Unraveling new molecular players involved in the autoregulation of nodulation in<i>Medicago truncatula</i>

Gautrat, Pierre; Mortier, Virginie; Laffont, Carole; Keyser, Annick De; Fromentin, Justine; Frugier, Florian; Goormachtig, Sofie

doi:10.1093/jxb/ery465

Cited by 48 publications

(54 citation statements)

References 67 publications

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“…As a proof of concept, we first described in M. truncatula the detection of epistatic selection between the Super Numeric Nodule MtSUNN gene, encoding a receptor which is central for the negative regulation of symbiotic root nodulation, and the CLAVATA3-like (CLE) signaling peptide MtCLE02 . This finding is reminiscent of the functional interaction proposed for other CLE signalling peptides, MtCLE12 and MtCLE13 previously shown to require the MtSUNN receptor to regulate negatively the number of nodule organs on the plant root system (29, 30). Accordingly, an ectopic expression of the MtCLE02 gene in M. truncatula wild-type and sunn mutant roots experimentally demonstrated a MtSUNN -dependent negative role of the MtCLE02 gene on nodulation, hence validating functionally the genetic interaction between these two genes.…”

Section: Introductionsupporting

confidence: 63%

A fast linkage disequilibrium-based statistical test for Genome-Wide Epistatic Selection Scans in structured populations

Boyrie

Moreau

Frugier

et al. 2020

Preprint

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22The quest for genome-wide signatures of selection in populations using SNP data has 23 proven efficient to uncover genes involved in conserved or adaptive molecular functions, but 24 none of the statistical methods were designed to identify interacting genes as targets of 25 selective processes. Here, we propose a straightforward statistical test aimed at detecting 26 epistatic selection, based on a linkage disequilibrium (LD) measure accounting for population 27 structure and heterogeneous relatedness between individuals. SNP-based ( ) and window-28 based ( 1 ) statistics fit a Student distribution, allowing to easily and quickly test the 29 significance of correlation coefficients in the frame of Genome-Wide Epistatic Selection 30 Scans (GWESS) using candidate genes as baits. As a proof of concept, use of SNP data from 31 the Medicago truncatula symbiotic legume plant uncovered a previously unknown gene 32 coadaptation between the MtSUNN (Super Numeric Nodule) receptor and the MtCLE02 33 (CLAVATA3-Like) signalling peptide, and experimental evidence accordingly supported a 34 MtSUNN-dependent negative role of MtCLE02 in symbiotic root nodulation. Using human 35 HGDP-CEPH SNP data, our new statistical test uncovered strong LD between SLC24A5 and 36 EDAR worldwide, which persists after correction for population structure and relatedness in 37 Central South Asian populations. This result suggests adaptive genetic interaction or 38 coselection between skin pigmentation and the ectodysplasin pathway involved in the 39 development of ectodermal organs (hairs, teeth, sweat glands), in some human populations. 40 Applying this approach to genome-wide SNP data will foster the identification of 41 evolutionary coadapted gene networks. 42 43 Author summary 46 Population genomic methods have allowed to identify many genes associated with 47 adaptive processes in populations with complex histories. However, they are not designed to 48 identify gene coadaptation between genes through epistatic selection, in structured 49 populations. To tackle this problem, we developed a straightforward LD-based statistical test 50 accounting for population structure and heterogeneous relatedness between individuals, using 51 SNP-based ( ) or windows-based ( 1 ) statistics. This allows easily and quickly testing 52 for significance of correlation coefficients between polymorphic loci in the frame of Genome 53 Wide Epistatic Selection Scans (GWESS). Following detection of gene coadaptation using 54 SNP data from human and the model plant Medicago truncatula, we report experimental 55 evidence of genetic interaction between two receptors involved in the regulation of root 56 nodule symbiosis in Medicago truncatula. This test opens new avenues for exploring the 57 evolution of genes as interacting units and thus paves the way to infer new networks based on 58 evolutionary coadaptation between genes. 59 60 65 selection against deleterious mutations (1-3). Identifying genes showing such selection 66 signatures has been a major goal of population...

