Light signaling and phytohormones both influence plant growth, development, and stress responses; however, cross talk between these two signaling pathways in response to cold remains underexplored. Here, we report that far-red light (FR) and red light (R) perceived by phytochrome A (phyA) and phyB positively and negatively regulated cold tolerance, respectively, in tomato (Solanum lycopersicum), which were associated with the regulation of levels of phytohormones such as abscisic acid (ABA) and jasmonic acid (JA) and transcript levels of ABA- and JA-related genes and the C-REPEAT BINDING FACTOR (CBF) stress signaling pathway genes. A reduction in the R/FR ratio did not alter cold tolerance, ABA and JA accumulation, and transcript levels of ABA- and JA-related genes and the CBF pathway genes in phyA mutant plants; however, those were significantly increased in wild-type and phyB plants with the reduction in the R/FR ratio. Even though low R/FR treatments did not confer cold tolerance in ABA-deficient (notabilis [not]) and JA-deficient (prosystemin-mediated responses2 [spr2]) mutants, it up-regulated ABA accumulation and signaling in the spr2 mutant, with no effect on JA levels and signaling in the not mutant. Foliar application of ABA and JA further confirmed that JA functioned downstream of ABA to activate the CBF pathway in light quality-mediated cold tolerance. It is concluded that phyA and phyB function antagonistically to regulate cold tolerance that essentially involves FR light-induced activation of phyA to induce ABA signaling and, subsequently, JA signaling, leading to an activation of the CBF pathway and a cold response in tomato plants.

During the transition from warm to cool seasons, plants experience decreased temperatures, shortened days, and decreased red/far-red (R/FR) ratios of light. The mechanism by which plants integrate these environmental cues to maintain plant growth and adaptation remains poorly understood. Here, we report that low temperature induced the transcription of PHYTOCHROME A and accumulation of LONG HYPOCOTYL5 (SlHY5, a basic Leu zipper transcription factor) in tomato (Solanum lycopersicum) plants, especially under short day conditions with low R/FR light ratios. Reverse genetic approaches and physiological analyses revealed that silencing of SlHY5 increased cold susceptibility in tomato plants, whereas overexpression of SlHY5 enhanced cold tolerance. SlHY5 directly bound to and activated the transcription of genes encoding a gibberellin-inactivation enzyme, namely GIBBERELLIN2-OXIDASE4, and an abscisic acid biosynthetic enzyme, namely 9-CIS-EPOXYCAROTENOID DIOXYGENASE6 (SlNCED6). Thus, phytochrome A-dependent SlHY5 accumulation resulted in an increased abscisic acid/gibberellin ratio, which was accompanied by growth cessation and induction of cold response. Furthermore, silencing of SlNCED6 compromises short day- and low R/FR-induced tomato resistance to cold stress. These findings provide insight into the molecular genetic mechanisms by which plants integrate environmental stimuli with hormones to coordinate their growth with impending cold temperatures. Moreover, this work reveals a molecular mechanism that plants have evolved for growth and survival in response to seasonal changes.

Summary: The ability to interpret daily and seasonal fluctuations, latitudinal and vegetation canopy variations in light and temperature signals is essential for plant survival. However, the precise molecular mechanisms transducing the signals from light and temperature perception to maintain plant growth and adaptation remain elusive. We show that far‐red light induces PHYTOCHROME‐INTERACTING TRANSCRIPTION 4 (SlPIF4) accumulation under low‐temperature conditions via phytochrome A in Solanum lycopersicum (tomato). Reverse genetic approaches revealed that knocking out SlPIF4 increases cold susceptibility, while overexpressing SlPIF4 enhances cold tolerance in tomato plants. SlPIF4 not only directly binds to the promoters of the C‐REPEAT BINDING FACTOR (SlCBF) genes and activates their expression but also regulates plant hormone biosynthesis and signals, including abscisic acid, jasmonate and gibberellin (GA), in response to low temperature. Moreover, SlPIF4 directly activates the SlDELLA gene (GA‐INSENSITIVE 4, SlGAI4) under cold stress, and SlGAI4 positively regulates cold tolerance. Additionally, SlGAI4 represses accumulation of the SlPIF4 protein, thus forming multiple coherent feed‐forward loops. Our results reveal that plants integrate light and temperature signals to better adapt to cold stress through shared hormone pathways and transcriptional regulators, which may provide a comprehensive understanding of plant growth and survival in a changing environment.

Photoreceptor-mediated light signaling plays a critical role in plant growth, development, and stress responses but its contribution to the spatial regulation of photoinhibition and photoprotection within the canopy remains unclear. Here, we show that low-red/far-red (L-R/FR) ratio light conditions significantly alleviate PSII and PSI photoinhibition in the shade leaves of tomato (Solanum lycopersicum) plants. This protection is accompanied by a phytochrome A-dependent induction of LONG HYPOCOTYL5 (HY5). HY5 binds to the promoter of ABA INSENSITIVE5 (ABI5), triggering RESPIRATORY BURST OXIDASE HOMOLOG1 (RBOH1)-dependent H₂O₂ production in the apoplast. Decreased levels of HY5, ABI5, and RBOH1 transcripts increased cold-induced photoinhibition and abolished L-R/FR-induced alleviation of photoinhibition. L-R/FR illumination induced nonphotochemical quenching (NPQ) of chlorophyll a fluorescence and increased the activities of Foyer-Halliwell-Asada cycle enzymes and cyclic electron flux (CEF) around PSI. In contrast, decreased HY5, ABI5, and RBOH1 transcript levels abolished the positive effect of L-R/FR on photoprotection. Loss of PROTON GRADIENT REGULATION5-dependent CEF led to increased photoinhibition and attenuated L-R/FR-dependent NPQ. These data demonstrate that HY5 is an important hub in the cross talk between light and cold response pathways, integrating ABA and reactive oxygen species signaling, leading to the attenuation of photoinhibition by enhanced induction of photoprotection in shade leaves.