Plant geographic distribution influences chemical defences in native and introduced Plantago lanceolata populations

Plants growing outside their native range may be confronted by new regimes of herbivory, but how this affects plant chemical defence profiles has rarely been studied. Using Plantago lanceolata as a model species, we investigated whether introduced populations show significant differences from native...

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Veröffentlicht in:Functional ecology 2024-04, Vol.38 (4), p.883-896
Hauptverfasser: Medina‐van Berkum, Pamela, Schmöckel, Eric, Bischoff, Armin, Carrasco‐Farias, Natalia, Catford, Jane A., Feldmann, Reinart, Groten, Karin, Henry, Hugh A. L., Bucharova, Anna, Hänniger, Sabine, Luong, Justin C., Meis, Julia, Oetama, Vincensius S. P., Pärtel, Meelis, Power, Sally A., Villellas, Jesus, Welk, Erik, Wingler, Astrid, Rothe, Beate, Gershenzon, Jonathan, Reichelt, Michael, Roscher, Christiane, Unsicker, Sybille B.
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container_issue 4
container_start_page 883
container_title Functional ecology
container_volume 38
creator Medina‐van Berkum, Pamela
Schmöckel, Eric
Bischoff, Armin
Carrasco‐Farias, Natalia
Catford, Jane A.
Feldmann, Reinart
Groten, Karin
Henry, Hugh A. L.
Bucharova, Anna
Hänniger, Sabine
Luong, Justin C.
Meis, Julia
Oetama, Vincensius S. P.
Pärtel, Meelis
Power, Sally A.
Villellas, Jesus
Welk, Erik
Wingler, Astrid
Rothe, Beate
Gershenzon, Jonathan
Reichelt, Michael
Roscher, Christiane
Unsicker, Sybille B.
description Plants growing outside their native range may be confronted by new regimes of herbivory, but how this affects plant chemical defence profiles has rarely been studied. Using Plantago lanceolata as a model species, we investigated whether introduced populations show significant differences from native populations in several growth and chemical defence traits. Plantago lanceolata (ribwort plantain) is an herbaceous plant species native to Europe and Western Asia that has been introduced to numerous countries worldwide. We sampled seeds from nine native and 10 introduced populations that covered a broad geographic and environmental range and performed a greenhouse experiment, in which we infested half of the plants in each population with caterpillars of the generalist herbivore Spodoptera littoralis . We then measured size‐related and resource‐allocation traits as well as the levels of constitutive and induced chemical defence compounds in roots and shoots of P. lanceolata . When we considered the environmental characteristics of the site of origin, our results revealed that populations from introduced ranges were characterized by an increase in chemical defence compounds without compromising plant biomass. The concentrations of iridoid glycosides and verbascoside, the major anti‐herbivore defence compounds of P. lanceolata , were higher in introduced populations than in native populations. In addition, introduced populations exhibited greater rates of herbivore‐induced volatile organic compound emission and diversity, and similar chemical diversity based on untargeted analyses of leaf methanol extracts. In conclusion, the geographic origin of the populations had a significant influence on morphological and chemical plant traits, suggesting that P. lanceolata populations are not only adapted to different environments in their native range, but also in their introduced range. Read the free Plain Language Summary for this article on the Journal blog. Las plantas que crecen fuera de su distribución nativa pueden enfrentarse a nuevos patrones de herbivoría. No obstante, existen pocos estudios enfocados en explicar cómo la introducción a una nueva área puede afectar los perfiles de defensas químicas de dichas plantas. El objetivo de este estudio fue determinar si existen diferencias significativas en aspectos morfológicos y químicos entre las poblaciones nativas e introducidas utilizando Plantago lanceolata como especie modelo, una herbácea originaria de Europa y
