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.

Center for Desert Agriculture Biological and Environmental Science and Engineering Division Thuwal Saudi Arabia

Laboratory of Growth Regulators Institute of Experimental Botany The Czech Academy of Sciences and Palacký University Šlechtitelů Olomouc Czech Republic

Max Planck Institut für Molekulare Pflanzenphysiologie Am Mühlenberg1 D 14476 Potsdam Golm Germany

Zobrazit více v PubMed

Al-Babili S, Bouwmeester HJ. 2015. Strigolactones, a novel carotenoid-derived plant hormone. Annual Review of Plant Biology 66, 161–186. PubMed

Albus CA, Salinas A, Czarnecki O, Kahlau S, Rothbart M, Thiele W, Lein W, Bock R, Grimm B, Schöttler MA. 2012. LCAA, a novel factor required for magnesium protoporphyrin monomethylester cyclase accumulation and feedback control of aminolevulinic acid biosynthesis in tobacco. Plant Physiology 160, 1923–1939. PubMed PMC

Aluru MR, Bae H, Wu D, Rodermel SR. 2001. The Arabidopsis PubMed PMC

Aluru MR, Zola J, Foudree A, Rodermel SR. 2009. Chloroplast photooxidation-induced transcriptome reprogramming in Arabidopsis PubMed PMC

Andrade-Souza V, Costa MG, Chen CX, Gmitter Jr FG, Costa MA. 2011. Physical location of the carotenoid biosynthesis genes PubMed

Apel W, Bock R. 2009. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiology 151, 59–66. PubMed PMC

Armarego-Marriott T, Kowalewska Ł, Burgos A, et al. 2019. Highly resolved systems biology to dissect the etioplast-to-chloroplast transition in tobacco leaves. Plant Physiology 180, 654–681. PubMed PMC

Austin JR 2nd, Staehelin LA. 2011. Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiology 155, 1601–1611. PubMed PMC

Avendaño-Vázquez AO, Cordoba E, Llamas E, et al. 2014. An uncharacterized apocarotenoid-derived signal generated in ζ-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in PubMed PMC

Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, Niyogi KK. 2004. Photo-oxidative stress in a xanthophyll-deficient mutant of PubMed

Biemelt S, Tschiersch H, Sonnewald U. 2004. Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiology 135, 254–265. PubMed PMC

Bock R. 2001. Transgenic plastids in basic research and plant biotechnology. Journal of Molecular Biology 312, 425–438. PubMed

Bock R. 2007. Plastid biotechnology: prospects for herbicide and insect resistance, metabolic engineering and molecular farming. Current Opinion in Biotechnology 18, 100–106. PubMed

Bouvier F, Rahier A, Camara B. 2005. Biogenesis, molecular regulation and function of plant isoprenoids. Progress in Lipid Research 44, 357–429. PubMed

Brewer PB, Koltai H, Beveridge CA. 2013. Diverse roles of strigolactones in plant development. Molecular Plant 6, 18–28. PubMed

Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L, Fernie AR, Willmitzer L, Giavalisco P. 2013. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in PubMed

Carretero-Paulet L, Cairó A, Botella-Pavía P, Besumbes O, Campos N, Boronat A, Rodríguez-Concepción M. 2006. Enhanced flux through the methylerythritol 4-phosphate pathway in PubMed

Cazzaniga S, Li Z, Niyogi KK, Bassi R, Dall’Osto L. 2012. The Arabidopsis PubMed PMC

Cazzonelli CI, Pogson BJ. 2010. Source to sink: regulation of carotenoid biosynthesis in plants. Trends in Plant Science 15, 266–274. PubMed

Chen X, Han H, Jiang P, Nie L, Bao H, Fan P, Lv S, Feng J, Li Y. 2011. Transformation of beta-lycopene cyclase genes from PubMed

Clarke JL, Daniell H. 2011. Plastid biotechnology for crop production: present status and future perspectives. Plant Molecular Biology 76, 211–220. PubMed PMC

Coles JP, Phillips AL, Croker SJ, García-Lepe R, Lewis MJ, Hedden P. 1999. Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. The Plant Journal 17, 547–556. PubMed

Cuadros-Inostroza A, Caldana C, Redestig H, Kusano M, Lisec J, Peña-Cortés H, Willmitzer L, Hannah MA. 2009. TargetSearch—a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics 10, 428. PubMed PMC

Cunningham FX, Gantt E. 1998. Genes and enzymes of carotenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 557–583. PubMed

Dall’Osto L, Bassi R, Ruban A. 2014. Photoprotective mechanisms: carotenoids. Plastid Biology 5, 393–435.

