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Summary Flavonoids have a major contribution to the fruit quality in cultivated strawberries and are regulated by MYB, bHLH and WD40 transcriptional factors. We reported here the identification of the FaMYB5, an R2R3‐MYB transcription factor, which positively regulated the accumulation of anthocyanins and proanthocyanidins through the trans‐activation of the F3'H and LAR. The strawberry FaEGL3 and FaLWD1/FaLWD1‐like interact with the R2R3‐FaMYB5 to form an MYB‐bHLH‐WD40 complex (MBW), enhancing the regulatory efficiency. The R2R3‐FaMYB5 was constitutively expressed in various tissues and in fruits of different developmental stages, which was strikingly contrasting to the fruit‐specific expression patterns of FaMYB10. Meanwhile, R2R3‐FaMYB5 failed to promote a stable accumulation of anthocyanin glycosides in the mature fruits of the myb10 mutant, mainly due to the suppressed expression of TT19. The R2R3‐FaMYB5 was regulated by an antisense long noncoding RNA lncRNA‐myb5. Additionally, the R2R3‐FaMYB5 protein could interact with FaBT2 and was degraded through the ubiquitin/26 S proteasome pathway. Transcriptome and metabolome data showed that R2R3‐FaMYB5 enhanced the gene expression and the metabolite accumulation involved in the flavonoid, phenylpropanoid and lignin biosynthesis pathways. Collectively, we conclude that the FaMYB5 is an R2R3‐MYB activator involved in the composition of MBW, which positively regulates the biosynthesis of anthocyanin and proanthocyanidin. These findings provided new insights into the molecular mechanisms that regulate flavonoids in strawberry fruits.

Anthocyanin accumulation in plants plays important roles in plant growth and development, as well as the response to environmental stresses. Anthocyanins have antioxidant properties and play an important role in maintaining the reactive oxygen species (ROS) homeostasis in plant cells. Furthermore, anthocyanins also act as a “sunscreen”, reducing the damage caused by ultraviolet radiation under high-light conditions. The biosynthesis of anthocyanin in plants is mainly regulated by an MYB-bHLH-WD40 (MBW) complex. In recent years, many new regulators in different signals involved in anthocyanin biosynthesis were identified. This review focuses on the regulation network mediated by different environmental factors (such as light, salinity, drought, and cold stresses) and phytohormones (such as jasmonate, abscisic acid, salicylic acid, ethylene, brassinosteroid, strigolactone, cytokinin, and auxin). We also discuss the potential application value of anthocyanin in agriculture, horticulture, and the food industry.

Anthocyanins are natural water-soluble pigments that are important in plants because they endow a variety of colors to vegetative tissues and reproductive plant organs, mainly ranging from red to purple and blue. The colors regulated by anthocyanins give plants different visual effects through different biosynthetic pathways that provide pigmentation for flowers, fruits and seeds to attract pollinators and seed dispersers. The biosynthesis of anthocyanins is genetically determined by structural and regulatory genes. MYB (v-myb avian myeloblastosis viral oncogene homolog) proteins are important transcriptional regulators that play important roles in the regulation of plant secondary metabolism. MYB transcription factors (TFs) occupy a dominant position in the regulatory network of anthocyanin biosynthesis. The TF conserved binding motifs can be combined with other TFs to regulate the enrichment and sedimentation of anthocyanins. In this study, the regulation of anthocyanin biosynthetic mechanisms of MYB-TFs are discussed. The role of the environment in the control of the anthocyanin biosynthesis network is summarized, the complex formation of anthocyanins and the mechanism of environment-induced anthocyanin synthesis are analyzed. Some prospects for MYB-TF to modulate the comprehensive regulation of anthocyanins are put forward, to provide a more relevant basis for further research in this field, and to guide the directed genetic modification of anthocyanins for the improvement of crops for food quality, nutrition and human health.

