IBENS - ENS

Pierre Baduel

Erwann Caillieux (équipe Colot) — 2018-04-18T13:52:38Z

CNRS Researcher

My research focuses on the evolution of plant genomes to understand the genetic mechanisms involved and their consequences for adaptation and evolution. I am particularly interested in the evolutionary consequences of transposable element (TE) dynamics and polyploidy, which are both major drivers of genome evolution.

Assessing how the genetic and environmental determinants of natural transposition shape its adaptive potential in Arabidopsis thaliana

Standing genetic variation is generally thought to be the main source of rapid adaptation to environmental changes. As a result, genomic studies aimed at estimating the evolutionary potential of native populations in future climates have mostly focused on SNPs. However, there is increasing evidence that the rare and typically large effect alleles created by TE insertions, even though mostly deleterious, can be sometimes beneficial and contribute significantly to local adaption. Leveraging the multi-omic and bio-climatic data for more than 1,000 wild A. thaliana accessions sequenced as part of the 1001 Genomes project, we set out to determine the rate of TE mobilization and its potential to create adaptive variation in natural settings.

Using an updated pipeline to detect TE insertion polymorphisms (TIPs) from short-read sequencing data, we identified >23,000 TIPs across >1000 accessions from across the globe. Based on this dataset, we determined the substitution rate of TIPs in nature to be almost a third of that of SNPs (between 0.06-0.08 TE insertion per genome per generation) and very close to the actual transposition rate we measured experimentally. However, unlike SNPs, TE insertions tend to have large deleterious effects when they insert within or near genes (which occurs at least 50% of the time for some TE families) and are therefore rapidly purged by purifying selection. Nonetheless, we found some gene loci to be recurrently targeted by TE insertions (most notably FLC's 1st intron), and these tended to be found in disturbed environments where they showed signatures of positive selection.

Furthermore, we also found that a naturally truncated variant of NRPE1 (a key component of the RdDM pathway which targets DNA methylation over TEs) causes lower CHH methylation and higher levels of transposition, largely by enhancing the environmental sensitivity (GxE) of TEs. Strikingly, this mutator NRPE1 allele is enriched at the edge of the environmental niche of A. thaliana where it itself shows signature of positive selection, akin in a way to bacterial mutator alleles that can be temporarily beneficial in harsh environments. How such an allele has been retained over long term in A. thaliana opens exciting avenues of inquiry, especially in times of climate crisis where TEs may be essential genomic players in the demise or rescue of native populations.

Evaluating transposable elements dynamics following auto-polyploidization in Arabidopsis arenosa

During my PhD with Professor Bomblies at Harvard University, followed by a short postdoc at the John Innes Centre in Norwich, UK, I investigated the impact of whole-genome duplication (WGD) on genome evolution in the young natural diploid / autotetraploid system offered by A. arenosa. Leveraging a large genome resequencing dataset encompassing 300 samples of both diploid and tetraploid A. arenosa, I showed that polyploids present increased non-synonymous sequence diversity, and established it was due mainly to increased effective population sizes with an additional effect from the genetic masking of deleterious mutations associated with polysomy.

In the group of Dr. Colot at the IBENS in Paris, I have initiated a collaborative project to further investigate the genome evolution of autopolyploids in relation to transposable elements (TEs) dynamics. Due to their mostly deleterious effects, TE insertions are indeed predicted to benefit significantly from the genetic masking I showed was at play in autotetraploids. In addition, transposition bursts have been proposed to follow the genome shock of auto-polyploidization, and both mechanisms have been hypothesized to underlie the increased TE content typically observed in polyploids. Using the bioinformatics tools developed by the Colot group to analyze the genomic sequences available in A. arenosa, I was able to comprehensively measure TE mobilization in both diploids and tetraploids. Thus, I showed that the increased TE content observed in tetraploid A. arenosa was mostly driven by the genetic masking associated with polyploidy. In contrast, I could not find any evidence of a transposition burst dating back to the ancestral polyploidization event, demonstrating that WGD is not sufficient to induce such a response and may require additional genetic or environmental determinants.

Nonetheless, I find evidence that TE insertions can be more than just a burden and occasionally contribute to the adaptive potential of polyploid populations. In tetraploid A. arenosa, TE insertions appear to be under local positive selection when within environmentally responsive genes notably the major flowering-time repressor gene FLOWERING LOCUS C (FLC). At this locus, I identified an exonic TE insertion that is specifically associated with the rapid-cycling tetraploid lineage that colonized railways, supporting the idea that TEs can generate alleles enabling rapid adaptation to novel habitats. Yet, the higher TE load in polyploids suggests that in the long run, the accumulation of deleterious mutations, in particular genic TE insertions, could have a major negative impact on the evolution of polyploids. This is one of the main reasons why I argued that, unless selected for, polyploidy is a transient state that will likely eventually result in extinction, or stabilization of the lineage by re-diploidization. I envision something we called a ‘polyploid hop', in which the increased genetic diversity, as well as other mechanistic and physiological advantages of polyploid populations, may enable adaptation to new and more challenging environments. In the process, TEs might potentially also reshape genomes by causing ectopic recombination, which could lead to genome divergence and reproductive isolation.

