Adaptation of <i>Medicago truncatula</i> to nitrogen limitation is modulated via local and systemic nodule developmental responses

Jeudy, Christian; Ruffel, Sandrine; Freixes, Sandra; Tillard, Pascal; Santoni, Anne Lise; Morel, Sylvain; Journet, Etienne-Pascal; Duc, Gérard; Gojon, Alain; Lepetit, Marc; Salon, Christophe

doi:10.1111/j.1469-8137.2009.03103.x

Cited by 114 publications

(163 citation statements)

References 64 publications

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“…In the roots, carbon content increased during nodulation, while nitrogen levels remained stable. The observation that the increased number of nodules found in HCT down-regulated roots does not correlate with increased nitrogen fixation is consistent with reports of Medicago species hypernodulating mutants (Jeudy et al, 2010). Interestingly, relative lignin content decreased by 32% in control and by 41% in HCT down-regulated roots following nodulation.…”

Section: Carbon/nitrogen Allocation During Nodulation In Low-lignin Psupporting

confidence: 91%

Lignin Modification Leads to Increased Nodule Numbers in Alfalfa

et al. 2014

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Reduction of lignin levels in the forage legume alfalfa (Medicago sativa) by down-regulation of the monolignol biosynthetic enzyme hydroxycinnamoyl coenzyme A:shikimate hydroxycinnamoyl transferase (HCT) results in strongly increased digestibility and processing ability of lignocellulose. However, these modifications are often also associated with dwarfing and other changes in plant growth. Given the importance of nitrogen fixation for legume growth, we evaluated the impact of constitutively targeted lignin modification on the belowground organs (roots and nodules) of alfalfa plants. HCT downregulated alfalfa plants exhibit a striking reduction in root growth accompanied by an unexpected increase in nodule numbers when grown in the greenhouse or in the field. This phenotype is associated with increased levels of gibberellins and certain flavonoid compounds in roots. Although HCT down-regulation reduced biomass yields in both the greenhouse and field experiments, the impact on the allocation of nitrogen to shoots or roots was minimal. It is unlikely, therefore, that the altered growth phenotype of reduced-lignin alfalfa is a direct result of changes in nodulation or nitrogen fixation efficiency. Furthermore, HCT down-regulation has no measurable effect on carbon allocation to roots in either greenhouse or 3-year field trials.

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Section: Carbon/nitrogen Allocation During Nodulation In Low-lignin Psupporting

confidence: 91%

Lignin Modification Leads to Increased Nodule Numbers in Alfalfa

et al. 2014

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“…I n hypernodulating mutants, which are characterised by defective AON regulation, the loss of nodule number regulation occurs simultaneously with loss of nitrate sensitivity of nodulation (Oka-Kira and Kawaguchi 2006). This suggests that the AON pathway shares common elements with the control of nodule development by the whole plant N status (Jeudy et al 2010). Therefore, we hypothesized that hypernodulation would first impact the relationships between nodule number and the plant N status, and that this would in turn impact carbon nutrition traits.…”

Section: Introductionmentioning

confidence: 99%

“…Two main reasons can account for this particularity of legume plants: first, nodule number is limited by the host plant (see below); second, legume plant response to restore its N status following a stress mainly relies on the enhancement of nodule biomass and on the increase of nodule number, as shown in split-root experiments in which one part of the nodulated root system was deprived of N 2 (Jeudy et al 2010). Indeed, no short-term increase of N 2 -specific activity of the nodules still exposed to N 2 could be observed, whereas this was the case for root-specific nitrate uptake in root systems partly deprived of nitrate (Jeudy et al 2010). Therefore, increasing symbiotic fixation through an increase of nodule number and/or biomass could be a promising perspective.…”

Section: Introductionmentioning

confidence: 99%

“…The regulation of nodule development by the whole plant N status was shown to be the second major pathway involved in the control of nodule number by the host plant (Jeudy et al 2010). When nodulation occurs in wild types, whole plant studies have shown a positive environmental correlation between nodule number and plant growth rate (Voisin et al 2010).…”

Section: Introductionmentioning

confidence: 99%

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

Voisin

Prudent

Duc

et al. 2015

Agron. Sustain. Dev.

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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.

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“…Similarly, the improvement of LR deployment in crops is of significant interest to breeders to maximize water, nutrient, and fertilizer acquisition and alleviate pollution issues that arise from poor fertilizer uptake (Gamuyao et al, 2012); therefore legumes provide a system to study both nodule and LR organogenesis programs and how they interact. Although both LRs and nodules are induced by common environmental cues such as low N-availability (Ruffel et al, 2008;Jeudy et al, 2010;Jin et al, 2012), the common and specific pathways that regulate these different developmental competencies are poorly understood. Therefore, understanding signaling molecules, receptors, and downstream pathways that regulate both nodule and LR development in legumes under different environmental conditions is essential to improve nutrient acquisition by the root system.…”

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.

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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Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses

Cited by 114 publications

References 64 publications

Lignin Modification Leads to Increased Nodule Numbers in Alfalfa

Lignin Modification Leads to Increased Nodule Numbers in Alfalfa

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

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

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