{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T10:22:28Z","timestamp":1790418148004,"version":"4.1.0"},"reference-count":116,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T00:00:00Z","timestamp":1616457600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004543","name":"China Scholarship Council","doi-asserted-by":"publisher","award":["201404910206"],"award-info":[{"award-number":["201404910206"]}],"id":[{"id":"10.13039\/501100004543","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>Increasing demands to reduce fertilizer and pesticide input in agriculture has triggered interest in arbuscular mycorrhizal fungi (AMF) that can enhance plant growth and confer mycorrhiza-induced resistance (MIR). MIR can be based on a variety of mechanisms, including induction of defense compounds, and sensitization of the plant\u2019s immune system (priming) for enhanced defense against later arriving pests or pathogens signaled through jasmonic acid (JA). However, growth and resistance benefits of AMF highly depend on environmental conditions. Low soil P and non-limiting light conditions are expected to enhance MIR, as these conditions favor AMF colonization and because of observed positive cross-talk between the plant\u2019s phosphate starvation response (PSR) and JA-dependent immunity. We therefore tested growth and resistance benefits of the AMF<jats:italic>Funneliformis mosseae<\/jats:italic>in<jats:italic>Plantago lanceolata<\/jats:italic>plants grown under different levels of soil P and light intensity. Resistance benefits were assessed in bioassays with the leaf chewing herbivore<jats:italic>Mamestra brassicae<\/jats:italic>. Half of the plants were induced by jasmonic acid prior to the bioassays to specifically test whether AMF primed plants for JA-signaled defense under different abiotic conditions. AMF reduced biomass production but contrary to prediction, this reduction was not strongest under conditions considered least optimal for carbon-for-nutrient trade (low light, high soil P). JA application induced resistance to<jats:italic>M. brassicae<\/jats:italic>, but its extent was independent of soil P and light conditions. Strikingly, in younger plants, JA-induced resistance was annulled by AMF under high resource conditions (high soil P, ample light), indicating that AMF did not prime but repressed JA-induced defense responses. In older plants, low soil P and light enhanced susceptibility to<jats:italic>M. brassicae<\/jats:italic>due to enhanced leaf nitrogen levels and reduced leaf levels of the defense metabolite catalpol. By contrast, in younger plants, low soil P enhanced resistance. Our results highlight that defense priming by AMF is not ubiquitous and calls for studies revealing the causes of the increasingly observed repression of JA-mediated defense by AMF. Our study further shows that in our system abiotic factors are significant modulators of defense responses, but more strongly so by directly modulating leaf quality than by modulating the effects of beneficial microbes on resistance.<\/jats:p>","DOI":"10.3389\/fpls.2021.647372","type":"journal-article","created":{"date-parts":[[2021,3,23]],"date-time":"2021-03-23T06:55:10Z","timestamp":1616482510000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":37,"title":["Interactive Effects of Mycorrhizae, Soil Phosphorus, and Light on Growth and Induction and Priming of Defense in Plantago lanceolata"],"prefix":"10.3389","volume":"12","author":[{"given":"Laiye","family":"Qu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Minggang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arjen","family":"Biere","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,3,23]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1007\/s11738-012-1130-8","article-title":"Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants","volume":"35","author":"Andrade","year":"2013","journal-title":"Acta Physiol. Plant."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1111\/j.1365-2745.2006.01103.x","article-title":"Interactions between arbuscular mycorrhizal fungi and intraspecific competition affect size, and size inequality, of Plantago lanceolata L","volume":"94","author":"Ayres","year":"2006","journal-title":"J. Ecol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"697","DOI":"10.14348\/molcells.2017.0192","article-title":"Cross-talk between phosphate starvation and other environmental stress signaling pathways in plants","volume":"40","author":"Baek","year":"2017","journal-title":"Mol. Cell"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"171","DOI":"10.1093\/jpe\/rts026","article-title":"Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus","volume":"6","author":"Barber","year":"2013","journal-title":"J. Plant Ecol."