Melatonin, the most widely distributed hormone in nature, plays important roles in plants. Many physiological processes in plants are linked to melatonin, including seed germination, anisotropic cell growth, and senescence. Compared with animals, different plants possess diverse melatonin biosynthetic pathways and regulatory networks. Whereas melatonin biosynthesis in animals is known to be regulated by ambient signals, little is known about how melatonin biosynthesis in plants responds to environmental signals. Plants are affected by numerous environmental factors, such as light, temperature, moisture, carbon dioxide, soil conditions, and nutrient availability at all stages of development and in different tissues. Melatonin content exhibits dynamic changes that affect plant growth and development. Melatonin plays various species-specific roles in plant responses to different environmental conditions. However, much remains to be learned, as not all environmental factors have been studied, and little is known about the mechanisms by which these factors influence melatonin biosynthesis. In this review, we provide a detailed, systematic description of melatonin biosynthesis and signaling and of the roles of melatonin in plant responses to different environmental factors, providing a reference for in-depth research on this important issue.

Melatonin is a functionally conserved broad-spectrum physiological regulator found in most biological organisms in nature. Enrichment of tomato fruit with melatonin not only enhances its agronomic traits but also provides extra health benefits. In this study, we elucidate the full melatonin biosynthesis pathway in tomato fruit by identifying biosynthesis-related genes that encode caffeic acid O-methyltransferase 2 (SlCOMT2) and N-acetyl-5-hydroxytryptamine-methyltransferases 5/7 (SlASMT5/7). We further reveal that red light supplementation significantly enhances the melatonin content in tomato fruit. This induction relies on the “serotonin—N-acetylserotonin—melatonin” biosynthesis route via the SlphyB2-SlPIF4-SlCOMT2 module. Based on the regulatory mechanism, we design a gene-editing strategy to target the binding motif of SlPIF4 in the promoter of SlCOMT2, which significantly enhances the production of melatonin in tomato fruit. Our study provides a good example of how the understanding of plant metabolic pathways responding to environmental factors can guide the engineering of health-promoting foods.

Plant flowering time is induced by environmental and endogenous signals perceived by the plant. The MCM1-AGAMOUSDEFICIENS-SRF-box (MADS-box) protein SHORT VEGETATIVE PHASE (SVP) is a pivotal repressor that negatively regulates the floral transition during the vegetative phase; however, the transcriptional regulatory mechanism remains poorly understood. Here, we report CmSVP, a chrysanthemum (Chrysanthemum morifolium Ramat.) homologue of SVP, can repress the expression of a key flowering gene, a chrysanthemum FLOWERING LOCUS T-like gene (CmFTL3), by binding its promoter CArG element to delay flowering in the ambient temperature pathway in chrysanthemum. Protein–protein interaction assays identified an interaction between CmSVP and CmTPL1-2, a chrysanthemum homologue of TOPLESS (TPL) that plays critical roles as transcriptional corepressor in many aspects of plant life. Genetic analyses revealed the CmSVP-CmTPL1-2 transcriptional complex is a prerequisite for CmSVP to act as a floral repressor. Furthermore, overexpression of CmSVP rescued the phenotype of the svp-31 mutant in Arabidopsis (Arabidopsis thaliana), overexpression of AtSVP or CmSVP in the Arabidopsis dominant negative mutation tpl-1 led to ineffective late flowering, and AtSVP interacted with AtTPL, confirming the conserved function of SVP in chrysanthemum and Arabidopsis. We have validated a conserved machinery wherein SVP partially relies on TPL to inhibit flowering via a thermosensory pathway.

The flowering time of Chrysanthemum morifolium predominantly depends on day length but is also sensitive to ambient temperature. However, the mechanisms underlying the response of Chrysanthemum to ambient temperature are mainly unknown. This study identified a MADS-box transcription factor called FLOWERING LOCUS C-like (CmFLC-like), a representative low ambient temperature-responsive factor induced in Chrysanthemum leaves and shoot apical meristems at 15 °C. Subsequently, CmFLC-like localized to the cell nucleus and membrane and functioned as a transcriptional repressor. Overexpression of CmFLC-like increased plants sensitivity to low-temperature-induced late flowering, whereas the chimeric activator CmFLC-like-VP64 was less sensitive at 15 °C, indicating that CmFLC-like was involved in thermosensory flowering. Transcriptome profiling of CmFLC-like transgenic plants suggested that the potential target genes for low ambient temperature-responsive CmFLC-like regulation are predominantly flowering integrators, MADS-box transcription factors, and APETALA2 genes. Subsequent examination revealed that the orchestrated repression of CmAFL1 and FLOWERING LOCUS T-like 3 by CmFLC-like was mediated by its direct binding to the CArG-box element of their promoters. This study offers novel insights into the molecular mechanisms of flowering in Chrysanthemum, and highlights the essential role of CmFLC-like proteins in the thermosensory pathway.