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Planta

, Volume 247, Issue 3, pp 733–743 | Cite as

Characterization of a gene regulatory network underlying astringency loss in persimmon fruit

  • Soichiro Nishiyama
  • Noriyuki Onoue
  • Atsushi Kono
  • Akihiko Sato
  • Keizo Yonemori
  • Ryutaro Tao
Original Article

Abstract

Main conclusion

Transcriptome analysis of a persimmon population segregating for an astringency trait in fruit suggested central roles for a limited number of transcriptional regulators in the loss of proanthocyanidin accumulation.

Persimmon (Diospyros kaki; 2n = 6x = 90) accumulates a large amount of proanthocyanidins (PAs) in its fruit, resulting in an astringent taste. Persimmon cultivars are classified into four types based on the nature of astringency loss and the amount of PAs at maturity. Pollination constant and non-astringent (PCNA)-type cultivars stop accumulating PAs in the early stages of fruit development and their fruit can be consumed when still firm without the need for artificial deastringency treatments. While the PCNA trait has been shown to be conferred by a recessive allele at a single locus (ASTRINGENCY; AST), the exact genetic determinant remains unidentified. Here, we conducted transcriptome analyses to elucidate the regulatory mechanism underlying this trait using developing fruits of an F1 population segregating for the PCNA trait. Comparisons of the transcriptomes of PCNA and non-PCNA individuals and hierarchical clustering revealed that genes related to the flavonoid pathway and to abiotic stress responses involving light stimulation were expressed coordinately with PA accumulation. Furthermore, coexpression network analyses suggested that three putative transcription factors were central to the PA regulatory network and that at least DkMYB4 and/or DkMYC1, which have been reported to form a protein complex with each other for PA regulation, may have a central role in the differential expression of PA biosynthetic pathway genes between PCNA and non-PCNA.

Keywords

Abiotic stress Coexpression network analysis Diospyros kaki Fruit transcriptome Proanthocyanidins 

Abbreviations

AST

ASTRINGENCY

CIPK

CBL-interacting protein kinase

GO

Gene ontology

PA

Proanthocyanidin

PCNA

Pollination constant and non-astringent

RPKM

Reads per kilobase of exon per million reads

Notes

Acknowledgements

We thank Dr. Takashi Akagi (Kyoto University) for critical advice and discussions on data interpretation. We also appreciate bioinformatics support from Dr. Luca Comai and Dr. Isabelle M Henry (UC Davis).

Compliance with ethical standards

Funding

This work was supported by Grant-in-Aid for JSPS Research Fellow to SN (Grant number JP16J10408), and for Scientific Research (B) to KY (Grant number JP16H04876) from Japan Society for the Promotion of Science.

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

425_2017_2819_MOESM1_ESM.pptx (821 kb)
Supplementary material 1 (PPTX 821 kb)
425_2017_2819_MOESM2_ESM.xlsx (58 kb)
Supplementary material 2 (XLSX 57 kb)

