Quantifying the associations between fungal endophytes and biocontrol-induced herbivory of invasive purple loosestrife (Lythrum salicaria L.)

Literature cited

• AbarenkovKNilssonRHLarssonKHAlexanderIJEberhardtUErlandSHøilandKKjøllerRLarssonEPennanenTSenRTaylorAFSTedersooLUrsingBMVrålstadTLiimatainenKPeintnerUKõljalgU. 2010. The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285, doi:10.1111/j.1469-8137.2009.03160.x
   PubMed Web of Science ®Google Scholar
• AbràmoffM. 2004. Image processing with ImageJ. Biophotonics 11:36–42.
   Google Scholar
• AlbrectsenBRBjörkénLVaradAHagnerÅWedinMKarlssonJJanssonS. 2010. Endophytic fungi in European aspen (Populus tremula) leaves—diversity, detection and a suggested correlation with herbivory resistance. Fungal Divers 41:17–28, doi:10.1007/s13225-009-0011-y
   Web of Science ®Google Scholar
• Almeida-NetoMGuimaraesP. 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 1227–1239, doi:10.1111/j.2008.0030-1299.16644.x
   Google Scholar
• ArnoldAE. 2007. Understanding the diversity of foliar endophytic fungi: progress, challenges and frontiers. Fungal Biol Rev 21:51–66, doi:10.1016/j.fbr.2007.05.003
   Google Scholar
• ArnoldAEHenkDEellsRLLutzoniFVilgalysR. 2007. Diversity and phylogenetic affinities of foliar fungal endophytes in loblolly pine inferred by culturing and environmental PCR. Mycologia 99:185–206, doi:10.3852/mycologia.99.2.185
   PubMed Web of Science ®Google Scholar
• ArnoldAEMejíaLCKylloDRojasEIMaynardZRobbinsNHerreEA. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654, doi:10.1073/pnas.2533483100
   PubMed Web of Science ®Google Scholar
• AschehougEMetlenKCallawayRNewcombeG. 2012. Fungal endophytes directly increase the competitive effects of an invasive forb. Ecology 93:3–8, doi:10.1890/11-1347.1
   PubMed Web of Science ®Google Scholar
• BarberNAMarquisRJ. 2011. Leaf quality, predators and stochastic processes in the assembly of a diverse herbivore community. Ecology 92:699–708, doi:10.1890/10-0125.1
   Google Scholar
• BatesDMächlerMBolkerBWalkerS. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–51, doi:10.18637/jss.v067.i01
   Web of Science ®Google Scholar
• BennettAE. 2013. Can plant-microbe-insect interactions enhance or inhibit the spread of invasive species? Funct Ecol 27:661–671, doi:10.1111/1365-2435.12099
   Google Scholar
• BlaalidRDaveyMLKauserudHCarlsenTHalvorsenRHøilandKEidesenPB. 2014. Arctic root-associated fungal community composition reflects environmental filtering. Mol Ecol 23:649–59, doi:10.1111/mec.12622
   Web of Science ®Google Scholar
• BlosseyBSkinnerLCTaylorJ. 2001. Impact and management of purple loosestrife (Lythrum salicaria) in North America. p. 1787–1807.
   Google Scholar
• BorerETKinkelLLMayGSeabloomEW. 2013. The world within: quantifying the determinants and outcomes of a host’s microbiome. Basic Appl Ecol 14:533–539, doi:10.1016/j.baae.2013.08.009
   Google Scholar
• BusbyPEPeayKGNewcombeG. 2015. Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity. New Phytol 209:1681–1692, doi:10.1111/nph.13742
   Google Scholar
• CaporasoJGKuczynskiJStombaughJBittingerKBushmanFDCostelloEKFiererNPeñaAGGoodrichJKGordonJIHuttleyGAKelleySTKnightsDKoenigJELeyRELozuponeCAMcDonaldDMueggeBDPirrungMReederJSevinskyJRTurnbaughPJWaltersWAWidmannJYatsunenkoTZaneveldJKnightR. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336, doi:10.1038/nmeth.f.303
   PubMed Web of Science ®Google Scholar
• CordierTRobinCCapdevielleXDesprez-LoustauM-LVacherC. 2012. Spatial variability of phyllosphere fungal assemblages: genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica). Fungal Ecol 5:509–520, doi:10.1016/j.funeco.2011.12.004
   Web of Science ®Google Scholar
• DavidASKaserJMMoreyACRothAMAndowDA. 2013. Release of genetically engineered insects: a framework to identify potential ecological effects. Ecol Evol 3:4000–4015, doi:10.1002/ece3.737
   PubMed Web of Science ®Google Scholar
• DavidASSeabloomEWMayG. 2016. Plant host species and geographic distance affect the structure of aboveground fungal symbiont communities, and environmental filtering affects belowground communities in a coastal dune ecosystem. Microb Ecol, doi:10.1007/s00248-015-0712-6
   Google Scholar
• de CalAPascualSMelgarejoP. 1997. Involvement of resistance induction by Penicillum oxalicum in the biocontrol of tomato wilt. Plant Pathol 46:72–79, doi:10.1046/j.1365-3059.1997.d01-204.x
   Web of Science ®Google Scholar
• de la PeñaEEcheverríaSRvan der PuttenWHFreitasHMoensM. 2006. Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829–840, doi:10.1111/j.1469-8137.2005.01602.x
   PubMed Web of Science ®Google Scholar
• DevarajanPTSuryanarayananTS. 2006. Evidence for the role of phytophagous insects in dispersal of non-grass fungal endophytes. p. 111–119.
