When the genome lowers its epigenetic shield: Transposable elements on the move Etienne Bucher IRHS, Angers, France www.plantepigenetics.ch @methylcytosine MAIN ACTIVITIES OF THE GROUP Basic research identifying novel epigenetic regulators in Arabidopsis Epigenetic regulation of flowering in rose Genomics and epigenomics in apple Transposable element biology WHY CARE ABOUT TRANSPOSONS? What are transposable elements (TEs or jumping genes)? - TEs are mobile repetitive sequences in the genome - All organisms have TEs Why are TEs important? - TEs drive evolution - epigenetic regulation - crop domestication - regulate stress response CROP TRAITS INFLUENCED BY TRANSPOSONS What is the relation between stress and TEs? Vezzulli, S. et al. J Exp Bot 63 Butelli, E. et al. Plant Cell 24 Walker, A.R. et al. Plant J 49 SILENCING OF TRANSPOSABLE ELEMENTS TE bursts are repressed by silencing silencing TE burst TE chromosome centromere TRANSPOSONS AND EPIGENETICS MuLE Dfr-B MuLE Dfr-B IAP Agouti Slotkin RK & Martienssen R Nat Rev Genet 2007, 8:272–285. Cubas P et al. Nature 1999, 401:157–161. TRANSPOSONS ARE EFFICIENTLY SILENCED Matzke, M.A., and Mosher, R.A. (2014). Nat Rev Genet 15, 394–408. STRESS AND EPIGENETICS Does stress induce stable heritable epigenetic changes in plants? STRESS AND EPIGENETICS So far there is no true stress-induced epi-mutation Holeski et al. (2012) TRANSIENT ACTIVATION OF ENDOGENOUS REPEATS MULE- F19G14 18S rRNA 106B 5S-210 180 bp 18S rRNA RT minus Tittel-Elmer (PLOS Gen 2010) TRANSCRIPTOME AFTER HEAT STRESS Chr 1 Chr 2 Chr 3 Chr 4 Chr 5 ITS ITS+2d ATCOPIA78 Tittel-Elmer (PLOS Gen 2010) SILENCING BY RNA POL IV ATCOPIA78 Ito H et al. Nature 2011, 472:115–119. RETROTRANSPOSON LIFE CYCLE DNA LTR polyprotein LTR DNA Pol II LTR polyprotein LTR RNA RT ACCUMULATION OF EXTRACHROMOSOMAL DNA copy number copy ATCOPIA78 ATCOPIA78 Ito H et al. Nature 2011, 472:115–119. N E W A T C O P I A 7 8 INSERTIONS IN THE MUTANT LINE Ito H et al. Nature 2011, 472:115–119. ONSEN : JAPANESE FOR HOT SPRING ONSEN REGULATES HEAT STRESS RESPONSE LTR poOlyNpSroENtein LTR host gene Ito H et al. Nature 2011, 472:115–119. POL IV AND POL V LIMIT TE MOBILITY Ito H et al. Nature 2011, 472:115–119. TE SILENCING MECHANISMS: POL II? Matzke, M.A., and Mosher, R.A. (2014). Nat Rev Genet 15, 394–408. POL II REPRESSES THE ACTIVATION OF ONSEN A= a-amanitin (Pol II inhibitor) Z= zebularine (DNA methylation inhibitor) Amanita phalloides death cap Thieme, M. et al Genome Biol; 2017;18: 134. INHIBITION OF POL II REDUCES DNA METHYLATION IN PLANTS Thieme, M. et al Genome Biol; 2017;18: 134. MOBILIZATION OF ONSEN I N W I L D - TYPE ARABIDOPSIS PLANTS HS control HS+A+Z Thieme, M. et al Genome Biol; 2017;18: 134. N E W ONSEN INSERTIONS ARE STABLE 90 80 F1 F2 F3 70 60 copy number copy 50 40 ONSEN 30 20 10 0 a b c I II III IV V VI VII control lines treated lines Thieme, M. et al Genome Biol; 2017;18: 134. INDUCED PHENOTYPIC DIVERSITY wild-type ONSEN high-copy lines a b c I II III IV V VII Thieme, M. et al Genome Biol; 2017;18: 134. INDUCED PHENOTYPIC DIVERSITY (SD) Thieme, M. et al Genome Biol; 2017;18: 134. TE MOBILIZATION IN RICE irri.org WT control A Z A&Z A Z A+Z confirmation by PCR Houba whole genome sequencing of circular DNA Thieme, M. et al Genome Biol; 2017;18: 134. B U N G E E : BREEDING USING JUMPING GENES stress TE gene active gene stress BUNGEE and controlled TE burst selection step 1 step 2 The stress defines which set of TEs will be activated ONSEN - MEDIATED HEAT - S T R E S S TOLERANCE? control ONSEN high copy lines We can use TEs for plant breeding it is fast, directed and stable CONCLUSIONS AND A QUESTION RNA Pol II plays an important role in TE defense ONSEN mobility results in phenotypic diversity We can use TEs to breed stress tolerance in crops! Evolutionary question: How important is adaptive evolution? WHY TRANSPOSONS COULD BE A GREAT TOOL TO MONITOR RADIATION TEs are definitely heritable! They react to virtually all stresses Easy to identify active TEs One can date the age of TE insertions PLANT EPI/GENETICS MEETING save the date: 29-31st October 2018 Invited Speakers: Isabel Bäuerle, Claude Becker, Tetsuji Kakutani, Marie Mirouze, Olivier Panaud, Bob Schmitz, Nathan Springer, Clémentine Vitte, Jian-Kang Zhu https://symposium.inra.fr/plantepigenetics2018 ACKNOWLEDGEMENTS Michael Thieme Nicolas Daccord Sandrine Balzergue Sophie Lanciano Marie Mirouze MOBILOME SEQUENCING developed by Marie Mirouze Lanciano S, et al. PLoS Genet. 2017;13 POL II ACTS UPSTREAM OF DCL2/3/4 Thieme, M. et al Genome Biol; 2017;18: 134. CURRENT CHALLENGES IN CROP BREEDING Climate change stress objective temperature rapid breeding of drought stress-tolerant crops salt Current breeding tools Classic genetic crosses slow GMOs no public acceptance Transposable elements fast, directed, not GMO POL II PLAYS A ROLE IN DNA METHYLATION AND TE SILENCING release of a TE transcript in nrpb2 Pol II AGO4 Zheng, B et al Genes Dev 23, 2850–2860..