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Molecular Breeding

, 38:144 | Cite as

An R2R3-MYB transcription factor ODORANT1 regulates fragrance biosynthesis in lilies (Lilium spp.)

  • Kyosuke Yoshida
  • Naomi Oyama-Okubo
  • Masumi YamagishiEmail author
Article
  • 130 Downloads

Abstract

Flower fragrance is an important character for economic and ecological reasons. Lilies (Lilium spp.), important ornamental crops, mainly emit benzenoids/phenylpropanoids and terpenoids. Oriental hybrid lilies emit a strong fragrance, while Asiatic hybrid lilies often emit a weak fragrance. To delineate the genetic backgrounds that regulate volatile benzenoid/phenylpropanoid production in lilies, we isolated an R2R3-MYB transcription factor similar to Petunia × hybrida ODORANT1 (ODO1) from Oriental and Asiatic hybrid lilies. An identified gene, named Lilium hybrid ODO1 (LhODO1), could upregulate the expression of shikimate pathway genes and phenylalanine ammonia lyase (PAL) genes in transgenic petunia plants. The expression of LhODO1 in the Oriental hybrid lily ‘Casa Blanca’ exhibited a diurnal rhythm, which was highest at 16:00 and lowest at 4:00, and was attuned to the expressional rhythms of shikimate pathway and PAL genes. These diurnal changes in gene expression preceded changes in the production of endogenous volatile compounds. Expression of LhODO1 was specific to tepals, which are major sources of floral scent, and began at anthesis. These results indicate that LhODO1 plays a key role in the regulation of volatile benzenoid/phenylpropanoid production in lilies. In addition, LhODO1 may be responsible for the different fragrance intensities observed between the Oriental and Asiatic hybrid lilies, because LhODO1 expression was high in the Oriental hybrid lily cultivars but very low in wild lilies in sections Sinomartagon and Daurolirion, which are parental species of Asiatic hybrid lilies.

Keywords

Asiatic hybrid lilies Benzenoids/phenylpropanoids Diurnal rhythm LhODO1 Oriental hybrid lilies Terpenoids 

Notes

Funding information

This work was supported by a Grant-In-Aid for Scientific Research (No. 15H04447) from the Japan Society for the Promotion of Science.

Supplementary material

11032_2018_902_MOESM1_ESM.pdf (471 kb)
ESM 1 (PDF 470 kb)