References

  1. 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 230:899–915.  https://doi.org/10.1007/s00425-009-0991-6 CrossRefPubMedGoogle Scholar
  2. 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 151:2028–2045.  https://doi.org/10.1104/pp.109.146985 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Akagi T, Ikegami A, Yonemori K (2010) DkMyb2 wound-induced transcription factor of persimmon (Diospyros kaki Thunb.), contributes to proanthocyanidin regulation. Planta 232:1045–1059.  https://doi.org/10.1007/s00425-010-1241-7 CrossRefPubMedGoogle Scholar
  4. Akagi T, Katayama-Ikegami A, Yonemori K (2011) Proanthocyanidin biosynthesis of persimmon (Diospyros kaki Thunb.) fruit. Sci Hortic 130:373–380.  https://doi.org/10.1016/j.scienta.2011.07.021 CrossRefGoogle Scholar
  5. Akagi T, Katayama-Ikegami A, Kobayashi S, Sato A, Kono A, Yonemori K (2012a) Seasonal abscisic acid signal and a basic leucine zipper transcription factor, DkbZIP5, regulate proanthocyanidin biosynthesis in persimmon fruit. Plant Physiol 158:1089–1102.  https://doi.org/10.1104/pp.111.191205 CrossRefPubMedGoogle Scholar
  6. Akagi T, Tao R, Tsujimoto T, Kono A, Yonemori K (2012b) Fine genotyping of a highly polymorphic ASTRINGENCY-linked locus reveals variable hexasomic inheritance in persimmon (Diospyros kaki Thunb.) cultivars. Tree Genet Genomes 8:195–204.  https://doi.org/10.1007/s11295-011-0432-0 CrossRefGoogle Scholar
  7. Akagi T, Henry IM, Tao R, Comai L (2014) A Y-chromosome-encoded small RNA acts as a sex determinant in persimmons. Science 346:646–650.  https://doi.org/10.1126/science.1257225 CrossRefPubMedGoogle Scholar
  8. Aron PM, Kennedy JA (2008) Flavan-3-ols: nature, occurrence and biological activity. Mol Nutr Food Res 52:79–104.  https://doi.org/10.1002/mnfr.200700137 CrossRefPubMedGoogle Scholar
  9. Bagchi D, Swaroop A, Preuss HG, Bagchi M (2014) Free radical scavenging, antioxidant and cancer chemoprevention by grape seed proanthocyanidin: an overview. Mutat Res 768:69–73.  https://doi.org/10.1016/j.mrfmmm.2014.04.004 CrossRefPubMedGoogle Scholar
  10. Berry JO, Yerramsetty P, Zielinski AM, Mure CM (2013) Photosynthetic gene expression in higher plants. Photosynth Res 117:91–120.  https://doi.org/10.1007/s11120-013-9880-8 CrossRefPubMedGoogle Scholar
  11. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40CrossRefPubMedGoogle Scholar
  12. del Mar Naval M, Gil-Muñoz F, Lloret A, Besada C, Salvador A, Badenes ML, Ríos G (2016) A WD40-repeat protein from persimmon interacts with the regulators of proanthocyanidin biosynthesis DkMYB2 and DkMYB4. Tree Genet Genomes 12:1–11.  https://doi.org/10.1007/s11295-016-0969-z CrossRefGoogle Scholar
  13. Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28.  https://doi.org/10.1111/j.1469-8137.2004.01217.x CrossRefPubMedGoogle Scholar
  14. Edel KH, Kudla J (2016) Integration of calcium and ABA signaling. Curr Opin Plant Biol 33:83–91.  https://doi.org/10.1016/j.pbi.2016.06.010 CrossRefPubMedGoogle Scholar
  15. Epple P, Mack AA, Morris VR, Dangl JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci USA 100:6831–6836.  https://doi.org/10.1073/pnas.1130421100 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711.  https://doi.org/10.4161/psb.6.5.15069 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50:473–503.  https://doi.org/10.1146/annurev.arplant.50.1.473 CrossRefPubMedGoogle Scholar
  18. Hu Z, Mellor J, Wu J, DeLisi C (2004) VisANT: an online visualization and analysis tool for biological interaction data. BMC Bioinform 5:17.  https://doi.org/10.1186/1471-2105-5-17 CrossRefGoogle Scholar
  19. Ikeda I, Yamada M, Kurihara A, Nishida T (1985) Inheritance of astringency in Japanese persimmon. J Jpn Soc Hortic Sci 54:39–45CrossRefGoogle Scholar
  20. 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 172:1037–1047.  https://doi.org/10.1016/j.plantsci.2007.02.010 CrossRefGoogle Scholar
  21. Jaakola L, Hohtola A (2010) Effect of latitude on flavonoid biosynthesis in plants. Plant Cell Environ 33:1239–1247.  https://doi.org/10.1111/j.1365-3040.2010.02154.x PubMedGoogle Scholar
  22. Kanzaki S, Akagi T, Masuko T, Kimura M, Yamada M, Sato A, Mitani N, Ustunomiya N, Yonemori K (2010) SCAR markers for practical application of marker-assisted selection in persimmon (Diospyros kaki Thunb.) breeding. J Jpn Soc Hortic Sci 79:150–155.  https://doi.org/10.2503/jjshs1.79.150 CrossRefGoogle Scholar
  23. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinform 9:559.  https://doi.org/10.1186/1471-2105-9-559 CrossRefGoogle Scholar