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"338","DOI":"10.3389\/fpls.2013.00338","article-title":"Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem","volume":"4","author":"Barber","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1086\/650722","article-title":"The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis","volume":"175","author":"Barton","year":"2010","journal-title":"Am. Nat."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1086\/499379","article-title":"Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis","volume":"167","author":"Bennett","year":"2006","journal-title":"Am. Nat."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1007\/s00442-009-1338-5","article-title":"Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory","volume":"160","author":"Bennett","year":"2009","journal-title":"Oecologia"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"747","DOI":"10.3389\/fpls.2018.00747","article-title":"Belowground inoculation with arbuscular mycorrhizal fungi increases local and systemic susceptibility of rice plants to different pest organisms","volume":"9","author":"Bernaola","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1111\/1365-2435.12100","article-title":"Three-way interactions between plants, microbes and insects","volume":"27","author":"Biere","year":"2013","journal-title":"Funct. Ecol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1007\/s00442-004-1603-6","article-title":"Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs?","volume":"140","author":"Biere","year":"2004","journal-title":"Oecologia"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1016\/j.tree.2005.05.001","article-title":"Facing herbivory as you grow up: the ontogeny of resistance in plants","volume":"20","author":"Boege","year":"2005","journal-title":"Trends Ecol. Evol."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1778","DOI":"10.2307\/1939936","article-title":"Effects of plant age, genotype, and herbivory on Plantago performance and chemistry","volume":"74","author":"Bowers","year":"1993","journal-title":"Ecology"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1002","DOI":"10.1111\/j.1365-313X.2010.04385.x","article-title":"Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning","volume":"64","author":"Breuillin","year":"2010","journal-title":"Plant J."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"e1001102","DOI":"10.1371\/journal.pgen.1001102","article-title":"A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis","volume":"6","author":"Bustos","year":"2010","journal-title":"PLoS Genet."},{"key":"ref200","first-page":"539","article-title":"Mycorrhiza-induced resistance: more than the sum of its parts?","volume-title":"Trends Plant Sci.","author":"Cameron","year":"2013"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1038\/nature21417","article-title":"Root microbiota drive direct integration of phosphate stress and immunity","volume":"543","author":"Castrillo","year":"2017","journal-title":"Nature"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1046\/j.1469-8137.2003.00654.x","article-title":"Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis","volume":"157","author":"Cavagnaro","year":"2003","journal-title":"New Phytol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1146\/annurev-arplant-042110-103849","article-title":"Signaling network in sensing phosphate availability in plants","volume":"62","author":"Chiou","year":"2011","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref20","doi-asserted-by":"crossref","DOI":"10.1007\/978-981-10-2854-0","volume-title":"Plant-microbe interaction: An approach to sustainable agriculture. Singapore: springer.","author":"Choudhary","year":"2016"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1111\/j.2006.0030-1299.14928.x","article-title":"The effects of plant quality on caterpillar growth and defense against natural enemies","volume":"115","author":"Coley","year":"2006","journal-title":"Oikos"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1146\/annurev-phyto-080614-120132","article-title":"Priming for enhanced defense","volume":"53","author":"Conrath","year":"2015","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1023\/A:1020991229072","article-title":"Effects of herbivore damage and nutrient level on induction of iridoid glycosides in Plantago lanceolata","volume":"25","author":"Darrow","year":"1999","journal-title":"J. Chem. Ecol."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1007\/s00442-009-1312-2","article-title":"Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L","volume":"160","author":"De Deyn","year":"2009","journal-title":"Oecologia"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"1789","DOI":"10.1104\/pp.106.093971","article-title":"WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis","volume":"143","author":"Devaiah","year":"2007","journal-title":"Plant Physiol."