iForest - Biogeosciences and Forestry


Arbuscular mycorrhizal colonization in black poplar roots after defoliation by a non-native and a native insect

Elisa Zampieri (1), Edoardo Petrucco Toffolo (2), Antonietta Mello (3), Achille Giorcelli (4), Massimo Faccoli (2), Raffaella Balestrini (3), Paolo Gonthier (1)   

iForest - Biogeosciences and Forestry, Volume 9, Issue 6, Pages 868-874 (2016)
doi: https://doi.org/10.3832/ifor1911-009
Published: Aug 29, 2016 - Copyright © 2016 SISEF

Research Articles

A major goal in ecology is to understand how interactions among organisms influence ecosystem services. This work compares the effects of two Lepidoptera defoliators, one non-native (Hyphantria cunea) and one native (Lymantria dispar) to Europe, on the colonization of black poplar (the Populus nigra clone “Jean Pourtet”) roots by an arbuscular mycorrhizal (AM) symbiotic fungus (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 neither the expression of genes coding for a fungal and a plant phosphate transporter 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.


Exotic, Defoliators, Arbuscular Mycorrhizal Symbiosis, qPCR, Poplar, Gene Expression

Authors’ address

Elisa Zampieri
Paolo Gonthier
Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA), Università di Torino, l.go Paolo Braccini 2, 10095 Grugliasco, TO (Italy)
Edoardo Petrucco Toffolo
Massimo Faccoli
Dipartimento di Agronomia, Animali, Alimenti, Risorse naturali e Ambiente -Agripolis-, Università di Padova, v.le dell’Università 16, 35020 Legnaro, PD (Italy)
Antonietta Mello
Raffaella Balestrini
Istituto per la Protezione Sostenibile delle Piante, CNR, SS Torino, v.le Mattioli 25, I-10125 Torino (Italy)
Achille Giorcelli
CREA - Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria - Unità di Ricerca per le Produzioni Legnose Fuori Foresta (CREA-PLF), str. Frassineto 35, 15033 Casale M.to, AL (Italy)

Corresponding author

Paolo Gonthier


Zampieri E, Petrucco Toffolo E, Mello A, Giorcelli A, Faccoli M, Balestrini R, Gonthier P (2016). Arbuscular mycorrhizal colonization in black poplar roots after defoliation by a non-native and a native insect. iForest 9: 868-874. - doi: 10.3832/ifor1911-009

Academic Editor

Alberto Santini

Paper history

Received: Nov 06, 2015
Accepted: May 21, 2016

First online: Aug 29, 2016
Publication Date: Dec 14, 2016
Publication Time: 3.33 months

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 41935
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 35691
Abstract Page Views: 1955
PDF Downloads: 3077
Citation/Reference Downloads: 63
XML Downloads: 1149

Web Metrics
Days since publication: 2822
Overall contacts: 41935
Avg. contacts per week: 104.02

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2016): 2
Average cites per year: 0.25


