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Regulation of anthocyanin biosynthesis in peach fruits

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Abstract

Main Conclusion

MYB10.1 and MYB10.3, with bHLH3, are the likely regulators of anthocyanin biosynthesis in peach fruit. MYB10.1/2/3 forms a cluster on the same genomic fragment where the Anther color ( Ag ) trait is located.

Anthocyanins are bioactive compounds responsible for the pigmentation of many plant parts such as leaves, flowers, fruits and roots, and have potential benefits to human health. In peach [Prunus persica (L.) Batsch], peel color is a key determinant for fruit quality and is regulated by flavonoids including anthocyanins. The R2R3 MYB transcription factors (TFs) control the expression of anthocyanin biosynthetic genes with the help of co-activators belonging to the basic-helix-loop-helix (bHLH) and WD40 repeat families. In the peach genome six MYB10-like and three bHLH-like TFs were identified as candidates to be the regulators of the anthocyanin accumulation, which, in yellow flesh fruits, is highest in the peel, abundant in the part of the mesocarp surrounding the stone and lowest in the mesocarp. The expression of MYB10.1 and MYB10.3 correlates with anthocyanin levels of different peach parts. They also have positive correlation with the expression of key structural genes of the anthocyanin pathway, such as CHS, F3H, and UFGT. Functions of peach MYB10s were tested in tobacco and shown to activate key genes in the anthocyanin pathway when bHLHs were co-expressed as partners. Overexpression of MYB10.1/bHLH3 and MYB10.3/bHLH3 activated anthocyanin production by up-regulating NtCHS, NtDFR and NtUFGT while other combinations were not, or much less, effective. As three MYB10 genes are localized in a genomic region where the Ag trait, responsible for anther pigmentation, is localized, it is proposed they are key determinant to introduce new peach cultivars with higher antioxidant level and pigmented fruit.

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Abbreviations

ANR:

anthocyanidin reductase

bHLH:

basic helix-loop-helix

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

DFR:

Dihydroflavonol 4-reductase

F3H:

Flavanone 3-hydroxylase

LAR:

Leucoanthocyanidin reductase

LDOX:

Leucoanthocyanidin dioxygenase

PA:

Proanthocyanidin

TF:

Transcription factor

UFGT:

UDP-flavonoid glucosyl transferase

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Acknowledgments

The authors wish to thank Prof. Patrizia Torrigiani, Department of Fruit Tree and Woody Plant Sciences, University of Bologna, Italy for providing primers of peach anthocyanin biosynthetic genes and Dr. Ian Moore, Department of Plant Sciences, University of Oxford, for providing vectors of the pOp/LhG4 system. This research work was supported by Ministero delle Politiche Agricole Alimentari e Forestali-Italy through the project ‘DRUPOMICS’ (Grant DM14999/7303/08) and University of Padova (Grant no. CPDA072133/07). MAR was supported by a “Fondazione CARIPARO” fellowship.

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Author notes

  1. Md. Abdur Rahim

    Present address: Department of Genetics and Plant Breeding, Sher-e-Bangla Agricultural University, Dhaka, 1207, Bangladesh

  2. Nicola Busatto

    Present address: Department of Agricultural Sciences, Bologna University, Via Fanin 46, 40127, Bologna, Italy

Authors and Affiliations

  1. Department of Biology, University of Padova, Viale G. Colombo 3, 35121, Padova, Italy

    Md. Abdur Rahim, Nicola Busatto & Livio Trainotti

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  1. Md. Abdur Rahim
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  2. Nicola Busatto
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Correspondence to Livio Trainotti.

Additional information

Special topic: Anthocyanins. Guest editor: Stefan Martens.

Electronic supplementary material

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425_2014_2078_MOESM1_ESM.jpg

Phylogenetic tree showing relationships between Arabidopsis and peach MYB TFs. Green solid squares: Arabidopsis (given as TAIR nos) anthocyanin promoting MYB TFs; red solid circles: peach (given as Phytozome nos) MYB10-like TFs located on pseudomolecule 3; black solid circles: peach MYB TFs named according to Ravaglia et al. (2013). Please note that ppa016711m (MYB10.2) was previously named MYB10 by Lin-Wang et al. 2010 and by Ravaglia et al., 2013 and correspond to GenBank record EU155160. Phylogenetic and molecular evolutionary analyses were conducted using neighbor-joining method and 1000 bootstrap replicates using MEGA version 5. Numbers close to the nodes indicates bootstrap values (JPEG 8973 kb)

