Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies
Plants perceive and respond to herbivore insect eggs. Upon egg deposition on leaves, a strong hypersensitive response (HR)-like cell death can be activated leading to egg desiccation and/or dropping. In Brassica spp., including many crops, the HR-like mechanism against eggs of cabbage white butterfl...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Ecology and Evolution |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fevo.2022.1070859/full |
| _version_ | 1828047976942010368 |
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| author | Lotte Caarls Niccolò Bassetti Patrick Verbaarschot Roland Mumm Joop J. A. van Loon M. Eric Schranz Nina E. Fatouros |
| author_facet | Lotte Caarls Niccolò Bassetti Patrick Verbaarschot Roland Mumm Joop J. A. van Loon M. Eric Schranz Nina E. Fatouros |
| author_sort | Lotte Caarls |
| collection | DOAJ |
| description | Plants perceive and respond to herbivore insect eggs. Upon egg deposition on leaves, a strong hypersensitive response (HR)-like cell death can be activated leading to egg desiccation and/or dropping. In Brassica spp., including many crops, the HR-like mechanism against eggs of cabbage white butterflies (Pieris spp.) is poorly understood. Using two Brassica species, the crop B. rapa and its wild relative B. nigra, we studied the cellular and molecular plant response to Pieris brassicae eggs and characterized potential insect egg-associated molecular patterns (EAMPs) inducing HR-like cell death. We found that eggs of P. brassicae induced typical hallmarks of early immune responses, such as callose deposition, production of reactive oxygen species and cell death in B. nigra and B. rapa leaf tissue, also in plants that did not express HR-like cell death. However, elevated levels of ethylene production and upregulation of salicylic acid-responsive genes were only detected in a B. nigra accession expressing HR-like cell death. Eggs and egg wash from P. brassicae contains compounds that induced such responses, but the eggs of the generalist moth Mamestra brassicae did not. Furthermore, wash made from hatched Pieris eggs, egg glue, and accessory reproductive glands (ARG) that produce this glue, induced HR-like cell death, whereas washes from unfertilized eggs dissected from the ovaries or removal of the glue from eggs resulted in no or a reduced response. This suggests that there is one or multiple egg associated molecular pattern (EAMP) located in the egg glue a that teresponse in B. nigra is specific to Pieris species. Lastly, our results indicate that the EAMP is neither lipidic nor proteinaceous. Our study expands the knowledge on the mechanism of Brassica-Pieris-egg interaction and is a step closer toward identification of EAMPs in Pieris egg glue and corresponding receptor(s) in Brassica. |
| first_indexed | 2024-04-10T18:50:16Z |
| format | Article |
| id | doaj.art-4f0c7e9beb614052ab175227d96855cf |
| institution | Directory Open Access Journal |
| issn | 2296-701X |
| language | English |
| last_indexed | 2024-04-10T18:50:16Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Ecology and Evolution |
| spelling | doaj.art-4f0c7e9beb614052ab175227d96855cf2023-02-01T07:38:16ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2023-02-011010.3389/fevo.2022.10708591070859Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterfliesLotte Caarls0Niccolò Bassetti1Patrick Verbaarschot2Roland Mumm3Joop J. A. van Loon4M. Eric Schranz5Nina E. Fatouros6Biosystematics Group, Wageningen University & Research, Wageningen, NetherlandsBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsBioscience, Wageningen University & Research, Wageningen, NetherlandsLaboratory of Entomology, Wageningen University & Research, Wageningen, NetherlandsBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsBiosystematics Group, Wageningen University & Research, Wageningen, NetherlandsPlants perceive and respond to herbivore insect eggs. Upon egg deposition on leaves, a strong hypersensitive response (HR)-like cell death can be activated leading to egg desiccation and/or dropping. In Brassica spp., including many crops, the HR-like mechanism against eggs of cabbage white butterflies (Pieris spp.) is poorly understood. Using two Brassica species, the crop B. rapa and its wild relative B. nigra, we studied the cellular and molecular plant response to Pieris brassicae eggs and characterized potential insect egg-associated molecular patterns (EAMPs) inducing HR-like cell death. We found that eggs of P. brassicae induced typical hallmarks of early immune responses, such as callose deposition, production of reactive oxygen species and cell death in B. nigra and B. rapa leaf tissue, also in plants that did not express HR-like cell death. However, elevated levels of ethylene production and upregulation of salicylic acid-responsive genes were only detected in a B. nigra accession expressing HR-like cell death. Eggs and egg wash from P. brassicae contains compounds that induced such responses, but the eggs of the generalist moth Mamestra brassicae did not. Furthermore, wash made from hatched Pieris eggs, egg glue, and accessory reproductive glands (ARG) that produce this glue, induced HR-like cell death, whereas washes from unfertilized eggs dissected from the ovaries or removal of the glue from eggs resulted in no or a reduced response. This suggests that there is one or multiple egg associated molecular pattern (EAMP) located in the egg glue a that teresponse in B. nigra is specific to Pieris species. Lastly, our results indicate that the EAMP is neither lipidic nor proteinaceous. Our study expands the knowledge on the mechanism of Brassica-Pieris-egg interaction and is a step closer toward identification of EAMPs in Pieris egg glue and corresponding receptor(s) in Brassica.https://www.frontiersin.org/articles/10.3389/fevo.2022.1070859/fullPieriscabbagecell deathplant-insect interactionoviposition-induced responseegg-associated molecular pattern |
| spellingShingle | Lotte Caarls Niccolò Bassetti Patrick Verbaarschot Roland Mumm Joop J. A. van Loon M. Eric Schranz Nina E. Fatouros Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies Frontiers in Ecology and Evolution Pieris cabbage cell death plant-insect interaction oviposition-induced response egg-associated molecular pattern |
| title | Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies |
| title_full | Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies |
| title_fullStr | Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies |
| title_full_unstemmed | Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies |
| title_short | Hypersensitive-like response in Brassica plants is specifically induced by molecules from egg-associated secretions of cabbage white butterflies |
| title_sort | hypersensitive like response in brassica plants is specifically induced by molecules from egg associated secretions of cabbage white butterflies |
| topic | Pieris cabbage cell death plant-insect interaction oviposition-induced response egg-associated molecular pattern |
| url | https://www.frontiersin.org/articles/10.3389/fevo.2022.1070859/full |
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