AON rather than be involved in the perception of the return signal from the shoot (Li et al, 2009;Novák, 2010;Schnabel et al, 2011). In view of this hypothesis, our results on the nod3 mutant demonstrate that AON CLE peptides might act upstream or at the level of the RDN1/ NOD3 protein.…”

Section: Discussionmentioning

confidence: 64%

“…During this AON process, the first nodules that are formed inhibit further nodule development on the entire root system via currently unknown longdistance signals (Kosslak and Bohlool, 1984). AON is activated early after the perception of the Nod factors, at the onset of cell division for primordium formation, and its strength increases as nodule development proceeds (Pierce and Bauer, 1983;Caetano-Anollés and Gresshoff, 1991;Li et al, 2009).…”

mentioning

confidence: 99%

“…In addition to the CLE peptides, several mutants have been identified that might be affected in genes involved in the control of AON in the root, such as nod3, rdn1, rdh1, tml, and plenty (Postma et al, 1988;Ishikawa et al, 2008;Magori et al, 2009;Novák, 2010;Yoshida et al, 2010;Novák et al, 2011;Schnabel et al, 2011). These mutants might be defective in the genes that control the root-derived signals or the root-to-shoot processing/transducing signals or vice versa (Li et al, 2009;Novák, 2010). Recently, rdn1 and nod3 have been found to encode unknown proteins that act in the vascular system, suggesting that these proteins might be involved in the vascular transport of a mobile signal acting between roots and shoots (Schnabel et al, 2011).…”

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confidence: 99%

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WUSCHEL-RELATED HOMEOBOX5Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation

et al. 2012

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In legumes, the symbiotic nodules are formed as a result of dedifferentiation and reactivation of cortical root cells. A shootacting receptor complex, similar to the Arabidopsis (Arabidopsis thaliana) CLAVATA1 (CLV1)/CLV2 receptor, regulating development of the shoot apical meristem, is involved in autoregulation of nodulation (AON), a mechanism that systemically controls nodule number. The targets of CLV1/CLV2 in the shoot apical meristem, the WUSCHEL (WUS)-RELATED HOMEOBOX (WOX) family transcription factors, have been proposed to be important regulators of apical meristem maintenance and to be expressed in apical meristem "organizers." Here, we focus on the role of the WOX5 transcription factor upon nodulation in Medicago truncatula and pea (Pisum sativum) that form indeterminate nodules. Analysis of temporal WOX5 expression during nodulation with quantitative reverse transcription-polymerase chain reaction and promoter-reporter fusion revealed that the WOX5 gene was expressed during nodule organogenesis, suggesting that WOX genes are common regulators of cell proliferation in different systems. Furthermore, in nodules of supernodulating mutants, defective in AON, WOX5 expression was higher than that in wild-type nodules. Hence, a conserved WUS/WOX-CLV regulatory system might control cell proliferation and differentiation not only in the root and shoot apical meristems but also in nodule meristems. In addition, the link between nodule-derived CLE peptides activating AON in different legumes and components of the AON system was investigated. We demonstrate that the identified AON component, NODULATION3 of pea, might act downstream from or beside the CLE peptides during AON.Legume plants can thrive on nitrogen-poor soils because they interact symbiotically with soil-resident bacteria, the rhizobia. After a complex signal exchange between both partners, new root organs are formed: the nodules, in which the bacteria fix atmospheric nitrogen for the plant in return for a protective niche and carbon sources. Nodulation requires well-controlled bacterial invasion and initiation of cortical cell division after perception of the bacterially produced Nodulation (Nod) factors. Studies in several legumes have elucidated many elements of the signaling cascade (Catoira et al.,

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Section: Discussionmentioning

confidence: 64%

mentioning

confidence: 99%

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confidence: 99%

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WUSCHEL-RELATED HOMEOBOX5Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation

et al. 2012

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“…Interestingly, the expression of MtCLE12 and MtCLE13 coincides with the activation and progression of AON that is first initiated when the first nodule primordia are formed and is strengthened as more nodules develop (Nutman, 1952;Delves et al, 1986;Takats, 1990;Wopereis et al, 2000;Krusell et al, 2002;Nishimura et al, 2002;Searle et al, 2003;Schnabel et al, 2005;Li et al, 2009). Besides the long-distance effect on nodulation, 35S:MtCLE12 and 35S:MtCLE13 transgenic roots induced elongation of the petioles of the composite plants.…”

Section: Mtcle12 Mtcle13 or A Peptide With A Related Sequence Mightmentioning

confidence: 99%

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Mortier

Herder²,

Whitford³

et al. 2010

Plant Physiology

297

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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“…Nodule number is regulated negatively by a variety of mechanisms including the systemic autoregulation of nodulation that involves signaling by CLE peptides (6)(7)(8). Bacterial infection of root tissues is controlled by the plant at the epidermal cell layer in close coordination with nodule development (2,9).…”

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confidence: 99%

Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti–Medicago symbiosis

Tian

Garnerone

Mathieu-Demazière

et al. 2012

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

100

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Legumes and soil bacteria called rhizobia have coevolved a facultative nitrogen-fixing symbiosis. Establishment of the symbiosis requires bacterial entry via root hair infection threads and, in parallel, organogenesis of nodules that subsequently are invaded by bacteria. Tight control of nodulation and infection is required to maintain the mutualistic character of the interaction. Available evidence supports a passive bacterial role in nodulation and infection after the microsymbiont has triggered the symbiotic plant developmental program. Here we identify in Sinorhizobium meliloti , the Medicago symbiont, a cAMP-signaling regulatory cascade consisting of three receptor-like adenylate cyclases, a Crp-like regulator, and a target gene of unknown function. The cascade is activated specifically by a plant signal during nodule organogenesis. Cascade inactivation results in a hyperinfection phenotype consisting of abortive epidermal infection events uncoupled from nodulation. These findings show that, in response to a plant signal, rhizobia play an active role in the control of infection. We suggest that rhizobia may modulate the plant’s susceptibility to infection. This regulatory loop likely aims at optimizing legume infection.

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Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation

Cited by 47 publications

References 93 publications

WUSCHEL-RELATED HOMEOBOX5Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation

WUSCHEL-RELATED HOMEOBOX5Gene Expression and Interaction of CLE Peptides with Components of the Systemic Control Add Two Pieces to the Puzzle of Autoregulation of Nodulation

CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Plant-activated bacterial receptor adenylate cyclases modulate epidermal infection in the Sinorhizobium meliloti–Medicago symbiosis

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