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Zampieri E, Petrucco Toffolo E, Mello A, Giorcelli A, Faccoli M, Balestrini R, Gonthier P (2016). Arbuscular Mycorrhizal Coloniz

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Zampieri E, Petrucco Toffolo E, Mello A, Giorcelli A, Faccoli M, Balestrini R, Gonthier P (2016). Arbuscular Mycorrhizal Coloniz Research Article ii FF o o r r e e s s t t doi: 10.3832/ifor1911-009 Biogeosciences and Forestry vol. 9, pp. 868-874 Arbuscular mycorrhizal colonization in black poplar roots after defoliation by a non-native and a native insect Elisa Zampieri (1), Edoardo A major goal in ecology is to understand how interactions among organisms Petrucco Toffolo (2), Antonietta influence ecosystem services. This work compares the effects of two Lepidop- Mello (3), Achille Giorcelli (4), tera defoliators, one non-native (Hyphantria cunea) and one native (Lyman- (2) tria dispar) to Europe, on the colonization of black poplar (the Populus nigra Massimo Faccoli , Raffaella clone “Jean Pourtet”) roots by an arbuscular mycorrhizal (AM) symbiotic fun- (3) (1) Balestrini , Paolo Gonthier gus (Funneliformis mosseae) in a pot experiment. The effects of defoliation have also been assessed on the expression of fungal and plant genes playing a role during symbiosis. Both control and defoliated poplars have shown a low level of mycorrhization. Additionally, neither the non-native nor the native insect seem to strongly affect the AM colonization, at least at the time of observation (eight days from the end of the defoliation). Concerning the gene expression analysis, our results suggest that defoliation does not influence nei- ther the expression of genes coding for a fungal and a plant phosphate trans- porter nor that of a gene coding for a fungal ATPase, and that there were no differences between defoliation carried out by the non-native and the native insect. Keywords: Exotic, Defoliators, Arbuscular Mycorrhizal Symbiosis, qPCR, Poplar, Gene Expression Introduction the host plant with water and mineral nu- phae, coils, and arbuscules (Genre & Bon- Terrestrial ecosystems can be roughly di- trients and can lead to an improved toler- fante 2005). Despite the improved mineral vided into above- and below-ground, linked ance against biotic and abiotic stresses nutrition, AM fungi cause a significant car- together by plants (Wardle 2002). A major (e.g., salinity, drought, heavy metals), in bon cost for the host plant, allocating up to goal in ecology is to understand how inter- exchange for photoassimilates (Smith & 20% of the photosynthates (Saravesi et al. actions among organisms influence ecosys- Read 2008). In particular, arbuscular myc- 2014). AM fungi are obligate biotrophs and tems (Bezemer & Van Dam 2005). Invasive orrhizal (AM) symbiosis involves fungi be- they are thus not able to survive long peri- organisms – i.e. non-native organisms, longing to Glomeromycota (Schüssler et al. ods without the host plant (Bécard et al. which threaten ecosystems, habitat or in- 2001) and the majority of land plants, in- 2004). Enzymes for saprotrophic behavior digenous species – are a major element of cluding both important crop species, such are lacking in the genome of the AM fun- global change and are contributing to bio- as tomato, wheat, rice, maize, soybean, gus Rhizophagus irregularis, which has diversity loss, ecosystem degradation and and forest tree species, such as poplars been recently sequenced (Tisserant et al. impairment of ecosystem services world- (Populus spp. – Tisserant et al. 2012). The 2013). Over long-term, leaf herbivory (and wide (Baker et al. 2005). root colonization process involves both clipping) may eventually result in reduced More than 90% of plants form root inter- epidermal and cortical cells, where the fun- carbon accessibility for the host plant and actions with mycorrhizal fungi that provide gus develops inter- and intra-cellular hy- fungal partners (Barto & Rillig 2010, Sar- avesi et al. 2014), although, in spite of the re-growth of the above-ground tissue, car- (1) Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Università di Torino, bon allocation to roots often increases im- l.go Paolo Braccini 2, 10095 Grugliasco, TO (Italy); (2) Dipartimento di Agronomia, Animali, mediately after defoliation, while alloca- Alimenti, Risorse naturali e Ambiente -Agripolis-, Università di Padova, v.le dell’Università tion to shoots decreases (Dyer et al. 1991, 16, 35020 Legnaro, PD (Italy); (3) Istituto per la Protezione Sostenibile delle Piante, CNR, SS Holland et al. 1996). Although the impact Torino, v.le Mattioli 25, I-10125 Torino (Italy); (4) CREA - Consiglio per la Ricerca in Agri- of leaf herbivory on colonization by mycor- coltura e l’Analisi dell’Economia Agraria - Unità di Ricerca per le Produzioni Legnose Fuori rhizal fungi has mainly been reported as Foresta (CREA-PLF), str. Frassineto 35, 15033 Casale M.to, AL (Italy) negative, sometimes even positive or nil effects on fungal symbiosis have been de- @ Paolo Gonthier ([email protected]), Raffaella Balestrini (raffaella.balestrini@ipsp. tected (Gehring & Whitham 