Perceiving incoming environmental information is critical for optimizing plant growth and development. Multiple B-box proteins (BBXs) play essential roles in light-dependent developmental processes in plants. However, whether BBXs function as a signal integrator between light and temperature in tomato plants remains elusive. In this study, 31 SlBBX genes were identified from the newly released tomato (Solanum lycopersicum) genome sequences and were clustered into five subgroups. Gene structure and protein motif analyses showed relatively high conservation of closely clustered SlBBX genes within each subgroup; however, genome mapping analysis indicated the uneven distribution of the SlBBX genes on tomato chromosomes. Promoter cis-regulatory elements prediction and gene expression indicated that SlBBX genes were highly responsive to light, hormones, and stress conditions. Reverse genetic approaches revealed that disruption of SlBBX7, SlBBX9, and SlBBX20 largely suppressed the cold tolerance of tomato plants. Furthermore, the impairment of SlBBX7, SlBBX9, and SlBBX20 suppressed the photosynthetic response immediately after cold stress. Due to the impairment of non-photochemical quenching (NPQ), the excess photon energy and electron flow excited by low temperature were not consumed in SlBBX7-, SlBBX9-, and SlBBX20- silenced plants, leading to the over reduction of electron carriers and damage of the photosystem. Our study emphasized the positive roles of light signaling transcription factors SlBBXs in cold tolerance in tomato plants, which may improve the current understanding of how plants integrate light and temperature signals to adapt to adverse environments.

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Plants have evolved sophisticated regulatory networks to cope with dynamically changing light and temperature environments during day-night and seasonal cycles. However, the integration mechanisms of light and low temperature remain largely unclear.Here, we show that low red : far-red ratio (LR : FR) induces FAR-RED ELONGATED HYPOCOTYL3 (SlFHY3) transcription under cold stress in tomato (Solanum lycopersicum). Reverse genetic approaches revealed that knocking out SlFHY3 decreases myo-inositol accumulation and increases cold susceptibility, whereas overexpressing SlFHY3 induces myoinositol accumulation and enhances cold tolerance in tomato plants.SlFHY3 physically interacts with ELONGATED HYPOCOTYL5 (SlHY5) to promote the transcriptional activity of SlHY5 on MYO-INOSITOL-1-PHOSPHATE SYNTHASE 3 (SlMIPS3) and induce myo-inositol accumulation in tomato plants under cold stress. Disruption of SlHY5 and SlMIPS3 largely suppresses the cold tolerance of SlFHY3-overexpressing plants and myoinositol accumulation in tomato. Furthermore, silencing of SlMIPS3 drastically reduces myo-inositol accumulation and compromises LR : FR-induced cold tolerance in tomato.Together, our results reveal a crucial role of SlFHY3 in LR : FR-induced cold tolerance in tomato and unravel a novel regulatory mechanism whereby plants integrate dynamic environmental light signals and internal cues (inositol biosynthesis) to induce and control cold tolerance in tomato plants.

Cold stress is a key environmental constraint that dramatically affects the growth, productivity, and quality of tomato (Solanum lycopersicum); however, the underlying molecular mechanisms of cold tolerance remain poorly understood. In this study, we identified REDUCED CHLOROPLAST COVERAGE 2 (SlREC2) encoding a tetratricopeptide repeat (TPR) protein that positively regulates tomato cold tolerance. Disruption of SlREC2 largely reduced abscisic acid (ABA) levels, photoprotection and the expression of C-REPEAT BINDING FACTOR (CBF) pathway genes in tomato plants under cold stress. ABA deficiency in the notabilis (not) mutant, which carries a mutation in 9-CIS-EPOXYCAROTENOID DIOXYGENASE 1 (SlNCED1), strongly inhibited the cold tolerance of SlREC2-silenced plants and empty vector control plants and resulted in a similar phenotype. In addition, foliar application of ABA rescued the cold tolerance of SlREC2-silenced plants, which confirms that SlNCED1-mediated ABA accumulation is required for SlREC2-regulated cold tolerance. Strikingly, SlREC2 physically interacted with β-RING CAROTENE HYDROXYLASE 1b (SlBCH1b), a key regulatory enzyme in the xanthophyll cycle. Disruption of SlBCH1b severely impaired photoprotection, ABA accumulation and CBF-pathway gene expression in tomato plants under cold stress. Taken together, this study reveals that SlREC2 interacts with SlBCH1b to enhance cold tolerance in tomato via integration of SlNCED1-mediated ABA accumulation, photoprotection, and the CBF-pathway, thus providing further genetic knowledge for breeding cold-resistant tomato varieties.

Background: Perceiving incoming environmental information is critical for optimizing plant growth and development. Multiple B-box proteins (BBXs) play essential roles in light-dependent developmental processes in plants. However, whether BBXs function as a signal integrator between light and temperature in tomato plants remains elusive.Results: In this study, 31 SlBBX genes were identified from the newly released tomato (Solanum lycopersicum) genome sequences, and were clustered into five subgroups with phylogenetic analysis. Gene structure and protein motif analyses showed relatively high conservation of closely clustered SlBBX genes within each subgroup; however, genome mapping analysis indicated the uneven distribution of the SlBBX genes on tomato chromosomes. Synteny analysis indicated that segmental duplication events happened in the expansion of the SlBBX genes in tomato. Promoter cis-regulatory elements prediction indicated that SlBBX genes were highly responsive to light, hormones, and stress conditions. Furthermore, the transcript analysis revealed that various SlBBX genes differed significantly in expression after exposure to different light quality and low temperatures, while 61.3% of SlBBX genes were responsive to both light and low temperatures. Conclusions: Our study presented a genome-wide survey of SlBBX gene family in tomato, and emphasized their functions in perceiving light quality and low temperature, which may improve the current understanding of SlBBX gene functions in integrating light and temperature signals for plant adaptation to adverse environments.