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1078\/1439-1791-00129","article-title":"Induced plant defences: from molecular biology to evolutionary ecology","volume":"4","author":"Dicke","year":"2003","journal-title":"Basic Appl. Ecol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1086\/285436","article-title":"The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago\u2014a test of the carbon nutrient balance hypothesis","volume":"140","author":"Fajer","year":"1992","journal-title":"Am. Nat."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"646","DOI":"10.1111\/nph.12827","article-title":"Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants","volume":"203","author":"Fellbaum","year":"2014","journal-title":"New Phytol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1007\/s10886-009-9654-0","article-title":"The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L","volume":"35","author":"Fontana","year":"2009","journal-title":"J. Chem. Ecol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.soilbio.2018.08.019","article-title":"Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations","volume":"126","author":"Frew","year":"2018","journal-title":"Soil Biol. Biochem."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"1723","DOI":"10.1023\/B:JOEC.0000042398.13765.83","article-title":"Patterns of iridoid glycoside production and induction in Plantago lanceolata and the importance of plant age","volume":"30","author":"Fuchs","year":"2004","journal-title":"J. Chem. Ecol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1111\/j.1469-8137.1994.tb03989.x","article-title":"Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata","volume":"128","author":"Gange","year":"1994","journal-title":"New Phytol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1603\/022.038.0111","article-title":"Mycorrhizal fungal-plant-insect interactions: the importance of a community approach","volume":"38","author":"Gehring","year":"2009","journal-title":"Environ. Entomol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1111\/nph.12169","article-title":"Contrasting arbuscular mycorrhizal communities colonising different host plants show a similar response to a soil phosphorus concentration gradient","volume":"198","author":"Gosling","year":"2013","journal-title":"New Phytol."},{"key":"ref300","doi-asserted-by":"publisher","first-page":"938","DOI":"10.1111\/j.1469-8137.2008.02720.x","article-title":"Arbuscular mycorrhizal inhibition of growth in barley cannot be attributed to extent of colonization, fungal phosphorus uptake or effects on expression of plant phosphate transporter genes","volume":"181","author":"Grace","year":"2009","journal-title":"New Phytol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1890\/11-1358.1","article-title":"Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi","volume":"93","author":"Grman","year":"2012","journal-title":"Ecology"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"2294","DOI":"10.1038\/ismej.2017.90","article-title":"Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture","volume":"11","author":"Hannula","year":"2017","journal-title":"ISME J."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1146\/annurev.ento.54.110807.090614","article-title":"Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context","volume":"54","author":"Hartley","year":"2009","journal-title":"Annu. Rev. Entomol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1007\/s10886-005-1341-1","article-title":"Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids","volume":"31","author":"Harvey","year":"2005","journal-title":"J. Chem. Ecol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1139\/b86-162","article-title":"The influence of phosphorus fertilization, drought, fungal species, and nonsterile soil on mycorrhizal growth response in tall grass prairie plants","volume":"64","author":"Hetrick","year":"1983","journal-title":"Can. J. Bot."},{"key":"ref40","first-page":"1","volume-title":"The water culture method for growing plants without soil","author":"Hoagland","year":"1950"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1111\/j.1461-0248.2009.01430.x","article-title":"A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi","volume":"13","author":"Hoeksema","year":"2010","journal-title":"Ecol. Lett."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1034\/j.1600-0706.2000.880216.x","article-title":"Effects of plant phenology, nutrients and herbivory on growth and defensive chemistry of plantain, Plantago lanceolata","volume":"88","author":"Jarzomski","year":"2000","journal-title":"Oikos"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1111\/j.1469-8137.2009.03110.x","article-title":"Tansley review: resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales","volume":"185","author":"Johnson","year":"2010","journal-title":"New Phytol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1473","DOI":"10.1111\/nph.13172","article-title":"Mycorrhizal phenotypes and the law of the minimum","volume":"205","author":"Johnson","year":"2015","journal-title":"New Phytol."