1994, 2002, cnr.it) Cullings et al. 2001, Eom et al. 2001, Hokka et al. 2004, Kula et al. 2005, Pietikäinen et Received: Nov 06, 2015 - Accepted: May 21, 2016 al. 2005, Walling & Zabinski 2006, Gehring & Bennett 2009, Saravesi et al. 2014, Citation: Zampieri E, Petrucco Toffolo E, Mello A, Giorcelli A, Faccoli M, Balestrini R, Trocha et al. 2015). It has been reported Gonthier P (2016). Arbuscular mycorrhizal colonization in black poplar roots after defoliation that the variability in responses might by a non-native and a native insect. iForest 9: 868-874. – doi: 10.3832/ifor1911-009 [online depend on the type and extent of defolia- 2016-08-29] tion, the duration of the experiment, the mycorrhizal type or plant species consid- Communicated by: Alberto Santini ered, the availability of soil nutrients or other not yet known factors (Gehring & © SISEF http://www.sisef.it/iforest/ 868 iForest 9: 868-874 Zampieri E et al. - iForest 9: 868-874 y ® r Whitham 2002, Gehring & Bennett 2009). 180 °C for 3h. For one month, they were the DNeasy Plant Mini Kit (Qiagen, Valen- t s Barto & Rillig (2010) conducted a meta- watered twice a week with tap water in cia, CA, USA) according to the manufac- e r analysis study, focusing on the sensitivity order to obtain shoots and roots. turer’s instructions. o of AM and ectomycorrhizal (ECM) coloniza- Forty-five seedlings were then inoculated The RNA was extracted from about 100 F tion of roots to the removal of leaves or with Funneliformis mosseae BEG 12 (for- mg of roots using the “pine-tree method” d n shoots by herbivory or clipping. Meta-anal- merly Glomus mosseae) inoculum (MycAgro (Chang et al. 1993). After extraction, RNA a ysis results showed that the carbon-limita- Lab, France), by mixing the inoculum with was cleaned of DNA, using Promega DNase s ® e tion hypothesis of reduced mycorrhizal col- sterile quartz sand (30% v/v). All plants (RQ1 RNase-Free DNase , Promega Corp., c n onization following removal of above- were watered three times a week with tap Madison, WI, USA), and then measured e ® i ground biomass was generally not sup- water, and kept in a greenhouse for ap- using a NanoDrop (ThermoScientific, Hud- c s ported, and that herbivory (or clipping) did proximately 75 days, following the natural son, NH, USA). The absence of genomic o not reduce mycorrhizal colonization by bio- photoperiod (from March to June 2014). DNA was verified through one-step retro- e g logically meaningful levels in many types of transcription PCR (One-Step RT-PCR, Qia- o i plants (Barto & Rillig 2010). More recently, Defoliation of Populus nigra seedlings gen) with primers (Gmostef1, Gmostef2) B Saravesi et al. (2014) reported a different The defoliation occurred between the previously designed for the F. mosseae – th th effect of host plant defoliation on root AM 24 of June and the 16 of July 2014. The elongation factor reference gene (Cappel- t s and dark septate endophyte (DSE) fungi potted plants were kept in the field at lazzo et al. 2008). Briefly, the same ex- e r colonization. In particular, negative im- Agripolis campus (Legnaro, Italy) inside tracted RNA was used as template for o F pacts on AM colonization and a slightly po- cages to protect them from insect attack, retro-transcription and for PCR amplifica- i sitive impact on DSE colonization were ob- under conditions that mimic the natural tion or for PCR amplification only (RT- reac- served, suggesting divergent ecological ro- ones. Five theses were considered: undefo- tions). The absence of signal after PCR les of the two fungal associates in the plant liated control plants, partial and total defo- amplification without retrotranscription carbon economy. liation by H. cunea and partial and total was regarded as absence of DNA. Total The increasing threat of invasive species, defoliation by L. dispar. In the partial treat- RNA for each sample was used to synthe- among which are several defoliators, raises ment defoliation, about 50% of the leaves size the cDNA, according to the Super- a question about their possible impact on was exposed to defoliation, whereas in the Script II Reverse Transcriptase® (Invitrogen, the components of native ecosystems (Ke- total treatment defoliation experiment the Carlsbad, CA, USA) procedure using ran- nis et al. 2009). In Europe, Hyphantria cu- whole foliage was exposed to defoliation. dom primers. nea Drury, a moth native to North America, To achieve this, the half-lower part of plant became invasive in the 1940s (Warren & bearing about 50% of leaves was enclosed Selected genes and primers Tadic 1970). Being a polyphagous defolia- in the mesh bag in the partial defoliation The fungal genes selected for the analysis tor, it feeds on hundreds of host plants, thesis and the entire plant in the total defo- were an amino acid permease (GmosAAP1 including black poplars. P. nigra L. is also a liation thesis. Each thesis included nine – Cappellazzo et al. 2008), a phosphate host plant for native defoliators, such as replicates. Each plant had a single pot and transporter (GmosPT – Balestrini et al.
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