Carotenogenesis Is Regulated by 5ʹUTR-Mediated Translation of Phytoene Synthase Splice Variants

• Published in: Plant physiology (Bethesda) 2016-12, Vol.172 (4), p.2314-2326
• Main Authors: Álvarez, Daniel, Voß, Björn, Maass, Dirk, Wüst, Florian, Schaub, Patrick, Beyer, Peter, Welsch, Ralf
• Format: Article
• Language: English
• Subjects: 5' Untranslated Regions - genetics; Alternative Splicing - genetics; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Carotenoids - biosynthesis; Carotenoids - genetics; Carotenoids - metabolism; Computational Biology; Gene Expression Regulation, Plant; GENES, DEVELOPMENT, AND EVOLUTION; Genes, Reporter; Glucuronidase - metabolism; Models, Biological; Multienzyme Complexes - genetics; Multienzyme Complexes - metabolism; Plant Leaves - enzymology; Plant Leaves - genetics; Protein Biosynthesis - genetics
• ISSN: 0032-0889; 1532-2548

Phytoene synthase (PSY) catalyzes the highly regulated, frequently rate-limiting synthesis of the first biosynthetically formed carotene. While PSY constitutes a small gene family in most plant taxa, the Brassicaceae, including Arabidopsis (Arabidopsis thaliana), predominantly possess a single PSY gene. This monogenic situation is compensated by the differential expression of two alternative splice variants (ASV), which differ in length and in the exon/intron retention of their 5ʹUTRs. ASV1 contains a long 5ʹUTR (untranslated region) and is involved in developmentally regulated carotenoid formation, such as during deetiolation. ASV2 contains a short 5ʹUTR and is preferentially induced when an immediate increase in the carotenoid pathway flux is required, such as under salt stress or upon sudden light intensity changes. We show that the long 5ʹUTR of ASV1 is capable of attenuating the translational activity in response to high carotenoid pathway fluxes. This function resides in a defined 5ʹUTR stretch with two predicted interconvertible RNA conformations, as known from riboswitches, which might act as a flux sensor. The translation-inhibitory structure is absent from the short 5ʹUTR of ASV2 allowing to bypass translational inhibition under conditions requiring rapidly increased pathway fluxes. The mechanism is not found in the rice (Oryza sativa) PSY1 5ʹUTR, consistent with the prevalence of transcriptional control mechanisms in taxa with multiple PSY genes. The translational control mechanism identified is interpreted in terms of flux adjustments needed in response to retrograde signals stemming from intermediates of the plastid-localized carotenoid biosynthesis pathway.