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1007\/s10886-012-0134-6","article-title":"Mycorrhiza-induced resistance and priming of plant defenses","volume":"38","author":"Jung","year":"2012","journal-title":"J. Chem. Ecol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1111\/j.1365-3040.2011.02455.x","article-title":"Growth, respiration and nutrient acquisition by the arbuscular mycorrhizal fungus Glomus mosseae and its host plant Plantago lanceolata in cooled soil","volume":"35","author":"Karasawa","year":"2012","journal-title":"Plant Cell Environ."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"335","DOI":"10.3390\/metabo10080335","article-title":"Unraveling arbuscular mycorrhiza-induced changes in plant primary and secondary metabolome","volume":"10","author":"Kaur","year":"2020","journal-title":"Meta"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1104\/pp.16.00278","article-title":"Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory","volume":"171","author":"Khan","year":"2016","journal-title":"Plant Physiol."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"782","DOI":"10.3389\/fpls.2016.00782","article-title":"Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation","volume":"7","author":"Konvalinkova","year":"2016","journal-title":"Front. Plant Sci."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"65","DOI":"10.3389\/fpls.2015.00065","article-title":"Duration and intensity of shade differentially affects mycorrhizal growth and phosphorus uptake responses of Medicago truncatula","volume":"6","author":"Konvalinkova","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"2088","DOI":"10.1890\/08-1555.1","article-title":"Effects of mycorrhizal fungi on insect herbivores: a meta-analysis","volume":"90","author":"Koricheva","year":"2009","journal-title":"Ecology"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1111\/j.1469-8137.2007.02268.x","article-title":"A new model of carbon and phosphorus transfers in arbuscular mycorrhizas","volume":"177","author":"Landis","year":"2008","journal-title":"New Phytol."},{"key":"ref400","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1111\/j.1469-8137.2008.02410.x","article-title":"Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain?","volume":"178","author":"Li","year":"2008","journal-title":"New Phytol."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/PL00012667","article-title":"Two herbivore-deterrent iridoid glycosides reduce the in-vitro growth of a specialist but not of a generalist pathogenic fungus of Plantago lanceolata L","volume":"12","author":"Marak","year":"","journal-title":"Chemoecology"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"2429","DOI":"10.1023\/A:1021475800765","article-title":"Systemic, genotype-specific induction of two herbivore-deterrent iridoid glycosides in Plantago lanceolata L. in response to fungal infection by Diaporthe adunca (rob.) Niessel","volume":"28","author":"Marak","year":"","journal-title":"J. Chem. Ecol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"2519","DOI":"10.1111\/j.0014-3820.2003.tb01496.x","article-title":"Fitness costs of chemical defense in Plantago lanceolata L.: effects of nutrient and competition stress","volume":"57","author":"Marak","year":"2003","journal-title":"Evolution"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"818","DOI":"10.1016\/j.tplants.2016.07.009","article-title":"Recognizing plant defense priming","volume":"21","author":"Martinez-Medina","year":"2016","journal-title":"Trends Plant Sci."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1146\/annurev-arplant-042916-041132","article-title":"Defense priming: an adaptive part of induced resistance","volume":"68","author":"Mauch-Mani","year":"2017","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1111\/j.1469-8137.1990.tb00476.x","article-title":"A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi","volume":"115","author":"McGonigle","year":"1990","journal-title":"New Phytol."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"e0136073","DOI":"10.1371\/journal.pone.0136073","article-title":"Light and nutrient dependent responses in secondary metabolites of Plantago lanceolata offspring are due to phenotypic plasticity in experimental grasslands","volume":"10","author":"Miehe-Steier","year":"2015","journal-title":"PLoS One"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1111\/pce.12209","article-title":"Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum?","volume":"37","author":"Miller","year":"2014","journal-title":"Plant Cell Environ."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"157","DOI":"10.5091\/plecevo.2016.1176","article-title":"Effects of arbuscular mycorrhizal fungi on herbivory defense in two Solanum (Solanaceae) species","volume":"149","author":"Minton","year":"2016","journal-title":"Plant Ecol. Evol."