Dall’Osto L, Caffarri S, Bassi R. 2005. A mechanism of nonphotochemical energy dissipation, independent from PsbS, revealed by a conformational change in the antenna protein CP26. The Plant Cell 17, 1217–1232. PubMed PMC

Dall’Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R. 2007 PubMed PMC

Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R. 2007 PubMed

Dall’Osto L, Piques M, Ronzani M, Molesini B, Alboresi A, Cazzaniga S, Bassi R. 2013. The PubMed PMC

D’Ambrosio C, Giorio G, Marino I, Merendino A, Petrozza A, Salfi L, Stigliani AL, Cellini F. 2004. Virtually complete conversion of lycopene into β-carotene in fruits of tomato plants transformed with the tomato

Davière JM, Achard P. 2013. Gibberellin signaling in plants. Development 140, 1147–1151. PubMed

Davison PA, Hunter CN, Horton P. 2002. Overexpression of β-carotene hydroxylase enhances stress tolerance in PubMed

Demmig-Adams B, Gilmore AM, Adams WW 3rd. 1996. Carotenoids 3: In vivo function of carotenoids in higher plants. FASEB Journal 10, 403–412. PubMed

Dickinson AJ, Lehner K, Mi J, Jia KP, Mijar M, Dinneny J, Al-Babili S, Benfey PN. 2019. β-Cyclocitral is a conserved root growth regulator. Proceedings of the National Academy of Sciences, USA 116, 10563–10567. PubMed PMC

Doyle JJ, Doyle JL. 1990. A rapid total DNA preparation procedure for fresh plant tissue. Focus 12, 13–15.

Elghabi Z, Karcher D, Zhou F, Ruf S, Bock R. 2011. Optimization of the expression of the HIV fusion inhibitor cyanovirin-N from the tobacco plastid genome. Plant Biotechnology Journal 9, 599–608. PubMed

Fang J, Chai C, Qian Q, et al. 2008. Mutations of genes in synthesis of the carotenoid precursors of ABA lead to pre-harvest sprouting and photo-oxidation in rice. The Plant Journal 54, 177–189. PubMed PMC

Fernández-San Millán A, Aranjuelo I, Douthe C, Nadal M, Ancín M, Larraya L, Farran I, Flexas J, Veramendi J. 2018. Physiological performance of transplastomic tobacco plants overexpressing aquaporin AQP1 in chloroplast membranes. Journal of Experimental Botany 69, 3661–3673. PubMed PMC

Fernie AR, Aharoni A, Willmitzer L, Stitt M, Tohge T, Kopka J, Carroll AJ, Saito K, Fraser PD, DeLuca V. 2011. Recommendations for reporting metabolite data. The Plant Cell 23, 2477–2482. PubMed PMC

Fiore A, Dall’Osto L, Cazzaniga S, Diretto G, Giuliano G, Bassi R. 2012. A quadruple mutant of Arabidopsis reveals a β-carotene hydroxylation activity for LUT1/CYP97C1 and a regulatory role of xanthophylls on determination of the PSI/PSII ratio. BMC Plant Biology 12, 50. PubMed PMC

Formaggio E, Cinque G, Bassi R. 2001. Functional architecture of the major light-harvesting complex from higher plants. Journal of Molecular Biology 314, 1157–1166. PubMed

Frank HA, Cogdell RJ. 1993. Photochemistry and functions of carotenoids. In: Young A, Britton G, eds. Carotenoids in photosynthesis. Dordrecht: Springer, 252–326.

Frank HA, Cogdell RJ. 1996. Carotenoids in photosynthesis. Photochemistry and Photobiology 63, 257–264. PubMed

Krause GH, Weis E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.

Gallego-Giraldo L, Ubeda-Tomás S, Gisbert C, García-Martínez JL, Moritz T, López-Díaz I. 2008. Gibberellin homeostasis in tobacco is regulated by gibberellin metabolism genes with different gibberellin sensitivity. Plant & Cell Physiology 49, 679–690. PubMed

Garciarrubio A, Legaria JP, Covarrubias AA. 1997. Abscisic acid inhibits germination of mature Arabidopsis seeds by limiting the availability of energy and nutrients. Planta 203, 182–187. PubMed

Giavalisco P, Li Y, Matthes A, Eckhardt A, Hubberten HM, Hesse H, Segu S, Hummel J, Köhl K, Willmitzer L. 2011. Elemental formula annotation of polar and lipophilic metabolites using PubMed