Anthocyanins endowing strawberry fruit red color are regulated by the MYB-bHLH-WD40 complex. By analyzing the MYBs involved in the flavonoid biosynthesis in strawberry, we found that R2R3-FaMYB5 promoted the content of anthocyanin and proanthocyanidins in strawberry fruits. Yeast two-hybrid and BiFC assays confirmed that MBW complexes connected with flavonoid metabolism were FaMYB5/FaMYB10-FaEGL3 (bHLH)-FaLWD1/FaLWD1-like (WD40). Transient overexpression and qRT-PCR analysis revealed that disparate MBW models hold different patterns in the regulation of flavonoid biosynthesis in strawberry fruits. Compared with FaMYB10, FaMYB5 and its dominant complexes showed a more specific regulatory range on strawberry flavonoid biosynthetic pathway, while FaMYB10 was more extensive. In addition, the complexes involved in FaMYB5 facilitated PAs accumulation primarily through the LAR tributary while FaMYB10 mainly by the ANR branch. FaMYB9 and FaMYB11 tremendously elicited the accumulation of proanthocyanidins by up-regulating the expression levels of both LAR and ANR , and also affected anthocyanin metabolism by changing the ratio of Cy3G and Pg3G which were constituted as two major anthocyanin monomers in strawberries. Our study also illustrated that FaMYB5-FaEGL3-FaLWD1-like directly targeted the promoters of F3′H , LAR , and AHA10 thus committing to flavonoid accumulation. These results allow the specific members involved in the MBW complex to be deciphered and provide new insights into the regulatory mechanisms of anthocyanins and proanthocyanidins regulated by the MBW complex.

Anthocyanins are common secondary metabolites in plants that confer red, blue, and purple colorations in plants and are highly desired by consumers for their visual appearance and nutritional quality. In the last two decades, the anthocyanin biosynthetic pathway and transcriptional regulation of anthocyanin biosynthetic genes (ABGs) have been well characterized in many plants. From numerous studies on model plants and horticultural crops, many signaling regulators have been found to control anthocyanin accumulation via regulation of anthocyanin-promoting R2R3-MYB transcription factors (so-called R2R3-MYB activators). The regulatory mechanism of R2R3-MYB activators is mediated by multiple environmental factors (e.g., light, temperature) and internal signals (e.g., sugar, ethylene, and JA) in complicated interactions at multiple levels. Here, we summarize the transcriptional control of R2R3-MYB activators as a result of natural variations in the promoter of their encoding genes, upstream transcription factors and epigenetics, and posttranslational modifications of R2R3-MYB that determine color variations of horticultural plants. In addition, we focus on progress in elucidating the integrated regulatory network of anthocyanin biosynthesis mediated by R2R3-MYB activators in response to multiple signals. We also highlight a few gene cascade modules involved in the regulation of anthocyanin-related R2R3-MYB to provide insights into anthocyanin production in horticultural plants.

Sugars induce anthocyanin biosynthesis in plants. As a conserved energy sensor, SnRK1 (SNF1-related kinase 1) is involved in sucrose-induced anthocyanin accumulation. However, the exact molecular mechanism by which SnRK1 regulates the biosynthesis of anthocyanins and proanthocyanidins (PAs) in response to sucrose in plants is not clear. In this study, it was found that MdSnRK1.1 interacted with MdJAZ18 protein which acts as a repressor in the jasmonate (JA) signaling pathway. MdSnRK1.1 then phosphorylated MdJAZ18 to facilitate its 26S proteasome-mediated degradation, which released MdbHLH3 thereby activating the expression of the regulatory and structural genes, thus finally promoting the biosynthesis of anthocyanins and PAs. Taken together, these results demonstrate the involvement of MdSnRK1.1 in sucrose-induced accumulation of anthocyanins and PAs. For the first time, our findings shed light on the molecular mechanism by which the crosstalk of sucrose and JA signaling regulates flavonoid biosynthesis.

Background WD40 transcription factors, a large gene family in eukaryotes, are involved in a variety of growth regulation and development pathways. WD40 plays an important role in the formation of MYB-bHLH-WD (MBW) complexes associated with anthocyanin synthesis, but studies of Qingke barley are lacking. Results In this study, 164 barley HvWD40 genes were identified in the barley genome and were analyzed to determine their relevant bioinformatics. The 164 HvWD40 were classified into 11 clusters and 14 subfamilies based on their structural and phylogenetic protein profiles. Co-lineage analysis revealed that there were 43 pairs between barley and rice, and 56 pairs between barley and maize. Gene ontology (GO) enrichment analysis revealed that the molecular function, biological process, and cell composition were enriched. The Kyoto Encyclopedia of Genes and Genomes (KEGG) results showed that the RNA transport pathway was mainly enriched. Based on the identification and analysis of the barley WD40 family and the transcriptome sequencing (RNA-seq) results, we found that HvWD40-140 (WD40 family; Gene ID: r1G058730), HvANT1 (MYB family; Gene ID: HORVU7Hr1G034630), and HvANT2 (bHLH family; Gene ID: HORVU2Hr1G096810) were important components of the MBW complex related to anthocyanin biosynthesis in Qingke, which was verified via quantitative real-time fluorescence polymerase chain reaction (qRT-PCR), subcellular location, yeast two-hybrid (Y2H), and bimolecular fluorescent complimentary (BiFC) and dual-luciferase assay analyses. Conclusions In this study, we identified 164 HvWD40 genes in barley and found that HvnANT1, HvnANT2, and HvWD40-140 can form an MBW complex and regulate the transcriptional activation of the anthocyanin synthesis related structural gene HvDFR . The results of this study provide a theoretical basis for further study of the mechanism of HvWD40-140 in the MBW complex related to anthocyanin synthesis in Qingke.

