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A MYB transcription factor regulates anthocyanin biosynthesis in mangosteen (Garcinia mangostana L.) fruit during ripening

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Abstract

Mangosteen (Garcinia mangostana L.) fruit undergo rapid red colour development, both on the tree and after harvest, resulting in high anthocyanin production in the pericarp. Here, we report the isolation of three full-length mangosteen MYB transcription factors (GmMYB1, GmMYB7 and GmMYB10) and all the anthocyanin biosynthetic pathway genes (GmPal to GmUFGT). Phylogenetic analysis at the protein level of the R2R3-MYB transcription factor family showed GmMYB10 had a high degree of similarity with production of anthocyanin pigment1 in Arabidopsis and as well as sequences from other plant species related to the elevation of anthocyanin pigmentation. In transient transactivation assays, GmMYB10, co-expressed with AtbHLH2, strongly activated the GmDFR and AtDFR promoters. Transcripts of GmMYB10 and GmUFGT were highly abundant with onset of pigmentation and subsequently during red colouration. Our results suggest that GmMYB10 plays an important role in regulating anthocyanin biosynthesis both on the tree and after harvest, while GmUFGT may be a key biosynthetic gene in mangosteen pigmentation. The expression patterns of GmMYB10 and GmUFGT correlated with ethylene production that increased linearly until stage 5 (dark purple) and decreased thereafter. 1-Methycyclopropene (1-MCP) clearly delayed red colouration with resulting down-regulation of GmMYB10. These results suggest that the effect of ethylene on anthocyanin biosynthesis may be via the regulation of GmMYB10 expression.

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Abbreviations

bHLH:

Basic helix-loop-helix

CHS:

Chalcone synthase

CHI:

Chalcone isomerase

DFR:

Dihydroflavonol 4-reductase

F3H:

Flavanone 3-hydroxylase

F3′H:

Flavonoid 3′-hydroxylase

LDOX:

Leucoanthocyanidin dioxygenase

PAL:

Phenylalanine ammonia lyase

TFs:

Transcription factors

PERE:

Primary ethylene response element

UFGT:

UDP-glucose:flavonoid 3-O-glucosyltransferase

References

  • Aharoni A, De Vos CHR, Wein M, Sun Z, Greco R, Kroon A, Mol JNM, O’Connell AP (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J 28:319–332

    Article  PubMed  CAS  Google Scholar 

  • Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    Article  PubMed  CAS  Google Scholar 

  • Ban Y, Honda C, Hatsuyama Y, Igarashi M, Bessho H, Moriguchi T (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant Cell Physiol 48:958–970

    Article  PubMed  CAS  Google Scholar 

  • Bogs J, Jaffe FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143:1347–1361

    Article  PubMed  CAS  Google Scholar 

  • Borevitz JO, Xia Y, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2394

    Article  PubMed  CAS  Google Scholar 

  • Boss PK, Davies C, Robinson SP (1996) Analysis of the expression of anthocyanin pathway genes in developing Vitis vinifera L. cv Shiraz grape berries and the implications for pathway regulation. Plant Physiol 111:1059–1066

    PubMed  CAS  Google Scholar 

  • Broun P (2005) Transcriptional control of flavonoid biosynthesis: a complex network of conserved regulators involved in multiple aspects of differentiation in Arabidopsis. Curr Opin Plant Biol 8:272–279

    Article  PubMed  CAS  Google Scholar 

  • Castellarin S, Di Gaspero G (2007) Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines. BMC Plant Biol 7:46

    Article  PubMed  Google Scholar 

  • Chervin C, El-Kereamy A, Roustan J-P, Latch A, Lamon J, Bouzayen M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167:1301–1305

    Article  CAS  Google Scholar 

  • Cox KA, McGhie TK, White A, Woolf AB (2004) Skin colour and pigment changes during ripening of ‘Hass’ avocado fruit. Postharvest Biol Technol 31:287–294

    Article  CAS  Google Scholar 

  • El-Kereamy A, Chervin C, Roustan JP, Cheynier V, Souquet JM, Moutounet M, Raynal J, Ford C, Latche A, Pech JC, Bouzayen M (2003) Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiol Plant 119:175–182

    Article  CAS  Google Scholar 

  • Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427

    Article  PubMed  CAS  Google Scholar 

  • Fu C, Loo AEK, Chia FPP, Huang D (2007) Oligomeric proanthocyanidins from mangosteen pericarps. J Agric Food Chem 55:7689–7694

    Article  PubMed  CAS  Google Scholar 

  • Gil MI, Holcroft DM, Kader AA (1997) Changes in strawberry anthocyanins and other polyphenols in response to carbon dioxide treatments. J Agric Food Chem 45:1662–1667

    Article  CAS  Google Scholar 

  • Hellens R, Allan A, Friel E, Bolitho K, Grafton K, Templeton M, Karunairetnam S, Gleave A, Laing W (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13

    Article  PubMed  Google Scholar 

  • Honda C, Kotoda N, Wada M, Kondo S, Kobayashi S, Soejima J, Zhang Z, Tsuda T, Moriguchi T (2002) Anthocyanin biosynthetic genes are coordinately expressed during red coloration in apple skin. Plant Physiol Biochem 40:955–962

