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Cappelletti, Valentina (2016) Global analysis of the genetic and epigenetic contributions to phenotypic plasticity in a wild yeast strain. [Ph.D. thesis]

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Abstract (english)

The natural M28 Saccharomyces cerevisiae strain, isolated from damaged grapes in Montalcino area (Tuscany), showed a fascinating 2:2 segregation of two unlinked loci: the recessive resistance to a toxic analogue of leucine (5’5’5 trifloroleucine, TFL) and the morphotype. Two of the four M28 meiotic products (spores) in fact grow as smooth colonies while the other two exhibit complex structured filigreed colonies. In this work, preliminary phenotypic investigations demonstrated the uniqueness of the M28 system since the four meiotic products displayed a remarkable phenotypic variability concerning the ability to generate pseudohyphal structures or to invade solid substrates. Additionally, we showed that each spore is able to spontaneously and reversibly switch between the two described morphotypes at high frequencies. Seduced by this puzzling system where Mendelian and Lamarckian theories seems to be reconciled we started a global investigation of the genetic, proteomic and chromatin profiles across the four spores. Using cutting-edge mass spectrometry and sequencing technologies we obtained the following results:

i) we confirmed the genetic determinant of the TFL-phenotype additionally illustrating how this loss of function can massively reshape the amino acid metabolism through the alteration of chromatin accessibility via histone modifications (trimethylation of lysine 4 of histone H3 and acetylation of histone H4);

ii) we demonstrated there are no genetic polymorphisms segregating with the morphotype but rather we identified few epialleles segregating 2:2 with the morphotype;

iii) for the first time we showed the extensive epigenome variability among four meiotic products of a natural S. cerevisiae strain;

iv) we found structural protein rearrangements in several prion-like proteins during the dimorphic transition from filigreed to smooth and vice-versa and showed that for Hrp1 protein this switch is accompanied by a significant change in the number of cells per population bearing the Hrp1p-aggregate.

These results evidenced that both genetic and epigenetic contributions are affecting the phenotypic plasticity in the M28 system proposing an update of the “genome renewal” theory that introduces chromatin reshaping as a rapid adaptive mechanism allowing the appearance of new stable and potentially advantageous traits in the progeny of diploid strains.

Abstract (italian)

M28 è un ceppo naturale di Saccharomyces cerevisiae, isolato da vitigni di Montalcino (Toscana), che mostra una affascinante segregazione 2:2 di due tratti non collegati tra loro: la resistenza recessiva ad un analogo tossico della leucina (5’5’5 trifloroleucina, TFL) ed il morfotipo di colonia. Due dei quattro prodotti meiotici (spore) di M28, infatti, crescono generando colonie lisce mentre gli altri due generano complesse strutture filamentose. Analisi preliminari a questo lavoro di tesi hanno dimostrato l’unicità di questo sistema data dall’osservazione che i quattro prodotti meiotici di M28 mostrano una elevata variabilità fenotipica riguardo l’abilità di differenziare in strutture pseudo-ifali nonché la capacità di invadere substrati solidi. Abbiamo successivamente dimostrato che ogni spora è capace di passare da un fenotipo di colonia liscio ad un rugoso, e viceversa, in un processo spontaneo e reversibile che avviene ad alte frequenze. Sedotti da questo intrigante sistema dove le teorie Lamarckiane e Darwiniane sembrano riconciliarsi abbiamo iniziato una investigazione globale volta ad investigare il genoma, il proteoma e la struttura cromatinica di tutti e quattro i prodotti meiotici di una tetrade di M28. Abbiamo così utilizzato tecnologie all’avanguardia sia nel campo della spettrometria di massa che del sequenziamento di ultima generazione, ottenendo i seguenti risultati:

i) abbiamo confermato il determinante genetico della resistenza alla TFL mostrando inoltre come una mutazione associata alla perdita di funzione di un gene possa interferire sul metabolismo cellulare, degli amino acidi in questo caso, alterando l’accessibilità della cromatina attraverso modifiche istoniche quali la bi- e tri-metilazione della lisina 4 dell’istone H3 o l’acetilazione dell’istone H4;

ii) abbiamo dimostrato che non vi sono polimorfismi che segregano con il tratto “morfologia di colonia” ma piuttosto abbiamo identificato alcuni epi-alleli che segregrano 2:2 con il morfotipo e che potrebbero essere quindi responsabili della segregazione osservata;

iii) abbiamo mostrato per la prima volta l’elevata variabilità a livello dell’epigenoma di quattro prodotti meiotici di un ceppo naturale di S. cerevisiae;

iv) abbiamo identificato riarrangiamenti proteici strutturali, a carico di alcune proteine associabili ai prioni, durante la transizione da morfotipo di colonia filamentoso a liscio (e viceversa) mostrando che la proteina Hrp1 genera aggregati proteici a localizzazione nucleare il cui numero cambia statisticamente durante la transizione dimorfica.

In conclusione i risultati di questo lavoro evidenziano come meccanismi di tipo genetico ed epigenetico possano regolare la plasticità fenotipica in M28 portandoci ad ipotizzare un aggiornamento della teoria del “rinnovamento del genoma” che introduca le variazioni della struttura cromatinica come un meccanismo di adattamento evolutivo che permette l’insorgere di nuovi tratti, potenzialmente vantaggiosi, nella progenie di ceppi di lievito diplodi.

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EPrint type:Ph.D. thesis
Tutor:Romualdi, Chiara
Supervisor:Csikász-Nagy, Attila
Ph.D. course:Ciclo 28 > Scuole 28 > BIOSCIENZE E BIOTECNOLOGIE > GENETICA E BIOLOGIA MOLECOLARE DELLO SVILUPPO
Data di deposito della tesi:01 August 2016
Anno di Pubblicazione:01 August 2016
Key Words:Genetica Epigenetica Cromatina S.cerevisiae Multicellularità / Genetics Epigenetics Chromatin Yeast Multicellularity
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/18 Genetica
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:9725
Depositato il:03 Nov 2017 09:44
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