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Planta

, Volume 233, Issue 5, pp 883–894 | Cite as

Effects of seasonal temperature changes on DkMyb4 expression involved in proanthocyanidin regulation in two genotypes of persimmon (Diospyros kaki Thunb.) fruit

  • Takashi Akagi
  • Tomoyuki Tsujimoto
  • Ayako Ikegami
  • Keizo YonemoriEmail author
Original Article

Abstract

Persimmon fruits accumulate a large amount of proanthocyanidin (PA). Fruits of the mutant non-astringent (NA) type lose their ability to accumulate PA at an early stage of fruit development, whereas fruits of the normal astringent (A) type sustain PA accumulation until ripening. This allelotype is determined by the genotype of a single ASTRINGENCY (AST) locus. It is possible that the reduction in PA accumulation in NA-type fruits is due to phenological down-regulation of DkMyb4 (a PA regulator) and the resultant down-regulation of structural genes in the PA pathway. In this study, attempts were made to identify the regulatory mechanisms of phenological PA accumulation in A- and NA-type fruits, focusing particularly on the effects of ambient temperature. Continuous cool temperature conditions caused sustained expression of DkMyb4 in NA-type fruits, as well as in A-type fruits, resulting in increased expression of PA pathway genes and PA accumulation. However, the expression of some A/NA phenotypic marker genes was not significantly affected by the cool temperature conditions. In addition, PA composition in NA-type fruits exposed to cool temperatures differed from that in A-type fruits. These results indicate that a cool ambient temperature may have induced DkMyb4 expression and resultant PA accumulation, but did not directly affect the expression of the AST gene.

