In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula
BACKGROUND Trichoderma spp. are soil fungi that interact with plant roots and associated biota such as other microorganisms and soil fauna. However, information about their interactions with root‐feeding insects is limited. Here, interactions between Trichoderma harzianum and the root‐feeding insect...
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| Veröffentlicht in: | Pest management science 2021-09, Vol.77 (9), p.3952-3963 |
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| creator | Contreras‐Cornejo, Hexon Angel Macías‐Rodríguez, Lourdes Real‐Santillán, Raúl Omar López‐Carmona, Dante García‐Gómez, Griselda Galicia‐Gallardo, Ana Paola Alfaro‐Cuevas, Ruth González‐Esquivel, Carlos E Najera‐Rincón, Miguel Bernardo Adame‐Garnica, Sandra Goretti Rebollar‐Alviter, Angel Álvarez‐Navarrete, Mariana Larsen, John |
| description | BACKGROUND
Trichoderma spp. are soil fungi that interact with plant roots and associated biota such as other microorganisms and soil fauna. However, information about their interactions with root‐feeding insects is limited. Here, interactions between Trichoderma harzianum and the root‐feeding insect Phyllophaga vetula, a common insect pest in maize agroecosystems, were examined.
RESULTS
Applications of T. harzianum and P. vetula to the root system increased and decreased maize growth, respectively. Induced tolerance against herbivore attack was provided by T. harzianum maintaining a robust and functional root system as evidenced by the increased uptake of Cu, Ca, Mg, Na and K. Herbivore tolerance also coincided with changes in the emission of root volatile terpenes known to induce indirect defense responses and attract natural enemies of the herbivore. More importantly, T. harzianum induced de novo emission of several sesquiterpenes such as β‐caryophyllene and δ‐cadinene. In addition, single and combined applications of T. harzianum and P. vetula altered the sucrose content of the roots. Finally, T. harzianum produced 6‐pentyl‐2H‐pyran‐2‐one (6‐PP) a volatile compound that may act as an antifeedant‐signaling compound mitigating root herbivory by P. vetula.
CONCLUSION
Our results provide novel information about belowground multitrophic plant–microbe–arthropod interactions between T. harzianum and P. vetula in the maize rhizosphere resulting in alterations in maize phenotypic plant responses, inducing root herbivore tolerance.
Effects of T. harzianumon maize roots infested with P. vetula. (a) Grubs on their natural soil substrate. Morphological characteristics of a P. vetula second‐instar larva showing in (b) the presence of palidia in the raster observed with an objetive of 1.6X, (c) the cephalic capsule (head), and (d) the ventral plane of the clypeus showing the typical structures as the laeophoba, haotomerum and helus at the epipharynx observed with a manification of 5.0 X. (e) Effects of T. harzianum, P. vetula and their interaction on the maize roots. The image in the right side shows the bochemical componets involved in the root herbivore tolerance induced by the plant beneficial fungus.
© 2021 Society of Chemical Industry. |
