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Paccanaro, Maria Chiara (2016) Fungal cell wall degrading enzymes and plant inhibitors: role during plant infection and strategies to increase plant resistance. [Ph.D. thesis]

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Abstract (english)

During the infection process pathogens produce high amounts of cell wall-degrading enzymes (CWDE) such as endo-xylanases and polygalacturonases (PGs), in order to overcome the barrier constituted by the plant cell wall and obtain nutrients. The first class of enzymes hydrolyzes xylan, a polysaccharide particularly abundant in monocot plants, and some of them have been shown to cause necrosis and hypersensitive response (HR) in the host tissue. The PGs are secreted by pathogenic microorganisms at the early stage of the infection process and are involved in the degradation of the pectin polymer. Fungal PGs and xylanases have been shown to play an important role during pathogenesis of some fungal pathogens, but little is known about their contribution to the virulence of the fungal pathogen Fusarium graminearum, the causal agent of the Fusarium Head Blight disease. Therefore we focused our attention on the F. graminearum xyr1 and pg1 genes (encoding the major regulator of xylanase genes expression and the main PG isoform of the fungus, respectively) by producing single gene disruption mutants (∆xyr and ∆pg). Targeted disruption of the pg1 gene produced a mutant with a PG activity nearly abolished and a reduced virulence on soybean but not on wheat spikes; besides, the ∆xyr mutant, although dramatically impaired in xylanase activity, showed a virulence comparable with wild type on both soybean and wheat. In order to establish a possible synergistic effect between the F. graminearum xylanase and PG activities, a ΔΔxyr/pg double mutant was produced by transforming protoplasts of a ∆pg mutant strain. As expected, when grown on xylan and pectin as carbon sources, the xylanase and PG activities of the double mutant strains were dramatically reduced compared to the wild type strain, while the growth of the double mutant was affected only on xylan containing medium. Infection experiments on soybean seedlings and wheat spikes showed that the virulence of the double mutant strains was significantly reduced compared to the single mutants. The synergistic effect of PG and xylanase activities was confirmed incubating the F. graminearum PG1 and two main purified fungal xylanases in presence of wheat cell walls.
Since one of these xylanases (FGSG_03624) has been previously shown to cause HR in wheat tissues, we also evaluated the ability of this xylanase to induce defence responses in Arabidopsis. Exogenous treatments with this protein induced the expression of PDF1.2 defense gene, marker of the jasmonate/ethylene pathways. Treatment of xylanase leaves reduced symptoms of the bacterium Pseudomonas syringae pv. maculicola but not those of the fungus Botrytis cinerea. A site-directed mutagenesis of the FGSG_03624 catalytic site abolished the xylanase activity. This mutagenized protein was transiently expressed in tobacco leaves and also constitutively expressed in Arabidopsis plants. Transformed tobacco and Arabidopsis plants were as susceptible as the untransformed plants to B. cinerea infections. Differently from what observed with exogenous treatments, transgenic Arabidopsis plants were not more resistance to P. syringae infection. As a defense mechanism to counteract pathogens infection, plants have evolved specific inhibitors, usually localized in the plant cell wall, able to reduce or completely block the fungal CWDE. A Triticum aestivum family of xylanase inhibitor proteins (TAXI) have been shown to inhibit the B. cinerea Xyn11A xylanase, a well-known virulence factor of this fungus. TAXI encoding genes were expressed in tobacco leaves and Arabidopsis plants and these plants were infected with B. cinerea. While tobacco leaves transiently expressing TAXIs showed increased resistance against the fungus compared to control leaves, transgenic Arabidopsis plants resulted as susceptible as the untransformed plants.

Abstract (italian)

