Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts
Plants are under constant attack by a suite of insect herbivores. Over millions of years of coexistence, plants have evolved the ability to sense insect feeding via herbivore-associated elicitors in oral secretions, which can mobilize defense responses. However, herbivore-associated elicitors and th...
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| Format: | Article |
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MDPI AG
2020-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/21/21/8297 |
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| author | Akanksha Gandhi Rupesh R. Kariyat Cruz Chappa Mandeep Tayal Nirakar Sahoo |
| author_facet | Akanksha Gandhi Rupesh R. Kariyat Cruz Chappa Mandeep Tayal Nirakar Sahoo |
| author_sort | Akanksha Gandhi |
| collection | DOAJ |
| description | Plants are under constant attack by a suite of insect herbivores. Over millions of years of coexistence, plants have evolved the ability to sense insect feeding via herbivore-associated elicitors in oral secretions, which can mobilize defense responses. However, herbivore-associated elicitors and the intrinsic downstream modulator of such interactions remain less understood. In this study, we show that tobacco hornworm caterpillar (<i>Manduca sexta</i>) oral secretion (OS) induces reactive oxygen species (ROS) in tomato (<i>Solanum lycopersicum</i>) protoplasts. By using a dye-based ROS imaging approach, our study shows that application of plant-fed (PF) <i>M. sexta</i> OS generates significantly higher ROS while artificial diet-fed (DF) caterpillar OS failed to induce ROS in isolated tomato protoplasts. Elevation in ROS generation was saturated after ~140 s of PF OS application. ROS production was also suppressed in the presence of an antioxidant NAC (<i>N</i>-acetyl-<i>L</i>-cysteine). Interestingly, PF OS-induced ROS increase was abolished in the presence of a Ca<sup>2+</sup> chelator, BAPTA-AM (1,2-bis(o-aminophenoxy)ethane-<i>N</i>,<i>N</i>,<i>N</i>′,<i>N</i>′-tetraacetic acid). These results indicate a potential signaling cascade involving herbivore-associated elicitors, Ca<sup>2+</sup>, and ROS in plants during insect feeding. In summary, our results demonstrate that plants incorporate a variety of independent signals connected with their herbivores to regulate and mount their defense responses. |
| first_indexed | 2024-03-09T06:04:16Z |
| format | Article |
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| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T06:04:16Z |
| publishDate | 2020-11-01 |
| publisher | MDPI AG |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-552b0192e8dc4b9a919a0d01ecfee7412023-12-03T12:05:36ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-11-012121829710.3390/ijms21218297Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato ProtoplastsAkanksha Gandhi0Rupesh R. Kariyat1Cruz Chappa2Mandeep Tayal3Nirakar Sahoo4Department of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USADepartment of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USADepartment of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USADepartment of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USADepartment of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USAPlants are under constant attack by a suite of insect herbivores. Over millions of years of coexistence, plants have evolved the ability to sense insect feeding via herbivore-associated elicitors in oral secretions, which can mobilize defense responses. However, herbivore-associated elicitors and the intrinsic downstream modulator of such interactions remain less understood. In this study, we show that tobacco hornworm caterpillar (<i>Manduca sexta</i>) oral secretion (OS) induces reactive oxygen species (ROS) in tomato (<i>Solanum lycopersicum</i>) protoplasts. By using a dye-based ROS imaging approach, our study shows that application of plant-fed (PF) <i>M. sexta</i> OS generates significantly higher ROS while artificial diet-fed (DF) caterpillar OS failed to induce ROS in isolated tomato protoplasts. Elevation in ROS generation was saturated after ~140 s of PF OS application. ROS production was also suppressed in the presence of an antioxidant NAC (<i>N</i>-acetyl-<i>L</i>-cysteine). Interestingly, PF OS-induced ROS increase was abolished in the presence of a Ca<sup>2+</sup> chelator, BAPTA-AM (1,2-bis(o-aminophenoxy)ethane-<i>N</i>,<i>N</i>,<i>N</i>′,<i>N</i>′-tetraacetic acid). These results indicate a potential signaling cascade involving herbivore-associated elicitors, Ca<sup>2+</sup>, and ROS in plants during insect feeding. In summary, our results demonstrate that plants incorporate a variety of independent signals connected with their herbivores to regulate and mount their defense responses.https://www.mdpi.com/1422-0067/21/21/8297reactive oxygen species<i>Manduca sexta</i>oral secretionsprotoplastcalciumantioxidant |
| spellingShingle | Akanksha Gandhi Rupesh R. Kariyat Cruz Chappa Mandeep Tayal Nirakar Sahoo Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts International Journal of Molecular Sciences reactive oxygen species <i>Manduca sexta</i> oral secretions protoplast calcium antioxidant |
| title | Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts |
| title_full | Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts |
| title_fullStr | Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts |
| title_full_unstemmed | Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts |
| title_short | Tobacco Hornworm (<i>Manduca sexta</i>) Oral Secretion Elicits Reactive Oxygen Species in Isolated Tomato Protoplasts |
| title_sort | tobacco hornworm i manduca sexta i oral secretion elicits reactive oxygen species in isolated tomato protoplasts |
| topic | reactive oxygen species <i>Manduca sexta</i> oral secretions protoplast calcium antioxidant |
| url | https://www.mdpi.com/1422-0067/21/21/8297 |
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