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Zanella, Filippo Giacomo (2018) Plant growth promotion and biocontrol traits of Vitis vinifera "Glera" bacterial endophytes in the sustainable management of viticulture. [Ph.D. thesis]

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Abstract (english)

This thesis describes the results obtained during the three years PhD course which was focused on plant-bacteria interactions, in particular Vitis vinifera cultivar Glera and endophytes, previously isolated from the same plant species.
The project aimed to investigate the possible beneficial effects that four selected endophyte strains, belonging to Pantoea and Bacillus genera, can give to Glera rooting cuttings and their potential utility as environmental-friendly alternative approach in plant growth promotion, stress alleviation, and biocontrol. The project was prompted to reduce the extensive use of agro-chemicals in agriculture and to promote a sustainable management of viticulture.
As a first step, P. agglomerans (GL83) and B. licheniformis (GL174) selected for their valuable plant growth promoting traits were GFP-tagged and used to inoculate in vitro Glera apical cuttings in order to confirm their endophytic nature. Exploiting laser scanning confocal microscopy and a cultivation dependent method the colonization of stem endosphere of Glera apical cuttings after 20 and 30 days post inoculation (dpi) was demonstrated. The analysis was then extended at 45, 52 and 60 dpi in Glera cuttings which were in the meantime transferred in hydroponic non-sterile medium. Both strains were mostly visualized inside the xylem vessels of the stem until 60 dpi confirming the strains endophytic attitude and persistence. Then, the four strains were directly applied in the field by inoculating rootstocks (Kober 5BB) and Glera buds with each bacteria suspension (GL83, GL174, GL189, GL452 and the consortium of these four) both during the hydration step of rooting cuttings production line and by administering the bacterial suspensions at the root level, after plants have developed roots. Then, both the morphological and physiological plant parameters were recorded sampling plants at different time-point of their development.
GL83 and GL174 were the most promising grapevine bio-fertilizer strains, especially when rootstocks and buds were inoculated during the hydration step of rooting cuttings production line. Inoculated plants presented improved leaf physiological parameters such as photosynthesis rate and transpiration flux linked to an increase of root and shoot fresh biomasses compared to the control plants. Moreover, an experiment aimed to simulate a fertilization procedure using 1-year-old Glera grapevine plants, which were bio-fertilized once a week for seven consecutive weeks with GL83 and GL174 confirmed these strains as promising bio-fertilizer candidates. Furthermore, GL83 was able to relieve the effects of drought stress in inoculated Glera rooting cuttings. In fact, stressed-inoculated plants presented enhanced physiological parameters compared to stressed-control plants and, in addition, GL83 plant growth promoting traits seemed to be water stress dependent.
Another issue investigated during these three PhD years was the role of Bacillus cyclic lipopeptides (LPs) families as elicitors of plant defence responses, through induced systemic resistance (ISR) pathway.
LPs are amphiphilic compounds produced by some beneficial bacterial strains freely living in the soil or undergoing mutualistic interactions with plants. The natural functions of LPs suggest their role in antagonism toward other microorganisms, like plant pathogens, and their involvement in motility and attachment to surfaces encouraging bacteria biofilm formation and development.