Research papers

Baduel P, Leduque B, Ignace A, Gy I, Gil J, Loudet O, Colot V, Quadrana L. (2021) Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana. Genome Biol.
Baduel P, Quadrana L, Colot V. (2021) Efficient detection of transposable element insertion polymorphisms between genomes using short-read sequencing data. Methods Mol Biol.
Baduel P, Colot V (2021) The epiallelic potential of transposable elements and its evolutionary significance in plants. Philosophical Transactions of the Royal Society
Baduel P, Quadrana L, Hunter B, Bomblies K, Colot V. (2019) Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation. Nat Commun.
Monnahan P, Kolář F, Baduel P, Sailer C, Koch J, Horvath R, Laenen B, Schmickl R, Paajanen P, Fuxová G, Holcová M, Arnold B, Weismann C, Marhold K, Slotte T, Bomblies K, Yant L (2018) Pervasive population genomic consequences of genome duplication in A. arenosa. Nat Ecol Evol.
Baduel P, Bray S, Vallejo-Marin M, Kolář F, Yant L (2018) The ‘Polyploid Hop' : shifting challenges and opportunities over the evolutionary lifespan of genome duplications. Frontiers in Ecology and Evolution.
Baduel P, Hunter B, Yeola S, Bomblies K (2018) Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa. PLoS Genetics. 14(7):e1007510.
Wilton PR, Baduel P, Landon MM, and Wakeley J (2017) Population structure and coalescence in pedigrees : Comparisons to the structured coalescent and a framework for inference. Theor. Popul. Biol. 115, pp. 1–12.
Baduel P, Arnold B, Weisman CM, Hunter B, and Bomblies K (2016) Habitat-associated life history and stress-tolerance variation in Arabidopsis arenosa. Plant Physiol. 171(1) pp. 437–451.

Publications

Erwann Caillieux (équipe Colot) — 2017-11-02T15:55:41Z

Sasaki T, Ro K, Caillieux E, Manabe R, Bohl-Viallefond G, Baduel P, Colot V, Kakutani T, Quadrana L. (2022) Fast co-evolution of anti-silencing systems shapes the invasiveness of Mu-like DNA transposons in eudicots. EMBO J.

Baduel P, Leduque B, Ignace A, Gy I, Gil J, Loudet O, Colot V, Quadrana L. (2021) Genetic and environmental modulation of transposition shapes the evolutionary potential of Arabidopsis thaliana. Genome Biol.

Baduel P, Quadrana L, Colot V. (2021) Efficient detection of transposable element insertion polymorphisms between genomes using short-read sequencing data. Methods Mol Biol.

Quadrana L, Silveira AB, Caillieux E, Colot V. (2021) Detection of transposable element insertions in Arabidopsis using sequence capture. Methods Mol Biol.

Baduel P, Colot V (2021) The epiallelic potential of transposable elements and its evolutionary significance in plants. Philos. Trans. R. Soc. Lond. B Biol. Sci.

Khouider S, Borges F, LeBlanc C, Ungru A, Schnittger A, Martienssen R, Colot V, Bouyer D (2021) Male fertility in Arabidopsis requires active DNA demethylation of genes that control pollen tube function. Nat Commun

Domínguez M, Dugas E, Benchouaia M, Leduque B, Jiménez-Gómez JM, Colot V, Quadrana L. (2020) The impact of transposable elements on tomato diversity. Nat Commun

Van Dooren TJM, Silveira AB, Gilbault E, Jiménez-Gómez JM, Martin A, Bach L, Tisné S, Quadrana L, Loudet O, Colot V. (2020) Mild drought in the vegetative stage induces phenotypic, gene expression, and DNA methylation plasticity in Arabidopsis but no transgenerational effects. J Exp Bot

Baduel P, Quadrana L, Hunter B, Bomblies K, Colot V. (2019) Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation. Nat Commun

Quadrana L, Etcheverry M, Gilly A, Caillieux E, Madoui MA, Guy J, Bortolini Silveira A, Engelen S, Baillet V, Wincker P, Aury JM, Colot V. (2019) Transposition favors the generation of large effect mutations that may facilitate rapid adaption. Nat Commun

Yang L, Perrera V, Saplaoura E, Apelt F, Bahin M, Kramdi A, Olas J, Mueller-Roeber B, Sokolowska E, Zhang W, Li R, Pitzalis N, Heinlein M, Zhang S, Genovesio A, Colot V, Kragler F. (2019). m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr Biol

