Regulation of carotenoid biosynthesis by shade relies on specific subsets of antagonistic transcription factors and co-factors

Abstract

Carotenoids are photosynthetic pigments essential for the protection against excess light. During deetiolation, their production is regulated by a dynamic repression-activation module formed by PHYTOCHROME-INTERACTING FACTOR1 (PIF1) and LONG HYPOCOTYL5 (HY5). These transcription factors directly and oppositely control the expression of the gene encoding PHYTOENE SYNTHASE (PSY), the first and main rate-determining enzyme of the carotenoid pathway. Antagonistic modules also regulate the responses of deetiolated plants to vegetation proximity and shade (i.e. to the perception of far-red light-enriched light filtered through or reflected from neighboring plants). These responses, aimed to adapt to eventual shading from plant competitors, include a reduced accumulation of carotenoids. Here, we show that PIF1 and related photolabile PIFs (but not photostable PIF7) promote the shade-triggered decrease in carotenoid accumulation. While HY5 does not appear to be required for this process, other known PIF antagonists were found to modulate the expression of the Arabidopsis (Arabidopsis thaliana) PSY gene and the biosynthesis of carotenoids early after exposure to shade. In particular, PHYTOCHROME-RAPIDLY REGULATED1, a transcriptional cofactor that prevents the binding of true transcription factors to their target promoters, was found to interact with PIF1 and hence directly induce PSY expression. By contrast, a change in the levels of the transcriptional cofactor LONG HYPOCOTYL IN FAR RED1, which also binds to PIF1 and other PIFs to regulate shade-related elongation responses, did not impact PSY expression or carotenoid accumulation. Our data suggest that the fine-regulation of carotenoid biosynthesis in response to shade relies on specific modules of antagonistic transcriptional factors and cofactors.

A kiwifruit (Actinidia deliciosa) R2R3‐MYB transcription factor modulates chlorophyll and carotenoid accumulation

“…There are examples of common regulators between these two metabolic pathways (Park et al ., ; Luo et al ., ). Phytochrome interaction factor 1 (PIF1) has been implicated in regulating Chl and chloroplast development as well as in carotenogenesis, as a post‐transcriptional regulator of PSY (Toledo‐Ortiz et al ., ; Cheminant et al ., ; Bou‐Torrent et al ., ). PIF1 is induced by low light conditions created by high Chl levels in the fruit, which subsequently represses PSY expression.…”

DRACULA2, a dynamic nucleoporin with a role in the regulation of the shade avoidance syndrome in Arabidopsis

“…PIF stability and/or activity was also shown to be increased by low R:FR perception (Lorrain et al, 2008;Li et al, 2012). Genetic analyses unraveled roles for these factors in the negative (including BBX21, BBX22, HFR1, PAR1, PAR2 and PIL1) or positive (including BBX24, BBX25, PIFs, BIMs and BEEs) regulation of SAS (Sessa et al, 2005;Roig-Villanova et al, 2006Crocco et al, 2010;Cifuentes-Esquivel et al, 2013;Gangappa et al, 2013;Bou-Torrent et al, 2015). Therefore, the low R:FR perception rapidly changes the balance of positive and negative factors, resulting in the appropriate SAS responses.…”

Transcriptome Profiling of Tomato Uncovers an Involvement of Cytochrome P450s and Peroxidases in Stigma Color Formation

“…Total chlorophylls and carotenoids were extracted and quantified by spectrophotometric method as described previously (Lichtenthaler, 1987; Bou-Torrent et al, 2015). …”