The <i>Clavata2</i> genes of pea and <i>Lotus japonicus</i> affect autoregulation of nodulation

Krusell, Lene; Sato, Naoto; Fukuhara, Izumi; Koch, Bjørn E. V.; Grossmann, Christina; Okamoto, Satoru; Oka-Kira, Erika; Otsubo, Yoko; Aubert, Grégoire; Nakagawa, Tomomi; Sato, Shusei; Tabata, Satoshi; Duc, Gérard; Parniske, Martin; Wang, Trevor L.; Kawaguchi, Masayoshi; Stougaard, Jens

doi:10.1111/j.1365-313x.2010.04474.x

Cited by 116 publications

(123 citation statements)

References 54 publications

Supporting

Mentioning

114

Contrasting

Order By: Relevance

“…Identification of factors targeted by TML is important for understanding how NIN expression is regulated by AON. Legumes have coopted receptor proteins responsible for the SAM homeostatic regulation as shoot-acting AON factors (8,9,30,31). Cytokinin signaling is commonly implicated in nodule organogenesis as well as in the SAM homeostatic regulation and protoxylem vessel formation regulated by CLE10 (32)(33)(34).…”

Section: Discussionmentioning

confidence: 99%

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.

Self Cite

183

200

View full text Add to dashboard Cite

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 ...

show abstract

Section: Discussionmentioning

confidence: 99%

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.

Self Cite

183

200

View full text Add to dashboard Cite

show abstract

“…This type of information has been used successfully to clone other genes in peas (e.g., Weller et al 2009;Hellens et al 2010). Interestingly, there may also be a link between fasciation and nodulation in peas (Krusell et al 2011), and detailed work will be required to examine these possibilities.…”

Section: Position Of the Flowersmentioning

confidence: 99%

Mendel’s Genes: Toward a Full Molecular Characterization

Reid

Ross

2011

Genetics

View full text Add to dashboard Cite

The discipline of classical genetics is founded on the hereditary behavior of the seven genes studied by Gregor Mendel. The advent of molecular techniques has unveiled much about the identity of these genes. To date, four genes have been sequenced: A (flower color), LE (stem length), I (cotyledon color), and R (seed shape). Two of the other three genes, GP (pod color) and FA (fasciation), are amenable to candidate gene approaches on the basis of their function, linkage relationships, and synteny between the pea and Medicago genomes. However, even the gene (locus) identity is not known for certain for the seventh character, the pod form, although it is probably V. While the nature of the mutations used by Mendel cannot be determined with certainty, on the basis of the varieties available in Europe in the 1850s, we can speculate on their nature. It turns out that these mutations are attributable to a range of causes-from simple base substitutions and changes to splice sites to the insertion of a transposon-like element. These findings provide a fascinating connection between Mendelian genetics and molecular biology that can be used very effectively in teaching new generations of geneticists. Mendel's characters also provide novel insights into the nature of the genes responsible for characteristics of agronomic and consumer importance.

show abstract

“…In the case of pea (Pisum sativum L.), hypernodulating mutants have been selected after mutagenesis and three genes have been shown to be involved in the regulation of nodulation, namely NOD3 (Postma et al 1988), SYM29, and SYM28 (Sagan and Duc 1996). On the basis of homologies with Medicago truncatula or Lotus japonicus, these three genes have been identified (Krusell et al 2002(Krusell et al , 2011Schnabel et al 2011), NOD3 being of unknown function when the two other genes encode a leucine-rich receptor like kinase.…”

Section: Introductionmentioning

confidence: 99%

Pea nodule gradients explain N nutrition and limited symbiotic fixation in hypernodulating mutants

Voisin

Prudent

Duc

et al. 2015

Agron. Sustain. Dev.

View full text Add to dashboard Cite

Legumes fix atmospheric nitrogen by symbiosis with soil bacteria in root nodules. Legume yields are limited by the low capacity of N 2 fixation. Hypernodulating mutants have been selected decades ago to try to increase nodule number. However, literature data show that N fixation of hypernodulating mutants was not increased compared to parental lines. Here, we study the functional basis of limited N fixation associated to hypernodulation. We grew two wild type genotypes and nine hypernodulating mutants of pea in hydroponics in three greenhouse experiments. We measured the following traits related to N nutrition during the vegetative period: nodule number, plant N uptake, nodule-specific activity, and plant and nodule concentrations. Genetic and environmental variations induced nodule gradients. These gradients were used to set quantitative relationships between N nutrition traits and nodule number. We compared the relationships obtained for hypernodulating and for wild types. N nutrition traits were analysed together with C nutrition traits, through correlation networks. Our results show that higher nodule number of hypernodulating mutants is correlated with lower levels of nodule activity, from −25 to −60 %, by comparison to the wild type. Higher nodule number of hypernodulating mutants is also correlated with lower total N uptake by symbiotic fixation, from −0 to −60 %, by comparison to the wild type. Findings demonstrate that N nutrition is not a factor limiting growth in hypernodulating mutants, as shown by N nutrition index higher than 1, indicating N nutrition in excess. The correlations suggest that limited N 2 fixation in hypernodulating mutants arises from restricted shoot growth, which limits the plant capacity to accumulate N. Furthermore, symbiotic efficiency decreased with increasing nodule number, down to a minimal value for hypernodulating mutants. Thus, to overcome the trade-off between N benefits from N 2 fixation and carbon nodulation costs, the hypernodulation trait should be associated with high shoot growth capacity in breeding programs.

show abstract

The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation

Cited by 116 publications

References 54 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

Mendel’s Genes: Toward a Full Molecular Characterization

Pea nodule gradients explain N nutrition and limited symbiotic fixation in hypernodulating mutants

Contact Info

Product

Resources

About