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Zaffalon, Valerio (2014) Dissecting the transcriptional regulatory network of seed and mesocarp development in peach. [Ph.D. thesis]

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Abstract (english)

Peach (Prunus persica) is one of the most important fleshy fruit crops worldwide and model species for drupe plant species. Peach fruit development is characterized by a tight relationship between seed and pericarp during the early stages, followed in later stages by an uncoupling in the pattern of development due to the lignification of the endocarp. Diverse peach cultivars may have fruit developmental periods of very different length, while having a similar development for the seed. Understanding the relationship between seed and pericarp sheds light onto the mechanism regulating fruit development. Transcriptomic approach is a powerful tool to investigate this relationship, as it gives broad information on the transcription of a large amount of genes in a single experiment.

Chapter II is a published article regarding the use of the µPEACH1.0 array for the understanding of the relationships between seed and mesocarp and between early and late stages of development in the cultivar Fantasia. Peach mRNA samples were taken from early and late developmental stages of the two organs and then hybridized on the 4 806 probes of the µPEACH1.0 array. The transcriptomic data obtained from these samples were then cross-compared.
Marker genes for the four peach developmental stages (S1 stage: fruit cells division and enlargement, S2: lignification of the endocarp, S3: mesocarp cell expansion, S4: ripening) were found for both mesocarp and seed and their expression confirmed by qRT-PCR. Stage- specific markers found for the mesocarp were a RD22-like protein, a serin- carboxypeptidase, a senescence-related protein and an Aux/IAA, for S1, S2, S3 and S4 stages, respectively, while seed markers were a lipid transfer protein(LTP1), a pathogenesis-related (PR) protein, a prunin and Late Embryogenesis Abundant (LEA) protein, for S1, S2, S3 and S4 stages, respectively. By qRT-PCR it was confirmed that these genes act as markers also in an early cultivar (SpringCrest) and a slow ripening genotype (slr).
Then, the data were analyzed with the HORMONOMETER tool in order to indirectly measure the relative amounts of hormones in the different organs and developmental stages. It was found that auxins, cytokinins, and gibberellins may be involved in signaling during the early development, when there is cross-talk between the two organs.

Chapter III is an unpublished article in which it is described how a new microarray platform, µPEACH3.0, was employed to study peach mesocarp and seed development. The recent publication of the peach genome allowed the development of a whole-genome microarray which overcame the problem of having an array assessing gene expression of only one part of the genome. In respect of the study described in Chapter II, also the number of samples were increased: three biological replicates for each of six time-points for each of the two organs were used, giving a larger overview on the development of these two tissues.
The whole genome microarray, µPEACH3.0, performed well, with a correlation with qRT-PCR data of 0.77, a number similar to that found for other arrays. The transcriptomic data easily distinguished the two tissues and the six time-points, as shown by principal component analysis. 69% of the probes gave a significant signal from at least one of the samples. Anyway, considering that the number of functioning probes diminishes if only the samples of one tissue are taken into account, it is probable that testing the microarray with mRNA coming from other tissues (such as leaves or roots) will increase the number of significant signals coming from the array.
Global analysis of gene activity was focused into the early stages of development. Data allowed us to identify several genes involved in cell cycle processes that occur at the onset of both mesocarp and seed development. In particular genes of the TITAN family were found to be active in the endosperm containing seed. The analysis of the cell cycle genes in the mesocarp showed the existence of two different patterns of expression: while mitosis related genes were expressed only in stage S1, DNA replication genes showed a double peak of expression, in S1 and then in S3/S4, suggesting that events of endoreduplication may occur in these late stages. By qRT-PCR the expression levels of these genes were tested also in other cultivars, the data obtained suggest that the lack of endoreduplication may be involved in the slow rate of growth in S3 stage of the slr genotype.
The patterns of expression of transcription factors (TFs) families were then assessed, as transcription factors are thought to be the proteins with the most important regulatory roles during development. It was found that TFs of the SQUAMOSA promoter Binding Protein (SBP) family have an high expression level at the beginning of the development of both the organs considered, which then quickly decreases. The transcription of Growth Regulating Factors (GRFs) has been discovered to be induced in the mature seed. The data were confirmed by qRT-PCR also in an ‘SpringCrest’ and the slow ripening genotype slr.
Given that the mRNA abundance of genes belonging to these TFs families is regulated by specific microRNAs (miRNAs) in other plant species, the expression of the peach homologues of these miRNAs was measured. In three different cultivars a negative correlation in the RNA abundance was found for the following miRNA/target TF couples: miR156/SBP, miR396/GRF and mir167/ARF8, suggesting not only that these miRNAs have the same activity also in peach, but also that miRNAs are deeply involved in the regulatory network underlying the peach fruit development.

