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A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant

Insect-induced galls are microhabitats distinct from the outer environment that support inhabitants by providing improved nutrients, defence against enemies, and other unique features. It is intriguing as to how insects reprogram and modify plant morphogenesis. Because most of the gall systems are f...

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Autores principales: Murakami, Ryo, Ushima, Ryo, Sugimoto, Ryoma, Tamaoki, Daisuke, Karahara, Ichirou, Hanba, Yuko, Wakasugi, Tatsuya, Tsuchida, Tsutomu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8217554/
https://www.ncbi.nlm.nih.gov/pubmed/34155293
http://dx.doi.org/10.1038/s41598-021-92417-3
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author Murakami, Ryo
Ushima, Ryo
Sugimoto, Ryoma
Tamaoki, Daisuke
Karahara, Ichirou
Hanba, Yuko
Wakasugi, Tatsuya
Tsuchida, Tsutomu
author_facet Murakami, Ryo
Ushima, Ryo
Sugimoto, Ryoma
Tamaoki, Daisuke
Karahara, Ichirou
Hanba, Yuko
Wakasugi, Tatsuya
Tsuchida, Tsutomu
author_sort Murakami, Ryo
collection PubMed
description Insect-induced galls are microhabitats distinct from the outer environment that support inhabitants by providing improved nutrients, defence against enemies, and other unique features. It is intriguing as to how insects reprogram and modify plant morphogenesis. Because most of the gall systems are formed on trees, it is difficult to maintain them in laboratories and to comprehend the mechanisms operative in them through experimental manipulations. Herein, we propose a new model insect, Smicronyx madaranus, for studying the mechanisms of gall formation. This weevil forms spherical galls on the shoots of Cuscuta campestris, an obligate parasitic plant. We established a stable system for breeding and maintaining this ecologically intriguing insect in the laboratory, and succeeded in detailed analyses of the gall-forming behaviour, gall formation process, and histochemical and physiological features. Parasitic C. campestris depends on host plants for its nutrients, and usually shows low chlorophyll content and photosynthetic activity. We demonstrate that S. madaranus-induced galls have significantly increased CO(2) absorbance. Moreover, chloroplasts and starch accumulated in gall tissues at locations inhabited by the weevil larvae. These results suggest that the gall-inducing weevils enhance the photosynthetic activity in C. campestris, and modify the plant tissue to a nutrient-rich shelter for them.
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spelling pubmed-82175542021-06-22 A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant Murakami, Ryo Ushima, Ryo Sugimoto, Ryoma Tamaoki, Daisuke Karahara, Ichirou Hanba, Yuko Wakasugi, Tatsuya Tsuchida, Tsutomu Sci Rep Article Insect-induced galls are microhabitats distinct from the outer environment that support inhabitants by providing improved nutrients, defence against enemies, and other unique features. It is intriguing as to how insects reprogram and modify plant morphogenesis. Because most of the gall systems are formed on trees, it is difficult to maintain them in laboratories and to comprehend the mechanisms operative in them through experimental manipulations. Herein, we propose a new model insect, Smicronyx madaranus, for studying the mechanisms of gall formation. This weevil forms spherical galls on the shoots of Cuscuta campestris, an obligate parasitic plant. We established a stable system for breeding and maintaining this ecologically intriguing insect in the laboratory, and succeeded in detailed analyses of the gall-forming behaviour, gall formation process, and histochemical and physiological features. Parasitic C. campestris depends on host plants for its nutrients, and usually shows low chlorophyll content and photosynthetic activity. We demonstrate that S. madaranus-induced galls have significantly increased CO(2) absorbance. Moreover, chloroplasts and starch accumulated in gall tissues at locations inhabited by the weevil larvae. These results suggest that the gall-inducing weevils enhance the photosynthetic activity in C. campestris, and modify the plant tissue to a nutrient-rich shelter for them. Nature Publishing Group UK 2021-06-21 /pmc/articles/PMC8217554/ /pubmed/34155293 http://dx.doi.org/10.1038/s41598-021-92417-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Murakami, Ryo
Ushima, Ryo
Sugimoto, Ryoma
Tamaoki, Daisuke
Karahara, Ichirou
Hanba, Yuko
Wakasugi, Tatsuya
Tsuchida, Tsutomu
A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title_full A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title_fullStr A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title_full_unstemmed A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title_short A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
title_sort new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8217554/
https://www.ncbi.nlm.nih.gov/pubmed/34155293
http://dx.doi.org/10.1038/s41598-021-92417-3
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