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Transcriptional regulation of anthocyanin biosynthesis in red cabbage
In Arabidopsis, ethylene suppresses anthocyanin accumulation by binding to redundant receptors such as ETR1, ETR2, ERS1 and ERS2, with ETR1 possibly playing a dominant regulatory role. Slightly reduced anthocyanin levels in ctr1 loss-of-function mutants suggest that CTR1 may function immediately downstream of or within the ethylene receptor complex. EIN2, which acts downstream of CTR1 and functions in a wide range of ethylene responses in plants, is involved in the ethylene signaling pathway. EIN3 and its homologue EIL1 appear to function redundantly in the ethylene pathway, as anthocyanin accumulation is increased significantly in the ein3 eil1 double mutant but not in the ein3-1 or eil1-3 single mutants. Therefore, the effect of ethylene on the suppression of sugar-induced anthocyanin biosynthesis likely involves the ethylene triple response ().
Ethylene has been associated with the increase in the soluble sugar contents of ripening fruit and the synthesis of flavonoids (). Treatment of grape berries with the ethylene-releasing compound 2-chloroethylphosphonic acid activated the transcription of structural genes encoding the key enzymes of anthocyanin biosynthesis and increased anthocyanin accumulation (). Ethylene also plays a negative regulatory role in anthocyanin biosynthesis. Anthocyanin accumulation in red cabbage grown in the dark and etiolated cabbage was markedly suppressed by ethylene (; ) and the inhibition of ethylene biosynthesis by cobalt increased anthocyanin accumulation in corn (). Transgenic tobacco transformed with the ethylene receptor gene was used to demonstrate the role of ethylene as a negative regulator of anthocyanin biosynthesis. Anthocyanin accumulation was increased in the petals of tobacco plants over-expressing the mutated ethylene receptor gene, ethylene response 1 (ETR1H69A) (). In contrast, constitutive triple response (ctr1) mutants grown in the presence of high levels of Suc had similar levels of anthocyanin than wild-type plants ().
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JAs, which include jasmonic acid and its cyclopentane precursors as well as cyclopentenones, modulate anthocyanin accumulation (). In the absence of sugar, JA treatment failed to induce the accumulation of anthocyanin and the DFR transcript, indicating that JA synergistically modulates sugar-induced anthocyanin biosynthesis by regulating the expression of the DFR gene (). The F-box protein Coronatine Insensitive-1 (COI1), which forms the SCFCOI1 complex with ASK1/ASK2, Cullin1, and Rbx1, is involved in diverse JA responses (), most of which are disrupted in the Arabidopsis mutant coronatine insensitive 1 (coi1). A coi1-1 mutant with a premature stop codon at W467 failed to accumulate anthocyanin in response to methyl JA (; ). Analysis of several transcript levels in coi1-1 mutants showed reduced expression of three anthocyanin regulatory factors, PAP1, PAP2 and GL3, which transcriptionally regulate the LBGs DFR, LDOX and UF3GT ().
CK signaling, which involves a phosphorelay mechanism similar to the bacterial two-component system (), is mediated by sensor His kinases (AHKs), His-containing phosphotransfer proteins (AHPs), and type-B and -A response regulators (ARRs) (). AHKs are positive and functionally overlapping regulators of CK signaling (; ; ). Several Arabidopsis CK signaling pathway mutants have been used to investigate the role of CK in the regulation of anthocyanin accumulation. The double mutants ahk2/3 and ahk3/4 showed significant reduction of anthocyanin accumulation in response to treatment with Suc and CK (; ). The type-B ARRs are redundant positive regulators of CK signaling and are the immediate upstream activators of type-A ARR gene expression (; ). Of 11 known type-B ARRs in Arabidopsis, the subfamily 1 contains 7 ARRs that are associated with CK signaling (). Suc-induced anthocyanin accumulation was significantly reduced in the single mutants arr1, arr10, and arr12, the double mutants arr1/10, arr1/12, and arr10/12, and the triple mutant arr1/10/12 treated with CK, indicating that ARR1, 10 and 12 act as positive regulators of CK signaling (; ). Furthermore, it turns out that CK enhances Suc induction of anthocyanin accumulation by affecting the PET signaling pathway via transcriptional activation of the positive regulators PAP1, (E)GL3 and TT8, and by repressing the MYBL2 transcript level () ().
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The JA-ZIM-domain (JAZ) family proteins, which are substrates of the SCFCOI1 complex, consist of 12 members and function as negative regulators of JA responses, probably by directly inhibiting various transcriptional regulators (; ). Protein-protein interaction studies revealed that JAZs directly interact with bHLHs (TT8, GL3, and EGL3) and R2R3-MYB TFs (PAP1 and GL1) in the MBW complex (; ). Recently, a model describing the COI1 regulation of JAZ proteins was proposed. Upon perception of the JA signal, COI1 recruits JAZs to the SCFCOI1 complex for ubiquitination and subsequent degradation by the 26S proteasome, which triggers the release of the MBW complexes to activate JA-induced anthocyanin biosynthesis.
