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Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus

Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to...

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Autores principales: Maeda, Taro, Takahashi, Shunichi, Yoshida, Takao, Shimamura, Shigeru, Takaki, Yoshihiro, Nagai, Yukiko, Toyoda, Atsushi, Suzuki, Yutaka, Arimoto, Asuka, Ishii, Hisaki, Satoh, Nori, Nishiyama, Tomoaki, Hasebe, Mitsuyasu, Maruyama, Tadashi, Minagawa, Jun, Obokata, Junichi, Shigenobu, Shuji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8079154/
https://www.ncbi.nlm.nih.gov/pubmed/33902812
http://dx.doi.org/10.7554/eLife.60176
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author Maeda, Taro
Takahashi, Shunichi
Yoshida, Takao
Shimamura, Shigeru
Takaki, Yoshihiro
Nagai, Yukiko
Toyoda, Atsushi
Suzuki, Yutaka
Arimoto, Asuka
Ishii, Hisaki
Satoh, Nori
Nishiyama, Tomoaki
Hasebe, Mitsuyasu
Maruyama, Tadashi
Minagawa, Jun
Obokata, Junichi
Shigenobu, Shuji
author_facet Maeda, Taro
Takahashi, Shunichi
Yoshida, Takao
Shimamura, Shigeru
Takaki, Yoshihiro
Nagai, Yukiko
Toyoda, Atsushi
Suzuki, Yutaka
Arimoto, Asuka
Ishii, Hisaki
Satoh, Nori
Nishiyama, Tomoaki
Hasebe, Mitsuyasu
Maruyama, Tadashi
Minagawa, Jun
Obokata, Junichi
Shigenobu, Shuji
author_sort Maeda, Taro
collection PubMed
description Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug, Plakobranchus ocellatus, and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the phenotype acquisition without horizontal gene transfer.
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spelling pubmed-80791542021-04-30 Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus Maeda, Taro Takahashi, Shunichi Yoshida, Takao Shimamura, Shigeru Takaki, Yoshihiro Nagai, Yukiko Toyoda, Atsushi Suzuki, Yutaka Arimoto, Asuka Ishii, Hisaki Satoh, Nori Nishiyama, Tomoaki Hasebe, Mitsuyasu Maruyama, Tadashi Minagawa, Jun Obokata, Junichi Shigenobu, Shuji eLife Evolutionary Biology Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug, Plakobranchus ocellatus, and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the phenotype acquisition without horizontal gene transfer. eLife Sciences Publications, Ltd 2021-04-27 /pmc/articles/PMC8079154/ /pubmed/33902812 http://dx.doi.org/10.7554/eLife.60176 Text en © 2021, Maeda et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Maeda, Taro
Takahashi, Shunichi
Yoshida, Takao
Shimamura, Shigeru
Takaki, Yoshihiro
Nagai, Yukiko
Toyoda, Atsushi
Suzuki, Yutaka
Arimoto, Asuka
Ishii, Hisaki
Satoh, Nori
Nishiyama, Tomoaki
Hasebe, Mitsuyasu
Maruyama, Tadashi
Minagawa, Jun
Obokata, Junichi
Shigenobu, Shuji
Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_full Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_fullStr Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_full_unstemmed Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_short Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus
title_sort chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, plakobranchus ocellatus
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8079154/
https://www.ncbi.nlm.nih.gov/pubmed/33902812
http://dx.doi.org/10.7554/eLife.60176
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