Giuliano G, Al-Babili S, von Lintig J. 2003. Carotenoid oxygenases: cleave it or leave it. Trends in Plant Science 8, 145–149. PubMed

Götz T, Sandmann G, Römer S. 2002. Expression of a bacterial carotene hydroxylase gene ( PubMed

Green BR, Durnford DG. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 47, 685–714. PubMed

Gruszecki WI, Strzałka K. 2005. Carotenoids as modulators of lipid membrane physical properties. Biochimica et Biophysica Acta 1740, 108–115. PubMed

Gupta R, Chakrabarty SK. 2013. Gibberellic acid in plant: still a mystery unresolved. Plant Signaling and Behaviour 8, e25504. PubMed PMC

Han H, Li Y, Zhou S. 2008. Overexpression of phytoene synthase gene from PubMed

Havaux M. 1998. Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science 3, 147–151.

Havaux M, Dall’osto L, Bassi R. 2007. Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. Plant Physiology 145, 1506–1520. PubMed PMC

Havaux M, Dall’Osto L, Cuiné S, Giuliano G, Bassi R. 2004. The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in PubMed

Havaux M, Niyogi KK. 1999. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences, USA 96, 8762–8767. PubMed PMC

Hedden P, Thomas SG. 2012. Gibberellin biosynthesis and its regulation. The Biochemical Journal 444, 11–25. PubMed

Hirschberg J. 2001. Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4, 210–218. PubMed

Ji J, Wang G, Wang J, Wang P. 2009. Functional analysis of multiple carotenogenic genes from PubMed

Just BJ, Santos CA, Fonseca ME, Boiteux LS, Oloizia BB, Simon PW. 2007. Carotenoid biosynthesis structural genes in carrot ( PubMed

Just BJ, Santos CA, Yandell BS, Simon PW. 2009. Major QTL for carrot color are positionally associated with carotenoid biosynthetic genes and interact epistatically in a domesticated × wild carrot cross. Theoretical and Applied Genetics 119, 1155–1169. PubMed

Kang C, Zhai H, Xue L, Zhao N, He S, Liu Q. 2018. A lycopene β-cyclase gene, PubMed

Kassambara A. 2018. ggpubr: ‘ggplot2’ based publication ready plots: R package version 0.2. https://rpkgs.datanovia.com/ggpubr/

Kirchsteiger K, Ferrández J, Pascual MB, González M, Cejudo FJ. 2012. NADPH thioredoxin reductase C is localized in plastids of photosynthetic and nonphotosynthetic tissues and is involved in lateral root formation in Arabidopsis. The Plant Cell 24, 1534–1548. PubMed PMC

Kolde R. 2019. pheatmap: Pretty Heatmaps. R package version 1.0.12. https://CRAN.R-project.org/package=pheatmap

Kramer DM, Johnson G, Kiirats O, Edwards GE. 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209. PubMed

Krinsky NI. 1989. Antioxidant functions of carotenoids. Free Radical Biology & Medicine 7, 617–635. PubMed

Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP. 2016. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857–861. PubMed

Kumar S, Hahn FM, Baidoo E, Kahlon TS, Wood DF, McMahan CM, Cornish K, Keasling JD, Daniell H, Whalen MC. 2012. Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts. Metabolic Engineering 14, 19–28. PubMed PMC

Kuroda H, Maliga P. 2001. Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Research 29, 970–975. PubMed PMC

Li D, Heiling S, Baldwin IT, Gaquerel E. 2016. Illuminating a plant’s tissue-specific metabolic diversity using computational metabolomics and information theory. Proceedings of the National Academy of Sciences, USA 113, E7610–E7618. PubMed PMC

Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK. 2009. Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the PubMed PMC

Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387–396. PubMed

Llorente B, Torres-Montilla S, Morelli L, et al. 2020. Synthetic conversion of leaf chloroplasts into carotenoid-rich plastids reveals mechanistic basis of natural chromoplast development. Proceedings of the National Academy of Sciences, USA 117, 21796–21803. PubMed PMC

Lu Y, Rijzaani H, Karcher D, Ruf S, Bock R. 2013. Efficient metabolic pathway engineering in transgenic tobacco and tomato plastids with synthetic multigene operons. Proceedings of the National Academy of Sciences, USA 110, E623–E632. PubMed PMC

Lu Y, Stegemann S, Agrawal S, Karcher D, Ruf S, Bock R. 2017. Horizontal transfer of a synthetic metabolic pathway between plant species. Current Biology 27, 3034–3041.e3. PubMed

