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

Stella Kössler,Veronika Turečková,Anne Schadach,Arun Sampathkumar,Tegan Armarego-Marriott,Juan C Moreno,Ralph Bock,Salim Al-Babili,Mark Aurel Schöttler,Anja Fröhlich,Stephanie Ruf,Danuše Tarkowská,Jianing Mi,Shreya Agrawal,Leonardo Perez De Souza,Ian Dodd

doi:10.1093/jxb/erab029

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.

Highlights

Carotenoids are 40-carbon isoprenoids with polyene chains containing up to 15 conjugated double bonds (Hirschberg, 2001)
We show that plastid DcLCYB1 expression leads to increased LCYB activity and pigment content (β-carotene and violaxanthin), but not necessarily to increased biomass and photosynthesis, whereas reduced NtLCYB expression negatively affects plant physiology and development, primary and secondary metabolism, photosynthetic efficiency and plant biomass
An increased GA/abscisic acid (ABA) ratio played a key role in the higher growth phenotype in the nuclear DcLCYB1 tobacco lines (Fig. 8C)

Summary

Introduction

Carotenoids are 40-carbon isoprenoids with polyene chains containing up to 15 conjugated double bonds (Hirschberg, 2001). By contrast, reduced te NtLCYB expression in our RNAi lines were hypothesized to trigger reduced expression of key p genes of carotenoid and carotenoid-related pathways, causing a reduction in the content e of key isoprenoids (e.g. β-carotene, xanthophylls, chlorophylls, GA and ABA) and leading to reduced growth and biomass. If this is true, the reduced plant biomass might be due c to these additional disturbances and impaired photosynthetic performance, which is directly Ac related to the structural function of carotenoid in the photosynthetic apparatus. We show that plastid DcLCYB1 expression leads to increased LCYB activity (indirectly measured as increased CPTA tolerance) and pigment content (β-carotene and violaxanthin), but not necessarily to increased biomass and photosynthesis, whereas reduced NtLCYB expression negatively affects plant physiology and development, primary and secondary metabolism, photosynthetic efficiency and plant biomass

Materials and Methods

Findings

Discussion