Compact Root Architecture 2 Promotes Root Competence for Nodulation through the miR2111 Systemic Effector

Gautrat, Pierre; Laffont, Carole; Frugier, Florian

doi:10.1016/j.cub.2020.01.084

Cited by 83 publications

(123 citation statements)

References 31 publications

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“…Further investigations are needed to explore which downstream targets of the MtCRA2 pathway are recruited in shoots to drive the systemic regulation of root nodulation. A recent study notably identified that miR2111 is a systemic effector acting downstream of MtCRA2 to promote nodulation (Gautrat et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula

et al. 2020

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Because of the large amount of energy consumed during symbiotic nitrogen fixation, legumes must balance growth and symbiotic nodulation. Both lateral roots and nodules form on the root system, and the developmental coordination of these organs under conditions of reduced nitrogen (N) availability remains elusive. We show that the Medicago truncatula COMPACT ROOT ARCHITECTURE2 (MtCRA2) receptor-like kinase is essential to promote the initiation of early symbiotic nodulation and to inhibit root growth in response to low N. C-TERMINALLY ENCODED PEPTIDE (MtCEP1) peptides can activate MtCRA2 under N-starvation conditions, leading to a repression of YUCCA2 (MtYUC2) auxin biosynthesis gene expression, and therefore of auxin root responses. Accordingly, the compact root architecture phenotype of cra2 can be mimicked by an auxin treatment or by overexpressing MtYUC2, and conversely, a treatment with YUC inhibitors or an MtYUC2 knockout rescues the cra2 root phenotype. The MtCEP1-activated CRA2 can additionally interact with and phosphorylate the MtEIN2 ethylene signaling component at Ser 643 and Ser 924 , preventing its cleavage and thereby repressing ethylene responses, thus locally promoting the root susceptibility to rhizobia. In agreement with this interaction, the cra2 low nodulation phenotype is rescued by an ein2 mutation. Overall, by reducing auxin biosynthesis and inhibiting ethylene signaling, the MtCEP1/MtCRA2 pathway balances root and nodule development under low-N conditions.

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Section: Discussionmentioning

confidence: 99%

A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula

et al. 2020

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“…Various classes of small secretory peptides have been shown to play vital role in symbiosis Djordjevic et al, 2015;de Bang et al, 2017;Gautrat et al, 2020). Therefore, we examined stage-specific DEGs for transcripts coding for small secretory peptides.…”

Section: Small Secretory Peptides Contribute To Nodule Transcriptome mentioning

confidence: 99%

Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity

et al. 2020

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SUMMARY Soybean nodulation is a highly controlled process that involves complex gene regulation at both transcriptional and post‐transcriptional levels. In the present study, we profiled gene expression changes, alternative splicing events, and DNA methylation patterns during nodule formation, development, and senescence. The transcriptome data uncovered key transcription patterns of nodule development that included 9669 core genes and 7302 stage‐specific genes. Alternative splicing analysis uncovered a total of 2323 genes that undergo alternative splicing events in at least one nodule developmental stage, with activation of exon skipping and repression of intron retention being the most common splicing events in nodules compared to roots. Approximately 40% of the differentially spliced genes were also differentially expressed at the same nodule developmental stage, implying a substantial association between gene expression and alternative splicing. Genome‐wide‐DNA methylation analysis revealed dynamic changes in nodule methylomes that were specific to each nodule stage, occurred in a sequence‐specific manner, and impacted the expression of 1864 genes. An attractive hypothesis raised by our data is that increased DNA methylation may contribute to the efficiency of alternative splicing. Together, our results provide intriguing insights into the associations between gene expression, alternative splicing, and DNA methylation that may shape transcriptome complexity and proteome specificity in developing soybean nodules.

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“…Both processes initially require upregulation of CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) peptides that are perceived by a leucine-rich repeat receptor-like kinase (LRR-RLK) called MtSUNN/GmNARK/LjHAR1/PsSYM29/PvNARK (Krusell et al, 2002;Nishimura et al, 2002;Searle et al, 2003;Schnabel et al, 2005;Ferguson et al, 2014). The shoot-derived signal of AON has been identified as miR2111, which targets the Kelch-repeat factor, TOO MUCH LOVE (TML), for degradation to inhibit the development of new nodules (Takahara et al, 2013;Tsikou et al, 2018;Gautrat et al, 2020). Recent findings using Lotus japonicus suggest TML might not be required for nitrate-dependent inhibition (Nishida et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Characterisation ofMedicago truncatulaCLE34 and CLE35 in nodulation control

Mens

Hastwell

et al. 2020

Preprint

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Legume plants form a symbiosis with N2-fixing soil rhizobia, resulting in new root organs called nodules that enable N2-fixation. Nodulation is a costly process that is tightly regulated by the host through Autoregulation of Nodulation (AON) and nitrate-dependent regulation of nodulation. Both pathways require legume-specific CLAVATA/ESR-related (CLE) peptides. Nitrogen-induced nodulation-suppressing CLE peptides have not previously been characterised in Medicago truncatula, with only rhizobia-induced MtCLE12 and MtCLE13 identified. Here, we report on novel peptides MtCLE34 and MtCLE35 in nodulation control pathways. The nodulation-suppressing CLE peptides of five legume species were classified into three clades based on sequence homology and phylogeny. This approached identified MtCLE34 and MtCLE35 and four new CLE peptide orthologues of Pisum sativum. Whereas MtCLE12 and MtCLE13 are induced by rhizobia, MtCLE34 and MtCLE35 respond to both rhizobia and nitrate. MtCLE34 was identified as a pseudogene lacking a functional CLE-domain. Overexpression of MtCLE12, MtCLE13 and MtCLE35 inhibits nodulation. Together, our findings indicate that MtCLE12 and MtCLE13 have a distinct role in AON, while MtCLE35 regulates nodule numbers in a rhizobia- and nitrate-dependent manner. MtCLE34 likely had a similar role to MtCLE35 but its function was lost due to a nonsense mutation resulting in the loss of the mature peptide.

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Compact Root Architecture 2 Promotes Root Competence for Nodulation through the miR2111 Systemic Effector

Cited by 83 publications

References 31 publications

A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula

A CEP Peptide Receptor-Like Kinase Regulates Auxin Biosynthesis and Ethylene Signaling to Coordinate Root Growth and Symbiotic Nodulation in Medicago truncatula

Interactions of gene expression, alternative splicing, and DNA methylation in determining nodule identity

Characterisation ofMedicago truncatulaCLE34 and CLE35 in nodulation control

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