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When the genome lowers its epigenetic : 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 Genet 2007, 8:272–285. Cubas P et al. Nature 1999, 401:157–161. TRANSPOSONS ARE EFFICIENTLY SILENCED

Matzke, .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 L A M O S O M O R H C A R T X E F O N O I T A L U M DNA U C C A

ATCOPIA78 copy number 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.