| doi_str_mv | 10.1002/ps.6415 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2512729689</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2512729689</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3455-5c4b21610b7fbcf6da69dd7e82c6d48d58b261e66b5ccbfbac40ea7858c39fcd3</originalsourceid><addsrcrecordid>eNp10U1rFTEUBuAgiq1V_AcScKGgtyaZSWayLMWPQsGCFdwN-TjTSckkY5JpuV36y8311i4EVzmB57wceBF6SckxJYR9WPKxaCl_hA4pZ2LTStk_fpj7HwfoWc7XhBApJXuKDpqm55TT9hD9OgtYYQ0-3l6luAaL59UXV1JcJmewCwWSMsXF8B5fJmemaCHNCk8q3TkV1rkSuxrIeFbuDnCKseAJknY3MQEu0df9YACrK-VCLvhi2npfw-sf30BZvXqOnozKZ3hx_x6h758-Xp5-2Zx__Xx2enK-MU3L-YabVjMqKNHdqM0orBLS2g56ZoRte8t7zQQFITQ3Ro9amZaA6nrem0aOxjZH6O0-d0nx5wq5DLPLBrxXAeKaB8Yp65gUvaz09T_0Oq4p1Ouq4rLtKCM79WavTIo5JxiHJblZpe1AybCrZVjysKulylf3eauewT64vz1U8G4Pbp2H7f9yhotvf-J-A4BcmSg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2559471209</pqid></control><display><type>article</type><title>In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula</title><source>Wiley Online Library All Journals</source><creator>Contreras‐Cornejo, Hexon Angel ; Macías‐Rodríguez, Lourdes ; Real‐Santillán, Raúl Omar ; López‐Carmona, Dante ; García‐Gómez, Griselda ; Galicia‐Gallardo, Ana Paola ; Alfaro‐Cuevas, Ruth ; González‐Esquivel, Carlos E ; Najera‐Rincón, Miguel Bernardo ; Adame‐Garnica, Sandra Goretti ; Rebollar‐Alviter, Angel ; Álvarez‐Navarrete, Mariana ; Larsen, John</creator><creatorcontrib>Contreras‐Cornejo, Hexon Angel ; Macías‐Rodríguez, Lourdes ; Real‐Santillán, Raúl Omar ; López‐Carmona, Dante ; García‐Gómez, Griselda ; Galicia‐Gallardo, Ana Paola ; Alfaro‐Cuevas, Ruth ; González‐Esquivel, Carlos E ; Najera‐Rincón, Miguel Bernardo ; Adame‐Garnica, Sandra Goretti ; Rebollar‐Alviter, Angel ; Álvarez‐Navarrete, Mariana ; Larsen, John</creatorcontrib><description>BACKGROUND
Trichoderma spp. are soil fungi that interact with plant roots and associated biota such as other microorganisms and soil fauna. However, information about their interactions with root‐feeding insects is limited. Here, interactions between Trichoderma harzianum and the root‐feeding insect Phyllophaga vetula, a common insect pest in maize agroecosystems, were examined.
RESULTS
Applications of T. harzianum and P. vetula to the root system increased and decreased maize growth, respectively. Induced tolerance against herbivore attack was provided by T. harzianum maintaining a robust and functional root system as evidenced by the increased uptake of Cu, Ca, Mg, Na and K. Herbivore tolerance also coincided with changes in the emission of root volatile terpenes known to induce indirect defense responses and attract natural enemies of the herbivore. More importantly, T. harzianum induced de novo emission of several sesquiterpenes such as β‐caryophyllene and δ‐cadinene. In addition, single and combined applications of T. harzianum and P. vetula altered the sucrose content of the roots. Finally, T. harzianum produced 6‐pentyl‐2H‐pyran‐2‐one (6‐PP) a volatile compound that may act as an antifeedant‐signaling compound mitigating root herbivory by P. vetula.
CONCLUSION
Our results provide novel information about belowground multitrophic plant–microbe–arthropod interactions between T. harzianum and P. vetula in the maize rhizosphere resulting in alterations in maize phenotypic plant responses, inducing root herbivore tolerance.
Effects of T. harzianumon maize roots infested with P. vetula. (a) Grubs on their natural soil substrate. Morphological characteristics of a P. vetula second‐instar larva showing in (b) the presence of palidia in the raster observed with an objetive of 1.6X, (c) the cephalic capsule (head), and (d) the ventral plane of the clypeus showing the typical structures as the laeophoba, haotomerum and helus at the epipharynx observed with a manification of 5.0 X. (e) Effects of T. harzianum, P. vetula and their interaction on the maize roots. The image in the right side shows the bochemical componets involved in the root herbivore tolerance induced by the plant beneficial fungus.