Furci L, Jain R, Stassen J, Berkowitz O, Whelan J, Roquis D, Baillet V, Colot V, Johannes F, Ton J. (2019). Identification and characterisation of hypomethylated DNA loci controlling quantitative resistance in Arabidopsis. Elife

Liégard B, Baillet V, Etcheverry M, Joseph E, Lariagon C, Lemoine J, Evrard A, Colot V, Gravot A, Manzanares-Dauleux M.J, Jubault M. (2018). Quantitative resistance to clubroot infection mediated by transgenerational epigenetic variation in Arabidopsis. New Phytol

Morao AK, Caillieux E, Colot V, and Roudier F. (2018). Cell type-specific profiling of chromatin modifications and associated proteins. Methods Mol Biol

Chica C, Louis A, Roest Crollius H, Colot V, Roudier F. (2017). Comparative epigenomics in the Brassicaceae reveals two evolutionarily conserved modes of PRC2-mediated gene regulation. Genome Biol

Bouyer D, Kramdi A, Kassam M, Heese M, Schnittger A, Roudier F, Colot, V. (2017). DNA methylation dynamics during early plant life. Genome Biol

Rosspopoff O, Chelysheva L, Saffar J, Lecorgne L, Gey D, Caillieux E, Colot V, Roudier F, Hilson P, Berthome R, Da Costa M, Rech P. (2017). Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development

Morao AK, Bouyer D, Roudier F. (2016). Emerging concepts in chromatin-level regulation of plant cell differentiation : timing, counting, sensing and maintaining. Curr Opin Plant Biol

Quadrana L, Colot V. (2016). Plant Transgenerational Epigenetics. Annu Rev Genet

de Lucas M, Pu L, Turco G, Gaudinier A, Morao AK, Harashima H, Kim D, Ron M, Sugimoto K, Roudier F, Brady SM. (2016). Transcriptional regulation of Arabidopsis Polycomb Repressive Complex 2 coordinates cell-type proliferation and differentiation. Plant Cell

Fransz P, Linc G, Lee CR, Aflitos SA, Lasky JR, Toomajian C, Ali H, Peters J, van Dam P, Ji X, Kuzak M, Gerats T, Schubert I, Schneeberger K, Colot V, Martienssen R, Koornneef M, Nordborg M, Juenger TE, de Jong H, Schranz ME. (2016). Molecular, genetic and evolutionary analysis of a paracentric inversion in Arabidopsis thaliana. Plant J

Schalk C, Drevensek S, Kramdi A, Kassam M, Ahmed I, Cognat V, Graindorge S, Bergdoll M, Baumberger N, Heintz D, Bowler C, Genschik P, Barneche F, Colot V, Molinier J. (2016). DNA DAMAGE BINDING PROTEIN 2 (DDB2) shapes the DNA methylation landscape. Plant Cell

Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, Colot, V. (2016). The Arabidopsis thaliana mobilome and its impact at the species level.Elife

Marques-Bueno MDM, Morao AK, Cayrel A, Platre MP, Barberon M, Caillieux E, Colot V, Jaillais Y, Roudier F, Vert G. (2016). A versatile Multisite Gateway-compatible promoter and transgenic line collection for cell type-specific functional genomics in Arabidopsis. Plant J

Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, Brkljacic J, Browse J, Chapple C, Colot V, Cutler S, Dangl J, Ehrhardt D, Friesner JD, Frommer WB, Grotewold E, Meyerowitz E, Nemhauser J, Nordborg M, Pikaard C, Shanklin J, Somerville C, Stitt M, Torii KU, Waese J, Wagner D, McCourt P. (2016). 50 years of Arabidopsis research : highlights and future directions. New Phytol

Membres de l'équipe

Erwann Caillieux (équipe Colot) — 2016-01-08T16:05:11Z

Permanent staff

Vincent Colot Group Leader DR, CNRS	Pierre Baduel CR, CNRS Webpage	Barbara Després MdC, ENS
Erwann Caillieux IE, CNRS

Non-permanent staff

Louna De Oliveira

IE, CNRS

Mounia El Messaoudi

PhD student

Lab alumni

Mattéo Barois

Leandro Quadrana

Mireia Bueno

Basile Leduque

Sébastien Lemaire

Vipin Singh

Souraya Khouider

Daniel Bouyer

Marisol Dominguez

Amira Kramdi

Victoire Baillet

Elise Dugas

Ana Karina Morao

François Roudier

Amanda Bortolini Silveira

Valentina Perrera

Benoit Lahouze

Mohamed Kassam

Mathilde Etcheverry

Claudia Chica

Romy Chen-Min-Tao

Alexis Sarazin

Evelyne Duvernois-Berthet

Ikhlak Ahmed

Martine Boccara

Sandra Cortijo

Tony Heitkam

Antoine Martin

Bogna Szarzinska

Felipe Karam Teixeira

Voir en ligne : Site web de l'équipe