},{"key":"ref500","doi-asserted-by":"publisher","first-page":"1238","DOI":"10.3389\/fmicb.2019.01238","article-title":"Arbuscular mycorrhizal symbiosis: plant friend or foe in the fight against viruses?","volume":"10","author":"Miozzi","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1111\/j.1365-3040.2006.01608.x","article-title":"Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus","volume":"30","author":"Morcuende","year":"2007","journal-title":"Plant Cell Environ."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1016\/j.pbi.2019.05.004","article-title":"Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis","volume":"50","author":"Mueller","year":"2019","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/S0003-2670(00)88444-5","article-title":"A modified single solution method for determination of phosphate in natural waters","volume":"27","author":"Murphy","year":"1962","journal-title":"Anal. Chim. Acta"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1007\/s00572-016-0698-z","article-title":"Phosphorus supply, arbuscular mycorrhizal fungal species, and plant genotype impact on the protective efficacy of mycorrhizal inoculation against wheat powdery mildew","volume":"26","author":"Mustafa","year":"2016","journal-title":"Mycorrhiza"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"950","DOI":"10.1111\/j.1469-8137.2008.02721.x","article-title":"Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated","volume":"181","author":"Nagy","year":"2009","journal-title":"New Phytol."},{"key":"ref600","doi-asserted-by":"publisher","first-page":"1298","DOI":"10.3389\/fmicb.2020.01298","article-title":"Modulation of plant defense system in response to microbial interactions","volume":"11","author":"Nishad","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref67","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1111\/j.1574-6941.2009.00833.x","article-title":"Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits","volume":"72","author":"Olsson","year":"2010","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.envpol.2012.04.026","article-title":"Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in Plantago lanceolata L","volume":"168","author":"Orlowska","year":"2012","journal-title":"Environ. Pollut."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.phytochem.2013.04.016","article-title":"Role of plant beta-glucosidases in the dual defense system of iridoid glycosides and their hydrolyzing enzymes in Plantago lanceolata and Plantago major","volume":"94","author":"Pankoke","year":"2013","journal-title":"Phytochemistry"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.phytochem.2015.07.014","article-title":"The effects of mineral nitrogen limitation, competition, arbuscular mycorrhiza, and their respective interactions, on morphological and chemical plant traits of Plantago lanceolata","volume":"118","author":"Pankoke","year":"2015","journal-title":"Phytochemistry"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1146\/annurev-phyto-082712-102340","article-title":"Induced systemic resistance by beneficial microbes","volume":"52","author":"Pieterse","year":"2014","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"1073","DOI":"10.1111\/nph.15754","article-title":"Tansley review: a meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance","volume":"223","author":"Poorter","year":"2019","journal-title":"New Phytol."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1016\/j.pbi.2007.05.004","article-title":"Unraveling mycorrhiza-induced resistance","volume":"10","author":"Pozo","year":"2007","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"1431","DOI":"10.1111\/nph.13252","article-title":"Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses","volume":"205","author":"Pozo","year":"2015","journal-title":"New Phytol."},{"key":"ref75","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1007\/BF01022550","article-title":"Effect of qualitative and quantitative variation in allelochemicals on generalist insects: iridoid glycosides and the southern army worm","volume":"14","author":"Puttick","year":"1988","journal-title":"J. Chem. Ecol."},{"key":"ref76","doi-asserted-by":"publisher","first-page":"992","DOI":"10.1007\/s10886-011-0007-4","article-title":"Plant induced defenses depend more on plant age than previous history of damage: implications for plant-herbivore interactions","volume":"37","author":"Quintero","year":"2011","journal-title":"J. Chem. Ecol."