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Verna, Michela (2015) An epigenetic approach to study gene regulation in two different grapevine rootstocks: from histone modifications to gene expression. [Ph.D. thesis]

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Summary
In the nineteenth century European viticulture was devastated by the introduction of phylloxera (Daktuloshaira vitifoliae) from North America. Since this moment a new era for viticulture started out based on grafting of a scion of V. vinifera varieties onto rootstocks from the pest’s origin. The introduction of root system from American or non vinifera species was initially focused on the protection of viticulture from the pest but very soon it has been realized that grapevine rootstocks were not only capable to confer disease resistance, but they could imply a large range of advantages by influencing numerous physiological process at the scion level such as response to abiotic stresses. At the light of the climate changes that are affecting the earth, the viticulture, as well as the agriculture, need to develop plants able to cope with situations of long drought period. DiSAA research group of University of Milan establish till 1985 novel candidate grapevine genotypes that could be used as rootstocks with the objective to obtain new hybrids more performant in response to abiotic stress. In a preliminary screening, one of these, called M4 [(V. vinifera x V. berlandieri) x V. berlandieri x cv Resseguier n.1], was selected for its relatively high tolerance to water deficit and salt exposure. Biochemical and physiological studies were performed within Ager-Serres project 2010-2105 for the comparison between rootstock M4 and a commercial one susceptible to drought stress, 101.14 (V. riparia x V. rupestris). Furthermore the project used Next Generation Sequencing (NGS) techniques to investigate the genomes and transcriptome profiles of the two rootstocks grown in drought and in controlled conditions. The aim of this multidisciplinary project was the identification of marker genes for the selection of rootstocks with high performances under water stress conditions. It is within the Ager-Serres project that this PhD research project takes place with the objective to study the relation between transcriptional profile and histone modifications in the rootstocks 101.14 and M4. Our research represent the first study aimed to clarify the relation between histone modifications and gene expression in the genus Vitis. Literature data from other species showed, indeed, that chromatin remodeling, histone modifications and chromatin related processes act on chromatin structure in a dynamic manner for the regulation of gene expression. Nucleosomes are the building block of chromatin that can be defined like a highly condensed structured that form the scaffold of fundamental nuclear processes such as transcription, replication and DNA repair. Nowadays it is clear in fact that the function of chromatin doesn’t end with the packaging and the protection of DNA but it also act controlling gene expression. Cells have evolved mechanisms that alter the structure of chromatin allowing the access of transcriptional complexes.
To reach our objective a pool of plants of each genotype were grown in vitro, leaf materials were collected and gene expression was evaluated with mRNA-Sequencing (mRNA-seq) while distribution of acetylation of lysine 9 of histone three (H3K9ac) and trimethylation of lysine 4 of histone three (H3K4me3) were evaluated through a ChIP-Sequencing (ChIP-seq) approach. Nowadays mRNA-seq has become a routine analysis for the evaluation of transcriptome profile of a large number of plant species while the use of ChIP-seq is still limited to plant model species. During this PhD a lot of work was done for the development of a chromatin immunoprecipitation protocol suitable for the sequencing of chromatin extracted and immunoprecipitated from grapevine.
Literature data for other plant species established that H3K9ac and H3K4me3 histone modifications were positive related to gene expression and that these marks preferentially lied in the transcription starting site (TSS) of the genes but the identification of this feature is still missing in grapevine genome annotation. For this reason we decided to perform the enrichment analyses on immunoprecipitated chromatin keeping, in an arbitrary manner, a window of 1000 bp above the start codon (ATG) of the genes and considering for each gene the number of reads that aligned in this region. The reads upstream of each gene were normalized and the genes were studied in terms of enrichment or depletion respect their sequencing profile without immunoprecipitation. The groups of genes enriched in one genotype and depleted in the other were related to transcriptional profile discovering a positive correlation between histone mark H3K9ac and gene expression. This trend was not confirmed analyzing the mark of H3K4me3. Considering, however, the genes with enrichment in one genotype and depletion in the other for both the histone marks at the same time we discovered a positive correlation with expression profile.
The results of this study are the first evidences of a positive correlation between histone modifications H3K9ac and H3K4me3, when present simultaneously with H3K9ac, and gene expression in grapevine.

Abstract (a different language)