Durante il processo infettivo i patogeni producono un gran numero di enzimi degradativi della parete cellulare, tra cui endo-xilanasi e poligalatturonasi, così da superare la barriera rappresentata dalla parete cellulare della pianta ospite e ottenere sostanze nutritive. Le xilanasi idrolizzano lo xilano, un polisaccaride particolarmente abbondante nella piante monocotiledoni, e alcune sono state dimostrate essere in grado di causare necrosi e risposta ipersensibile nel tessuto ospite. Le poligalatturonasi sono secrete da microorganismi patogeni durante le prime fasi del processo infettivo e sono implicate nella degradazione della pectina. Le poligalatturonasi e le xilanasi fungine svolgono un ruolo importante durante la patogenesi, ma non si conosce in modo approfondito come contribuiscano alla virulenza del fungo patogeno Fusarium graminearum, l’agente causale della fusariosi della spiga. In questo lavoro sono stati deleti, tramite ricombinazione omologa sito-specifica, il fattore trascrizionale Xyr1 (che regola putativamente l’espressione di diversi geni codificanti per enzimi xilanolitici) e la principale poligalatturonasi del fungo, codificata dal gene pg1, producendo i mutanti singoli ∆xyr and ∆pg. I mutanti derivati dalla delezione del gene pg1 hanno mostrato una bassissima attività poligalatturonasica e una virulenza ridotta su soia ma non su frumento; il mutante ∆xyr ha presentato una drastica diminuzione dell’attività xilanasica, ma una virulenza comparabile al wild type sia su soia che su frumento. Per stabilire quindi un possibile effetto sinergico tra le attività xilanasica e poligalatturonasica di F. graminearum, è stato prodotto il doppio mutante ΔΔxyr/pg trasformando i protoplasti del mutante singolo ∆pg. I mutanti ΔΔxyr/pg hanno presentato una ridotta capacità di crescere quando sono stati allevati in coltura liquida con xilano come unica fonte di carbonio e una forte diminuzione delle attività xilanasica e poligalatturonasica rispetto al ceppo wild type. La virulenza dei mutanti ΔΔxyr/pg su soia e spighe di frumento è rimasta notevolmente ridotta rispetto a quella dei mutanti singoli. L’effetto sinergico delle attività xilanasica e poligalatturonasica è stato quindi confermato incubando le pareti cellulari di frumento in presenza di PG1 e di due tra le più espresse xilanasi di F. graminearum purificate.
Siccome precedentemente è stato dimostrato che la xilanasi FGSG_03624 di F. graminearum causa risposta ipersensibile in frumento, è stata indagata l’abilità di questa xilanasi nell’indurre risposte di difesa in Arabidopsis. Trattamenti esogeni con questa proteina hanno indotto l’espressione del gene di difesa PDF1.2 e hanno mostrato una riduzione dei sintomi causati dal batterio Pseudomonas syringae pv. maculicola ma nessun effetto contro il fungo Botrytis cinerea. La proteina è stata quindi transientemente espressa in foglie di tabacco e costitutivamente espressa in Arabidopsis dopo una mutagenesi nel sito catalitico che ha abolito l’attività xilanasica. Quando infettate con B. cinerea, le foglie di tabacco e di Arabidopsis hanno mostrato uguale suscettibilità rispetto alle rispettive foglie di controllo. Contrariamente a quanto osservato con i trattamenti esogeni, le piante transgeniche di Arabidopsis non erano più resistenti all’infezione di P. syringae. Tra i meccanismi di difesa sviluppati per contenere l’ infezione di patogeni, le piante possiedono specifici inibitori, solitamente presenti nella parete cellulare, capaci di ridurre o bloccare completamente l’attività degli enzimi degradativi secreti dei funghi patogeni. In Triticum aestivum è stata identificata una famiglia di inibitori xilanasici (TAXI) capace di inibire la xilanasi Xyn11A di B. cinerea, un fattore di virulenza del fungo. Geni codificanti TAXI sono stati espressi in tabacco e Arabidopsis e le piante trasformate sono state infettate con B. cinerea. Mentre l’espressione transiente di TAXI nelle foglie di tabacco ha determinato una maggiore resistenza contro il fungo, l’espressione costitutiva in Arabidopsis non ha prodotto nessun effetto positivo.

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EPrint type:Ph.D. thesis
Tutor:Sella, Luca
Supervisor:Favaron, Francesco
Ph.D. course:Ciclo 28 > Scuole 28 > SCIENZE DELLE PRODUZIONI VEGETALI
Data di deposito della tesi:17 July 2016
Anno di Pubblicazione:July 2016
Key Words:Fusarium head blight, gene disruption, virulence, xylanase, polygalacturonase, TAXI, transgenic plants
Settori scientifico-disciplinari MIUR:Area 07 - Scienze agrarie e veterinarie > AGR/12 Patologia vegetale
Struttura di riferimento:Dipartimenti > Dipartimento Territorio e Sistemi Agro-Forestali
Codice ID:9667
Depositato il:02 Nov 2017 17:38
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