Ma XW, Ma FW, Mi YF, Ma YH, Shu HR. 2008. Morphological and physiological responses of two contrasting

Mhamdi A, Van Breusegem F. 2018. Reactive oxygen species in plant development. Development 145, dev164376. PubMed

Mi J, Jia KP, Wang JY, Al-Babili S. 2018. A rapid LC-MS method for qualitative and quantitative profiling of plant apocarotenoids. Analytica Chimica Acta 1035, 87–95. PubMed

Moreno JC, Cerda A, Simpson K, Lopez-Diaz I, Carrera E, Handford M, Stange C. 2016. Increased PubMed PMC

Moreno JC, Mi J, Agrawal S, Kössler S, Turečková V, Tarkowská D, Thiele W, Al-Babili S, Bock R, Schöttler MA. 2020. Expression of a carotenogenic gene allows faster biomass production by redesigning plant architecture and improving photosynthetic efficiency in tobacco. The Plant Journal 103, 1967–1984. PubMed

Moreno JC, Pizarro L, Fuentes P, Handford M, Cifuentes V, Stange C. 2013. Levels of lycopene β-cyclase 1 modulate carotenoid gene expression and accumulation in PubMed PMC

Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.

Nagel OW, Konings H, Lambers H. 1994. Growth-rate, plant development and water relations of the ABA-deficient tomato mutant

Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165–185. PubMed

Nitsch L, Kohlen W, Oplaat C, et al. 2012. ABA-deficiency results in reduced plant and fruit size in tomato. Journal of Plant Physiology 169, 878–883. PubMed

Niyogi KK. 2000. Safety valves for photosynthesis. Current Opinion in Plant Biology 3, 455–460. PubMed

Niyogi KK, Grossman AR, Björkman O. 1998. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. The Plant Cell 10, 1121–1134. PubMed PMC

Oey M, Lohse M, Kreikemeyer B, Bock R. 2009. Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. The Plant Journal 57, 436–445. PubMed

Olson JA. 1996. Benefits and liabilities of vitamin A and carotenoids. The Journal of Nutrition 126, 1208S–1212S. PubMed

Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V. 2005. Genetic and molecular identification of genes required for female gametophyte development and function in PubMed

Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ. 2002. Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. The Plant Cell 14, 321–332. PubMed PMC

Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45. PubMed PMC

Pogson BJ, Niyogi KK, Björkman O, DellaPenna D. 1998. Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in PubMed PMC

Porra RJ, Thompson WA, Kriedemann PE. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls

Pulido P, Perello C, Rodriguez-Concepcion M. 2012. New insights into plant isoprenoid metabolism. Molecular Plant 5, 964–967. PubMed

Qin G, Gu H, Ma L, Peng Y, Deng XW, Chen Z, Qu LJ. 2007. Disruption of phytoene desaturase gene results in albino and dwarf phenotypes in PubMed

Ralley L, Schuch W, Fraser PD, Bramley PM. 2016. Genetic modification of tomato with the tobacco lycopene β-cyclase gene produces high β-carotene and lycopene fruit. Zeitschrift für Naturforschung 71, 295–301. PubMed

R Core Team . 2018. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rittenberg D, Foster GL. 1940. A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. The Journal of Biological Chemistry 737–744.

Rosahl S, Schell J, Willmitzer L. 1987. Expression of a tuber-specific storage protein in transgenic tobacco plants: demonstration of an esterase activity. The EMBO Journal 6, 1155–1159. PubMed PMC

Rosati C, Aquilani R, Dharmapuri S, Pallara P, Marusic C, Tavazza R, Bouvier F, Camara B, Giuliano G. 2000. Metabolic engineering of beta-carotene and lycopene content in tomato fruit. The Plant Journal 24, 413–419. PubMed

Ruf S, Bock R. 2011. In vivo analysis of RNA editing in plastids. Methods in Molecular Biology 718, 137–150. PubMed

Ruf S, Hermann M, Berger IJ, Carrer H, Bock R. 2001. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nature Biotechnology 19, 870–875. PubMed

Ruf S, Karcher D, Bock R. 2007. Determining the transgene containment level provided by chloroplast transformation. Proceedings of the National Academy of Sciences, USA 104, 6998–7002. PubMed PMC

Ruiz-Sola MÁ, Rodríguez-Concepción M. 2012. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. The Arabidopsis Book 10, e0158. PubMed PMC

