DNA methylation is an important epigenetic mark required for proper gene expression and silencing of transposable elements. DNA methylation patterns can be modified by environmental factors such as pathogen infection, where modification of DNA methylation can be associated with plant resistance. To counter the plant defense pathways, pathogens produce effectors molecule, several of which act as proteasome inhibitors. Here we investigated the effect of proteasome inhibition by the bacterial virulence factor Syringolin A on genome-wide DNA methylation. We show that Syringolin A treatment results in an increase of DNA methylation at centromeric and pericentromeric regions of Arabidopsis chromosomes. We identify several CHH DMRs that are enriched in the proximity of transcriptional start sites. Syringolin A treatment does not result in significant changes in small RNA composition. However, significant changes in genome transcriptional activity can be observed, including a strong upregulation of resistance genes that are located on chromosomal arms. We hypothesize that DNA methylation changes could be linked to the upregulation of some atypical members of the de novo DNA methylation pathway: AGO3, AGO9 and DRM1. Our data suggests that modification of genome-wide DNA methylation resulting from an inhibition of the proteasome by bacterial effectors could be part of a epi-genomic arms race against pathogens.
In recent years, small RNA movement has been both hypothesized and shown to be an integral part of the epigenetic DNA methylation reprogramming occurring during plant reproduction. It was suggested that the release of epigenetic silencing in accessory cell types or tissues is necessary to reinforce epigenetic silencing in the gametes (egg cell and sperm cells) which would in turn ensure the genomic stability of the next generation plant. Small RNA movement was indeed shown to occur during male gametogenesis. However, the situation within the female gametophyte and in early seed development is mostly unknown. Here, we show that small RNA can induce non-cell autonomous silencing from the central cell towards the egg cell but also from the synergids to the egg cell and central cell. In addition, we also observe a non-cell-autonomous silencing from the central cell or endosperm towards the early embryo. Our data shows, that in addition to the movement of sRNAs during pollen development, sRNA movement also occurs in the female gametes.
JA Schröder, DMV Bonnet, PE Jullien*. Non-cell autonomous small RNA silencing in female gametes and early embryo of Arabidopsis. bioRxiv 2022. doi: https://doi.org/10.1101/2022.03.21.485150
Tirot L, Bonnet DMV, Jullien PE*. DNA Methyltransferase 3 (MET3) is regulated by Polycomb group complex during Arabidopsis endosperm development. PlantReprod. 2022 Jan 28. doi: 10.1007/s00497-021-00436-x.
Oliver C, Annacondia ML, Wang Z, Jullien PE, Slotkin RK, Köhler C, Martinez G. The miRNome function transitions from regulating developmental genes totransposable elements during pollen maturation. Plant Cell. 2022 Feb3;34(2):784-801. doi: 10.1093/plcell/koab280.
Jullien PE*, Schröder JA, Bonnet DMV, Pumplin N, Voinnet O. Asymmetric
expression of Argonautes in reproductive tissues. Plant Physiol. 2022 Jan
20;188(1):38-43. doi: 10.1093/plphys/kiab474.
Tirot, L.; Jullien, P.E*.; Ingouff, M*. Evolution of CG Methylation Maintenance Machinery in Plants. Epigenomes 2021, 5, 19. https://doi.org/10.3390/epigenomes5030019
Bonnet DMV, Grob S, Tirot L and Jullien PE*. Methylome dynamics upon proteasome inhibition by the pseudomonas virulence factor Syringolin A. BioXriv. https://doi.org/10.1101/2021.01.19.
Devers, Emanuel A.; Brosnan, Christopher A.; Sarazin, Alexis; Albertini, Daniele; Amsler, Andrea C.; Brioudes, Florian; Jullien, Pauline E.; Lim, Peiqi; Schott, Gregory; Voinnet, Olivier (2020). Movement and differential consumption of short interfering RNA duplexes underlie mobile RNA interference. Nature plants, 6(7), pp. 789-799. 10.1038/s41477-020-0687-2
Jullien, P.E., Grob, S., Marchais, A., Pumplin, N., Chevalier, C., Bonnet, D.M., Otto, C., Schott, G. and Voinnet, O. (2020), Functional characterization of Arabidopsis ARGONAUTE 3 in reproductive tissues. Plant J. doi:10.1111/tpj.14868
2018 and older
Tschopp, MA; Iki; T, Brosnan, CA; Jullien, PE; Pumplin, N. (2017). A complex of Arabidopsis DRB proteins can impair dsRNA processing. RNA, 23, pp. 782-797. 10.1261/rna.059519.116
Pumplin, N; Sarazin, A; Jullien, PE; Bologna, NG; Oberlin, S; Voinnet, O. (2016). DNA Methylation Influences the Expression of DICER-LIKE4 Isoforms, Which Encode Proteins of Alternative Localization and Function. The Plant Cell, 28(11), pp. 2786-2804. 10.1105/tpc.16.00554
Calarco, JP; Borges, F; Donoghue, MT; van Ex, F; Jullien, PE; Lopes, T; Gardner, R; Berger, F; Feijó, JA; Becker, JD; Martienssen, RA. (2012). Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell, 151(1), pp. 194-205. 10.1016/j.cell.2012.09.001
Jullien, PE; Susaki, D; Yelagandula, R; Higashiyama, T; Berger, F. (2012). DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Current Biology, 22(19), pp. 1825-1830. 10.1016/j.cub.2012.07.061
Jullien, PE; Berger, F. (2010). DNA methylation reprogramming during plant sexual reproduction? Trends in Genetics, 26(9), pp. 394-399. 10.1016/j.tig.2010.06.001
Jullien, PE; Berger, F. (2010). Parental Genome Dosage Imbalance Deregulates Imprinting in Arabidopsis. PLoS Genetics, 6(3), e1000885. 10.1371/journal.pgen.1000885
Jullien, PE; Berger, F. (2009). Gamete-specific epigenetic mechanisms shape genomic imprinting. Current Opinion in Plant Biology 12(5), pp. 637-642. 10.1016/j.pbi.2009.07.004
Jullien, PE; Berger, F. (2008). Parental genomic imprinting in plants: significance for reproduction. Medecine sciences, 24(8-9), pp. 753-757. 10.1051/medsci/20082489753
Jullien, PE; Mosquna, A; Ingouff, M; Sakata, T; Ohad, N; Berger, F. (2008). Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biology, 6(8), e194. 10.1371/journal.pbio.0060194
Aubourg, S; Martin-Magniette, ML; Brunaud, V; Taconnat, L; Bitton, F; Balzergue, S; Jullien, PE; Ingouff, M; Thareau, V; Schiex, T; Lecharny, A; Renou, JP. (2007). Analysis of CATMA transcriptome data identifies hundreds of novel functional genes and improves gene models in the Arabidopsis genome. BMC Genomics, 8, 401. 10.1186/1471-2164-8-401
Ingouff, M; Jullien, PE; Berger, F. (2006). The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. The Plant Cell, 18(12), pp. 3491-3501. 10.1105/tpc.106.047266
Jullien, PE; Kinoshita, T; Ohad, N; Berger, F. (2006). Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. The Plant Cell, 18(6), pp. 1360-1372. 10.1105/tpc.106.041178
Jullien, PE; Katz, A; Oliva, M; Ohad, N; Berger, F. (2006) Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Current Biology, 16(5), pp. 486-492. 10.1016/j.cub.2006.01.020