Keywords

Astringency Myb Persimmon Proanthocyanidin Temperature 

Abbreviations

ANR

Anthocyanidin reductase

A-type

Astringent type

CA

Catechin

CHS

Chalcone synthase

EC

Epicatechin

EC-G

Epicatechin-gallate

EGC

Epigallocatechin

EGC-G

Epigallocatechin-gallate

F3′H

Flavonoid 3′-hydroxylase

F3′5′H

Flavonoid 3′5′-hydroxylase

GC

Gallocatechin

LAR

Leucoanthocyanidin reductase

NA-type

Non-astringent type

PA

Proanthocyanidin

TF

Transcription factor

References

  1. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. Plant Cell 9:1859–1868PubMedCentralPubMedGoogle Scholar
  2. Akagi T, Ikegami A, Suzuki Y, Yoshida J, Yamada M, Sato A, Yonemori K (2009a) Expression balances of structural genes in shikimate and flavonoid biosynthesis cause a difference in proanthocyanidin accumulation in persimmon (Diospyros kaki Thunb.) fruit. Planta 230:899–915PubMedCrossRefGoogle Scholar
  3. Akagi T, Ikegami A, Tsujimoto T, Kobayashi S, Sato A, Kono A, Yonemori K (2009b) DkMyb4 is a Myb transcription factor involved in proanthocyanidin biosynthesis in persimmon fruit. Plant Physiol 151:2028–2045PubMedCentralPubMedCrossRefGoogle Scholar
  4. Akagi T, Kanzaki S, Gao M, Tao R, Parfitt DE, Yonemori K (2009c) Quantitative real-time PCR to determine allele number for the astringency locus by analysis of a linked marker in Diosypros kaki Thunb. Tree Genet Genomes 5:483–492CrossRefGoogle Scholar
  5. Akagi T, Ikegami A, Yonemori K (2010a) DkMyb2 wound-induced transcription factor of persimmon (Diospyros kaki Thunb.), contributes to proanthocyanidin regulation. Planta. doi:  10.1007/s00425-010-1241-7
  6. Akagi T, Suzuki Y, Ikegami A, Kamitakahara H, Takano T, Nakatsubo F, Yonemori K (2010b) Condensed tannin composition analysis in persimmon (Diospyros kaki Thunb.) fruit by acid catalysis in the presence of excess phloroglucinol. J Jap Soc Hort Sci 79:275–281CrossRefGoogle Scholar
  7. Aron PM, Kennedy JA (2008) Flavan-3-ols: nature, occurrence and biological activity. Mol Nutr Food Res 52:79–104PubMedCrossRefGoogle Scholar
  8. Bagchi D, Bagchi M, Stohs SJ, Das DK, Ray SD, Kuszynski CA, Joshi SS, Pruess HG (2000) Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention. Toxicology 148:187–197PubMedCrossRefGoogle Scholar
  9. Bogs J, Jaffé FW, Takos AM, Walker AR, Robinson SP (2007) The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol 143:1347–1361PubMedCentralPubMedCrossRefGoogle Scholar
  10. Deluc L, Bogs J, Walker AR, Ferrier T, Decendit A, Merillon JM, Robinson SP, Barrieu F (2008) The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanidin biosynthesis in developing grape berries. Plant Physiol 147:2041–2053PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dixon RA, Xie D-Y, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28PubMedCrossRefGoogle Scholar
  12. Downey MO, Harvey JS, Robinson SP (2003) Analysis of tannins in seeds and skins of Shiraz grapes throughout berry development. Aust J Grape Wine Res 9:15–27CrossRefGoogle Scholar
  13. Gagné S, Lacampagnea S, Claissea O, Gény L (2009) Leucoanthocyanidin reductase and anthocyanidin reductase gene expression and activity in flowers, young berries and skins of Vitis vinifera L. cv. Cabernet-Sauvignon during development. Plant Physiol Biochem 47:282–290PubMedCrossRefGoogle Scholar
  14. Harborne JB, Grayer RJ (1993) Flavonoids and insects. In: Harborne JB (ed) The flavonoids: advances in research since 1986. Chapman & Hall, London, pp 589–618CrossRefGoogle Scholar
  15. Hattori T, Vasil V, Rosenkrans L, Hannah LC, McCarty DR, Vasil K (1992) The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev 6:609–618PubMedCrossRefGoogle Scholar
  16. Hoballah ME, Gübitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell’Olivo A, Arnold M, Kuhlemeier C (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19:779–790PubMedCentralPubMedCrossRefGoogle Scholar
  17. Ikegami A, Kitajima A, Yonemori K (2005) Inhibition of flavonoid biosynthetic gene expression coincides with loss of astringency in pollination-constant, non-astringent (PCNA)-type persimmon fruit. J Hort Sci Biotech 80:225–228Google Scholar
  18. Ikegami A, Eguchi S, Kitajima A, Inoue K, Yonemori K (2007) Identification of genes involved in proanthocyanidin biosynthesis of persimmon (Diospyros kaki) fruit. Plant Sci 172:1037–1047CrossRefGoogle Scholar
  19. Ikegami A, Akagi T, Potter D, Yamada M, Sato A, Yonemori K, Kitajima A, Inoue K (2009) Molecular identification of 1-cys peroxiredoxin and anthocyanidin/flavonol 3-O-galactosyltransferase from proanthocyanidin-rich young fruits of persimmon (Diospyros kaki Thunb.). Planta 230:841–855PubMedCentralPubMedCrossRefGoogle Scholar
  20. Kennedy JA, Jones GP (2001) Analysis of proanthocyanidin cleavage products following acid-catalysis in the presence of excess phloroglucinol. J Agric Food Chem 49:1740–1746PubMedCrossRefGoogle Scholar
  21. Kobayashi S (2009) Regulation of anthocyanin biosynthesis in grape. J Jap Soc Hort Sci 78:387–393CrossRefGoogle Scholar
  22. Kojima K, Shiozaki K, Koshita Y, Ishida M (1999) Changes of endogenous levels of ABA, IAA and GA-like substances in fruitlets of parthenocarpic persimmon [Diospyros kaki]. J Jap Soc Hort Sci 68:242–247CrossRefGoogle Scholar