References

  1. Amrad A, Moser M, Mandel T, De Vries M, Schuurink RC, Freitas L, Kuhlemeier C (2016) Gain and loss of floral scent production through changes in structural genes during pollinator-mediated speciation. Curr Biol 26:3303–3312CrossRefGoogle Scholar
  2. Ando T, Nomura M, Tsukahara J, Watanabe H, Kokubun H, Tsukamoto T, Hashimoto G, Marchesi E, Kitching IJ (2001) Reproductive isolation in a native population of Petunia sensu Jussieu (Solanaceae). Ann Bot 88:403–413CrossRefGoogle Scholar
  3. Asano Y (1989) Lilium L. In: Tsukamoto Y (ed) The grand dictionary of horticulture, vol vol. 5. Syogakukan, Tokyo, pp 198–209 (in Japanese)Google Scholar
  4. Ban Y, Bessho H, Moriguchi T (2009) A putative PhODO1 homologous MYB transcription factor gene, MdMYBB, is not involved in the regulation of aroma volatile biosynthesis in apple. Biol Plant 53:755–758CrossRefGoogle Scholar
  5. Boatright J, Negre F, Chen X, Kish CM, Wood B, Peel G, Orlova I, Gang D, Rhodes D, Dudareva N (2004) Understanding in vivo benzenoid metabolism in petunia petal tissue. Plant Physiol 135:1993–2011CrossRefGoogle Scholar
  6. Byers KJRP, Bradshaw HD, Riffell JA (2014) Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J Exp Biol 217:614–623CrossRefGoogle Scholar
  7. Cavallini E, Matus JT, Finezzo L, Zenoni S, Loyola R, Guzzo F, Schlechter R, Ageorges A, Arce-johnson P, Tornielli GB (2015) The phenylpropanoid pathway is controlled at different branches by a set of R2R3-MYB C2 repressors in grapevine. Plant Physiol 167:1448–1470CrossRefGoogle Scholar
  8. Colquhoun TA, Kim JY, Wedde AE, Levin LA, Schmitt KC, Schuurink RC, Clark DG (2011) PhMYB4 fine-tunes the floral volatile signature of Petunia×hybrida through PhC4H. J Exp Bot 62:1133–1143CrossRefGoogle Scholar
  9. Comber HF (1949) A new classification of the genus Lilium. Lily year book, vol. 13. Royal Horticultural Society, pp 86–105Google Scholar
  10. Du Y, He H, Wang Z, Li S, Wei C, Yuan X, Cui Q, Jia G (2014) Molecular phylogeny and genetic variation in the genus Lilium native to China based on the internal transcribed spacer sequences of nuclear ribosomal DNA. J Plant Res 127:249–263CrossRefGoogle Scholar
  11. Fenske MP, Hewett Hazelton KD, Hempton AK, Shim JS, Yamamoto BM, Riffell JA, Imaizumi T (2015) Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. Proc Natl Acad Sci U S A 112:9775–9780CrossRefGoogle Scholar
  12. Guterman I, Shalit M, Menda N, Piestun D, Dafny-yelin M, Shalev G, Bar E, Davydov O, Ovadis M, Emanuel M, Wang J, Adam Z, Pichersky E, Lewinsohn E, Zamir D, Vainstein A, Weiss D (2002) Rose scent : genomics approach to discovering novel floral fragrance-related genes. Plant Cell 14:2325–2338CrossRefGoogle Scholar
  13. Horsch RB, Fry JE, Hoffman NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231CrossRefGoogle Scholar
  14. Hu Z, Tang B, Wu Q, Zheng J, Leng P (2017) Transcriptome sequencing analysis reveals a difference in monoterpene biosynthesis between scented Lilium ‘Siberia’ and unscented Lilium ‘Novano’. Front Plant Sci 8:1351CrossRefGoogle Scholar
  15. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161CrossRefGoogle Scholar
  16. Johnson TS, Schwieterman ML, Young J, Cho KH, Clark DG, Colquhoun TA (2016) Lilium floral fragrance: a biochemical and genetic resource for aroma and flavor. Phytochemistry 122:103–112CrossRefGoogle Scholar
  17. Kishimoto K, Maeda H, Haketa T, Oyama-Okubo N (2014) Odor components and the control of odor development in ornamental cabbage. J Jpn Soc Hortic Sci 83:252–258CrossRefGoogle Scholar
  18. Kong Y, Sun M, Pan H, Zhang Q (2012) Composition and emission rhythm of floral scent volatiles from eight lily cut flowers. J Am Soc Hortic Sci 137:376–382Google Scholar
  19. Kong Y, Bai J, Lang L, Bao F, Dou X, Wang H, Shang H (2017) Floral scents produced by Lilium and Cardiocrinum species native to China. Biochem Syst Ecol 70:222–229CrossRefGoogle Scholar
  20. Lai Y, Yamagishi M, Suzuki T (2011) Elevated temperature inhibits anthocyanin biosynthesis in the tepals of an Oriental hybrid lily via the suppression of LhMYB12 transcription. Sci Hortic 132:59–65CrossRefGoogle Scholar
  21. Lai Y, Shimoyamada Y, Nakayama M, Yamagishi M (2012) Pigment accumulation and transcription of LhMYB12 and anthocyanin biosynthesis genes during flower development in the Asiatic hybrid lily (Lilium spp.). Plant Sci 193–194:136–147CrossRefGoogle Scholar
  22. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X Version 2.0. Bioinformatics 23:2947–2948CrossRefGoogle Scholar
  23. Leslie AC (1982) The international lily register, 3rd edn. The Royal Horticultural Society, LondonGoogle Scholar
  24. Lim KB, van Tuyl JM (2006) Lily: Lilium hybrids. In: Anderson NO (ed) Flower breeding and genetics: issues, challenges and opportunities for the 21st century. Springer, Dordrecht, pp 513–532Google Scholar
  25. Lim KB, Barba-Gonzalez R, Zhou S, Ramanna MS, van Tuyl JM (2008) Interspecific hybridization in lily (Lilium): Taxonomic and commercial aspects of using species hybrids in breeding. In: Teixeira da Silva JA (ed) Floriculture, ornamental and plant biotechnology, vol vol V. Global Science Books Ltd., Kagawa, pp 146–151Google Scholar
