Photosynthesis without β-carotene.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
25 09 2020
Historique:
received: 15 05 2020
accepted: 24 09 2020
pubmed: 26 9 2020
medline: 4 3 2021
entrez: 25 9 2020
Statut: epublish

Résumé

Carotenoids are essential in oxygenic photosynthesis: they stabilize the pigment-protein complexes, are active in harvesting sunlight and in photoprotection. In plants, they are present as carotenes and their oxygenated derivatives, xanthophylls. While mutant plants lacking xanthophylls are capable of photoautotrophic growth, no plants without carotenes in their photosystems have been reported so far, which has led to the common opinion that carotenes are essential for photosynthesis. Here, we report the first plant that grows photoautotrophically in the absence of carotenes: a tobacco plant containing only the xanthophyll astaxanthin. Surprisingly, both photosystems are fully functional despite their carotenoid-binding sites being occupied by astaxanthin instead of β-carotene or remaining empty (i.e. are not occupied by carotenoids). These plants display non-photochemical quenching, despite the absence of both zeaxanthin and lutein and show that tobacco can regulate the ratio between the two photosystems in a very large dynamic range to optimize electron transport. Most life on Earth depends on photosynthesis, the process used by plants and many other organisms to store energy from sunlight and produce oxygen. The first steps of photosynthesis, the capture and conversion of sunlight into chemical energy, happen in large assemblies of proteins containing many pigment molecules called photosystems. In plants, the pigments involved in photosynthesis are green chlorophylls and carotenoids. In addition to harvesting light, carotenoids have an important role in preventing damage caused by overexposure to sunlight There are over one thousand different carotenoids in living beings, but only one, β-carotene, is present in every organism that performs the type of photosynthesis in which oxygen is released, and is thought to be essential for the process. However, this could never be proved because it is impossible to remove β-carotene from cells using typical genetic approaches without affecting all other carotenoids. Xu et al. used genetic engineering to create tobacco plants that produced a pigment called astaxanthin in place of β-carotene. Astaxanthin is a carotenoid from salmon and shrimp, not normally found in plants. These plants are the first living things known to perform photosynthesis without β-carotene and demonstrate that this pigment is not essential for photosynthesis as long as other carotenoids are present. Xu et al. also show that the photosystems can adapt to using different carotenoids, and can even operate with a reduced number of them. Xu et al’s findings show the high flexibility of photosynthesis in plants, which are able to incorporate non-native elements to the process. These results are also important in the context of increasing the photosynthetic efficiency, and thus the productivity of crops, since they show that a radical redesign of the photosynthetic machinery is feasible.

Autres résumés

Type: plain-language-summary (eng)
Most life on Earth depends on photosynthesis, the process used by plants and many other organisms to store energy from sunlight and produce oxygen. The first steps of photosynthesis, the capture and conversion of sunlight into chemical energy, happen in large assemblies of proteins containing many pigment molecules called photosystems. In plants, the pigments involved in photosynthesis are green chlorophylls and carotenoids. In addition to harvesting light, carotenoids have an important role in preventing damage caused by overexposure to sunlight There are over one thousand different carotenoids in living beings, but only one, β-carotene, is present in every organism that performs the type of photosynthesis in which oxygen is released, and is thought to be essential for the process. However, this could never be proved because it is impossible to remove β-carotene from cells using typical genetic approaches without affecting all other carotenoids. Xu et al. used genetic engineering to create tobacco plants that produced a pigment called astaxanthin in place of β-carotene. Astaxanthin is a carotenoid from salmon and shrimp, not normally found in plants. These plants are the first living things known to perform photosynthesis without β-carotene and demonstrate that this pigment is not essential for photosynthesis as long as other carotenoids are present. Xu et al. also show that the photosystems can adapt to using different carotenoids, and can even operate with a reduced number of them. Xu et al’s findings show the high flexibility of photosynthesis in plants, which are able to incorporate non-native elements to the process. These results are also important in the context of increasing the photosynthetic efficiency, and thus the productivity of crops, since they show that a radical redesign of the photosynthetic machinery is feasible.

Identifiants

pubmed: 32975516
doi: 10.7554/eLife.58984
pii: 58984
pmc: PMC7609050
doi:
pii:

Substances chimiques

Xanthophylls 0
beta Carotene 01YAE03M7J
astaxanthine 8XPW32PR7I

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Nederlandse Organisatie voor Wetenschappelijk Onderzoek
ID : Vici
Pays : International
Organisme : H2020 European Research Council
ID : ERC CON 281341
Pays : International
Organisme : H2020 European Research Council
ID : ERC ADG 669982
Pays : International

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2020, Xu et al.

Déclaration de conflit d'intérêts

PX, VC, WN, GS, LB, YL, DK, RB, RC No competing interests declared

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Auteurs

Pengqi Xu (P)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

Volha U Chukhutsina (VU)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

Wojciech J Nawrocki (WJ)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

Gert Schansker (G)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

Ludwik W Bielczynski (LW)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

Yinghong Lu (Y)

Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.

Daniel Karcher (D)

Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.

Ralph Bock (R)

Max Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany.

Roberta Croce (R)

Biophysics of Photosynthesis, Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam and LaserLab Amsterdam, Amsterdam, Netherlands.

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