So far, the mechanisms underlying the induced physiological responses in host plants, upon the exposure to these compounds remain unclear. Challenging Arabidopsis cell suspension cultures with the commercial Bacillus LPs families (surfactin, fengycin and iturin) both the early cell response and the later events like defence-gene expression were evaluated. Through Evans blue test no cell death increase was detected challenging Arabidopsis cell culture with three different concentrations of the LPs families. The administration of the highest concentration of surfactin (50 µg/ml) to A. thaliana cell cultures expressing the Ca2+-sensitive photoprotein aequorin in the cytosol evoked a cytosolic Ca2+ transient, suggesting that the perception of surfactin could be mediated by Ca2+, which is one of the main important intracellular messenger that generate a wide range of different spatial and temporal signals depending on the stimulus perceived.
Then, to evaluate the possible long-term effects generated upon the perception of LPs, a semi-quantitative PCR defence-gene expression analysis was performed at 2 and 6 hours after LPs cell culture-exposure. Lipoxygenase 1 (LOX1), Pathogen-related protein 1 (PR1), Phenylalanine ammonia lyase (PAL1), Non-expressor of Pathogenesis-Related genes 1 (NPR1) and Mitogen-Activated Protein Kinase 3 (MAPK3) were the main genes investigated which are considered reliable markers of ISR and systemic acquired resistance (SAR).
The results showed that ~3-fold increase of LOX1 and PAL1 expression was recorded in treated samples respect to controls. A ~2-fold increase in the NPR1 gene expression was observed comparing samples at 2 h with control. No differences in PR1 and MAPK3 gene expression were detected between samples and controls. The up-regulation of the LOX1 and NPR1 could suggest that surfactin elicits the activation of jasmonate-mediated pathway that could culminate in ISR. Instead, up-regulation of PAL1 without PR1 expression may indicate an initial SAR triggering, afterwards inhibited by some steps of ISR pathway.
A UPLC-MS analysis performed at the Gembloux Agro-Bio Tech (University of Liège, Belgium) revealed that some selected Glera Bacillus endophytes produce surfactin and fengycin. Moreover, a quite uncommon type of surfactin called pumilacidin was detected and semi-purified. An in vitro antagonism assays against some plant pathogen bacteria showed that pumilacidin had a quite strong antibacterial effect. This is a preliminary result and other tests against, for example, infectious fungi such as B. cinerea need to be performed. Nevertheless, this is an important starting point for developing new sustainable practices with potential application in disease control.
In conclusion, among grapevine cultivable endophytic strains, GL83 and GL174 showed to be promising candidates as bio-fertilizer enhancing both the grapevine growth and health: GL83 was able to promote growth and to confer an increased tolerance to drought stress whereas GL174 seemed to have a protecting action against some fungal grapevine pathogens.
The possibility of endophyte exploitation to help plants to cope with abiotic as well as biotic environmental stresses, interfering with plant morphology and physiology or priming their systemic responses against pathogens, opens new scenarios for an environmentally friendly shift in agricultural practices with much lower impact of synthetic agro-chemicals.
Results obtained from this work are aligned with the huge amount of studies, grown exponentially in the last years, in which the endophytes abilities and properties are often assayed in a single plant species or within groups of closely related plant genotypes. In addition, investigations are usually performed using microbial species that are relatively easy to cultivate leaving out that plant biome is always characterized by wide and complex interactions. The plant phenotype is determined not only by the plant responses to the environment but it is also orchestrated by the associated microbiota, the responses of the microbiota to the environment, and the complex interactions between individuals in the endosphere microbial plant community. Future exciting challenges, based on classical approaches and new valuable technologies (i.e. next-generation sequencing) applied to greenhouse and field conditions would allow to explore and characterize the contributions of genetic and metabolic elements involved in the interactions between host plants and endophytes, providing new ecological and evolutionary insights and a better knowledge of the plant-microbiome-environment relationships.