Publication Metrics

by Dimensions ©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

Baker R, Cannon R, Bartlett P, Barker IA (2005)
Novel strategies for assessing and managing the risks posed by invasive alien species to global crop production and biodiversity. Annals of Applied Biology 146: 177-191.
CrossRef | Gscholar
Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P (2007)
Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Molecular Plant Microbe Interaction 20: 1055-1062.
CrossRef | Gscholar
Barto EK, Rillig MC (2010)
Does herbivory really suppress mycorrhiza? A meta-analysis. Journal of Ecology 98: 745-753.
CrossRef | Gscholar
Bécard G, Kosuta S, Tamasloukht M, Sejalon-Delmas N, Roux C (2004)
Partner communication in the arbuscular mycorrhizal interaction. Canadian Journal of Botany 8: 1186-1197.
CrossRef | Gscholar
Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005)
Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 5: 620-627.
CrossRef | Gscholar
Bezemer TM, Van Dam NM (2005)
Linking aboveground and belowground interactions via induced plant defenses. Trends in Ecology and Evolution 20: 617-624.
CrossRef | Gscholar
Bucher M (2007)
Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173: 11-26.
CrossRef | Gscholar
Chang S, Puryear J, Cairney J (1993)
Simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11: 113-116.
CrossRef | Gscholar
Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P (2008)
Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiology 147: 429-437.
CrossRef | Gscholar
Cullings KW, Vogler DR, Parker VT, Makhija S (2001)
Defoliation effects on the ectomycorrhizal community of a mixed Pinus contorta/ Picea engelmannii stand in Yellowstone Park. Oecologia 127: 533-539.
CrossRef | Gscholar
Dyer MI, Acra MA, Wang GM, Coleman DC, Freckman DW, McNaughton SJ, Strain BR (1991)
Source-sink carbon relations in two Panicum coloratum ecotypes in response to herbivory. Ecology 72: 1472-1483.
CrossRef | Gscholar
Eom AH, Wilson GWT, Hartnett DC (2001)
Effects of ungulate grazers on arbuscular mycorrhizal symbiosis and fungal community structure in tallgrass prairie. Mycologia 93: 233-242.
CrossRef | Gscholar
García I, Mendoza R (2012)
Impact of defoliation intensities on plant biomass, nutrient uptake and arbuscular mycorrhizal symbiosis in Lotus tenuis growing in a saline-sodic soil. Plant Biology 14: 964-971.
CrossRef | Gscholar
Gehring CA, Bennett AE (2009)
Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environmental Entomology 38: 93-102.
CrossRef | Gscholar
Gehring CA, Whitham TG (1994)
Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends in Ecology and Evolution 9: 251-255.
CrossRef | Gscholar
Gehring CA, Whitham TG (2002)
Mycorrhizae-herbivore interactions: population and community consequences. In: “Mycorrhizal Ecology” (van der Heijden MGA, Sanders IR eds). Springer, Berlin, Germany, pp. 295-320.
CrossRef | Gscholar
Genre A, Bonfante P (2005)
Building a mycorrhizal cell: how to reach compatibility between plants and arbuscular mycorrhizal fungi. Journal of Plant Interaction 1: 3-13.
CrossRef | Gscholar
Gomez-Ariza J, Balestrini R, Novero M, Bonfante P (2009)
Cell-specific gene expression of phosphate transporters in mycorrhizal tomato roots. Biology and Fertility of Soils 45: 845-853.
CrossRef | Gscholar
Hjältén J (2004)
Simulating herbivory: problems and possibilities. In: “Insects and Ecosystem Function” (Weisser WW, Siemann E eds). Springer-Verlag, Berlin Heidelberg, Germany, pp. 243-255.
CrossRef | Gscholar
Hokka V, Mikola J, Vestberg M, Setala H (2004)
Interactive effects of defoliation and an AM fungus on plants and soil organisms in experimental legume-grass communities. Oikos 106: 73-84.
CrossRef | Gscholar
Holland JN, Cheng W, Crossley DA (1996)
Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107: 87-94.
CrossRef | Gscholar
Kenis M, Auger-Rozenberg MA, Roques A, Timms L, Péré C, Cock MJ, Settele J, Augustin S, Lopez-Vaamonde C (2009)
Ecological effects of invasive alien insects. Biological Invasions 11: 21-45.
CrossRef | Gscholar
Kosola KR, Durall DM, Robertson GP, Dickmann DI, Parry D, Russell CA, Paul EA (2004)
Resilience of mycorrhizal fungi on defoliated and fertilized hybrid poplars. Canadian Journal of Botany 82: 671-680.
CrossRef | Gscholar
Kula AAR, Hartnett DC, Wilson GWT (2005)
Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecology Letters 8: 61-69.
CrossRef | Gscholar
Lehtilä K, Boalt E (2004)
The use and usefulness of artificial herbivory in plant-herbivore studies. In: “Insects and Ecosystem Function” (Weisser WW, Siemann E eds). Springer-Verlag, Berlin Heidelberg, Germany, pp. 257-275.
CrossRef | Gscholar
Li S, Hartman GL, Domier LL, Boykin D (2008)