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L. ; Bucharova, Anna ; Hänniger, Sabine ; Luong, Justin C. ; Meis, Julia ; Oetama, Vincensius S. P. ; Pärtel, Meelis ; Power, Sally A. ; Villellas, Jesus ; Welk, Erik ; Wingler, Astrid ; Rothe, Beate ; Gershenzon, Jonathan ; Reichelt, Michael ; Roscher, Christiane ; Unsicker, Sybille B.</creator><creatorcontrib>Medina‐van Berkum, Pamela ; Schmöckel, Eric ; Bischoff, Armin ; Carrasco‐Farias, Natalia ; Catford, Jane A. ; Feldmann, Reinart ; Groten, Karin ; Henry, Hugh A. L. ; Bucharova, Anna ; Hänniger, Sabine ; Luong, Justin C. ; Meis, Julia ; Oetama, Vincensius S. P. ; Pärtel, Meelis ; Power, Sally A. ; Villellas, Jesus ; Welk, Erik ; Wingler, Astrid ; Rothe, Beate ; Gershenzon, Jonathan ; Reichelt, Michael ; Roscher, Christiane ; Unsicker, Sybille B.</creatorcontrib><description>Plants growing outside their native range may be confronted by new regimes of herbivory, but how this affects plant chemical defence profiles has rarely been studied. Using Plantago lanceolata as a model species, we investigated whether introduced populations show significant differences from native populations in several growth and chemical defence traits. Plantago lanceolata (ribwort plantain) is an herbaceous plant species native to Europe and Western Asia that has been introduced to numerous countries worldwide. We sampled seeds from nine native and 10 introduced populations that covered a broad geographic and environmental range and performed a greenhouse experiment, in which we infested half of the plants in each population with caterpillars of the generalist herbivore Spodoptera littoralis . We then measured size‐related and resource‐allocation traits as well as the levels of constitutive and induced chemical defence compounds in roots and shoots of P. lanceolata . When we considered the environmental characteristics of the site of origin, our results revealed that populations from introduced ranges were characterized by an increase in chemical defence compounds without compromising plant biomass. The concentrations of iridoid glycosides and verbascoside, the major anti‐herbivore defence compounds of P. lanceolata , were higher in introduced populations than in native populations. In addition, introduced populations exhibited greater rates of herbivore‐induced volatile organic compound emission and diversity, and similar chemical diversity based on untargeted analyses of leaf methanol extracts. In conclusion, the geographic origin of the populations had a significant influence on morphological and chemical plant traits, suggesting that P. lanceolata populations are not only adapted to different environments in their native range, but also in their introduced range. Read the free Plain Language Summary for this article on the Journal blog. Las plantas que crecen fuera de su distribución nativa pueden enfrentarse a nuevos patrones de herbivoría. No obstante, existen pocos estudios enfocados en explicar cómo la introducción a una nueva área puede afectar los perfiles de defensas químicas de dichas plantas. El objetivo de este estudio fue determinar si existen diferencias significativas en aspectos morfológicos y químicos entre las poblaciones nativas e introducidas utilizando Plantago lanceolata como especie modelo, una herbácea originaria de Europa y Asia occidental que se ha introducido en distintas partes del mundo. Para este estudio, se recolectaron muestras de semillas de nueve poblaciones nativas y diez poblaciones introducidas, cubriendo un amplio rango geográfico. Posteriormente, se llevó a cabo un experimento en invernadero, donde la mitad de las plantas de cada población fueron infestadas con orugas del herbívoro generalista, Spodoptera littoralis . Se midió los rasgos relacionados con el tamaño y la asignación de recursos así como, las diferencias químicas de las raíces y hojas de P. lanceolata , tanto perfiles químicos constitutivos como inducidos. Nuestros resultados revelaron que las poblaciones introducidas se caracterizaban por un aumento de los compuestos químicos de defensa sin comprometer la biomasa de la planta si considerábamos las características ambientales del lugar de origen. Las concentraciones de glucósidos de iridoides y verbascósido, compuestos de defensa predominantes de P. lanceolata , fueron mayores en las poblaciones introducidas que en las nativas. Además, las poblaciones introducidas mostraron mayores tasas de emisión y diversidad de los compuestos volátiles inducidos por herbívoros, así como una diversidad metabolómica similar en las hojas. En conclusión, el origen geográfico de las poblaciones tuvo una influencia significativa en los rasgos morfológicos y químicos de las plantas, lo que sugiere que las poblaciones de P. lanceolata no sólo están adaptadas a diferentes ambientes en su distribución nativa, sino también en su distribución introducida.