Floral pigmentation patterning is important for pollinator attraction as well as aesthetic appeal. Patterning of anthocyanin accumulation is frequently associated with variation in activity of the Myb, bHLH and WDR transcription factor complex (MBW) that regulates anthocyanin biosynthesis. Investigation of two classic mutants in Antirrhinum majus, mutabilis and incolorata I, showed they affect a gene encoding a bHLH protein belonging to subclade bHLH-2. The previously characterised gene, Delila, which encodes a bHLH-1 protein, has a bicoloured mutant phenotype, with residual lobe-specific pigmentation conferred by Incolorata I. Both Incolorata I and Delila induce expression of the anthocyanin biosynthetic gene DFR. Rosea 1 (Myb) and WDR1 proteins compete for interaction with Delila, but interact positively to promote Incolorata I activity. Delila positively regulates Incolorata I and WDR1 expression. Hierarchical regulation can explain the bicoloured patterning of delila mutants, through effects on both regulatory gene expression and the activity of promoters of biosynthetic genes like DFR that mediate MBW regulation. bHLH-1 and bHLH-2 proteins contribute to establishing patterns of pigment distribution in A. majus flowers in two ways: through functional redundancy in regulating anthocyanin biosynthetic gene expression, and through differences between the proteins in their ability to regulate genes encoding transcription factors.

A protein complex consisting of a MYB, basic Helix-Loop-Helix, and a WDR protein, the MBW complex, regulates five traits, namely the production of anthocyanidin, proanthocyanidin, and seed-coat mucilage, and the development of trichomes and root hairs. For complexes involved in trichome and root hair development it has been shown that the interaction of two MBW proteins can be counteracted by the respective third protein (called competitive complex formation). We examined competitive complex formation for selected MBW proteins from Arabidopsis thaliana, Arabis alpina, Gossypium hirsutum, Petunia hybrida, and Zea mays. Quantitative analyses of the competitive binding of MYBs and WDRs to bHLHs were done by pull-down assays using ProtA- and luciferase-tagged proteins expressed in human HEC cells. We found that some bHLHs show competitive complex formation whilst others do not. Competitive complex formation strongly correlated with a phylogenetic tree constructed with the bHLH proteins under investigation, suggesting a functional relevance. We demonstrate that this different behavior can be explained by changes in one amino acid and that this position is functionally relevant in trichome development but not in anthocyanidin regulation.

Anthocyanins accumulate in various organs of rice, and the regulatory genes involved in pigmentation of specific organs, such as pericarp, hull, leaf, apiculus, and stigma have been elucidated. However, the corresponding gene for rice culm pigmentation has not been clarified. The well-known MYB-bHLH-WD40 (MBW) complex plays vital role in regulating the anthocyanin biosynthesis pathway in plants. However, the core members of MBW and the hierarchical regulation between these members are not fully elucidated in rice. Here, by map-based cloning, we identified the culm-specific pigmentation gene S1 whose alleles are also known for hull/pericarp pigmentation. We also clarified that one WD40 protein encoding gene, WA1, is indispensable for anthocyanin biosynthesis in rice. In the cascading regulation among MBW members, S1 (bHLH) acts as the master gene by activating the expression of C1 (MYB), and then C1 activates the expression of WA1 (WD40), which is unique in plant species. This enables MBW members to be coordinated in a common way to efficiently regulate anthocyanin biosynthesis genes. Based on these studies, we explored the minimal gene set required for anthocyanin biosynthesis in rice. These findings will help us design new rice varieties with anthocyanin accumulation in specific organs as needed.