Fruit-localized phytochromes regulate plastid biogenesis, starch synthesis, and carotenoid metabolism in tomato

Ricardo Ernesto Bianchetti,Magdalena Rossi,Scarlet Santos Monteiro,Bruno Silvestre Lira,Christophe Rothan,Diego Demarco,Eduardo Purgatto,Luciano Freschi

doi:10.1093/jxb/ery145

Ricardo Ernesto Bianchetti, Magdalena Rossi + Show 6 more

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https://doi.org/10.1093/jxb/ery145

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Abstract

Light signaling has long been reported to influence fruit biology, although the regulatory impact of fruit-localized photoreceptors on fruit development and metabolism remains unclear. Studies performed in phytochrome (PHY)-deficient tomato (Solanum lycopersicum) mutants suggest that SlPHYA, SlPHYB2, and to a lesser extent SlPHYB1 influence fruit development and ripening. By employing fruit-specific RNAi-mediated silencing of SlPHY genes, we demonstrated that fruit-localized SlPHYA and SlPHYB2 play contrasting roles in regulating plastid biogenesis and maturation in tomato. Our data revealed that fruit-localized SlPHYA, rather than SlPHYB1 or SlPHYB2, positively influences tomato plastid differentiation and division machinery via changes in both light and cytokinin signaling-related gene expression. Fruit-localized SlPHYA and SlPHYB2 were also shown to modulate sugar metabolism in early developing fruits via overlapping, yet distinct, mechanisms involving the co-ordinated transcriptional regulation of genes related to sink strength and starch biosynthesis. Fruit-specific SlPHY silencing also drastically altered the transcriptional profile of genes encoding light-repressor proteins and carotenoid-biosynthesis regulators, leading to reduced carotenoid biosynthesis during fruit ripening. Together, our data reveal the existence of an intricate PHY-hormonal interplay during fruit development and ripening, and provide conclusive evidence on the regulation of tomato quality by fruit-localized phytochromes.

Highlights

Fleshy fruit growth, maturation, and ripening are under strict developmental, hormonal, and epigenetic regulation, which in turn are fine-tuned by a plethora of environmental stimuli (Kumar et al, 2014; Giovannoni et al, 2017)
To investigate the role played by distinct PHYs in tomato fruit development and ripening, we generated fruit-specific silenced tomato plants with reduced mRNA levels of SlPHYA, SlPHYB2, or both SlPHYB1 and SlPHYB2
Transcript abundance analysis revealed that SlPHYA, SlPHYB2, and both SlPHYB1 and SlPHYB2 were down-regulated in the SlPHYARNAi, SlPHYB2RNAi, and SlPHYB1/B2RNAi lines, respectively (Fig. 1B)

Summary

Introduction

Maturation, and ripening are under strict developmental, hormonal, and epigenetic regulation, which in turn are fine-tuned by a plethora of environmental stimuli (Kumar et al, 2014; Giovannoni et al, 2017). Once activated by R light, PHYs are transported from the cytosol to the nucleus, where they counteract light-signaling repressor proteins, such as CONSTITUTIVE PHOTOMORPHOGENESIS1 (COP1), CULLIN4 (CUL4), DNA DAMAGE-BINDING PROTEIN 1 (DDB1), DETIOLATED1 (DET1), and PHYTOCHROME INTERACTION FACTOR (PIF) (Deng and Quail, 1992; Pepper et al, 1994; Schroeder et al, 2002; Duek and Fankhauser, 2005; Thomann et al, 2005) In line with their role as repressors of photomorphogenic responses, either the down-regulation or loss-of-function of tomato genes encoding COP1, CUL4, DDB1, DET1, and PIF1a profoundly alter tomato fruit physiology and nutritional composition (Cookson et al, 2003; Liu et al, 2004; Davuluri et al, 2005; Kolotilin et al, 2007; Wang et al, 2008; Azari et al, 2010b; Enfissi et al, 2010; Llorente et al, 2016b)

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