  24. Lepiniec L, Debeaujon I, Routaboul J-M, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430.  https://doi.org/10.1146/annurev.arplant.57.032905.105252 CrossRefPubMedGoogle Scholar
  25. Li S (2014) Transcriptional control of flavonoid biosynthesis: fine-tuning of the MYB-bHLH-WD40 (MBW) complex. Plant Signal Behav 8:1–7.  https://doi.org/10.4161/psb.27522 Google Scholar
  26. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Li Y-G, Tanner G, Larkin P (1996) The DMACA-HCl protocol and the threshold proanthocyanidin content for bloat safety in forage legumes. J Sci Food Agric 70:89–101.  https://doi.org/10.1002/(SICI)1097-0010(199601)70:1<89:AID-JSFA470>3.0.CO;2-N CrossRefGoogle Scholar
  28. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550.  https://doi.org/10.1186/s13059-014-0550-8 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Nishiyama S, Yonemori K, Ueda J (2014) Effect of ABA treatment on tannin accumulation at an early stage of fruit development in persimmon. Acta Hortic 1042:217–222CrossRefGoogle Scholar
  30. Nishiyama S, Onoue N, Kono A, Sato A, Ushijima K, Yamane H, Tao R, Yonemori K (2017) Comparative mapping of the ASTRINGENCY locus controlling fruit astringency in hexaploid persimmon (Diospyros kaki Thunb.) with the diploid D. lotus reference genome. Hortic J (in press)Google Scholar
  31. Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277.  https://doi.org/10.1016/j.tplants.2007.04.001 CrossRefPubMedGoogle Scholar
  32. Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34.  https://doi.org/10.1016/j.plaphy.2013.02.001 CrossRefPubMedGoogle Scholar
  33. Sato A, Yamada M (2016) Persimmon breeding in Japan for pollination-constant non-astringent (PCNA) type with marker-assisted selection. Breed Sci 66:60–68.  https://doi.org/10.1270/jsbbs.66.60 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, Luan S, Kudla J (1999) Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. Plant Cell 11:2393–2405.  https://doi.org/10.1105/tpc.11.12.2393 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Su F, Hu J, Zhang Q, Luo Z (2012) Isolation and characterization of a basic helix-loop-helix transcription factor gene potentially involved in proanthocyanidin biosynthesis regulation in persimmon (Diospyros kaki Thunb.). Sci Hortic 136:115–121.  https://doi.org/10.1016/j.scienta.2012.01.013 CrossRefGoogle Scholar
  36. Taira S, Matsumto N, Ono M (1998) Accumulation of soluble and insoluble tannins during fruit development in nonastringent and astringent persimmon. J Jpn Soc Hortic Sci 67:572–576.  https://doi.org/10.1248/cpb.37.3229 CrossRefGoogle Scholar
  37. Terrier N, Torregrosa L, Ageorges A, Vialet S, Verries C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggest additional targets in the pathway. Plant Physiol 149:1028–1041.  https://doi.org/10.1104/pp.108.131862 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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 223:7–12CrossRefPubMedGoogle Scholar
  39. Weinl S, Kudla J (2009) The CBL–CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528.  https://doi.org/10.1111/j.1469-8137.2009.02938.x CrossRefPubMedGoogle Scholar
  40. Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185.  https://doi.org/10.1016/j.tplants.2014.12.001 CrossRefPubMedGoogle Scholar
  41. Yamada M, Sato A (2002) Segregation for fruit astringency type in progenies derived from crosses of ‘Nishimurawase’ × pollination constant non-astringent genotypes in oriental persimmon (Diospyros kaki Thunb.). Sci Hortic 92:107–111.  https://doi.org/10.1016/S0304-4238(01)00285-0 CrossRefGoogle Scholar
  42. Yonemori K, Matsushima J (1985) Property of development of tannin cells in non-astringent type fruits of Japanese persimmon (Diospyros kaki) and its relationship to natural deastringency. J Jpn Soc Hortic Sci 54:201–208CrossRefGoogle Scholar
  43. Yonemori K, Sugiura A, Yamada M (2000) Persimmon genetics and breeding. Plant Breed Rev 19:191–225Google Scholar
  44. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14.  https://doi.org/10.1186/gb-2010-11-2-r14 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zoratti L, Karppinen K, Luengo Escobar A, Häggman H, Jaakola L (2014) Light-controlled flavonoid biosynthesis in fruits. Front Plant Sci 5:534.  https://doi.org/10.3389/fpls.2014.00534 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Graduate School of AgricultureKyoto UniversityKyotoJapan
  2. 2.Institute of Fruit Tree and Tea ScienceNational Agriculture and Food Research Organization (NARO)HigashihiroshimaJapan
  3. 3.Faculty of AgricultureRyukoku UniversityOtsuJapan

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