© 2021 Society of Chemical Industry.</description><identifier>ISSN: 1526-498X</identifier><identifier>EISSN: 1526-4998</identifier><identifier>DOI: 10.1002/ps.6415</identifier><identifier>PMID: 33851514</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Agricultural ecosystems ; Biota ; Cadinene ; Caryophyllene ; Copper ; Corn ; Emission ; Emissions ; Fungi ; Herbivores ; Herbivory ; Insects ; Microorganisms ; Natural enemies ; Phyllophaga vetula ; plant defense ; Plant roots ; Rhizosphere ; root herbivory ; Roots ; secondary metabolites ; Sesquiterpenes ; Soil fauna ; Soil microorganisms ; Soils ; Sucrose ; Terpenes ; Trichoderma harzianum ; Volatile compounds</subject><ispartof>Pest management science, 2021-09, Vol.77 (9), p.3952-3963</ispartof><rights>2021 Society of Chemical Industry.</rights><rights>Copyright © 2021 Society of Chemical Industry</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3455-5c4b21610b7fbcf6da69dd7e82c6d48d58b261e66b5ccbfbac40ea7858c39fcd3</citedby><cites>FETCH-LOGICAL-c3455-5c4b21610b7fbcf6da69dd7e82c6d48d58b261e66b5ccbfbac40ea7858c39fcd3</cites><orcidid>0000-0001-8513-2501 ; 0000-0003-4576-5827 ; 0000-0002-6641-456X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fps.6415$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fps.6415$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33851514$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Contreras‐Cornejo, Hexon Angel</creatorcontrib><creatorcontrib>Macías‐Rodríguez, Lourdes</creatorcontrib><creatorcontrib>Real‐Santillán, Raúl Omar</creatorcontrib><creatorcontrib>López‐Carmona, Dante</creatorcontrib><creatorcontrib>García‐Gómez, Griselda</creatorcontrib><creatorcontrib>Galicia‐Gallardo, Ana Paola</creatorcontrib><creatorcontrib>Alfaro‐Cuevas, Ruth</creatorcontrib><creatorcontrib>González‐Esquivel, Carlos E</creatorcontrib><creatorcontrib>Najera‐Rincón, Miguel Bernardo</creatorcontrib><creatorcontrib>Adame‐Garnica, Sandra Goretti</creatorcontrib><creatorcontrib>Rebollar‐Alviter, Angel</creatorcontrib><creatorcontrib>Álvarez‐Navarrete, Mariana</creatorcontrib><creatorcontrib>Larsen, John</creatorcontrib><title>In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula</title><title>Pest management science</title><addtitle>Pest Manag Sci</addtitle><description>BACKGROUND
Trichoderma spp. are soil fungi that interact with plant roots and associated biota such as other microorganisms and soil fauna. However, information about their interactions with root‐feeding insects is limited. Here, interactions between Trichoderma harzianum and the root‐feeding insect Phyllophaga vetula, a common insect pest in maize agroecosystems, were examined.
RESULTS
Applications of T. harzianum and P. vetula to the root system increased and decreased maize growth, respectively. Induced tolerance against herbivore attack was provided by T. harzianum maintaining a robust and functional root system as evidenced by the increased uptake of Cu, Ca, Mg, Na and K. Herbivore tolerance also coincided with changes in the emission of root volatile terpenes known to induce indirect defense responses and attract natural enemies of the herbivore. More importantly, T. harzianum induced de novo emission of several sesquiterpenes such as β‐caryophyllene and δ‐cadinene. In addition, single and combined applications of T. harzianum and P. vetula altered the sucrose content of the roots. Finally, T. harzianum produced 6‐pentyl‐2H‐pyran‐2‐one (6‐PP) a volatile compound that may act as an antifeedant‐signaling compound mitigating root herbivory by P. vetula.
CONCLUSION
Our results provide novel information about belowground multitrophic plant–microbe–arthropod interactions between T. harzianum and P. vetula in the maize rhizosphere resulting in alterations in maize phenotypic plant responses, inducing root herbivore tolerance.
Effects of T. harzianumon maize roots infested with P. vetula. (a) Grubs on their natural soil substrate. Morphological characteristics of a P. vetula second‐instar larva showing in (b) the presence of palidia in the raster observed with an objetive of 1.6X, (c) the cephalic capsule (head), and (d) the ventral plane of the clypeus showing the typical structures as the laeophoba, haotomerum and helus at the epipharynx observed with a manification of 5.0 X. (e) Effects of T. harzianum, P. vetula and their interaction on the maize roots. The image in the right side shows the bochemical componets involved in the root herbivore tolerance induced by the plant beneficial fungus.