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Section: Introductionsupporting

confidence: 63%

A fast linkage disequilibrium-based statistical test for Genome-Wide Epistatic Selection Scans in structured populations

Boyrie

Moreau

Frugier

et al. 2020

Preprint

Self Cite

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“…In addition to the common symbiotic pathway essential for early signaling and infection events in nodulation and AM (Radhakrishnan et al, 2020), we might consider this negative regulation of symbioses via autoregulation as the bookend to this pathway and therefore a component of the so called 'common symbiotic pathway' (Chiu and Paszkowski, 2020). Indeed, recent studies have suggested AON may influence a subset of genes, including the Nod-factor receptor NFP (Gautrat et al, 2019), integrating these two programs. It is also interesting to consider that although the CLV-CLE pathway shares an orthologous role in shoot apical meristem control in non-legumes, no clear role for CLV1-like genes in shoot development of legumes has been observed (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…Key downstream root acting players include the kelch repeat-containing F-box protein TML (Gautrat et al, 2019;Magori et al, 2009;Takahara et al, 2013), and the transcriptional regulation of nod factor receptors (Gautrat et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

Wang

Velandia

Kwon

et al. 2020

Preprint

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AbstractPlants form mutualistic nutrient acquiring symbioses with microbes, including arbuscular mycorrhizal fungi. The formation of these symbioses is costly and plants employ a negative feedback loop termed autoregulation of mycorrhizae (AOM) to limit arbuscular mycorrhizae (AM) formation. We provide evidence for the role of one leucine-rich-repeat receptor like kinase (FAB), a hydroxyproline O-arabinosyltransferase enzyme (FIN), one CLE peptide, SlCLE11 and additional evidence for the one receptor like protein (SlCLV2) in the negative regulation of AM formation in tomato. Reciprocal grafting experiments suggest that the FAB gene acts locally in the root, while the SlCLV2 gene may act in both the root and the shoot. External nutrients including phosphate and nitrate can also strongly suppress AM formation. We found that FAB and FIN are required for nitrate suppression of AM but are not required for the powerful suppression of AM colonisation by phosphate. This parallels some of the roles of legume homologs in the autoregulation of the more recently evolved symbioses with nitrogen-fixing bacteria leading to nodulation. This deep homology in the symbiotic role of these genes suggests that in addition to the early signalling events that lead to the establishment of AM and nodulation, the autoregulation pathway might also be considered part of the common symbiotic toolkit that enabled plants to form beneficial symbioses.HighlightWe describe the role of CLV signalling elements in the negative regulation of arbuscular mycorrhizal symbioses of tomato, including influencing nitrate but not phosphate suppression of mycorrhizal colonisation.

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“…TOO MUCH LOVE (TML), the target of miR2111, restricts nodule formation [127]. However, in the absence of rhizobia, miR2111 is expressed in leaf CCs and translocates to the roots, where mature miR2111 post-transcriptionally regulates TML, which down-regulates genes that affect nodulation factor perception and thus inhibits repression of nodulation [182]. Following exposure to rhizobia, a CK-dependent signal from roots inhibits miR2111 production in the shoot, which allows TML to limit nodule formation [127,128].…”

Section: Nodulationmentioning

confidence: 99%

The interplay of phloem-mobile signals in plant development and stress response

Koenig

Hoffmann-Benning

2020

Bioscience Reports

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Plants integrate a variety of biotic and abiotic factors for optimal growth in their given environment. While some of these responses are local, others occur distally. Hence, communication of signals perceived in one organ to a second, distal part of the plant and the coordinated developmental response require an intricate signaling system. To do so, plants developed a bipartite vascular system that mediates the uptake of water, minerals, and nutrients from the soil; transports high-energy compounds and building blocks; and traffics essential developmental and stress signals. One component of the plant vasculature is the phloem. The development of highly sensitive mass spectrometry and molecular methods in the last decades has enabled us to explore the full complexity of the phloem content. As a result, our view of the phloem has evolved from a simple transport path of photoassimilates to a major highway for pathogens, hormones, and developmental signals. Understanding phloem transport is essential to comprehend the coordination of environmental inputs with plant development and, thus, ensure food security. This review discusses recent developments in its role in long-distance signaling and highlights the role of some of the signaling molecules. What emerges is an image of signaling paths that do not involve single molecules but rather, quite frequently an interplay of several distinct molecular classes, many of which appear to be transported and acting in concert.

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Unraveling new molecular players involved in the autoregulation of nodulation inMedicago truncatula

Abstract: We provide new insights into the autoregulation of nodulation that allow us to better understand how the legume Medicago truncatula restricts further nodulation once enough nodules have been formed.

Cited by 48 publications

References 67 publications

A fast linkage disequilibrium-based statistical test for Genome-Wide Epistatic Selection Scans in structured populations

A fast linkage disequilibrium-based statistical test for Genome-Wide Epistatic Selection Scans in structured populations

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

The interplay of phloem-mobile signals in plant development and stress response

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