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.
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Citation
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
© SISEF - The Italian Society of Silviculture and Forest Ecology 2016
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This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
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(1)
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
(2)
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
(3)
Barto EK, Rillig MC (2010)Does herbivory really suppress mycorrhiza? A meta-analysis. Journal of Ecology 98: 745-753.
CrossRef |
Gscholar
(4)
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
(5)
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
(6)
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
(7)
Bucher M (2007)Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173: 11-26.
CrossRef |
Gscholar
(8)
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
(9)
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
(10)
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
(11)
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
(12)
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
(13)
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
(14)
Gehring CA, Bennett AE (2009)Mycorrhizal fungal-plant-insect interactions: the importance of a community approach. Environmental Entomology 38: 93-102.
CrossRef |
Gscholar
(15)
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
(16)
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
(17)
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
(18)
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
(19)
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
(20)
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
(21)
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
(22)
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
(23)
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
(24)
Kula AAR, Hartnett DC, Wilson GWT (2005)Effects of mycorrhizal symbiosis on tallgrass prairie plant-herbivore interactions. Ecology Letters 8: 61-69.
CrossRef |
Gscholar
(25)
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
(26)
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
(27)
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
(28)
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
(29)
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
(30)
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
(31)
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
(32)
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
(33)
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
(34)
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
(35)
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
(36)
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
(37)
Schüssler A, Schwarzott D, Walker C (2001)A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
CrossRef |
Gscholar
(38)
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
(39)
Smith SE, Read DJ (2008)Mycorrhizal symbiosis (3rd edn). Academic Press, Amsterdam, the Netherlands, pp. 800.
Gscholar
(40)
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
(41)
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
(42)
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
(43)
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]
Gscholar
(44)
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
(45)
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
(46)
Wardle DA (2002)Communities and ecosystems. Linking the aboveground and belowground components. Princeton University Press, Princeton, NJ, USA, pp. 408.
Online |
Gscholar
(47)
Warren LO, Tadic M (1970)The fall webworm,
Hyphantria cunea (Durry). Arkansas Agricultural Experiment Station Bulletin 759:1-106.
Gscholar
(48)
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
(49)
Zhao S, Fernald RD (2005)Comprehensive algorithm for quantitative real-time polymerase chain reaction. Journal of Computational Biology 12: 1047-1064.
CrossRef |
Gscholar