Quantification of Fusarium solani f. sp. glycines isolates in soybean roots by colony-forming unit assays and real-time quantitative PCR. Theoretical and Applied Genetics 117: 343-352.
CrossRef | Gscholar
Lingua G, Franchin C, Todeschini V, Castiglione S, Biondi S, Burlando B, Parravicini V, Torrigiani P, Berta G (2008)
Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. Environmental Pollution 153: 137-147.
CrossRef | Gscholar
Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F, Berta G, Cavaletto M (2012)
Effects of heavy metals and arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. PLoS ONE 7: e38662.
CrossRef | Gscholar
Livak KJ, Schmittgen TD (2001)
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
CrossRef | Gscholar
Markkola A, Kuikka K, Rautio P, Härmä E, Riotto M, Tuomi J (2004)
Defoliation increases carbon limitation in ectomycorrhizal symbiosis of Betula pubescens. Oecologia 140: 234-240.
CrossRef | Gscholar
Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005)
The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. The Plant Journal 42: 236-250.
CrossRef | Gscholar
Pietikäinen A, Kytoviita MM, Vuoti U (2005)
Mycorrhiza and seedling establishment in a subarctic meadow: effects of fertilization and defoliation. Journal of Vegetation Science 16: 175-182.
CrossRef | Gscholar
Regier N, Streb S, Cocozza C, Schaub M, Cherubini P, Zeeman SC, Frey B (2009)
Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell and Environment 32: 1724-1736.
CrossRef | Gscholar
Requena N, Breuninger M, Franken P, Ocón A (2003)
Symbiotic status, phosphate and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiology 132: 1540-1549.
CrossRef | Gscholar
Saravesi K, Markkola A, Rautio P, Roitto M, Tuomi J (2008)
Defoliation causes parallel temporal responses in a host tree and its fungal symbionts. Oecologia 156: 117-123.
CrossRef | Gscholar
Saravesi K, Ruotsalainen AL, Cahill JF (2014)
Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa. Mycorrhiza 24: 239-245.
CrossRef | Gscholar
Schüssler A, Schwarzott D, Walker C (2001)
A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
CrossRef | Gscholar
Sillo F, Zampieri E, Giordano L, Lione G, Colpaert JV, Balestrini R, Gonthier P (2015)
Identification of genes differentially expressed during the interaction between the plant symbiont Suillus luteus and two plant pathogenic allopatric Heterobasidion species. Mycological Progress 14: 106.
CrossRef | Gscholar
Smith SE, Read DJ (2008)
Mycorrhizal symbiosis (3rd edn). Academic Press, Amsterdam, the Netherlands, pp. 800.
Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JP, Gianinazzi-Pearson V, Martin F (2012)
The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytologist 193:755-769.
CrossRef | Gscholar
Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JP, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013)
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proceedings of the National Academy of Sciences USA 110: 20117-20122.
CrossRef | Gscholar
Trocha LK, Weiser E, Robakowski P (2015)
Interactive effects of juvenile defoliation, light conditions and interspecific competition on growth and ectomycorrhizal colonization of Fagus sylvatica and Pinus sylvestris seedlings. Mycorrhiza 26: 47-56.
CrossRef | Gscholar
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986)
Mesure du taux de mycorrhization VA d’un syste me radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle [Evaluation of VAM infection levels in root systems. Research for estimation methods having a functional significance] In: “Mycorrhizae: Physiology and Genetics” (Gianinazzi-Pearson V, Gianinazzi S eds). INRA Press, Paris, France, pp. 217-221. [in French]
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006)
The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
CrossRef | Gscholar
Walling SZ, Zabinski CA (2006)
Defoliation effects on arbuscular mycorrhizae and plant growth of two native bunch grasses and an invasive forb. Applied Soil Ecology 32: 111-117.
CrossRef | Gscholar
Wardle DA (2002)
Communities and ecosystems. Linking the aboveground and belowground components. Princeton University Press, Princeton, NJ, USA, pp. 408.
Online | Gscholar
Warren LO, Tadic M (1970)
The fall webworm, Hyphantria cunea (Durry). Arkansas Agricultural Experiment Station Bulletin 759:1-106.
Xu GH, Chague V, Melamed-Bessudo C, Kapulnik Y, Jain A, Raghothama KG, Levy AA, Silber A (2007)
Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. Journal of Experimental Botany 58: 2491-2501.
CrossRef | Gscholar
Zhao S, Fernald RD (2005)
Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 12: 1047-1064.
CrossRef | Gscholar

This website uses cookies to ensure you get the best experience on our website. More info