© 2021 Society of Chemical Industry.</description><subject>Agricultural ecosystems</subject><subject>Biota</subject><subject>Cadinene</subject><subject>Caryophyllene</subject><subject>Copper</subject><subject>Corn</subject><subject>Emission</subject><subject>Emissions</subject><subject>Fungi</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Insects</subject><subject>Microorganisms</subject><subject>Natural enemies</subject><subject>Phyllophaga vetula</subject><subject>plant defense</subject><subject>Plant roots</subject><subject>Rhizosphere</subject><subject>root herbivory</subject><subject>Roots</subject><subject>secondary metabolites</subject><subject>Sesquiterpenes</subject><subject>Soil fauna</subject><subject>Soil microorganisms</subject><subject>Soils</subject><subject>Sucrose</subject><subject>Terpenes</subject><subject>Trichoderma harzianum</subject><subject>Volatile compounds</subject><issn>1526-498X</issn><issn>1526-4998</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp10U1rFTEUBuAgiq1V_AcScKGgtyaZSWayLMWPQsGCFdwN-TjTSckkY5JpuV36y8311i4EVzmB57wceBF6SckxJYR9WPKxaCl_hA4pZ2LTStk_fpj7HwfoWc7XhBApJXuKDpqm55TT9hD9OgtYYQ0-3l6luAaL59UXV1JcJmewCwWSMsXF8B5fJmemaCHNCk8q3TkV1rkSuxrIeFbuDnCKseAJknY3MQEu0df9YACrK-VCLvhi2npfw-sf30BZvXqOnozKZ3hx_x6h758-Xp5-2Zx__Xx2enK-MU3L-YabVjMqKNHdqM0orBLS2g56ZoRte8t7zQQFITQ3Ro9amZaA6nrem0aOxjZH6O0-d0nx5wq5DLPLBrxXAeKaB8Yp65gUvaz09T_0Oq4p1Ouq4rLtKCM79WavTIo5JxiHJblZpe1AybCrZVjysKulylf3eauewT64vz1U8G4Pbp2H7f9yhotvf-J-A4BcmSg</recordid><startdate>202109</startdate><enddate>202109</enddate><creator>Contreras‐Cornejo, Hexon Angel</creator><creator>Macías‐Rodríguez, Lourdes</creator><creator>Real‐Santillán, Raúl Omar</creator><creator>López‐Carmona, Dante</creator><creator>García‐Gómez, Griselda</creator><creator>Galicia‐Gallardo, Ana Paola</creator><creator>Alfaro‐Cuevas, Ruth</creator><creator>González‐Esquivel, Carlos E</creator><creator>Najera‐Rincón, Miguel Bernardo</creator><creator>Adame‐Garnica, Sandra Goretti</creator><creator>Rebollar‐Alviter, Angel</creator><creator>Álvarez‐Navarrete, Mariana</creator><creator>Larsen, John</creator><general>John Wiley & Sons, Ltd</general><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8513-2501</orcidid><orcidid>https://orcid.org/0000-0003-4576-5827</orcidid><orcidid>https://orcid.org/0000-0002-6641-456X</orcidid></search><sort><creationdate>202109</creationdate><title>In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula</title><author>Contreras‐Cornejo, Hexon Angel ; Macías‐Rodríguez, Lourdes ; Real‐Santillán, Raúl Omar ; López‐Carmona, Dante ; García‐Gómez, Griselda ; Galicia‐Gallardo, Ana Paola ; Alfaro‐Cuevas, Ruth ; González‐Esquivel, Carlos E ; Najera‐Rincón, Miguel Bernardo ; Adame‐Garnica, Sandra Goretti ; Rebollar‐Alviter, Angel ; Álvarez‐Navarrete, Mariana ; Larsen, John</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3455-5c4b21610b7fbcf6da69dd7e82c6d48d58b261e66b5ccbfbac40ea7858c39fcd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Agricultural ecosystems</topic><topic>Biota</topic><topic>Cadinene</topic><topic>Caryophyllene</topic><topic>Copper</topic><topic>Corn</topic><topic>Emission</topic><topic>Emissions</topic><topic>Fungi</topic><topic>Herbivores</topic><topic>Herbivory</topic><topic>Insects</topic><topic>Microorganisms</topic><topic>Natural enemies</topic><topic>Phyllophaga vetula</topic><topic>plant defense</topic><topic>Plant roots</topic><topic>Rhizosphere</topic><topic>root herbivory</topic><topic>Roots</topic><topic>secondary metabolites</topic><topic>Sesquiterpenes</topic><topic>Soil fauna</topic><topic>Soil microorganisms</topic><topic>Soils</topic><topic>Sucrose</topic><topic>Terpenes</topic><topic>Trichoderma harzianum</topic><topic>Volatile compounds</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Contreras‐Cornejo, Hexon Angel</creatorcontrib><creatorcontrib>Macías‐Rodríguez, Lourdes</creatorcontrib><creatorcontrib>Real‐Santillán, Raúl Omar</creatorcontrib><creatorcontrib>López‐Carmona, Dante</creatorcontrib><creatorcontrib>García‐Gómez, Griselda</creatorcontrib><creatorcontrib>Galicia‐Gallardo, Ana Paola</creatorcontrib><creatorcontrib>Alfaro‐Cuevas, Ruth</creatorcontrib><creatorcontrib>González‐Esquivel, Carlos E</creatorcontrib><creatorcontrib>Najera‐Rincón, Miguel Bernardo</creatorcontrib><creatorcontrib>Adame‐Garnica, Sandra