Far-red perception by vegetative organs and not fruits drives fruit growth responses in tomato plants

Responses to far-red light are mediated by phytochromes, specialized photoreceptors present in all organs of a tomato plant (Solanum lycopersicum L.). Although fruit-localized phytochromes can influence starch and sugar metabolism, their involvement in modulating fruit growth responses to far-red light is unknown. We explored whether fruit growth responses to far-red light are driven by local far-red perception within the fruits or by a systemic response initiated in the vegetative organs. We applied far-red light exclusively to the fruiting trusses, to the vegetative organs, to both, or to neither. Far-red light was added to a constant red-white LED background spectrum to simulate greenhouse supplementary lighting. We quantified plant and fruit growth responses to far-red and performed a transcriptomic analysis to establish the temporal dynamics of far-red light perception and signaling in leaves and fruits. Supplementing far-red light to the vegetative organs increased ripe fruit weight and sugar concentration, whereas far-red supplementation to the generative organs alone had no measurable effect. This study establishes that far-red perception by vegetative organs drives fruit growth responses in tomato. Local responses to far-red light included a transient increase in auxin concentration and upregulation of the auxin-signaling pathway in leaves, a conserved response to decreasing red/far-red ratios. In fruits, early transcriptomic responses carried signatures of auxin, cytokinin, and gibberellin biosynthesis and signaling, suggesting a role for hormones as mediators of far-red-induced fruit responses. This work reveals how responses to far-red light perception by vegetative organs promote sink strength and starch biosynthesis in early developing fruits, contributing to higher fruit weight and sugar concentration in ripe fruits.