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1007\/s00442-011-2114-x","article-title":"Changes in plant chemical defenses and nutritional quality as a function of ontogeny in Plantago lanceolata (Plantaginaceae)","volume":"168","author":"Quintero","year":"2012","journal-title":"Oecologia"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1007\/s00572-019-00920-3","article-title":"Increased maize growth and P uptake promoted by arbuscular mycorrhizal fungi coincide with higher foliar herbivory and larval biomass of the fall armyworm Spodoptera frugiperda","volume":"29","author":"Real-Santill\u00e1n","year":"2019","journal-title":"Mycorrhiza"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/S0176-1617(11)80844-8","article-title":"Interactions in the tripartite symbiosis of pea (Pisum sativum L) Glomus and rhizobium under non-limiting phosphorus supply","volume":"141","author":"Reinhard","year":"1993","journal-title":"J. Plant Physiol."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1007\/s10886-011-9983-7","article-title":"Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata","volume":"37","author":"Reudler","year":"2011","journal-title":"J. Chem. Ecol."},{"key":"ref81","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1023\/A:1007792332046","article-title":"Flight and oviposition behavior toward different host plant species by the cabbage moth, Mamestra brassicae (L.) (Lepidoptera: Noctuidae)","volume":"13","author":"Rojas","year":"2000","journal-title":"J. Insect Behav."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1093\/mp\/ssp120","article-title":"Regulation of phosphate starvation responses in plants: signaling players and cross-talks","volume":"3","author":"Rouached","year":"2010","journal-title":"Mol. Plant"},{"key":"ref83","doi-asserted-by":"publisher","first-page":"2432","DOI":"10.1104\/pp.16.00031","article-title":"Arabidopsis MYC transcription factors are the target of hormonal salicylic acid\/jasmonic acid cross talk in response to Pieris brassicae egg extract","volume":"170","author":"Schmiesing","year":"2016","journal-title":"Plant Physiol."},{"key":"ref84","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780198525943.001.0001","volume-title":"Insect-plant biology","author":"Schoonhoven","year":"2005"},{"key":"ref85","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/S0176-1617(11)81054-0","article-title":"Occurrence of trehalose in vesicular-arbuscular mycorrhizal fungi and in mycorrhizal roots","volume":"140","author":"Schubert","year":"1992","journal-title":"J. Plant Physiol."},{"key":"ref86","doi-asserted-by":"publisher","first-page":"3886","DOI":"10.1038\/ncomms4886","article-title":"High specificity in plant leaf metabolic responses to arbuscular mycorrhiza","volume":"5","author":"Schweiger","year":"","journal-title":"Nat. Comm."},{"key":"ref87","doi-asserted-by":"publisher","first-page":"1574","DOI":"10.1111\/pce.12257","article-title":"Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types","volume":"37","author":"Schweiger","year":"","journal-title":"Plant Cell Environ."},{"key":"ref88","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1146\/annurev.en.26.010181.001151","article-title":"The nutritional ecology of immature insects","volume":"26","author":"Scriber","year":"1981","journal-title":"Annu. Rev. Entomol."},{"key":"ref89","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1007\/s13199-015-0319-1","article-title":"Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect","volume":"65","author":"Shrivastava","year":"2015","journal-title":"Symbiosis"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1111\/j.1570-7458.1983.tb03245.x","article-title":"An artificial diet for sorghum shootfly larvae","volume":"33","author":"Singh","year":"1983","journal-title":"Entomol. Exp. Appl."},{"key":"ref91","volume-title":"Mycorrhizal Symbiosis","author":"Smith","year":"2008"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1146\/annurev-arplant-042110-103846","article-title":"Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales","volume":"62","author":"Smith","year":"2011","journal-title":"Annu. Rev. Plant Biol."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3852\/11-229","article-title":"Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth","volume":"104","author":"Smith","year":"2012","journal-title":"Mycologia"},{"key":"ref94","doi-asserted-by":"publisher","first-page":"1036","DOI":"10.1007\/s10886-013-0312-1","article-title":"Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway","volume":"39","author":"Song","year":"2013","journal-title":"J. Chem. Ecol."},{"key":"ref95","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1002\/jpln.201700569","article-title":"Phosphorus fertilization reduces the severity of charcoal rot (Macrophomina phaseolina) and the arbuscular mycorrhizal protection in soybean","volume":"181","author":"Spagnoletti","year":"2018","journal-title":"J. Plant Nutr. Soil Sci."},{"key":"ref96","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.1111\/j.1469-8137.2011.03768.x","article-title":"Mining for treatment-specific and general changes in target compounds and metabolic fingerprints in response to herbivory and phytohormones in Plantago lanceolata","volume":"191","author":"Sutter","year":"2011","journal-title":"New Phytol."