Riassunto
Durante il diciannovesimo secolo la viticoltura europea fu devastata dall’introduzione di un insetto fitofago di origine nord americana la Daktuloshaira vitifoliae nota comunemente con il nome di “Phylloxera della vite”. Da quel momento iniziò una nuova era per la viticoltura con l’utilizzo dell’innesto di varietà di V. vinifera in portinnesti provenienti dalle zone di origine del parassita. L’introduzione di sistemi radicali di specie americane e non vinifera si focalizzò inizialmente sugli aspetti della protezione della viticoltura dall’attacco del parassita. Molto presto, tuttavia, si capì che l’utilizzo del portinnesto non solo conferiva resistenza alla malattia ma implicava anche una serie di vantaggi influenzando numerosi processi fisiologici a livello del nesto, come ad esempio la resistenza agli stress abiotici. Alla luce dei cambiamenti climatici che stanno coinvolgendo il nostro pianeta, la viticoltura, così come l’intera agricoltura, necessita di sviluppare piante in grado di gestire situazioni di siccità prolungata. Il gruppo di ricerca del DiSAA dell’Università di Milano dal 1985 è coinvolto nello studio nuovi genotipi di vite con l’obbiettivo di ottenere nuovi ibridi utilizzabili come portinnesti e maggiormente performanti in situazioni di stress abiotico. In uno screening preliminare, uno di questi, denominato M4 [(V. vinifera x V. berlandieri) x V. berlandieri x cv Resseguier n.1], fu selezionato per la resistenza elevata allo stress idrico e salino. All’interno del progetto Ager-Serres 2010-2105 sono stati eseguiti degli studi biochimici e fisiologici comparando il genotipo sperimentale M4 con un portinnesto commerciale suscettibile allo stress idrico, 101.14 (V. riparia x V. rupestris). Questi dati sono stati integrati ad approcci di Next Generation Sequencing (NGS) volti a studiare i genomi ed i profili trascrizionali dei due portinnesti cresciuti in condizioni di stress idrico e di controllo. L’obiettivo principale del progetto Ager-Serres, risiede nell’identificazione di geni marcatori che possano essere utilizzati per la selezione di nuovi portinnesti con maggiori performance in situazioni di stress idrico.
Questo progetto di dottorato si inserisce all’interno del progetto Ager-Serres ed è volto a studiare la relazione tra profili trascrizionali e modifiche istoniche nei portinnesti 101.14 e M4. Dati di letteratura relativi ad altre specie hanno dimostrato infatti che il rimodellamento della cromatina, le modifiche istoniche ed i processi correlati alla cromatina, agiscono in maniera dinamica sulla struttura della cromatina stessa per la regolazione dell’espressione genica. I nucleosomi sono le unità fondamentali della cromatina che può essere definita come una struttura altamente condensata che costituisce la base per processi nucleari fondamentali come trascrizione, replicazione e riparazione del DNA. Oggigiorno è chiaro appunto che la funzione della cromatina non si esaurisce nell’impacchettamento del DNA e nella sua protezione ma risiede anche nel controllo dell’espressione genica. Gli organismi hanno infatti evoluto dei meccanismi atti a alterare la struttura della cromatina consentendo l’accesso o l’esclusione di complessi trascrizionali.
Per condurre questa ricerca, un gruppo di piante di ciascun genotipo (101.14 e M4) è stato fatto crescere in vitro. Il materiale fogliare è stato campionato e l’espressione genica studiata attraverso un mRNA-Sequencing (mRNA-seq). La distribuzione di modifiche istoniche, come l’acetilazione della lisina 9 dell’istone H3 (H3K9ac) e la trimetilazione della lisina 4 dello stesso istone (H3K4me3), sono state valutate attraverso un approccio di ChIP-Sequencing (ChIP-seq). Questa ricerca rappresenta il primo studio di questo tipo condotto nel genere Vitis.
Oggigiorno i sequenziamenti di mRNA sono divenuti analisi di routine per la valutazione dei profili trascrizionali in un gran numero di specie vegetali mentre l’utilizzo di approcci di ChIP-seq rimane limitato alle piante modello. Durante questo progetto di dottorato molto lavoro è stato investito nello sviluppo di un protocollo di immunoprecipitazione che fosse performante per l’estrazione ed il sequenziamento della cromatina di materiale fogliare di piante di vite.
Dati di letteratura riguardanti altre specie vegetali hanno individuato una correlazione positiva tra le modifiche istoniche H3K9ac ed H3K4me3 e l’espressione genica. Si è inoltre stabilito che questi marchi giacciono preferenzialmente nella regione del sito di inizio della trascrizione (TSS) dei geni ma l’identificazione di questi siti è ancora mancante nell’annotazione del genoma di vite. Per questo motivo si è deciso di effettuare analisi di arricchimento sulla cromatina immunoprecipitata scegliendo in maniera arbitraria un intervallo di 1000 paia di basi a monte del codone d’inizio (ATG) dei geni e considerando, per ogni gene, il numero di reads che allineano in questo intervallo. Le reads mappanti nella regione considerata sono state normalizzate ed i geni studiati in termini di arricchimento o deplezione della modifica rispetto alla cromatina non immunoprecipitata. I gruppi di geni arricchiti in un genotipo e depleti nell’altro, sono stati posti in relazione con i profili trascrizionali individuando così una correlazione positiva tra la modifica istonica H3K9ac e l’espressione genica. Questo andamento non è stato riscontrato analizzando la trimetilazione della lisina 4 dell’istone H3. Considerando, tuttavia, i geni che presentano un arricchimento in un genotipo e una deplezione nell’altro, contemporaneamente per entrambi i marchi istonici, è stata identificata una correlazione positiva con i profili trascrizionali.
I risultati di questo studio sono le prime evidenze di una correlazione positiva tra modifiche istoniche H3K9ac e H3K4me3, quando presente contemporaneamente ad H3K9ac ed espressione genica in vite.

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EPrint type:Ph.D. thesis
Tutor:Lucchin, Margherita
Ph.D. course:Ciclo 27 > scuole 27 > SCIENZE DELLE PRODUZIONI VEGETALI
Data di deposito della tesi:22 January 2015
Anno di Pubblicazione:21 January 2015
Key Words:Histone modifications; gene expression; ChIP-seq; mRNA-seq; Chromatin immunoprecipitation; grapevine rootstock
Settori scientifico-disciplinari MIUR:Area 07 - Scienze agrarie e veterinarie > AGR/07 Genetica agraria
Struttura di riferimento:Dipartimenti > Dipartimento di Agronomia Animali Alimenti Risorse Naturali e Ambiente
Codice ID:7517
Depositato il:10 Nov 2015 12:17
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