Abstract
The spatially and temporally distinct expression of R2R3-MYB positive regulators is among the major mechanisms that create various anthocyanin color patterns in many flowers. However, we do not know how these positive regulators have gained different expression profiles. In the Asiatic hybrid lily ‘Lollypop’ (derived from the crosses of species belonging to Sinomartagon/Daurolirion section), MYB12 and MYB19S regulate the pigmentation at whole tepals and raised tepal spots, respectively. In the Oriental hybrid lily ‘Sorbonne’ (derived from the crosses of species belonging to the Archelirion section), MYB12 regulates both whole tepal and raised spot pigmentation. The genes have similar amino acid sequences with similar protein functions but exhibit different expression profiles in lily flowers. As promoters are among the most significant factors affecting gene expression profiles, their promoter sequences were determined in this study. The three genes had very different promoter sequences, and putative cis-regulatory elements were not conserved in numbers or order. To further confirm the promoter functions, tobacco plants were transformed with native promoter-driven MYB12 or MYB19S genes of ‘Lollypop.’ Expression levels of MYB12 were higher in corolla tubes than in lobes, while those of MYB19S were higher in corolla lobes than in tubes. Thus, the diverse promoter functions were likely to be the leading causes of their different expression profiles and generation of unique color patterns. Finally, the history of R2R3-MYB gene establishment during lily evolution was estimated using sequence data.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data
The nucleotide sequences defined in this study were deposited in the DDBJ nucleotide sequence databases under the accession numbers LC612729 and LC612730.
References
Albert NW, Lewis DH, Zhang H, Schwinn KE, Jameson PE, Davies KM (2011) Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning. Plant J 65:771–784. https://doi.org/10.1111/j.1365-313X.2010.04465.x
Albert NW, Davies KM, Schwinn KE (2014) Gene regulation networks generate diverse pigmentation patterns in plants. Plant Signal Behav 9:e29526. https://doi.org/10.4161/psb.29526
Bird R (1991) Lilies: an illustrated identifier and guide to cultivation. Chartwell Books Inc, Secaucus, NJ
Chiou CY, Yeh KW (2008) Differential expression of MYB gene (OgMYB1) determines color patterning in floral tissue of Oncidium Gower Ramsey. Plant Mol Biol 66:379–388. https://doi.org/10.1007/s11103-007-9275-3
Comber HF (1949) A new classification of the genus Lilium. Lily Yearbook, vol 13. The Royal Horticultural Society, London, pp 85–105
Cooley AM, Modliszewski JL, Rommel ML, Willis JH (2011) Gene duplication in Mimulus underlies parallel floral evolution via independent trans-regulatory changes. Curr Biol 21:700–704. https://doi.org/10.1016/j.cub.2011.03.028
Davies KM, Albert NW, Schwinn KE (2012) From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct Plant Biol 39:619–638. https://doi.org/10.1071/FP12195
Fattorini R, Glover BJ (2020) Molecular mechanisms of pollination biology. Annu Rev Plant Biol 71:487–515. https://doi.org/10.1146/annurev-arplant-081519-040003
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279. https://doi.org/10.1093/nar/gkh458
Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53:814–827. https://doi.org/10.1111/j.1365-313X.2007.03373.x
Horsch RB, Fry JE, Hoffman NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231. https://doi.org/10.1126/science.227.4691.1229
Hsu CC, Chen YY, Tsai WC, Chen WH, Chen HH (2015) Three R2R3-MYB transcription factors regulate distinct floral pigmentation patterning in Phalaenopsis spp. Plant Physiol 168:175–191. https://doi.org/10.1104/pp.114.254599
