Tomato fruit carotenoid biosynthesis is adjusted to actual ripening progression by a light‐dependent mechanism

Abstract

SUMMARYCarotenoids are isoprenoid compounds that are essential for plants to protect the photosynthetic apparatus against excess light. They also function as health-promoting natural pigments that provide colors to ripe fruit, promoting seed dispersal by animals. Work in Arabidopsis thaliana unveiled that transcription factors of the phytochrome-interacting factor (PIF) family regulate carotenoid gene expression in response to environmental signals (i.e. light and temperature), including those created when sunlight reflects from or passes though nearby vegetation or canopy (referred to as shade). Here we show that PIFs use a virtually identical mechanism to modulate carotenoid biosynthesis during fruit ripening in tomato (Solanum lycopersicum). However, instead of integrating environmental information, PIF-mediated signaling pathways appear to fulfill a completely new function in the fruit. As tomatoes ripen, they turn from green to red due to chlorophyll breakdown and carotenoid accumulation. When sunlight passes through the flesh of green fruit, a self-shading effect within the tissue maintains high levels of PIFs that directly repress the master gene of the fruit carotenoid pathway, preventing undue production of carotenoids. This effect is attenuated as chlorophyll degrades, causing degradation of PIF proteins and boosting carotenoid biosynthesis as ripening progresses. Thus, shade signaling components may have been co-opted in tomato fruit to provide information on the actual stage of ripening (based on the pigment profile of the fruit at each moment) and thus finely coordinate fruit color change. We show how this mechanism may be manipulated to obtain carotenoid-enriched fruits.

Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits

“…Confirming the influence of light signaling on fruit biology, knockout/knockdown of tomato genes encoding HY5, COP1, DDB1, DET1, CUL4 and PIF1a has been shown to markedly impact fruit plastid biogenesis and nutritional quality (Liu et al, 2004;Kolotillin et al, 2007;Azari et al, 2010;Llorente et al, 2016).…”

“…In Arabidopsis thaliana, the master transcription factor of chloroplast development and maintenance GOLDEN-2 LIKE (GLK) as well as key carotenoid biosynthetic genes, including AtPSY1, are important targets of PIF proteins (Toledo-Ortiz et al, 2010;BouTorrent et al, 2015). Among the six tomato PIF-encoding genes , SlPIF1a has been shown to physically bind to SlPSY1 promotor, inhibiting fruit carotenoid synthesis (Llorente et al, 2016). As highlighted by Llorente et al (2016), the presence of chlorophylls may create a self-shading effect as sunlight passes through the flesh of green tomato fruits, resulting in a progressive reduction in R/FR ratios at increasing depths within the fruit tissues.…”

“…Among the six tomato PIF-encoding genes , SlPIF1a has been shown to physically bind to SlPSY1 promotor, inhibiting fruit carotenoid synthesis (Llorente et al, 2016). As highlighted by Llorente et al (2016), the presence of chlorophylls may create a self-shading effect as sunlight passes through the flesh of green tomato fruits, resulting in a progressive reduction in R/FR ratios at increasing depths within the fruit tissues. As tomato fruit ripens, chlorophylls are degraded and inner fruit cells are irradiated with progressively more R-enriched light, facilitating the activation of PHYs and consequently promoting the PHY-mediated targeting of SlPIFs for degradation.…”

“…As tomato fruit ripens, chlorophylls are degraded and inner fruit cells are irradiated with progressively more R-enriched light, facilitating the activation of PHYs and consequently promoting the PHY-mediated targeting of SlPIFs for degradation. According to the proposed model, by increasing R/FR ratio inside the fruit tissues and subsequently increasing SlPIF1a degradation, the reduction of fruit chlorophyll levels promotes SlPSY1 expression and therefore intensifies carotenoid accumulation in this organ (Llorente et al, 2016). (1) Upon red (R) light irradiation, cytosolic PHYPr is converted into its active Pfr form, which migrates to the nucleus.…”

“…In accordance with their key functions in light signal transduction, overexpression or knockout/knockdown of tomato genes encoding PIF, HY5, COP1, DET1, DDB1 or CUL4 have been shown to greatly impact the organoleptic and nutritional composition of tomato fruits (Liu et al, 2004;Kolotilin et al, 2007;Azari et al, 2010;Llorente et al, 2016).…”