Lycopene β-cyclase expression influences plant physiology, development, and metabolism in tobacco plants

Abstract Carotenoids are important isoprenoids produced in the plastids of photosynthetic organisms that play key roles in photoprotection and antioxidative processes. β-Carotene is generated from lycopene by lycopene β-cyclase (LCYB). Previously, we demonstrated that the introduction of the Daucus...

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Veröffentlicht in:Journal of experimental botany 2021-03, Vol.72 (7), p.2544-2569
Hauptverfasser: Kössler, Stella, Armarego-Marriott, Tegan, Tarkowská, Danuše, Turečková, Veronika, Agrawal, Shreya, Mi, Jianing, de Souza, Leonardo Perez, Schöttler, Mark Aurel, Schadach, Anne, Fröhlich, Anja, Bock, Ralph, Al-Babili, Salim, Ruf, Stephanie, Sampathkumar, Arun, Moreno, Juan C
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container_end_page 2569
container_issue 7
container_start_page 2544
container_title Journal of experimental botany
container_volume 72
creator Kössler, Stella
Armarego-Marriott, Tegan
Tarkowská, Danuše
Turečková, Veronika
Agrawal, Shreya
Mi, Jianing
de Souza, Leonardo Perez
Schöttler, Mark Aurel
Schadach, Anne
Fröhlich, Anja
Bock, Ralph
Al-Babili, Salim
Ruf, Stephanie
Sampathkumar, Arun
Moreno, Juan C
description Abstract Carotenoids are important isoprenoids produced in the plastids of photosynthetic organisms that play key roles in photoprotection and antioxidative processes. β-Carotene is generated from lycopene by lycopene β-cyclase (LCYB). Previously, we demonstrated that the introduction of the Daucus carota (carrot) DcLCYB1 gene into tobacco (cv. Xanthi) resulted in increased levels of abscisic acid (ABA) and especially gibberellins (GAs), resulting in increased plant yield. In order to understand this phenomenon prior to exporting this genetic strategy to crops, we generated tobacco (Nicotiana tabacum cv. Petit Havana) mutants that exhibited a wide range of LCYB expression. Transplastomic plants expressing DcLCYB1 at high levels showed a wild-type-like growth, even though their pigment content was increased and their leaf GA1 content was reduced. RNA interference (RNAi) NtLCYB lines showed different reductions in NtLCYB transcript abundance, correlating with reduced pigment content and plant variegation. Photosynthesis (leaf absorptance, Fv/Fm, and light-saturated capacity of linear electron transport) and plant growth were impaired. Remarkably, drastic changes in phytohormone content also occurred in the RNAi lines. However, external application of phytohormones was not sufficient to rescue these phenotypes, suggesting that altered photosynthetic efficiency might be another important factor explaining their reduced biomass. These results show that LCYB expression influences plant biomass by different mechanisms and suggests thresholds for LCYB expression levels that might be beneficial or detrimental for plant growth. A lycopene β-cyclase expression threshold influences plant biomass, development, and metabolism by modulating pigment and phytohormone content in transplastomic and RNAi tobacco lines.
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Previously, we demonstrated that the introduction of the Daucus carota (carrot) DcLCYB1 gene into tobacco (cv. Xanthi) resulted in increased levels of abscisic acid (ABA) and especially gibberellins (GAs), resulting in increased plant yield. In order to understand this phenomenon prior to exporting this genetic strategy to crops, we generated tobacco (Nicotiana tabacum cv. Petit Havana) mutants that exhibited a wide range of LCYB expression. Transplastomic plants expressing DcLCYB1 at high levels showed a wild-type-like growth, even though their pigment content was increased and their leaf GA1 content was reduced. RNA interference (RNAi) NtLCYB lines showed different reductions in NtLCYB transcript abundance, correlating with reduced pigment content and plant variegation. Photosynthesis (leaf absorptance, Fv/Fm, and light-saturated capacity of linear electron transport) and plant growth were impaired. Remarkably, drastic changes in phytohormone content also occurred in the RNAi lines. However, external application of phytohormones was not sufficient to rescue these phenotypes, suggesting that altered photosynthetic efficiency might be another important factor explaining their reduced biomass. These results show that LCYB expression influences plant biomass by different mechanisms and suggests thresholds for LCYB expression levels that might be beneficial or detrimental for plant growth. 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Previously, we demonstrated that the introduction of the Daucus carota (carrot) DcLCYB1 gene into tobacco (cv. Xanthi) resulted in increased levels of abscisic acid (ABA) and especially gibberellins (GAs), resulting in increased plant yield. In order to understand this phenomenon prior to exporting this genetic strategy to crops, we generated tobacco (Nicotiana tabacum cv. Petit Havana) mutants that exhibited a wide range of LCYB expression. Transplastomic plants expressing DcLCYB1 at high levels showed a wild-type-like growth, even though their pigment content was increased and their leaf GA1 content was reduced. RNA interference (RNAi) NtLCYB lines showed different reductions in NtLCYB transcript abundance, correlating with reduced pigment content and plant variegation. Photosynthesis (leaf absorptance, Fv/Fm, and light-saturated capacity of linear electron transport) and plant growth were impaired. Remarkably, drastic changes in phytohormone content also occurred in the RNAi lines. However, external application of phytohormones was not sufficient to rescue these phenotypes, suggesting that altered photosynthetic efficiency might be another important factor explaining their reduced biomass. These results show that LCYB expression influences plant biomass by different mechanisms and suggests thresholds for LCYB expression levels that might be beneficial or detrimental for plant growth. 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However, external application of phytohormones was not sufficient to rescue these phenotypes, suggesting that altered photosynthetic efficiency might be another important factor explaining their reduced biomass. These results show that LCYB expression influences plant biomass by different mechanisms and suggests thresholds for LCYB expression levels that might be beneficial or detrimental for plant growth. A lycopene β-cyclase expression threshold influences plant biomass, development, and metabolism by modulating pigment and phytohormone content in transplastomic and RNAi tobacco lines.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>33484250</pmid><doi>10.1093/jxb/erab029</doi><tpages>26</tpages><orcidid>https://orcid.org/0000-0001-9722-5262</orcidid><orcidid>https://orcid.org/0000-0001-7846-9472</orcidid><orcidid>https://orcid.org/0000-0003-4823-2882</orcidid><oa>free_for_read</oa></addata></record>
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source MEDLINE; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection
subjects Carotenoids
Gene Expression Regulation, Plant
Intramolecular Lyases - genetics
Intramolecular Lyases - metabolism
Nicotiana - genetics
Nicotiana - metabolism
Plant Proteins - genetics
Plant Proteins - metabolism
Plants, Genetically Modified - genetics
Plants, Genetically Modified - metabolism
Research Papers
title Lycopene β-cyclase expression influences plant physiology, development, and metabolism in tobacco plants
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