Jiang P, Rausher M (2018) Two genetic changes in cis-regulatory elements caused evolution of petal spot position in Clarkia. Nature Plants 4:14–22. https://doi.org/10.1038/s41477-017-0085-6
Kusters E, Pina SD, Castel R, Souer E, Koes R (2015) Changes in cis-regulatory elements of a key floral regulator are associated with divergence of inflorescence architectures. Development 142:2822–2831. https://doi.org/10.1242/dev.121905
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 193–194:136–147. https://doi.org/10.1016/j.plantsci.2012.05.013
Lescot M, Déhais P, Moreau Y, De Moor B, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Lin R-C, Rausher MD (2021) R2R3-MYB genes control petal pigmentation patterning in Clarkia gracilis ssp. sonomensis (Onagraceae). New Phytol 229:1147–1162. https://doi.org/10.1111/nph.16908
Marasek-Ciolakowska A, Nishikawa T, Shea DJ, Okazaki K (2018) Breeding of lilies and tulips—interspecific hybridization and genetic background. Breed Sci 68:35–52. https://doi.org/10.1270/jsbbs.17097
Martins TR, Jiang P, Rausher MD (2017) How petals change their spots: cis-regulatory re-wiring in Clarkia (Onagraceae). New Phytol 216:510–518. https://doi.org/10.1111/nph.14163
Matus JT, Cavallini E, Loyola R, Höll J, Finezzo L, Santo SD, Vialet S, Commisso M, Roman F, Schubert A, Alcalde JA, Bogs J, Ageorges A, Tornielli GB, Arce-Johnson P (2017) A group of grapevine MYBA transcription factors located in chromosome 14 control anthocyanin synthesis in vegetative organs with different specificities compared with the berry color locus. Plant J 91:220–236. https://doi.org/10.1111/tpj.13558
Ministry of Agriculture, Forestry and Fisheries of Japan (2019) The 93rd statistical yearbook of Ministry of Agriculture, Forestry and Fisheries. https://www.maff.go.jp/e/data/stat/93th/index.html#14Accessed 22 July 2020
Nakayama M (2014) A research strategy to understand the mechanisms that govern flower color pattern formation. Jpn Agric Res Q 48:271–277. https://doi.org/10.6090/jarq.48.271
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 49:238–249. https://doi.org/10.1007/PL00006546
Pattanaik S, Kong Q, Zaitlin D, Werkman JR, Xie CH, Patra B, Yuan L (2010) Isolation and functional characterization of a floral tissue-specific R2R3 MYB regulator from tobacco. Planta 231:1061–1076. https://doi.org/10.1007/s00425-010-1108-y
Sakai M, Yamagishi M, Matsuyama K (2019) Repression of anthocyanin biosynthesis by R3-MYB transcription factors in lily (Lilium spp.). Plant Cell Rep 38:609–622. https://doi.org/10.1007/s00299-019-02391-4
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. https://doi.org/10.1105/tpc.105.039255
Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456. https://doi.org/10.1016/S1369-5266(00)00199-0
Suzuki K, Tasaki K, Yamagishi M (2015) Two distinct spontaneous mutations involved in white flower development in Lilium speciosum. Mol Breed 35:193. https://doi.org/10.1007/s11032-015-0389-z
Suzuki K, Suzuki T, Nakatsuka T, Dohra H, Yamagishi M, Matsuyama K, Matsuura H (2016) RNA-seq-based evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies (Lilium spp.). BMC Genom 17:611. https://doi.org/10.1186/s12864-016-2995-5
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. https://doi.org/10.1111/j.1365-313X.2006.02997.x
Wang X, Yamagishi M (2019) Mechanisms suppressing carotenoid accumulation in flowers differ depending on the hybrid groups of lilies (Lilium spp.). Sci Hortic 243:159–168. https://doi.org/10.1016/j.scienta.2018.08.025
Yamagishi M (2011) Oriental hybrid lily Sorbonne homologue of LhMYB12 regulates anthocyanin biosyntheses in flower tepals and tepal spots. Mol Breed 28:381–389. https://doi.org/10.1007/s11032-010-9490-5
Yamagishi M (2013) How genes paint lily flowers: regulation of colouration and pigmentation patterning. Sci Hortic 163:27–36. https://doi.org/10.1016/j.scienta.2013.07.024