Goretti</creatorcontrib><creatorcontrib>Rebollar‐Alviter, Angel</creatorcontrib><creatorcontrib>Álvarez‐Navarrete, Mariana</creatorcontrib><creatorcontrib>Larsen, John</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Pest management science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Contreras‐Cornejo, Hexon Angel</au><au>Macías‐Rodríguez, Lourdes</au><au>Real‐Santillán, Raúl Omar</au><au>López‐Carmona, Dante</au><au>García‐Gómez, Griselda</au><au>Galicia‐Gallardo, Ana Paola</au><au>Alfaro‐Cuevas, Ruth</au><au>González‐Esquivel, Carlos E</au><au>Najera‐Rincón, Miguel Bernardo</au><au>Adame‐Garnica, Sandra Goretti</au><au>Rebollar‐Alviter, Angel</au><au>Álvarez‐Navarrete, Mariana</au><au>Larsen, John</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula</atitle><jtitle>Pest management science</jtitle><addtitle>Pest Manag Sci</addtitle><date>2021-09</date><risdate>2021</risdate><volume>77</volume><issue>9</issue><spage>3952</spage><epage>3963</epage><pages>3952-3963</pages><issn>1526-498X</issn><eissn>1526-4998</eissn><abstract>BACKGROUND
Trichoderma spp. are soil fungi that interact with plant roots and associated biota such as other microorganisms and soil fauna. However, information about their interactions with root‐feeding insects is limited. Here, interactions between Trichoderma harzianum and the root‐feeding insect Phyllophaga vetula, a common insect pest in maize agroecosystems, were examined.
RESULTS
Applications of T. harzianum and P. vetula to the root system increased and decreased maize growth, respectively. Induced tolerance against herbivore attack was provided by T. harzianum maintaining a robust and functional root system as evidenced by the increased uptake of Cu, Ca, Mg, Na and K. Herbivore tolerance also coincided with changes in the emission of root volatile terpenes known to induce indirect defense responses and attract natural enemies of the herbivore. More importantly, T. harzianum induced de novo emission of several sesquiterpenes such as β‐caryophyllene and δ‐cadinene. In addition, single and combined applications of T. harzianum and P. vetula altered the sucrose content of the roots. Finally, T. harzianum produced 6‐pentyl‐2H‐pyran‐2‐one (6‐PP) a volatile compound that may act as an antifeedant‐signaling compound mitigating root herbivory by P. vetula.
CONCLUSION
Our results provide novel information about belowground multitrophic plant–microbe–arthropod interactions between T. harzianum and P. vetula in the maize rhizosphere resulting in alterations in maize phenotypic plant responses, inducing root herbivore tolerance.
Effects of T. harzianumon maize roots infested with P. vetula. (a) Grubs on their natural soil substrate. Morphological characteristics of a P. vetula second‐instar larva showing in (b) the presence of palidia in the raster observed with an objetive of 1.6X, (c) the cephalic capsule (head), and (d) the ventral plane of the clypeus showing the typical structures as the laeophoba, haotomerum and helus at the epipharynx observed with a manification of 5.0 X. (e) Effects of T. harzianum, P. vetula and their interaction on the maize roots. The image in the right side shows the bochemical componets involved in the root herbivore tolerance induced by the plant beneficial fungus.
© 2021 Society of Chemical Industry.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>33851514</pmid><doi>10.1002/ps.6415</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-8513-2501</orcidid><orcidid>https://orcid.org/0000-0003-4576-5827</orcidid><orcidid>https://orcid.org/0000-0002-6641-456X</orcidid></addata></record> |
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| source | Wiley Online Library All Journals |
| subjects | Agricultural ecosystems Biota Cadinene Caryophyllene Copper Corn Emission Emissions Fungi Herbivores Herbivory Insects Microorganisms Natural enemies Phyllophaga vetula plant defense Plant roots Rhizosphere root herbivory Roots secondary metabolites Sesquiterpenes Soil fauna Soil microorganisms Soils Sucrose Terpenes Trichoderma harzianum Volatile compounds |
| title | In a belowground multitrophic interaction, Trichoderma harzianum induces maize root herbivore tolerance against Phyllophaga vetula |
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