   Google Scholar
• de VosMvan ZaanenWKoornneefAKorzeliusJPDickeMvan LoonLCPieterseCMJ. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol 142:352–363, doi:10.1104/pp.106.083907
   PubMed Web of Science ®Google Scholar
• DolinarNGaberscikA. 2010. Mycorrhizal colonization and growth of Phragmites australis in an intermittent wetland. Aquat Bot 93:93–98, doi:10.1016/j.aquabot.2010.03.012
   Google Scholar
• EdgarRCHaasBJClementeJCQuinceCKnightR. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200, doi:10.1093/bioinformatics/btr381
   PubMed Web of Science ®Google Scholar
• EvansH. 2008. The endophyte-enemy release hypothesis: implications for classical biological control and plant invasions. Proceedings of the 12th International Symposium.
   Google Scholar
• FröhlichJHydeKPetriniO. 2000. Endophytic fungi associated with palms. Mycol Res 104:1202–1212, doi:10.1017/S095375620000263X
   Google Scholar
• GardesMBrunsT. 1993. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118, doi:10.1111/j.1365-294X.1993.tb00005.x
   PubMed Web of Science ®Google Scholar
• GripenbergSRoslinT. 2005. Host plants as islands: resource quality and spatial setting as determinants of insect distribution. p. 335–345.
   Google Scholar
• GrünigCSieberTRogersSHoldenriederO. 2002. Spatial distribution of dark septate endophytes in a confined forest plot. Mycol Res 106:832–840, doi:10.1017/S0953756202005968
   Google Scholar
• HatcherPE. 1995. Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biol Rev 70:639–694, doi:10.1111/j.1469-185X.1995.tb01655.x
   Web of Science ®Google Scholar
• HayesLFowlerSVPaynterQGroentemanRPetersonPDoddSBellgardS. 2013. Biocontrol of weeds: achievements to date and future outlook. p. 375–385.
   Google Scholar
• HigginsKLArnoldAEColeyPDKursarT. 2014. Communities of fungal endophytes in tropical forest grasses: highly diverse host and habitat generalists characterized by strong spatial structure. Fungal Ecol 8:1–11, doi:10.1016/j.funeco.2013.12.005
   Web of Science ®Google Scholar
• HumphreyPTNguyenTTVillalobosMMWhitemanNK. 2014. Diversity and abundance of phyllosphere bacteria are linked to insect herbivory. Mol Ecol 23:1497–1515, doi:10.1111/mec.12657
   Google Scholar
• KearseMMoirRWilsonAStones-HavasSCheungMSturrockSBuxtonSCooperAMarkowitzSDuranCThiererTAshtonBMeintjesPDrummondAAAshtonBBuxtonSCheungMCooperAHeledJKearseMMoirRStones-HavasSSturrockSThiererTWilsonA. 2012. Geneious. Bioinformatics 28:1647–1649, doi:10.1093/bioinformatics/bts199
   PubMed Web of Science ®Google Scholar
• KivlinSNEmerySMRudgersJ. 2013. Fungal symbionts alter plant responses to global change. Am J Bot 100:1445–1457, doi:10.3732/ajb.1200558
   PubMed Web of Science ®Google Scholar
• LindgrenCJ. 2003. Using 1-min scans and stem height data in a post-release monitoring strategy for Galerucella calmariensis (L.) (Coleoptera: Chrysomelidae) on purple loosestrife, Lythrum salicaria L. (Lythraceae), in Manitoba. Biol Control 27:201–209, doi:10.1016/S1049-9644(03)00006-9
   Google Scholar
• MalTLovett-DoustJLovett-DoustLMulliganGA. 1992. The biology of Canadian weeds. 100. Lythrum salicaria. Can J Bot 1330:1305–1330.