Yamagishi M (2016) A novel R2R3-MYB transcription factor regulates light-mediated floral and vegetative anthocyanin pigmentation patterns in Lilium regale. Mol Breed 36:3. https://doi.org/10.1007/s11032-015-0426-y
Yamagishi M (2018) Involvement of a LhMYB18 transcription factor in large anthocyanin spot formation on the flower tepals of the Asiatic hybrid lily (Lilium spp.) cultivar “Grand Cru.” Mol Breed 38:60. https://doi.org/10.1007/s11032-018-0806-1
Yamagishi M (2020a) White with partially pink flower color in Lilium cernuum var album is caused by transcriptional regulation of anthocyanin biosynthesis genes. Sci Hortic 260:108880. https://doi.org/10.1016/j.scienta.2019.108880
Yamagishi M (2020b) Isolation and identification of MYB transcription factors (MYB19Long and MYB19Short) involved in raised spot anthocyanin pigmentation in lilies (Lilium spp.). J Plant Physiol 250:153164. https://doi.org/10.1016/j.jplph.2020.153164
Yamagishi M (2020c) MYB19LONG is involved in brush-mark pattern development in Asiatic hybrid lily (Lilium spp.) flowers. Sci Hortic 272:109570. https://doi.org/10.1016/j.scienta.2020.109570
Yamagishi M, Akagi K (2013) Morphology and heredity of tepal spots in Asiatic and Oriental hybrid lilies (Lilium spp.). Euphytica 194:325–334. https://doi.org/10.1007/s10681-013-0937-8
Yamagishi M, Nakatsuka T (2017) LhMYB12, regulating tepal anthocyanin pigmentation in Asiatic hybrid lilies, is derived from Lilium dauricum and L. bulbiferum. Hort J 86:528–533. https://doi.org/10.2503/hortj.OKD-057
Yamagishi M, Sakai M (2020) The microRNA828/MYB12 module mediates bicolor pattern development in Asiatic hybrid lily (Lilium spp.) flowers. Front Plant Sci 11:590791. https://doi.org/10.3389/fpls.2020.590791
Yamagishi M, Shimoyamada Y, Nakatsuka T, Masuda K (2010) Two R2R3-MYB genes, homologs of petunia AN2, regulate anthocyanin biosyntheses in flower tepals, tepal spots and leaves of Asiatic hybrid lily. Plant Cell Physiol 51:463–474. https://doi.org/10.1093/pcp/pcq011
Yamagishi M, Yoshida Y, Nakayama M (2012) The transcription factor LhMYB12 determines anthocyanin pigmentation in the tepals of Asiatic hybrid lilies (Lilium spp.) and regulates pigment quantity. Mol Breed 30:913–925. https://doi.org/10.1007/s11032-011-9675-6
Yamagishi M, Ihara H, Arakawa K, Toda S, Suzuki K (2014a) The origin of the LhMYB12 gene, which regulates anthocyanin pigmentation of tepals, in Oriental and Asiatic hybrid lilies (Lilium spp.). Sci Hortic 174:119–125. https://doi.org/10.1016/j.scienta.2014.05.017
Yamagishi M, Toda S, Tasaki K (2014b) The novel allele of the LhMYB12 gene is involved in splatter-type spot formation on the flower tepals of Asiatic hybrid lilies (Lilium spp.). New Phytol 201:1009–1020. https://doi.org/10.1111/nph.12572
Yuan Y-W, Sagawa JM, Frost L, Vela JP, Bradshaw HD (2014) Transcriptional control of floral anthocyanin pigmentation in monkeyflowers (Mimulus). New Phytol 204:1013–1027. https://doi.org/10.1111/nph.12968
Zhou H, Peng Q, Zhao J, Owiti A, Ren F, Liao L (2016) Multiple R2R3-MYB transcription tactors involved in the regulation of anthocyanin accumulation in peach flower. Front Plant Sci 7:1557. https://doi.org/10.3389/fpls.2016.01557
Funding
This work was supported by a Grant-in-Aid for Scientific Research (No. 19H02945) from the Japan Society for the Promotion of Science.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by the author.
Additional information
Communicated by Stefan Hohmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yamagishi, M. High promoter sequence variation in subgroup 6 members of R2R3-MYB genes is involved in different floral anthocyanin color patterns in Lilium spp.. Mol Genet Genomics 296, 1005–1015 (2021). https://doi.org/10.1007/s00438-021-01799-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-021-01799-6