</description><identifier>ISSN: 0269-8463</identifier><identifier>EISSN: 1365-2435</identifier><identifier>DOI: 10.1111/1365-2435.14535</identifier><language>eng</language><publisher>London: Wiley Subscription Services, Inc</publisher><subject>Biodiversity and Ecology ; Chemical compounds ; Chemical defense ; Chemical plants ; Defense ; Emission analysis ; Environmental Sciences ; Geographical distribution ; Glycosides ; Herbivores ; Herbivory ; Indigenous species ; Introduced species ; Organic compounds ; Plant biomass ; Plant species ; Plantago lanceolata ; Plants (botany) ; Populations ; Seeds ; Spodoptera littoralis ; VOCs ; Volatile organic compounds</subject><ispartof>Functional ecology, 2024-04, Vol.38 (4), p.883-896</ispartof><rights>2024. 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L.</creatorcontrib><creatorcontrib>Bucharova, Anna</creatorcontrib><creatorcontrib>Hänniger, Sabine</creatorcontrib><creatorcontrib>Luong, Justin C.</creatorcontrib><creatorcontrib>Meis, Julia</creatorcontrib><creatorcontrib>Oetama, Vincensius S. 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Using Plantago lanceolata as a model species, we investigated whether introduced populations show significant differences from native populations in several growth and chemical defence traits. Plantago lanceolata (ribwort plantain) is an herbaceous plant species native to Europe and Western Asia that has been introduced to numerous countries worldwide. We sampled seeds from nine native and 10 introduced populations that covered a broad geographic and environmental range and performed a greenhouse experiment, in which we infested half of the plants in each population with caterpillars of the generalist herbivore Spodoptera littoralis . We then measured size‐related and resource‐allocation traits as well as the levels of constitutive and induced chemical defence compounds in roots and shoots of P. lanceolata . When we considered the environmental characteristics of the site of origin, our results revealed that populations from introduced ranges were characterized by an increase in chemical defence compounds without compromising plant biomass. The concentrations of iridoid glycosides and verbascoside, the major anti‐herbivore defence compounds of P. lanceolata , were higher in introduced populations than in native populations. In addition, introduced populations exhibited greater rates of herbivore‐induced volatile organic compound emission and diversity, and similar chemical diversity based on untargeted analyses of leaf methanol extracts. In conclusion, the geographic origin of the populations had a significant influence on morphological and chemical plant traits, suggesting that P. lanceolata populations are not only adapted to different environments in their native range, but also in their introduced range. Read the free Plain Language Summary for this article on the Journal blog. Las plantas que crecen fuera de su distribución nativa pueden enfrentarse a nuevos patrones de herbivoría. No obstante, existen pocos estudios enfocados en explicar cómo la introducción a una nueva área puede afectar los perfiles de defensas químicas de dichas plantas. El objetivo de este estudio fue determinar si existen diferencias significativas en aspectos morfológicos y químicos entre las poblaciones nativas e introducidas utilizando Plantago lanceolata como especie modelo, una herbácea originaria de Europa y Asia occidental que se ha introducido en distintas partes del mundo. Para este estudio, se recolectaron muestras de semillas de nueve poblaciones nativas y diez poblaciones introducidas, cubriendo un amplio rango geográfico. Posteriormente, se llevó a cabo un experimento en invernadero, donde la mitad de las plantas de cada población fueron infestadas con orugas del herbívoro generalista, Spodoptera littoralis . Se midió los rasgos relacionados con el tamaño y la asignación de recursos así como, las diferencias químicas de las raíces y hojas de P. lanceolata , tanto perfiles químicos constitutivos como inducidos. Nuestros resultados revelaron que las poblaciones introducidas se caracterizaban por un aumento de los compuestos químicos de defensa sin comprometer la biomasa de la planta si considerábamos las características ambientales del lugar de origen. Las concentraciones de glucósidos de iridoides y verbascósido, compuestos de defensa predominantes de P. lanceolata , fueron mayores en las poblaciones introducidas que en las nativas. Además, las poblaciones introducidas mostraron mayores tasas de emisión y diversidad de los compuestos volátiles inducidos por herbívoros, así como una diversidad metabolómica similar en las hojas. En conclusión, el origen geográfico de las poblaciones tuvo una influencia significativa en los rasgos morfológicos y químicos de las plantas, lo que sugiere que las poblaciones de P. lanceolata no sólo están adaptadas a diferentes ambientes en su distribución nativa, sino también en su distribución introducida.