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Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use

Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria, which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically,...

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Autores principales: Hirooka, Shunsuke, Itabashi, Takeshi, Ichinose, Takako M., Onuma, Ryo, Fujiwara, Takayuki, Yamashita, Shota, Jong, Lin Wei, Tomita, Reiko, Iwane, Atsuko H., Miyagishima, Shin-ya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9565259/
https://www.ncbi.nlm.nih.gov/pubmed/36194630
http://dx.doi.org/10.1073/pnas.2210665119
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author Hirooka, Shunsuke
Itabashi, Takeshi
Ichinose, Takako M.
Onuma, Ryo
Fujiwara, Takayuki
Yamashita, Shota
Jong, Lin Wei
Tomita, Reiko
Iwane, Atsuko H.
Miyagishima, Shin-ya
author_facet Hirooka, Shunsuke
Itabashi, Takeshi
Ichinose, Takako M.
Onuma, Ryo
Fujiwara, Takayuki
Yamashita, Shota
Jong, Lin Wei
Tomita, Reiko
Iwane, Atsuko H.
Miyagishima, Shin-ya
author_sort Hirooka, Shunsuke
collection PubMed
description Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria, which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall–less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall–less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-to-diploid transition in Galdieria, providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae.
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spelling pubmed-95652592022-10-15 Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use Hirooka, Shunsuke Itabashi, Takeshi Ichinose, Takako M. Onuma, Ryo Fujiwara, Takayuki Yamashita, Shota Jong, Lin Wei Tomita, Reiko Iwane, Atsuko H. Miyagishima, Shin-ya Proc Natl Acad Sci U S A Biological Sciences Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria, which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall–less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall–less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-to-diploid transition in Galdieria, providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae. National Academy of Sciences 2022-10-04 2022-10-11 /pmc/articles/PMC9565259/ /pubmed/36194630 http://dx.doi.org/10.1073/pnas.2210665119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Hirooka, Shunsuke
Itabashi, Takeshi
Ichinose, Takako M.
Onuma, Ryo
Fujiwara, Takayuki
Yamashita, Shota
Jong, Lin Wei
Tomita, Reiko
Iwane, Atsuko H.
Miyagishima, Shin-ya
Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title_full Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title_fullStr Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title_full_unstemmed Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title_short Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use
title_sort life cycle and functional genomics of the unicellular red alga galdieria for elucidating algal and plant evolution and industrial use
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9565259/
https://www.ncbi.nlm.nih.gov/pubmed/36194630
http://dx.doi.org/10.1073/pnas.2210665119
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