},{"key":"ref97","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1626\/jcs.70.548","article-title":"Effects of temperature, shade, and nitrogen application on the growth and accumulation of bioactive compounds in cultivars of Plantago lanceolata L","volume":"70","author":"Tamura","year":"2001","journal-title":"Jpn. J. Crop Sci."},{"key":"ref98","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1111\/1365-2745.12535","article-title":"Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms","volume":"104","author":"Tao","year":"2016","journal-title":"J. Ecol."},{"key":"ref99","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1007\/s10886-016-0785-9","article-title":"Effects of arbuscular mycorrhiza on plant chemistry and the development and behavior of a generalist herbivore","volume":"42","author":"Tomczak","year":"2016","journal-title":"J. Chem. Ecol."},{"key":"ref100","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1023\/a:1010341022761","article-title":"Ontogeny constrains systemic protease inhibitor response in Nicotiana attenuata","volume":"27","author":"Van Dam","year":"2001","journal-title":"J. Chem. Ecol."},{"key":"ref101","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1016\/j.pbi.2008.05.005","article-title":"Plant immune responses triggered by beneficial microbes","volume":"11","author":"Van Wees","year":"2008","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref102","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1111\/j.1461-9563.2009.00445.x","article-title":"Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems","volume":"11","author":"Vannette","year":"2009","journal-title":"Agric. For. Entomol."},{"key":"ref103","doi-asserted-by":"publisher","first-page":"361","DOI":"10.3389\/fpls.2013.00361","article-title":"Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species","volume":"4","author":"Vannette","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref104","doi-asserted-by":"publisher","first-page":"5004","DOI":"10.1128\/AEM.64.12.5004-5007.1998","article-title":"Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi","volume":"64","author":"Vierheilig","year":"1998","journal-title":"Appl. Environ. Microbiol."},{"key":"ref105","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1016\/S0038-0717(99)00155-8","article-title":"Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi","volume":"32","author":"Vierheilig","year":"2000","journal-title":"Soil Biol. Biochem."},{"key":"ref106","doi-asserted-by":"publisher","first-page":"15159","DOI":"10.1038\/nplants.2015.159","article-title":"Regulation of resource exchange in the arbuscular mycorrhizal symbiosis","volume":"1","author":"Walder","year":"2015","journal-title":"Nat. Plants"},{"key":"ref107","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1007\/s10886-015-0644-0","article-title":"Effects of the timing of herbivory on plant defense induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status","volume":"41","author":"Wang","year":"2015","journal-title":"J. Chem. Ecol."},{"key":"ref108","doi-asserted-by":"publisher","first-page":"365","DOI":"10.3390\/insects11060365","article-title":"Effect of different combinations of phosphorus and nitrogen fertilization on arbuscular mycorrhizal fungi and aphids in wheat","volume":"11","author":"Wang","year":"2020","journal-title":"Insects"},{"key":"ref700","doi-asserted-by":"publisher","first-page":"2860","DOI":"10.1111\/pce.13632","article-title":"Beneficial microbes going underground of root immunity","volume":"42","author":"Yu","year":"2019","journal-title":"Plant Cell Environ."},{"key":"ref109","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/j.ejsobi.2011.03.001","article-title":"Soil sand content can alter effects of different taxa of mycorrhizal fungi on plant biomass production of grassland species","volume":"47","author":"Zaller","year":"2011","journal-title":"Eur. J. Soil Biol."},{"key":"ref110","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1094\/MPMI-06-11-0179","article-title":"Modulation of host immunity by beneficial microbes","volume":"25","author":"Zamioudis","year":"2012","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref111","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1111\/nph.13025","article-title":"Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist","volume":"205","author":"Zheng","year":"2015","journal-title":"New Phytol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.647372\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,26]],"date-time":"2024-08-26T16:13:07Z","timestamp":1724688787000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2021.647372\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,23]]},"references-count":116,"alternative-id":["10.3389\/fpls.2021.647372"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2021.647372","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,23]]},"article-number":"647372"}}