</description><subject>Biodiversity and Ecology</subject><subject>Chemical compounds</subject><subject>Chemical defense</subject><subject>Chemical plants</subject><subject>Defense</subject><subject>Emission analysis</subject><subject>Environmental Sciences</subject><subject>Geographical distribution</subject><subject>Glycosides</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Indigenous species</subject><subject>Introduced species</subject><subject>Organic compounds</subject><subject>Plant biomass</subject><subject>Plant species</subject><subject>Plantago lanceolata</subject><subject>Plants (botany)</subject><subject>Populations</subject><subject>Seeds</subject><subject>Spodoptera littoralis</subject><subject>VOCs</subject><subject>Volatile organic compounds</subject><issn>0269-8463</issn><issn>1365-2435</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNo9kU1PwzAMhiMEEmNw5hqJE4du-ezHcZqAIU2CA5yjNHW3TF1TknYS_550Rcshtl-9emzZCD1SsqDxLSlPZcIElwsqJJdXaHZRrtGMsLRIcpHyW3QXwoEQUkjGZih8Nrrt8Q7czutubw2ubOi9LYfeuhbbtm4GaA0EbPZwtEY3uIJ6UmyLW93bE2DdVrHqvasGAxU-M_XO4RgNuEb3GneuG2ISoeEe3dS6CfDwH-fo-_Xla71Jth9v7-vVNjFciD5JecHylILIBC1LyLSs85LHH8qayaJIOZUGuIRcZ7mBzNQgSy3SwugIqDM-R88Td68b1Xl71P5XOW3VZrVVo0aEZJxl7ESj92nydt79DBB6dXCDb-N4ihNOipTEjtG1nFzGuxA81BcsJWq8ghp3rsadq_MV-B-uF3u7</recordid><startdate>20240401</startdate><enddate>20240401</enddate><creator>Medina‐van Berkum, Pamela</creator><creator>Schmöckel, Eric</creator><creator>Bischoff, Armin</creator><creator>Carrasco‐Farias, Natalia</creator><creator>Catford, Jane A.</creator><creator>Feldmann, Reinart</creator><creator>Groten, Karin</creator><creator>Henry, Hugh A. 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L.</au><au>Bucharova, Anna</au><au>Hänniger, Sabine</au><au>Luong, Justin C.</au><au>Meis, Julia</au><au>Oetama, Vincensius S. P.</au><au>Pärtel, Meelis</au><au>Power, Sally A.</au><au>Villellas, Jesus</au><au>Welk, Erik</au><au>Wingler, Astrid</au><au>Rothe, Beate</au><au>Gershenzon, Jonathan</au><au>Reichelt, Michael</au><au>Roscher, Christiane</au><au>Unsicker, Sybille B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Plant geographic distribution influences chemical defences in native and introduced Plantago lanceolata populations</atitle><jtitle>Functional ecology</jtitle><date>2024-04-01</date><risdate>2024</risdate><volume>38</volume><issue>4</issue><spage>883</spage><epage>896</epage><pages>883-896</pages><issn>0269-8463</issn><eissn>1365-2435</eissn><abstract>Plants growing outside their native range may be confronted by new regimes of herbivory, but how this affects plant chemical defence profiles has rarely been studied. Using Plantago lanceolata as a model species, we investigated whether introduced populations show significant differences from native populations in several growth and chemical defence traits. Plantago lanceolata (ribwort plantain) is an herbaceous plant species native to Europe and Western Asia that has been introduced to numerous countries worldwide. We sampled seeds from nine native and 10 introduced populations that covered a broad geographic and environmental range and performed a greenhouse experiment, in which we infested half of the plants in each population with caterpillars of the generalist herbivore Spodoptera littoralis . We then measured size‐related and resource‐allocation traits as well as the levels of constitutive and induced chemical defence compounds in roots and shoots of P. lanceolata . When we considered the environmental characteristics of the site of origin, our results revealed that populations from introduced ranges were characterized by an increase in chemical defence compounds without compromising plant biomass. The concentrations of iridoid glycosides and verbascoside, the major anti‐herbivore defence compounds of P. lanceolata , were higher in introduced