In addition to their role as energy sources, sugars are important signaling molecules involved in the growth and development of higher plants (; ), and their signaling pathways have been studied extensively in free-living microorganisms such as cyanobacteria (; ; ), bacteria (), and yeast (). In Arabidopsis, anthocyanin production in cotyledons or leaves increases when seedlings are grown in a sugar-containing medium (; ). A similar phenomenon has been reported in radish hypocotyls () and grape cells (). In grape berry skin, sucrose (Suc) acts as an endogenous trigger, modulating the expression of anthocyanin biosynthesis genes (). The role of Suc was analyzed in detail in a study that examined the transcript levels of sugar responsive genes in Arabidopsis (). Exogenous Suc increased the transcript levels of the LBGs DFR, LDOX and UF3GT by several hundred-fold, while the transcripts levels of EBGs acting upstream of the DFR in anthocyanin biosynthesis, including CHI, CHS, and C4H, showed lower induction by Suc. This Suc effect on the induction of anthocyanin biosynthetic genes may be attributed to the greater than 2-fold upregulation of positive TFs such as GL3, TT8 and PAP1 concurrent with the 3.3-fold downregulation of the negative transcription factor MYBL2 (). Under these conditions, the active MBW complex would be dominant over the negative L2BW complex.
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Anthocyanins are ubiquitous flavonoid pigments found in most plant organs that play important roles in attracting pollinators and seed distributors, and protect the plant from pathogens, herbivores and environmental stresses such as UV-B light (). Anthocyanin biosynthesis is mainly regulated at the transcriptional level via a set of transcription factors including basic helix-loop-helix (bHLH), Leu-zipper, MADS-box, R2R3-MYB, WD40, WIP and WRKY factors (). In Arabidopsis, the phytochrome (PHY)-interacting transcription factor 3 (PIF3), a bHLH protein, interacts directly with PHYs and positively regulates anthocyanin biosynthesis (; ). LONG HYPOCOTYL5 (HY5), a Leu-zipper transcription factor (TF), serves as a point of convergence for phytochrome (PHY) and cryptochrome (CRY) signalings (), functioning as a positive regulator of anthocyanin biosynthesis (). It binds directly to the promoters of early biosynthesis genes (EBGs) such as chalcone synthase (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H) and flavonoid 3′-hydroxylase (F3′H), which are common to different flavonoid subpathways, and late biosynthesis genes (LBGs) such as dihydroflavonol 4-reductase (DFR), leucoanthocyanidin oxygenase (LDOX), anthocyanidin reductase (ANR) and UDP-glucose: flavonoid 3-O-glucosyltransferase (UF3GT) (; ). Transcription factors from the R2R3-MYB, bHLH and WD40 classes interact to form MBW regulatory complexes (; ; ; ). For instance, TRANSPARENT TESTA 2 (TT2; MYB123) requires the cofactors TT8 (bHLH42) and TTG1 (WD40-repeat protein) to form a ternary MBW complex that regulates the expression of the DFR and ANR genes, which are involved in the accumulation of proanthocyanidins in the seed coat (; ; ). Similarly, MYB75/PAP1 (PRODUCTION OF ANTHOCYANIN PIGMENT1) and MYB90/PAP2, which are members of the R2R3-MYB family, are responsible for bHLH co-factor-dependent transcriptional activation of phenylalanine-ammonia lyase (PAL), CHS, DFR and glutathione-S-transferase (GST), which are key enzymes of the anthocyanin biosynthesis pathway (). Contrary to the positive TFs, MYBL2, an R3 MYB protein, acts as a negative regulator of anthocyanin biosynthesis in response to environmental cues, such as high light and, presumably, nitrogen deficiency. It interacts with TT8 to form a transcriptional inhibitory complex, MYBL2/bHLH/TTG1 (L2BW). Anthocyanin biosynthesis in specific tissues and organs is therefore likely to be regulated by the balance between MBW and L2BW complexes (; ).
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Application of exogenous sugars and hormones can affect the expression of anthocyanin biosynthesis genes that is dependent on the presence of light. However, the signaling pathways triggered by sugars, hormones and light and the interactions between these signals, if any, are not well understood. A recent finding that the photosynthetic electron transport (PET) chain, in addition to the well-characterized HY5-dependent signaling, plays an important role in light signaling pathways in green, vegetative leaf tissues (; ) demonstrates the complexity of the cross-talk between various pathways. Sugar-induced anthocyanin biosynthesis is apparently modulated by the heterotrimeric M(L2)BW complexes that are under the regulation of hormones (; ; ; ), as schematically highlighted in . The present review summarizes the recent progress in our understanding of the interactions between sugars and hormones, primarily cytokinin (CK), ethylene, jasmonic acid (JA), abscisic acid (ABA) and gibberellic acid (GA), and their role in the light-dependent regulation of anthocyanin formation.
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