425_2014_2078_MOESM2_ESM.tif

Microarray expression profiles of MYB genes in different stages of seed and mesocarp development in peach cultivar. ‘Fantasia’. The highest value for each gene has been arbitrarily set to 100 (blue), and the others accordingly (0 = white). Val MAX: maximum expression value; F_m: mean expression in peach flowers at anthesis while 1 to 6 are various developmental stages of seed (S) and mesocarp (M), with 1 and 2 covering stage S1, 3 and 4 stage S2, 5 stage S3 and 6 stage S4 of peach development. ‘na’ indicates no expression values (TIFF 94 kb)

425_2014_2078_MOESM3_ESM.tif

Expression of six peach MYB10 like genes in anthocyanin-accumulating organs. Expression levels were tested in S4 (ripe) fruit peel, mature and senescing leaf and flower by qRT-PCR. The expression values of the target genes were normalized by the expression values of the PpN1 gene, used as internal standard. Error bars shown are ± SE from the means of triplicates (TIFF 13230 kb)

425_2014_2078_MOESM4_ESM.jpg

Phylogenetic tree showing relationships between Arabidopsis and peach bHLH TFs. Green solid squares: Arabidopsis (given as TAIR nos) bHLH TFs acting as co-regulators of MYB TFs for the regulation of anthocyanin production; red solid circles: peach (given as Phytozome nos) bHLH-like TFs belonging to the same clade of the Arabidopsis co-regulators. Phylogenetic and molecular evolutionary analyses were conducted using neighbor-joining method and 1000 bootstrap replicates using MEGA version 5 (JPEG 9464 kb)

425_2014_2078_MOESM5_ESM.tif

Microarray expression profiles of bHLH genes in different stages of seed and mesocarp development in peach cultivar. ‘Fantasia’. The highest value for each gene has been arbitrarily set to 100 (blue), and the others accordingly (0 = white). Val MAX: maximum expression value; F_m: mean expression in peach flowers at anthesis while 1 to 6 are various developmental stages of seed (S) and mesocarp (M), with 1 and 2 covering stage S1, 3 and 4 stage S2, 5 stage S3 and 6 stage S4 of peach development (TIFF 61 kb)

425_2014_2078_MOESM6_ESM.tif

Microarray expression profile of WD40 gene in different stages of seed and mesocarp development in peach cultivar. ‘Fantasia’. The highest value has been arbitrarily set to 100 (blue), and the others accordingly (0 = white). Val MAX: maximum expression value; F_m: mean expression in peach flowers at anthesis while 1 to 6 are various developmental stages of seed (S) and mesocarp (M), with 1 and 2 covering stage S1, 3 and 4 stage S2, 5 stage S3 and 6 stage S4 of peach development (TIFF 37 kb)

425_2014_2078_MOESM7_ESM.tif

Transcript level of peach MYB10 s and bHLHs detected by qRT-PCR from agroinfiltrated tobacco leaves. The expression values of the target genes were normalized by the expression values of the GUS gene, used as internal standard. Error bars shown are ± SE from the means of triplicates (TIFF 13870 kb)

425_2014_2078_MOESM8_ESM.tif

Total anthocyanin content in agroinfiltrated peach mesocarp. M1, M2, M3, B1, B2, B3 and S indicate plasmids for the expression of MYB10.1, MYB10.2, MYB10.3, bHLH3, bHLH33, GL3 and 35S::Lhg4, respectively. Error bars shown are ± SD of the means of three replicates (TIFF 7567 kb)

425_2014_2078_MOESM9_ESM.tif

Protein sequence alignment of peach MYB10 TFs with other MYB TFs that are known to be involved in anthocyanin and PA biosynthesis from other species. Two highly conserved MYB domains were shown above the alignment. The amino acids highlighted with a circle (R in the R2-MYB domain, V and A in the R3-MYB domain) are the three key amino acid residues mediating the specificity of either the anthocyanin or PA pathway (Heppel et al. 2013). The amino acid motif “[DE]Lx2[RK]x3Lx6Lx3R” below the alignment indicates the interacting site for bHLH TFs. The protein sequences have the same accession nos as described in Fig. 3 but for Arabidopsis AtMYB123 (AT5G35550); grape VvMYBPA1 (CAJ90831); peach MYB123 (ppa023768m) and MYBPA1 (ppa009439m) (TIFF 17095 kb)

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DNA and protein sequence alignments for the cloned MYB10 s and bHLHs with the reference sequence of the peach genome (www.phytozome.net) (TXT 43 kb)

Supplementary material 11 (DOCX 29 kb)

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Rahim, M.A., Busatto, N. & Trainotti, L. Regulation of anthocyanin biosynthesis in peach fruits. Planta 240, 913–929 (2014). https://doi.org/10.1007/s00425-014-2078-2

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