   Google Scholar
• MaleckiRABlosseyBHightSDSchroederDKokLTCoulsonJR. 1993. Biological control of purple loosestrife. Bioscience 43:680–686, doi:10.2307/1312339
   Web of Science ®Google Scholar
• McIntireEFajardoA. 2009. Beyond description: the active and effective way to infer processes from spatial patterns. Ecology 90:46–56, doi:10.1890/07-2096.1
   PubMed Web of Science ®Google Scholar
• MonacellJTCarboneI. 2014. Mobyle SNAP workbench: a web-based analysis portal for population genetics and evolutionary genomics. Bioinformatics 30:1–3, doi:10.1093/bioinformatics/btu055
   Google Scholar
• NewcombeGShipunovAEigenbrodeSDRaghavendraAKHDingHAndersonCLMenjivarRCrawfordMSchwarzländerM. 2009. Endophytes influence protection and growth of an invasive plant. p. 29–31, doi:10.3732/ajb.0800024.www.landesbioscience.com
   Google Scholar
• NguyenNHSmithDPPeayKKennedyP. 2014. Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol. doi:10.1111/nph.12923
   Google Scholar
• NilssonRHVeldreVHartmannMUnterseherMAmendABergstenJKristianssonERybergMJumpponenAAbarenkovK. 2010. An open source software package for automated extraction of ITS1 and ITS2 from fungal ITS sequences for use in high-throughput community assays and molecular ecology. Fungal Ecol 3:284–287, doi:10.1016/j.funeco.2010.05.002
   Web of Science ®Google Scholar
• OksanenJBlanchetFGKindtRLegendrePMinchinPRO’HaraRBSimpsonGLSolymosPStevensMHHWagnerH. 2013. Package vegan. R Packag 20–28. 254 p.
   Google Scholar
• OlsrudMCarlssonBÅSvenssonBMMichelsenAMelilloJM. 2009. Responses of fungal root colonization, plant cover and leaf nutrients to long-term exposure to elevated atmospheric CO2 and warming in a subarctic birch forest understory. Glob Chang Biol 16:1820–1829, doi:10.1111/j.1365-2486.2009.02079.x
   Web of Science ®Google Scholar
• OsonoT. 2006. Role of phyllosphere fungi of forest trees in the development of decomposer fungal communities and decomposition processes of leaf litter. doi:10.1139/W06-023
   Google Scholar
• PanJJMayG. 2009. Fungal-fungal associations affect the assembly of endophyte communities in maize (Zea mays). Microb Ecol 58:668–78, doi:10.1007/s00248-009-9543-7
   PubMed Web of Science ®Google Scholar
• PetriniO. 1991. Fungal endophytes of tree leaves. In: AndrewsJHHiranoS, eds. Microbial ecology of leaves. New York: Springer-Verlag. p. 179–197.
   Google Scholar
• PittJI. 2002. Biology and ecology of toxigenic Penicillium species. In: DeVriesJWTrucksessMWJacksonLS, eds. Advances in experimental medicine and biology. New York: Springer-Science+Business Media LLC. p. 29–41.
   Google Scholar
• PurahongWHydeKD. 2010. Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7, doi:10.1007/s13225-010-0083-8
   Google Scholar
• Quadt-HallmannA. 1997. Bacterial endophytes in cotton: mechanisms of entering the plant. Can J Microbiol 582:577–582, doi:10.1139/m97-081
   Google Scholar
• QuiramG. 2013. The ecology and evolution of an invasive perennial plant (Lythrum salicaria) in the context of biological control by specialist herbivores (Galerucella spp.) [doctoral dissertation]. Univ. Minnesota Press. 253 p.
   Google Scholar
• R Development Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org/) R Found Stat Comput Vienna.
