The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist
Abstract Background In native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses. The plant’s response to combined stresses is usually not the sum of the individual responses. Here we investigated the impact of cold on plant defense against...
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| Format: | Article |
| Language: | English |
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BMC
2019-08-01
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| Series: | BMC Plant Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s12870-019-1943-3 |
| _version_ | 1818304515352297472 |
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| author | Jana Oberländer Vivien Lortzing Monika Hilker Reinhard Kunze |
| author_facet | Jana Oberländer Vivien Lortzing Monika Hilker Reinhard Kunze |
| author_sort | Jana Oberländer |
| collection | DOAJ |
| description | Abstract Background In native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses. The plant’s response to combined stresses is usually not the sum of the individual responses. Here we investigated the impact of cold on plant defense against subsequent herbivory by a generalist and specialist insect. Results We determined transcriptional responses of Arabidopsis thaliana to low temperature stress (4 °C) and subsequent larval feeding damage by the lepidopteran herbivores Mamestra brassicae (generalist), Pieris brassicae (specialist) or artificial wounding. Furthermore, we compared the performance of larvae feeding upon cold-experienced or untreated plants. Prior experience of cold strongly affected the plant’s transcriptional anti-herbivore and wounding response. Feeding by P. brassicae, M. brassicae and artificial wounding induced transcriptional changes of 1975, 1695, and 2239 genes, respectively. Of these, 125, 360, and 681 genes were differentially regulated when cold preceded the tissue damage. Overall, prior experience of cold mostly reduced the transcriptional response of genes to damage. The percentage of damage-responsive genes, which showed attenuated transcriptional regulation when cold preceded the tissue damage, was highest in M. brassicae damaged plants (98%), intermediate in artificially damaged plants (89%), and lowest in P. brassicae damaged plants (69%). Consistently, the generalist M. brassicae performed better on cold-treated than on untreated plants, whereas the performance of the specialist P. brassicae did not differ. Conclusions The transcriptional defense response of Arabidopsis leaves to feeding by herbivorous insects and artificial wounding is attenuated by a prior exposure of the plant to cold. This attenuation correlates with improved performance of the generalist herbivore M. brassicae, but not the specialist P. brassicae, a herbivore of the same feeding guild. |
| first_indexed | 2024-12-13T06:11:55Z |
| format | Article |
| id | doaj.art-3856df3995644feba8713ede6e0688a1 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-13T06:11:55Z |
| publishDate | 2019-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-3856df3995644feba8713ede6e0688a12022-12-21T23:57:04ZengBMCBMC Plant Biology1471-22292019-08-0119111610.1186/s12870-019-1943-3The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialistJana Oberländer0Vivien Lortzing1Monika Hilker2Reinhard Kunze3Freie Universität Berlin, Institute of Biology - Applied Genetics, Dahlem Centre of Plant SciencesFreie Universität Berlin, Institute of Biology - Applied Zoology / Animal Ecology, Dahlem Centre of Plant SciencesFreie Universität Berlin, Institute of Biology - Applied Zoology / Animal Ecology, Dahlem Centre of Plant SciencesFreie Universität Berlin, Institute of Biology - Applied Genetics, Dahlem Centre of Plant SciencesAbstract Background In native environments plants frequently experience simultaneous or sequential unfavourable abiotic and biotic stresses. The plant’s response to combined stresses is usually not the sum of the individual responses. Here we investigated the impact of cold on plant defense against subsequent herbivory by a generalist and specialist insect. Results We determined transcriptional responses of Arabidopsis thaliana to low temperature stress (4 °C) and subsequent larval feeding damage by the lepidopteran herbivores Mamestra brassicae (generalist), Pieris brassicae (specialist) or artificial wounding. Furthermore, we compared the performance of larvae feeding upon cold-experienced or untreated plants. Prior experience of cold strongly affected the plant’s transcriptional anti-herbivore and wounding response. Feeding by P. brassicae, M. brassicae and artificial wounding induced transcriptional changes of 1975, 1695, and 2239 genes, respectively. Of these, 125, 360, and 681 genes were differentially regulated when cold preceded the tissue damage. Overall, prior experience of cold mostly reduced the transcriptional response of genes to damage. The percentage of damage-responsive genes, which showed attenuated transcriptional regulation when cold preceded the tissue damage, was highest in M. brassicae damaged plants (98%), intermediate in artificially damaged plants (89%), and lowest in P. brassicae damaged plants (69%). Consistently, the generalist M. brassicae performed better on cold-treated than on untreated plants, whereas the performance of the specialist P. brassicae did not differ. Conclusions The transcriptional defense response of Arabidopsis leaves to feeding by herbivorous insects and artificial wounding is attenuated by a prior exposure of the plant to cold. This attenuation correlates with improved performance of the generalist herbivore M. brassicae, but not the specialist P. brassicae, a herbivore of the same feeding guild.http://link.springer.com/article/10.1186/s12870-019-1943-3Plant stress responseHerbivoreDefenseLarval feedingPieris brassicaeMamestra brassicae |
| spellingShingle | Jana Oberländer Vivien Lortzing Monika Hilker Reinhard Kunze The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist BMC Plant Biology Plant stress response Herbivore Defense Larval feeding Pieris brassicae Mamestra brassicae |
| title | The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist |
| title_full | The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist |
| title_fullStr | The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist |
| title_full_unstemmed | The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist |
| title_short | The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist |
| title_sort | differential response of cold experienced arabidopsis thaliana to larval herbivory benefits an insect generalist but not a specialist |
| topic | Plant stress response Herbivore Defense Larval feeding Pieris brassicae Mamestra brassicae |
| url | http://link.springer.com/article/10.1186/s12870-019-1943-3 |
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