Salem MA, Jüppner J, Bajdzienko K, Giavalisco P. 2016. Protocol: a fast, comprehensive and reproducible one-step extraction method for the rapid preparation of polar and semi-polar metabolites, lipids, proteins, starch and cell wall polymers from a single sample. Plant Methods 12, 45. PubMed PMC

Schmidt GW, Delaney SK. 2010. Stable internal reference genes for normalization of real-time RT-PCR in tobacco ( PubMed

Schomburg FM, Bizzell CM, Lee DJ, Zeevaart JA, Amasino RM. 2003. Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. The Plant Cell 15, 151–163. PubMed PMC

Schreiber U, Klughammer C. 2016. Analysis of photosystem I donor and acceptor sides with a new type of online-deconvoluting kinetic LED-array spectrophotometer. Plant & Cell Physiology 57, 1454–1467. PubMed

Schuetz RD, Baldwin RA. 1958. The synthesis and properties of some substituted phenyl ω-(N,N-dialkylamino)-alkyl sulfides. Journal of the American Chemical Society 80, 162–164.

Shi Y, Guo J, Zhang W, et al. 2015. Cloning of the lycopene β-cyclase gene in PubMed PMC

Svab Z, Maliga P. 1991. Mutation proximal to the transfer-RNA binding region of the PubMed

Svab Z, Maliga P. 1993. High-frequency plastid transformation in tobacco by selection for a chimeric PubMed PMC

Tao L, Picataggio S, Rouvière PE, Cheng Q. 2004. Asymmetrically acting lycopene β-cyclases (CrtLm) from non-photosynthetic bacteria. Molecular Genetics and Genomics 271, 180–188. PubMed

Tata SK, Jung J, Kim YH, Choi JY, Jung JY, Lee IJ, Shin JS, Ryu SB. 2016. Heterologous expression of chloroplast-localized geranylgeranyl pyrophosphate synthase confers fast plant growth, early flowering and increased seed yield. Plant Biotechnology Journal 14, 29–39. PubMed PMC

Taylor I, Sonneveld T, Bugg TH, Thompson A. 2005. Regulation and manipulation of the biosynthesis of abscisic acid, including the supply of xanthophyll precursors. Journal of Plant Growth Regulation 24, 253–273.

Tureckova V, Novak O, Strnad M. 2009. Profiling ABA metabolites in PubMed

Urbanova T, Tarkowska D, Novak O, Hedden P, Strnad M. 2013. Analysis of gibberellins as free acids by ultra performance liquid chromatography-tandem mass spectrometry. Talanta 112, 85–94. PubMed

Vidal AM, Gisbert C, Talón M, Primo-Millo E, López-Díaz I, García-Martínez JL. 2001. The ectopic overexpression of a citrus gibberellin 20-oxidase enhances the non-13-hydroxylation pathway of gibberellin biosynthesis and induces an extremely elongated phenotype in tobacco. Physiologia Plantarum 112, 251–260. PubMed

Voorend W, Nelissen H, Vanholme R, De Vliegher A, Van Breusegem F, Boerjan W, Roldán-Ruiz I, Muylle H, Inzé D. 2016. Overexpression of PubMed PMC

Wang JY, Haider I, Jamil M, et al. 2019. The apocarotenoid metabolite zaxinone regulates growth and strigolactone biosynthesis in rice. Nature Communications 10, 810. PubMed PMC

Welsch R, Beyer P, Hugueney P, Kleinig H, von Lintig J. 2000. Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211, 846–854. PubMed

Weng JK, Ye M, Li B, Noel JP. 2016. Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166, 881–893. PubMed

Wurbs D, Ruf S, Bock R. 2007. Contained metabolic engineering in tomatoes by expression of carotenoid biosynthesis genes from the plastid genome. The Plant Journal 49, 276–288. PubMed

Yu X, Pasternak T, Eiblmeier M, et al. 2013. Plastid-localized glutathione reductase2-regulated glutathione redox status is essential for PubMed PMC

Zhao X, Hu K, Yan M, Yi B, Wen J, Ma C, Shen J, Fu T, Tu J. 2020. Disruption of carotene biosynthesis leads to abnormal plastids and variegated leaves in PubMed PMC

Zhu K, Zheng X, Ye J, Jiang Q, Chen H, Mei X, Wurtzel ET, Deng X. 2020. Building the synthetic biology toolbox with enzyme variants to expand opportunities for biofortification of provitamin A and other health-promoting carotenoids. Journal of Agricultural and Food Chemistry 68, 12048–12057. PubMed

LYCOPENE β-CYCLASE overexpression improves growth, modulates hormone content, and affects rhizospheric interactions in tobacco and tomato roots