Abstract (italian)

Questa tesi presenta e discute i risultati ottenuti durante i tre anni del corso in Evoluzione, Ecologia e Conservazione della scuola di dottorato in Bioscienze presso l’Università degli studi di Padova. Il progetto di dottorato si è focalizzato sulle interazioni piante-microrganismi, in particolare tra Vitis vinifera cultivar Glera e batteri endofiti, precedentemente isolati dalla stessa specie vegetale.
Il progetto mira a studiare i possibili effetti benefici che alcuni batteri endofiti, appartenenti ai generi Pantoea e Bacillus, possono conferire alle barbatelle di Glera in termini di promozione della crescita, riduzione di stress ambientali e protezione contro i patogeni. Il progetto ha come scopo la riduzione dell’utilizzo di sostanze inquinanti, come fertilizzanti chimici e pesticidi, in agricoltura e di promuovere una gestione più sostenibile della viticoltura.
Innanzitutto sono stati selezionati due ceppi, Pantoea agglomerans (GL83) e Bacillus licheniformis (GL174), sulla base delle loro attività di promozione della crescita precedentemente definite; quindi entrambi sono stati trasformati con il gene che codifica la proteina fluorescente GFP e utilizzati per inoculare, in vitro, talee apicali di Glera per confermare la loro natura endofitica. Sfruttando tecniche di microscopia confocale a fluorescenza e un metodo di coltivazione diretta in piastra, è stato possibile dimostrare la capacità di tali ceppi di colonizzare i tessuti interni del fusto dopo 20 e 30 giorni dall'inoculo. L'analisi è stata poi estesa a 45, 52 e 60 giorni dall’inoculo, durante i quali le talee di vite sono state trasferite in mezzo idroponico non sterile. Entrambi i ceppi sono stati visualizzati all'interno del sistema vascolare del fusto e nei tessuti interni della radice fino a 60 giorni dall’inoculo.
Il passo successivo ha previsto la messa a punto di esperimenti in campo utilizzando quattro ceppi endofiti (GL83, GL174, GL189, GL452 e il consorzio di questi quattro) i quali sono stati inoculati in due diversi momenti nella linea di produzione delle barbatelle. Nel primo test i batteri sono stati somministrati a portainnesti (Kober 5BB) e gemme di Glera durante la fase di idratazione, mentre nel secondo dopo che le barbatelle avevano sviluppato le radici.
Sono stati quindi valutati sia parametri di crescita sia parametri fisiologici campionando le barbatelle in diversi stadi del loro sviluppo.
I ceppi più promettenti sono stati GL83 e GL174 specialmente quando somministrati a portainnesti e gemme durante la fase di idratazione.
Le piante inoculate presentavano parametri fisiologici più elevati rispetto a quelli di piante di controllo, nonché un aumento della massa radicale e della parte aerea. E’ stato anche condotto un esperimento mirato a simulare la fertilizzazione in vigneto; questo ha previsto l’utilizzo di piante di vite di 1 anno, le quali sono state irrigate una volta alla settimana per sette settimane consecutive con GL83 e GL174. I risultati emersi confermano che questi due ceppi sono due ottimi candidati per un futuro utilizzo in vigneto come bio-fertilizzanti. Inoltre, GL83 è stato in grado di alleviare gli effetti del deficit idrico in barbatelle di Glera. Infatti, le piante inoculate soggette a stress idrico presentavano parametri morfologici e fisiologici più elevati rispetto a quelli delle relative piante di controllo.
Un altro tema trattato durante questo lavoro di dottorato è stato il ruolo delle tre famiglie di lipopeptidi prodotti dal genere Bacillus (surfactine, fengicine e iturine) nell’indurre risposte di difesa nelle piante. I lipopeptidi sono molecole anfipatiche prodotte come metaboliti secondari da alcuni generi batterici come Bacillus e Pseudomonas; la loro struttura li rende composti biologicamente attivi contro microrganismi potenzialmente patogeni quali batteri, funghi e micoplasmi. E’ stato inoltre riportato che queste sostanze sono in grado di scatenare risposte di difesa nelle piante, ma i meccanismi che sottendono all’attivazione di tali risposte e il percorso specifico che seguono, sono tuttora poco noti.
Tramite l’utilizzo di un sistema modello semplificato come le colture cellulari in sospensione di Arabidopsis thaliana, È stato possibile studiare sia la fase di percezione dei lipopeptidi sia eventi a valle come l’espressione di alcuni geni marker di difesa. Prima di tutto è stata valutata la possibile citotossicità di questi composti utilizzando l’Evans blue test; sono state somministrate tutte le tre famiglie di lipopeptidi in commercio del genere Bacillus in tre differenti concentrazioni e in alcun caso È stata riscontrata citotossicità .
Utilizzando poi una linea cellulare transgenica di Arabidopsis esprimente stabilmente la foto-proteina luminescente Ca2+-sensibile equorina nel citosol è stato possibile studiare l’eventuale coinvolgimento dello ione Ca2+ come trasduttore del segnale dopo la somministrazione di lipopeptidi. Solo la concentrazione più elevata di surfactine (50 µg/ml) ha indotto un transiente citosolico di Ca2+, suggerendo il coinvolgimento di questo ione nella percezione delle stesse.
Successivamente, per studiare i possibili effetti a lungo termine delle surfactine nell’indurre le risposte di difesa della pianta sono state effettuate delle analisi di espressione genica tramite PCR semi-quantitativa dopo 2 e 6 ore dal trattamento delle colture cellulari con surfactine 50 µg/ml. I geni studiati sono stati LOX1, PR1, PAL1, NPR1 e MAPK3 considerati geni marker per risposte di difesa sistemiche indotte o acquisite, ISR e SAR.
I risultati ottenuti dimostrano un’attivazione delle risposte di difesa della pianta; in particolare LOX1 e PAL1 sono risultati essere 3 volte più espressi nei campioni trattati rispetto al controllo, mentre NPR1 è risultato essere 2 volte più espresso dopo 2 ore dalla somministrazione del trattamento. Invece PR1 e MAPK3 sono risultati invariati nel livello di espressione tra cellule trattate e di controllo.
L’up-regolazione di geni come LOX1 e NPR1 suggerisce l’attivazione della via dipendente dall’acido jasmonico la quale conferisce alla pianta uno stato di allerta (priming) contro successivi attacchi da patogeno. PAL1 invece è uno dei geni up-regolati in seguito all’attivazione della SAR. E’ comunque risaputo che ISR e SAR possono agire in modo sinergico aumentando le difese indotte della pianta.