populations than in native populations. In addition, introduced populations exhibited greater rates of herbivore‐induced volatile organic compound emission and diversity, and similar chemical diversity based on untargeted analyses of leaf methanol extracts. In conclusion, the geographic origin of the populations had a significant influence on morphological and chemical plant traits, suggesting that P. lanceolata populations are not only adapted to different environments in their native range, but also in their introduced range. Read the free Plain Language Summary for this article on the Journal blog. Las plantas que crecen fuera de su distribución nativa pueden enfrentarse a nuevos patrones de herbivoría. No obstante, existen pocos estudios enfocados en explicar cómo la introducción a una nueva área puede afectar los perfiles de defensas químicas de dichas plantas. El objetivo de este estudio fue determinar si existen diferencias significativas en aspectos morfológicos y químicos entre las poblaciones nativas e introducidas utilizando Plantago lanceolata como especie modelo, una herbácea originaria de Europa y Asia occidental que se ha introducido en distintas partes del mundo. Para este estudio, se recolectaron muestras de semillas de nueve poblaciones nativas y diez poblaciones introducidas, cubriendo un amplio rango geográfico. Posteriormente, se llevó a cabo un experimento en invernadero, donde la mitad de las plantas de cada población fueron infestadas con orugas del herbívoro generalista, Spodoptera littoralis . Se midió los rasgos relacionados con el tamaño y la asignación de recursos así como, las diferencias químicas de las raíces y hojas de P. lanceolata , tanto perfiles químicos constitutivos como inducidos. Nuestros resultados revelaron que las poblaciones introducidas se caracterizaban por un aumento de los compuestos químicos de defensa sin comprometer la biomasa de la planta si considerábamos las características ambientales del lugar de origen. Las concentraciones de glucósidos de iridoides y verbascósido, compuestos de defensa predominantes de P. lanceolata , fueron mayores en las poblaciones introducidas que en las nativas. Además, las poblaciones introducidas mostraron mayores tasas de emisión y diversidad de los compuestos volátiles inducidos por herbívoros, así como una diversidad metabolómica similar en las hojas. En conclusión, el origen geográfico de las poblaciones tuvo una influencia significativa en los rasgos morfológicos y químicos de las plantas, lo que sugiere que las poblaciones de P. lanceolata no sólo están adaptadas a diferentes ambientes en su distribución nativa, sino también en su distribución introducida.</abstract><cop>London</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/1365-2435.14535</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8397-6292</orcidid><orcidid>https://orcid.org/0000-0003-2865-8720</orcidid><orcidid>https://orcid.org/0000-0003-4229-2497</orcidid><orcidid>https://orcid.org/0000-0002-2723-8671</orcidid><orcidid>https://orcid.org/0000-0001-7805-5683</orcidid><orcidid>https://orcid.org/0000-0001-8758-3568</orcidid><orcidid>https://orcid.org/0000-0003-2118-4788</orcidid><orcidid>https://orcid.org/0000-0003-0582-5960</orcidid><orcidid>https://orcid.org/0000-0002-5874-0138</orcidid><orcidid>https://orcid.org/0000-0001-9301-7909</orcidid><orcidid>https://orcid.org/0000-0002-7438-1454</orcidid><orcidid>https://orcid.org/0000-0002-9738-0075</orcidid><orcidid>https://orcid.org/0000-0003-0177-8810</orcidid><orcidid>https://orcid.org/0000-0002-1812-1551</orcidid><orcidid>https://orcid.org/0000-0002-5468-5426</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0269-8463
ispartof Functional ecology, 2024-04, Vol.38 (4), p.883-896
issn 0269-8463
1365-2435
language eng
recordid cdi_hal_primary_oai_HAL_hal_04523272v1
source Wiley Online Library Journals Frontfile Complete
subjects Biodiversity and Ecology
Chemical compounds
Chemical defense
Chemical plants
Defense
Emission analysis
Environmental Sciences
Geographical distribution
Glycosides
Herbivores
Herbivory
Indigenous species
Introduced species
Organic compounds
Plant biomass
Plant species
Plantago lanceolata
Plants (botany)
Populations
Seeds
Spodoptera littoralis
VOCs
Volatile organic compounds
title Plant geographic distribution influences chemical defences in native and introduced Plantago lanceolata populations
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