  26. Medina-Puche L, Molina-Hidalgo FJ, Boersma M, Schuurink RC, López-Vidriero I, Solano R, Franco-Zorrilla J-M, Caballero JL, Blanco-Portales R, Muñoz-Blanco J (2015) An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruit receptacles. Plant Physiol 168:598–614CrossRefGoogle Scholar
  27. Ministry of Agriculture, Forestry and Fisheries of Japan (2016) The 90th Statistical Yearbook of Ministry of Agriculture, Forestry and Fisheries. http://www.maff.go.jp/e/data/stat/90th/index.html#20. Accessed 16 November 2017
  28. van Moerkercke A, Haring MA, Schuurink RC (2011) The transcription factor EMISSION of BENZENOIDS II activates the MYB ODORANT1 promoter at a MYB binding site specific for fragrant petunias. Plant J 67:917–928CrossRefGoogle Scholar
  29. Morinaga SI, Kumano Y, Ota A, Yamaoka R, Sakai S (2009) Day-night fluctuations in floral scent and their effects on reproductive success in Lilium auratum. Popul Ecol 51:187–195CrossRefGoogle Scholar
  30. Muhlemann JK, Klempien A, Dudareva N (2014) Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:1936–1949CrossRefGoogle Scholar
  31. Nishikawa T, Okazaki K, Uchino T, Arakawa K, Nagamine T (1999) A molecular phylogeny of Lilium in the internal transcribed spacer region of nuclear ribosomal DNA. J Mol Evol 49:238–249CrossRefGoogle Scholar
  32. Nishikawa T, Okazaki K, Arakawa K, Nagamine T (2001) Phylogenic analysis of section Sinomartagon in genus Lilium using sequences of the internal transcribed spacer region in nuclear ribosomal DNA. Breed Sci 51:39–46CrossRefGoogle Scholar
  33. Oyama-Okubo N, Tsuji T (2013) Analysis of floral scent compounds and classification by scent quality in tulip cultivars. J Jpn Soc Hortic Sci 82:344–353CrossRefGoogle Scholar
  34. Oyama-Okubo N, Ando T, Watanabe N, Marchesi E, Uchida K, Nakayama M (2005) Emission mechanism of floral scent in Petunia axillaris. Biosci Biotechnol Biochem 69:773–777CrossRefGoogle Scholar
  35. Oyama-Okubo N, Nakayama M, Ichimura K (2011) Control of floral scent emission by inhibitors of phenylalanine ammonia-lyase in cut flower of Lilium cv. ‘Casa Blanca’. J Jpn Soc Hortic Sci 80:190–199CrossRefGoogle Scholar
  36. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL https://www.R-project.org/Google Scholar
  37. van Schie CC, Haring MA, Schuurink RC (2006) Regulation of terpenoid and benzenoid production in flowers. Curr Opin Plant Biol 9:203–208CrossRefGoogle Scholar
  38. Spitzer-Rimon B, Marhevka E, Barkai O, Marton I, Edelbaum O, Masci T, Prathapani NK, Shklarman E, Ovadis M, Vainstein A (2010) EOBII, a gene a flower-specific regulator of phenylpropanoid volatiles’ biosynthesis in petunia. Plant Cell 22:1961–1976CrossRefGoogle Scholar
  39. Spitzer-Rimon B, Farhi M, Albo B, Cna’ani A, MMB Z, Masci T, Edelbaum O, Yu Y, Shklarman E, Ovadis M, Vainstein A (2012) The R2R3-MYB–like factor EOBI, acting downstream of EOBII, regulates scent production by activating ODO1 and structural scent-related genes in petunia. Plant Cell 24:5089–5105CrossRefGoogle Scholar
  40. Suzuki K, Tasaki K, Yamagishi M (2015) Two distinct spontaneous mutations involved in white flower development in Lilium speciosum. Mol Breed 35:1–14CrossRefGoogle Scholar
  41. Suzuki K, Suzuki T, Nakatsuka T, Dohra H, Yamagishi M (2016) RNA-seq-based evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies (Lilium spp.). BMC Genomics 17:611CrossRefGoogle Scholar
  42. Verdonk JC, de Vos CHR, Verhoeven HA, Haring MA, van Tunen AJ, Schuurink RC (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 62:997–1008CrossRefGoogle Scholar
  43. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–1624CrossRefGoogle Scholar
  44. Vilsack T, Clark CZF (2009) US census of agriculture, 2007, vol 1. United States Department of Agriculture, p 51Google Scholar
  45. Wei Q, Luo Q, Wang R, Zhang F, He Y, Zhang Y, Qiu D (2017) A wheat R2R3-type MYB transcription factor TaODORANT1 positively regulates drought and salt stress responses in transgenic tobacco plants. Front Plant Sci 8:1374CrossRefGoogle Scholar
  46. Yamagishi M (2011) Oriental hybrid lily ‘Sorbonne’ homologue of LhMYB12 regulates anthocyanin biosyntheses in flower tepals and tepal spots. Mol Breed 28:381–389CrossRefGoogle Scholar
  47. Yamagishi M (2013) How genes paint lily flowers: regulation of colouration and pigmentation patterning. Sci Hortic 163:27–36CrossRefGoogle Scholar
  48. Yamagishi M, Nakatsuka T (2017) LhMYB12, regulating tepal anthocyanin pigmentation in Asiatic hybrid lilies, is derived from Lilium dauricum and L. bulbiferum. Hortic J 86:528–533CrossRefGoogle Scholar
  49. Yamagishi M, Ihara H, Arakawa K, Toda S, Suzuki K (2014) The origin of the LhMYB12 gene, which regulates anthocyanin pigmentation of tepals, in Oriental and Asiatic hybrid lilies (Lilium spp.). Sci Hortic 174:119–125CrossRefGoogle Scholar
  50. Yamagishi M, Uchiyama H, Handa T (2018) Floral pigmentation pattern in Oriental hybrid lily (Lilium spp.) cultivar ‘Dizzy’ is caused by transcriptional regulation of anthocyanin biosynthesis genes. J Plant Physiol 228:85–91CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Kyosuke Yoshida
    • 1
  • Naomi Oyama-Okubo
    • 2
  • Masumi Yamagishi
    • 3
    Email author
  1. 1.Graduate School of AgricultureHokkaido UniversitySapporoJapan
  2. 2.Institute of Vegetable and Floricultural ScienceTsukubaJapan
  3. 3.Research Faculty of AgricultureHokkaido UniversitySapporoJapan

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