Appendix is a published study in which µPEACH3.0 is used to study the effects of wounding in two peach cultivars with different tolerance to this stress. RNA samples from wounded and unwounded mesocarps of melting cultivar Glohaven (GH) and slow melting cultivar BigTop (BT) were used. Transcriptomic data, confirmed by qRT-PCR analysis, showed the involvement of WRKY, AP2/ERF and HSP20 transcription factors in the GH response to wounding. Along with them, also genes involved in response to stresses, cell wall metabolism, phenilpropanoid and triterpenoid biosynthesis were found to be up regulated in the wounded GH mesocarp.

Abstract (italian)

Il pesco (Prunus persica) è uno dei più importanti alberi da frutto al mondo e la specie modello per le drupacee. Lo sviluppo del frutto di pesco è caratterizzato da un stretto rapporto tra il seme e il pericarpo durante i primi stadi, seguito negli stadi successivi da un disaccoppiamento nello schema di sviluppo dovuto alla lignificazione dell’endocarpo. Le varie cultivar di pesco possono avere dei periodi di sviluppo del frutto dalla lunghezza estremamente variabile, pur avendo un seme che si sviluppa in maniera simile. Per questo, comprendere la relazione tra seme e pericarpo può chiarire il meccanismo che regola lo sviluppo del frutto nel suo complesso. L’approccio transcrittomico è uno strumento potente per analizzare questa relazione, dato che produce un gran numero di informazioni sulla trascrizione di un gran quantitativo di geni in un singolo esperimento.

Il Capitolo II consiste in un articolo pubblicato che descrive l’uso dell’array µPEACH1.0 nello studiare la relazione tra seme e mesocarpo e tra stadi iniziali e finali di sviluppo nella cultivar Fantasia. Campioni di mRNA di pesco sono stati raccolti dagli stadi iniziali e finali dei due organi e ibridizzati sulle 4 806 sonde dell’array µPEACH1.0. I dati trascrittomici ottenuti da questi campioni sono stati quindi confrontati.
Sono stati trovati dei geni marcatori per i quattro stadi di sviluppo del pesco (Stadio S1: divisione ed espansione cellulare nel frutto, S2: lignificazione dell’endocarpo, S3: espansione cellulare nel mesocarpo, S4: maturazione) sia per il mesocarpo che per il seme e la loro espressione confermata con la qRT-PCR: I marcatori stadio-specifici per il mesocarpo sono rispettivamente per S1, S2, S3 e S4: una proteina RD22-like, una serin-carbossipeptidasi, una proteina correlata alla senescenza e una Aux/IAA; mentre per il seme sono, rispettivamente: una proteina trasportatrice di lipidi (LTP1), una proteina correlata alla patogenesi (PR), una prunina e una proteina LATE EMBRYOGENESIS ABUNDANT (LEA). La qRT-PCR ha confermato che questi geni sono marcatori anche in una cultivar precoce (SpringCrest) e in un genotipo a maturazione lenta (slr).
Quindi i dati sono stati analizzati con lo strumento HORMONOMETER al fine di misurare indirettamente il quantitativo relativo di ormoni nei vari organi e stadi di sviluppo. E’ emerso che l’auxina, le citochinine e le gibberelline possono essere coinvolte nella segnalazione durante l’inizio dello sviluppo, quando vi è comunicazione tra i due organi.

