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Galla, Giulio (2009) Sexuality deviation in plants, a multilevel approach to study apomixis. [Tesi di dottorato]

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Abstract (inglese)

Plant life cycle is determined through the alternation of a sphorophytic (2n) and gametophytic (n) generations, the latter being constituted by the pollen grain and the embryo sac. Sexuality in plants, exemplified by the generation and fusion of gametes, represents the challenge of potentially new genotype formation by combining previous genome sets. By contrast to sexualtiy, apomixis defines a number of strategies leading to the production of seed without fertilization. Within angiosperms, both monocotyledons and dicotyledons plants are known to reproduce asexually by seeds, i.e. apomixis. Among the species used as a model for reproduction studies, Hypericum spp. and Boechera spp. are undoubtedly two of the most important ones. Moreover, the occurrence of mutants producing apomeiotic megaspores in wild populations have been reported in different sexual species. Besides the general definition of apomixis, two main models have been defined to explain the asexual behaviour on the basis on the functional characteristics of the final product of the illegitimate process. More in detail, gametophytic and sporophytic apomixis define reproductive strategies leading to the formation of a functional megagametophyte, as in Boechera spp. and Hypericum spp., or to a newly generated sporophyte, as in Citrus spp. and Malus spp. Focusing on the former category, the two aposporic and diplosporic models have been reported as actively present within the genera Hypericum and Boechera, respectively. A candidate gene for apomeiosis, named Mob1- like, was recently identified in a Medicago spp. mutant where non-conventional
production of 2n egg cells takes place. A computational approach was attempted to clarify the Mob1 multigene family structure and its member composition. Results suggested that an expansion of this family occurred concomitant to the evolution from unicellular to multicellular organisms. Moreover, in order to study the reproductive implications of the Mob1-like gene, its functional characterization was carried out by post-transcriptional gene silencing using the model species Arabidopsis as biological system. Morphological and cyto-histological analyses mainly were focused on the reproductive process and, besides an alteration of the plant architecture, partial plant sterility was documented in the transgenic lines. Moreover, detailed inspections of ovule development led to the identification of multiple alterations of the mega-sporogenesis and gametogenesis pathways responsible for the formation of unreduced megaspores and altered megagametophytes. Concerning the aposporous type of apomixis, recently gained information has shown that H. perforatum is an attractive model system for the study of the asexual process. A multidisciplinary approach was attempted to shed light on the molecular and cytological bases of apomixis in Hypericum spp. The embryo sac formation and the seed genetic constitution were studied by means of stain-clearing supported by DIC microscopy of ovules/ovaries and FCSS analyses of embryos/endosperm, respectively. Our detailed analyses of female sporogenesis and gametogenesis enabled to define the major morphological features of all elements playing a role in the formation of aposporic initials and embryo sacs. FCSS analysis provided a powerful tool to study the complex reproductive scenarios involving reduced and unreduced male and female gametes. Furthermore, the genome organization of H. perforatum along with H. maculatum and H. attenuatum was investigated by means of different genetic approaches. The hypothesis that H. perforatum arose from an ancient interspecific hybridization event between the diploids H. attenuatum and H. maculatum was tested by the isolation of codominant SNP markers and their investigation in H. perforatum and its putative ancestors. Moreover, a new technology of DNA fingerprint has been tested and applied for the construction of the first linkage maps in Hypericum perforatum. Finally, the temporal expression of two Apostart genes, potentially involved in the apomictic reproductive machinery, were investigated by Real-Time PCR, providing new insights on the genetic control of apomixis in H. perforatum.

Abstract (italiano)