    Article  CAS  Google Scholar 

  • Ji X, Avula B, Khan IA (2007) Quantitative and qualitative determination of six xanthones in Garcinia mangostana L. by LC-PDA and LC-ESI-MS. J Pharm Biomed Anal 43:1270–1276

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Joyce DC, Terry LA (2001) 1-Methylcyclopropene treatment affects strawberry fruit decay. Postharvest Biol Technol 23:227–232

    Article  CAS  Google Scholar 

  • Kobayashi S, Ishimaru M, Ding CK, Yakushiji H, Goto N (2001) Comparison of UDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci 160:543–550

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Ishimaru M, Hiraoka K, Honda C (2002) Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 215:924–933

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982

    Article  PubMed  Google Scholar 

  • Koes R, Verweij W, Quattrocchio F (2005) Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends Plant Sci 10:236–242

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Gomez R, Gomez-Lim MA (1992) A method for extracting intact RNA from fruits rich in polysaccharides using ripe mango mesocarp. HortScience 27:440–442

    CAS  Google Scholar 

  • Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol 149:851–862

    Article  PubMed  CAS  Google Scholar 

  • Martin C, Paz-Ares J (1997) MYB transcription factors in plants. Trends Genet 13:67–73

    Article  PubMed  CAS  Google Scholar 

  • Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8:83

    Article  PubMed  Google Scholar 

  • Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565

    Article  PubMed  CAS  Google Scholar 

  • Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3:212–217

    Article  Google Scholar 

  • Palapol Y, Ketsa S, Stevenson D, Cooney JM, Allan AC, Ferguson IB (2009) Colour development and quality of mangosteen (Garcinia mangostana L.) fruit during ripening and after harvest. Postharvest Biol Technol 51:349–353

    Article  CAS  Google Scholar 

  • Piccaglia R, Marotti M, Baldoni G (2002) Factors influencing anthocyanin content in red cabbage (Brassica oleracea var capitata L f rubra (L) Thell). J Sci Food Agric 82:1504–1509

    Article  CAS  Google Scholar 

  • Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851

    Article  PubMed  CAS  Google Scholar 

  • Solano R, Nieto C, Avila J, Canas L, Diaz I, Paz-Ares J (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 14:1773–1784

    PubMed  CAS  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev 12:3703–3714

    Article  PubMed  CAS  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  PubMed  CAS  Google Scholar 

  • Takos AM, Jaffe FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232

    Article  PubMed  CAS  Google Scholar 

  • Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C (1998) The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–154

    Article  PubMed  CAS  Google Scholar 

  • Tira-Umphon A, Roustan JP, Chervin C (2007) The stimulation by ethylene of the UDP glucose-flavonoid 3-O-glucosyltransferase (UFGT) in grape tissues is independent from the MybA transcription factors. Vitis 46:210–211

    CAS  Google Scholar 

  • Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima JI, Awazuhara M, Inoue E, Takahashi H, Goodenowe DB, Kitayama M, Noji M, Yamazaki M, Saito K (2005) Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. Plant J 42:218–235

    Article  PubMed  CAS  Google Scholar 

  • Walker AR, Lee E, Bogs J, McDavid DAJ, Thomas MR, Robinson SP (2007) White grapes arose through the mutation of two similar and adjacent regulatory genes. Plant J 49:772–785

    Article  PubMed  CAS  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann IM, Heim MA, Weisshaar B, Uhrig JF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40:22–34

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank members of the Fruit Genomics team for helpful information. The research was financially supported by the Thailand Research Fund (TRF), Commission on Higher Education, Ministry of Education and Postharvest Technology Innovation Center, and is the part of a collaborative programme with Plant & Food Research, New Zealand.

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Authors and Affiliations

  1. Department of Horticulture, Faculty of Agriculture, Kasetsart University, Bangkok, 10900, Thailand

    Yossapol Palapol & Saichol Ketsa

  2. Plant and Food Research, Private Bag 92169, Auckland, New Zealand

    Kui Lin-Wang, Ian B. Ferguson & Andrew C. Allan

Authors
  1. Yossapol Palapol
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  2. Saichol Ketsa
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  3. Kui Lin-Wang
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  4. Ian B. Ferguson
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  5. Andrew C. Allan
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Corresponding author

Correspondence to Saichol Ketsa.

Additional information

The nucleotide sequence data reported in this article were submitted to the GenBank Nucleotide Sequence Databases under the accession numbers FJ197127 (GmPAL), FJ197128 (GmCHS), FJ197129 (GmCHI), FJ197130 (GmDFR), FJ197131 (GmF3H), FJ197132 (GmF3′H), FJ197133 (GmLDOX), FJ197134 (GmUFGT), FJ197135 (GmMYB1), FJ197136 (GmMYB7), FJ197137 (GmMYB10), FJ197138 (GmDFR promoter), FJ197139 (GmLDOX promoter) and FJ197140 (GmUFGT promoter).

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Palapol, Y., Ketsa, S., Lin-Wang, K. et al. A MYB transcription factor regulates anthocyanin biosynthesis in mangosteen (Garcinia mangostana L.) fruit during ripening. Planta 229, 1323–1334 (2009). https://doi.org/10.1007/s00425-009-0917-3

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