Il Capitolo III è un articolo non pubblicato nel quale viene descritto come venga utilizzata una nuova piattaforma microarray (µPEACH3.0) nello studiare lo sviluppo del seme e del mesocarpo di pesco. La recente pubblicazione del genoma di pesco ha permesso lo sviluppo di un microarray che copre l’intero genoma, superando così il problema di avere un array che misura l’espressione genica solo di una parte del genoma. Rispetto allo studio descritto nel Capitolo I, anche il numero di campioni è stato incrementato: sono state usate tre repliche biologiche per sei diversi momenti per ciascuno dei due organi, dando così una visuale più vasta sullo sviluppo di questi due tessuti.
L’array µPEACH3.0 ha funzionato bene, dando una correlazione con i dati di qRT-PCR pari a 0.77, un numero simile a quello trovato per altri array. I dati trascrittomici hanno facilmente distinto i due tessuti e i sei campionamenti, come mostrato dall’analisi delle componenti principali. Il 69% delle sonde ha prodotto un segnale significativo in almeno uno dei campioni, ciò nonostante, considerando che il numero di sonde funzionanti decresce se si prende in considerazione un solo tessuto, è probabile che testando il microarray con mRNA proveniente da altri tessuti (come le foglie o le radici) aumenti il numero di segnali significativi provenienti dall’array.
L’analisi globale dell’attività genica è stata indirizzata ai primi stadi di sviluppo. I dati hanno permesso di indentificare parecchi geni coinvolti nei processi del ciclo cellulare che si verificano all’inizio dello sviluppo sia del mesocarpo che del seme. In particolare, è stato trovate che geni della famiglia TITAN sono attivi nel seme contenente endosperma. L’analisi dei geni del ciclo cellulare nel mesocarpo ha mostrato l’esistenza di due diversi profili di espressione: mentre i geni relativi alla mitosi erano espressi solo nello stadio S1, i geni della replicazione del DNA hanno mostrato un doppio picco di espressione, in S1 e poi in S3/S4, suggerendo che in questi stadi possono verificarsi eventi di endoreduplicazione. Con l’utilizzo di qRT-PCR, i livelli d’esrpessione di questi geni sono stati testati anche in altre cultivar; i dati ottenuti suggeriscono che nel genotipo slr la mancanza di endoreduplicazione possa essere coinvolta nel basso tasso di crescita durante lo stadio S3 di questo genotipo.
Sono stati quindi valutati i profili d’espressione di famiglie di fattori di trascrizione (FT), dato che si ritiene che i fattori di trascrizione siano le proteine con i ruoli più importanti nella regolazione durante lo sviluppo. E’ stato trovato che FT delle famiglia SQUAMOSA promoter Binding Protein (SBP) hanno un alto livello di espressione all’inizio dello sviluppo di entrambi gli organi considerati, il quale successivamente diminuisce velocemente. E’ stato scoperto che nel seme maturo è indotta la trascrizione di FT di tipo Growth-Regulating Factor (GRF). Questi dati sono stati confermati con l’utilizzo di qRT-PCR in ‘SpringCrest’ precoce e nel genotipo a lenta maturazione slr.
Dato che in altre specie vegetali l’abbondanza dell’mRNA di geni appartenenti a queste famiglie di FT è regolata da microRNA (miRNA) specifici, è stata misurata l’espressione degli omologhi di pesco di questi miRNA. In tre diverse cultivar è stata trovata una correlazione negativa nel contenuto di RNA per le seguenti coppie microRNA/FT: miR156/SBP, miR396/GRF e mir167/ARF8, suggerendo non solo che questi miRNA posseggono la stessa attività un pesco, ma anche che i miRNA sono profondamente coinvolti nella rete regolativa sottostante lo sviluppo del frutto di pesco.

In appendice vi è uno studio pubblicato nel quale viene descritto l’uso di µPEACH3.0 nello studiare gli effetti delle ferite su due cultivar con diversa tolleranza a questo stress. Sono stati utilizzati campioni di RNA estratti da mesocarpi feriti o intatti della cultivar “melting” Glohaven (GH) e della cultivar “slow melting” BigTop (BT). I dati trascrittomici, confermati dall’analisi tramite qRT-PCR, hanno mostrato il coinvolgimento di fattori di trascrizione di tipo WRKY, AP2/ERF, e HSP20 nella risposta di GH alla ferite. Insieme a questi, è stato trovato che nel mesocarpo ferito di GH viene indotta l’espressione anche di geni coinvolti nella risposta agli stress, nel metabolismo della parete cellulare, nella biosintesi dei fenilpropanoidi e triterpenoidi.

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EPrint type:Ph.D. thesis
Tutor:Bonghi, Claudio and Ramina, Angelo
Ph.D. course:Ciclo 25 > Scuole 25 > SCIENZE DELLE PRODUZIONI VEGETALI > AGROBIOTECNOLOGIE
Data di deposito della tesi:29 January 2014
Anno di Pubblicazione:31 January 2014
Key Words:peach microarray fruit seed microrna transcription factors hormones markers transcriptomics pesco frutto seme mirna fattori di trascrizione ormoni marcatori trascrittomica
Settori scientifico-disciplinari MIUR:Area 07 - Scienze agrarie e veterinarie > AGR/03 Arboricoltura generale e coltivazioni arboree
Struttura di riferimento:Dipartimenti > Dipartimento di Agronomia Animali Alimenti Risorse Naturali e Ambiente
Codice ID:6532
Depositato il:31 Oct 2014 13:37
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