  23. Koyama K, Goto-Yamamoto N (2008) Bunch shading during different developmental stages affects the phenolic biosynthesis in berry skins of ‘Cabernet Sauvignon’ grapes. J Am Soc Hort Sci 133:743–753Google Scholar
  24. Lacampagne S, Gagné S, Gény L (2010) Involvement of abscisic acid in controlling the proanthocyanidin biosynthesis pathway in grape skin: new elements regarding the regulation of tannin composition and leucoanthocyanidin reductase (LAR) and anthocyanidin reductase (ANR) activities and expression. J Plant Growth Regul 29:81–90CrossRefGoogle Scholar
  25. Lavola A (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiol 18:53–58PubMedCrossRefGoogle Scholar
  26. Lees GL (1992) Condensed tannins in some forage legumes: their role in the prevention of ruminant pasture bloat. Basic Life Sci 59:915–934PubMedGoogle Scholar
  27. Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonids. Annu Rev Plant Biol 57:405–430PubMedCrossRefGoogle Scholar
  28. Li YG, Tanner G, Larkin P (1996) The DMACA-HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J Sci Food Agric 70:89–101CrossRefGoogle Scholar
  29. Lin-Wang K, Bolitho K, Grafton K, Kortstee A, Karunairetnam S, McGhie TK, Espley RV, Hellens RP, Allan AC (2010) An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 10:50PubMedCentralPubMedCrossRefGoogle Scholar
  30. Matsuo T, Ito S (1978) The chemical structure of kaki-tannin from immature fruit of the persimmon (Diospyros kaki L.). Agric Biol Chem 42:1637–1643CrossRefGoogle Scholar
  31. Matus JT, Loyola R, Vega A, Peña-Neira A, Bordeu E, Arce-Johnson P, Alcalde JA (2009) Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera. J Exp Bot 60:853–867PubMedCrossRefGoogle Scholar
  32. Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and UV-B -responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941PubMedCentralPubMedCrossRefGoogle Scholar
  33. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa × P deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant-Microbe Interact 20:816–831PubMedCrossRefGoogle Scholar
  34. Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945PubMedCrossRefGoogle Scholar
  35. Nesi N, Jond C, Debeaujon I, Caboche M, Lepiniec L (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. Plant Cell 13:2099–2114PubMedCentralPubMedGoogle Scholar
  36. Pang Y, Peel GJ, Wright E, Wang Z, Dixon RA (2007) Early steps in proanthocyanidin biosynthesis in the model legume Medicago truncatula. Plant Physiol 145:601–615Google Scholar
  37. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32:701–712PubMedCrossRefGoogle Scholar
  38. Spayd SE, Tarara JM, Mee DL, Ferguson JC (2002) Separation of sunlight and temperature effects on the composition of Vitis vinifera cv. Merlot Berries. Am J Enol Vitic 53:171–182Google Scholar
  39. Taira S (1996) Astringency in persimmon. In: Linskens HF, Jackson JF (eds) Fruit analysis. Springer, Berlin, pp 97–110CrossRefGoogle Scholar
  40. Taira S, Matsumoto N, Ono M (1998) Accumulation of soluble and insoluble tannins during fruit development in nonastringent and astringent persimmon. J Jap Soc Hort Sci 67:572–576CrossRefGoogle Scholar
  41. 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 142:1216–1232PubMedCentralPubMedCrossRefGoogle Scholar
  42. Tanner GJ, Francki KT, Abrahams S, Watson JM, Larkin PJ, Ashton AR (2003) Proanthocyanidin biosynthesis in plants. Purification of legume leucoanthocyanidin reductase and molecular cloning of its cDNA. J Biol Chem 278:31647–31656PubMedCrossRefGoogle Scholar
  43. Terrier T, Torregrosa L, Ageorges A, Vialet S, Verries C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149:1028–1041PubMedCentralPubMedCrossRefGoogle Scholar
  44. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539PubMedCentralPubMedGoogle Scholar
  45. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12PubMedCrossRefGoogle Scholar
  46. Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493PubMedCentralPubMedCrossRefGoogle Scholar
  47. Xie D-Y, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonid biosynthesis. Science 299:396–399PubMedCrossRefGoogle Scholar
  48. Yamada M, Sato A (2002) Segregation for fruit astringency type in progenies derived from crosses of ‘Nishimura-wase’ × pollination constant non-astringent genotypes in oriental persimmon (Diospyros kaki Thunb). Sci Hort 92:107–111CrossRefGoogle Scholar
  49. Yamane H, Jeong ST, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57:49–54Google Scholar
  50. Yonemori K, Sugiura A, Yamada M (2000) Persimmon genetics and breeding. In: Janick J (ed) Plant breeding reviews 19. Wiley, New York, pp 191–225Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Takashi Akagi
    • 1
  • Tomoyuki Tsujimoto
    • 1
  • Ayako Ikegami
    • 2
  • Keizo Yonemori
    • 1
    Email author
  1. 1.Laboratory of Pomology, Graduate School of AgricultureKyoto UniversityKyotoJapan
  2. 2.Laboratory of Pomology, Department of Bioproduction SciencesIshikawa Prefectural UniversityNonoichiJapan

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