   Google Scholar
• RodriguezRJWhiteJFArnoldAERedmanRS. 2009. Fungal endophytes: diversity and functional roles. New Phytol. 182:314–30, doi:10.1111/j.1469-8137.2009.02773.x
   PubMed Web of Science ®Google Scholar
• RudgersJAClayK. 2008. An invasive plant-fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840, doi:10.1111/j.1461-0248.2008.01201.x
   Google Scholar
• RudgersJAKivlinSNWhitneyKDPriceMVWaserNMHarteJ. 2014. Responses of high-altitude graminoids and soil fungi to 20 years of experimental warming. Ecology, doi:doi.org/10.1890/13-1454.1
   Google Scholar
• RybergMKristianssonESjökvistENilssonRH. 2009. An outlook on the fungal internal transcribed spacer sequences in GenBank and the introduction of a web-based tool for the exploration of fungal diversity. New Phytol 181:471–477, doi:10.1111/j.1469-8137.2008.02667.x
   PubMed Web of Science ®Google Scholar
• SandbergDCBattistaLJArnoldAE. 2014. Fungal endophytes of aquatic macrophytes: diverse host generalists characterized by tissue preferences and geographic structure. Microb Ecol 67:735–747, doi:10.1007/s00248-013-0324-y
   Web of Science ®Google Scholar
• SaundersMGlennAEKohnLM. 2010. Exploring the evolutionary ecology of fungal endophytes in agricultural systems: using functional traits to reveal mechanisms in community processes. Evol Appl 3:525–537, doi:10.1111/j.1752-4571.2010.00141.x
   PubMed Web of Science ®Google Scholar
• SchardlCLLeuchtmannASpieringMJ. 2004. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340, doi:10.1146/annurev.arplant.55.031903.141735
   PubMed Web of Science ®Google Scholar
• SchlossPDWestcottSLRyabinTHallJRHartmannMHollisterEBLesniewskiRAOakleyBBParksDHRobinsonCJSahlJWStresBThallingerGGvan HornDJWeberCF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541, doi:10.1128/AEM.01541-09
   PubMed Web of Science ®Google Scholar
• ShipunovANewcombeGRaghavendraAKHAndersonCL. 2008. Hidden diversity of endophytic fungi in an invasive plant. Am J Bot 95:1096–1108, doi:10.3732/ajb.0800024
   PubMed Web of Science ®Google Scholar
• StoneLRobertsA. 1990. The checkerboard score and species distributions. Oecologia 74–79. In: SunYCaiYLiuLYuFFarrellMLFarmerieWMcKendreeW, eds. 2009. ESPRIT: estimating species richness using large collections of 16 rRNA pyrosequences. Nucleic Acids Res 37:1–13, doi:10.1093/nar/gkp285
   Google Scholar
• TackAJMOvaskainenOPulkkinenPRoslinT. 2010. Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology 91:2660–2672, doi:10.1890/09-1027.1
   Google Scholar
• ThommaB. 2003. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236, doi:10.1046/J.1364-3703.2003.00173.X
   PubMed Web of Science ®Google Scholar
• TscharntkeTBommarcoRCloughYCristTOKleijnDRandTTylianakisJMvan NouhuysSVidalS. 2008. Conservation biological control and enemy diversity on a landscape scale. Biol Control 45:238–253, doi:10.1016/S1049-9644(08)00082-0
   Google Scholar
• UlrichWGotelliNJ. 2007. Null model analysis of species nestedness patterns. Ecology 88:1824–1831, doi:10.1890/06-1208.1
   PubMed Web of Science ®Google Scholar
• UlrichWGotelliNJ. 2013. Pattern detection in null model analysis. Oikos 122:2–18, doi:10.1111/j.1600-0706.2012.20325.x
   Web of Science ®Google Scholar
• van BaelSAEstradaCRehnerSASantosJFWcisloWT. 2012. Leaf endophyte load influences fungal garden development in leaf-cutting ants. BMC Ecol 12:23, doi:10.1186/1472-6785-12-23
   Google Scholar
• van der PuttenWHVetLEMHarveyJWäckersFL. 2001. Linking above-and belowground multitrophic interactions of plants, herbivores, pathogens and their antagonists. Trends Ecol Evol 16:547–554, doi:10.1016/S0169-5347(01)02265-0
   Web of Science ®Google Scholar
• VilgalysRHesterM. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246.
   PubMed Web of Science ®Google Scholar
• WardleDBardgettRDKlironomosJNSetäläHvan der PuttenWHWallDH. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629–1633, doi:10.1126/science.1094875.
   PubMed Web of Science ®Google Scholar
• WrightDH. 1998. A comparative analysis of nested subset patterns of species composition. p. 1–20.
   Google Scholar
• YangFLiLYangB. 2012. Alternaria toxin-induced resistance against rose aphids and olfactory response of aphids to toxin-induced volatiles of rose plants. J Zhejiang Univ Sci B 13:126–135, doi:10.1631/jzus.B1100087
   Google Scholar
• YeatesAGSchoolerSSGaronoRJBuckleyYM. 2011. Biological control as an invasion process: disturbance and propagule pressure affect the invasion success of Lythrum salicaria biological control agents. Biol Invasions 14:255–271, doi:10.1007/s10530-011-0060-5
   Google Scholar
• ZimmermanNBVitousekPM. 2012. Fungal endophyte communities reflect environmental structuring across a Hawaiian landscape. Proc Natl Acad Sci U S A 109:13022–13027, doi:10.1073/pnas.1209872109
   Web of Science ®Google Scholar