Il ciclo vitale nelle piante è determinato dall’alternanza della generazione sporofitica e gametofitica, quest’ultima costituita dal granulo pollinico e dal sacco embrionale. La sessualità nelle piante, riassumibile con la generazione dei gameti e la loro fusione, dà la possibilità di originare nuovi genotipi nelle progenie, derivanti dalla ricombinazione dei geni durante la meiosi nei genotipi parentali e dalla loro combinazione attraverso la fecondazione. Al contrario, tra le angiosperme, diverse specie sia monocotiledoni che dicotiledoni sono caratterizzate da riproduzione apomittica, ovvero da formazione di seme geneticamente materno prodotto in maniera agamica, in assenza di meiosi e di fecondazione. Tra le specie utilizzate come modello per lo studio dell’apomissia, Hypericum spp. e Boechera spp. sono sicuramente due tra quelle più importanti. Inoltre, mutanti caratterizzati dalla produzione di megaspore apomeiotiche sono stati scoperti e descritti in popolazioni naturali di numerose specie sessuali. All’interno della definizione generale di apomissia, due principali modelli sono stati definiti per spiegare l’origine materna delle progenie in conformità alle caratteristiche genetiche e funzionali del prodotto finale del processo agamico. Più in dettaglio, le due tipologie di apomissia gametofitica e sporofitica definiscono due strategie riproduttive alternative che portano rispettivamente alla formazione di un gametofito apomeiotico, come nel caso di Boechera spp. e Hypericum spp., o alla generazione di un sporofito avventizio, come in Citrus spp. Concentrandosi sulla prima categoria, i due possibili modelli aposporico e diplosporico sono attivi, rispettivamente, nei due generi Hypericum e Boechera. Recentemente è stato ipotizzato il coinvolgimento del gene Mob1-simile nella progressione alterata della meiosi in un mutante apomeiotico di erba medica produttore di ovocellule non ridotte. Una dettagliata analisi bioinformatica, realizzata studiando 192 sequenze dedotte dai 43 genomi attualmente sequenziati, ha consentito di delucidare la struttura della famiglia multigenica di cui fa parte questo gene e di indagare l’evoluzione della famiglia passando da organismi unicellulari ad organismi pluricellulari. Lo studio delle possibili funzioni del gene in relazione al processo riproduttivo è stato realizzato nella pianta modello Arabidopsis thaliana, attraverso il silenziamento post-trascrizionale del gene mediante RNAi. Le analisi morfologiche e cito-istologiche condotte nelle linee transgeniche hanno evidenziato alterazioni nell’architettura della pianta e soprattutto una parziale sterilità, come dimostrato dalla forte riduzione della produzione di seme. Osservazioni citologiche condotte negli ovuli hanno messo in evidenza alterazioni multiple a carico dei processi di sporogenesi e gametogenesi femminile responsabili, rispettivamente, della formazione di megaspore binucleate e della degenerazione di megagametofiti. L’identificazione di piante poliploidi nelle progenie delle piante silenziate per il gene Mob1-simile suggerisce l’esistenza di meccanismi apomeiotici responsabili della produzione di ovocellule non ridotte funzionali. Informazioni recentemente acquisite hanno dimostrato che H. perforatum può essere considerato un sistema adatto allo studio del modello aposporico dell’apomissia. Un approccio multidisciplinare è stato perseguito nel tentativo di chiarire le basi genetico molecolari e citologiche dell’apomissia in Hypericum spp. La formazione del sacco embrionale e la costituzione genetica del seme sono stati analizzati, rispettivamente, per mezzo di indagini citologiche di ovuli ed ovari in combinazioni con analisi DIC e attraverso analisi di citometria di flusso di semi (FCSS). Una indagine dettagliata della sporogenesi e della gametogenesi femminile ha permesso di definire le principali caratteristiche morfologiche delle strutture che svolgono un ruolo chiave nella formazione del sacco embrionale. Al contempo le analisi FCSS, attraverso la stima del contenuto di DNA nucleare di embrione ed endosperma, hanno fornito un potente strumento per lo studio del complesso scenario di riproduzione che si origina in Hypericum attraverso la concomitante produzione di gameti maschili e femminili sia ridotti che non ridotti. Inoltre, l’organizzazione del genoma di H. perforatum, con H. maculatum e H. attenuatum è stata studiata per mezzo di diversi approcci genetico-molecolari. L’ipotesi che H. perforatum possa essersi originato da un antico evento di ibridazione interspecifica tra la specie diploidi H. attenuatum e H. maculatum è stato valutato attraverso l’isolamento di marcatori molecolari co-dominanti di tipo SNP e la loro applicazione in H. perforatum e nei putativi progenitori. Inoltre, una nuova tecnologia di marcatori molecolari è stata messa a punto per l’amplificazione selettiva di membri di famiglie multigeniche ed in seguito applicata per la costruzione di mappe genetico-molecolari funzionali di H. perforatum. Infine, l’espressione temporale di due geni della famiglia genica APOSTART, ritenuti potenzialmente coinvolti nella regolazione dell’apomissia, è stata studiata mediante Real-Time PCR al fine di chiarire il loro ruolo sul controllo genetico dell’apomissia in H. perforatum.

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Tipo di EPrint:Tesi di dottorato
Relatore:Barcaccia, Galla
Dottorato (corsi e scuole):Ciclo 21 > Scuole per il 21simo ciclo > SCIENZE DELLE PRODUZIONI VEGETALI > AGROBIOTECNOLOGIE
Data di deposito della tesi:31 Gennaio 2009
Anno di Pubblicazione:02 Febbraio 2009
Parole chiave (italiano / inglese):Megasporogenesis, Megagametogenesis, apomeiosis, apospory,
Settori scientifico-disciplinari MIUR:Area 07 - Scienze agrarie e veterinarie > AGR/07 Genetica agraria
Struttura di riferimento:Dipartimenti > Dipartimento di Agronomia Ambientale e Produzioni Vegetali
Codice ID:1844
Depositato il:31 Gen 2009
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