Analisi attraverso UPLC-MS condotte nel Lab. del Dott. Marc Ongena presso Gembloux Agro-Bio Tech (University of Liège, Gembloux, Belgio) hanno rivelato la capacità di altri ceppi endofiti di Glera del genere Bacillus di produrre lipopeptidi ciclici, surfactine e fengicine. Una sostanza in particolare, chiamata pumilacidina, è stata semi-purificata e testata in vitro tramite test di antagonismo contro alcuni batteri patogeni per le piante. I risultati hanno mostrato che questa sostanza ha una capacità anti microbica piuttosto marcata. Questo risultato preliminare deve essere confermato da ulteriori studi condotti con funghi patogeni come B. cinerea, ma è un punto di partenza importante per lo sviluppo di nuove pratiche sostenibili per il bio-controllo.
In conclusione, GL83 e GL174, tra i ceppi di endofiti di vite coltivabili, si sono dimostrati essere piuttosto promettenti come bio-fertilizzanti, in quanto capaci di migliorare sia la crescita che lo stato di salute della vite. In particolare, GL83 è stato capace di promuovere la crescita e di conferire maggiore tolleranza in situazioni di deficit idrico, mentre GL174 sembra avere un’azione protettiva nei confronti di alcuni patogeni della vite.
La possibilità di sfruttare gli endofiti per supportare la pianta in situazioni di stress biotici ed abiotici, in grado di interferire sulla morfologia e la fisiologia della pianta stessa e su risposte di difese sistemiche contro i patogeni, apre nuovi scenari nella gestione sostenibile della viticoltura che faccia meno uso di input chimici.

I risultati di questo lavoro confermano quelli ottenuti negli ultimi anni, in cui le proprietà degli endofiti sono state studiate in una singola specie vegetale o in gruppi di genotipi strettamente correlati. Inoltre, spesso gli studi vengono condotti con specie microbiche relativamente facili da coltivare, tralasciando che il bioma della pianta È caratterizzato da ampie e complesse interazioni. Il fenotipo vegetale infatti non è determinato unicamente dalla risposta della pianta all’ambiente, ma è anche orchestrato dalla risposta dell’intero microbiota all’ambiente e dalle complesse interazioni tra gli individui e la comunità microbica della rizosfera.
Le prospettive future, basate allo stesso tempo su approcci classici e tecnologie all’avanguardia (NGS), e applicate in differenti condizioni colturali, permetteranno di valutare e caratterizzare in termini genetici e metabolici gli effetti delle interazioni tra pianta ospite ed endofiti. Questo apporterà nuovi spunti e conoscenze sia dal punto di vista ecologico che evoluzionistico in merito alle interazioni pianta-microbioma-ambiente.

EPrint type:Ph.D. thesis
Tutor:Baldan, Barbara
Ph.D. course:Ciclo 30 > Corsi 30 > BIOSCIENZE
Data di deposito della tesi:12 January 2018
Anno di Pubblicazione:11 January 2018
Key Words:endofiti / endophytes lipopeptidi / lipopeptides vite / grapevine biocontrollo / biocontrol microscopia confocale / confocal microscopy
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/13 Biologia applicata
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:10692
Depositato il:25 Oct 2018 15:41
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