Research Advance in the Regulation Mechanism of Flower Spots Formation in Ornamental Plant

doi:10.13560/j.cnki.biotech.bull.1985.2023-0242

Abstract

Abstract:

Many ornamental plants have various coloration patterns on their flower petals; these flower color variations are called flower spots. Flower spot is a very important ornamental characteristic of plants and have great significance in evolutionary biology. It could help plants to attract pollinators, defend against natural enemies and adapt to environmental changes. In this paper we reviewed recent advances in the molecular mechanism of flower spots formation, and then summarized the genetic law and influencing factors of flower spots formation. Moreover, we described the important roles of structural genes and transcription factors（TFs）related to pigment synthesis in the formation of flower spots in detail, i.e., the spatiotemporal specific expression and competition mechanism of structural genes promote the pigments differential accumulation in petals. TFs participate in the coloration patterns formation by directly or indirectly regulating the positioning expressions of structural genes. Furthermore, we introduced other regulation mechanisms, such as post-transcriptional regulation, post-translation regulation and methylation, and gathered the molecular regulatory network of flower spots formation, aiming to provide a new perspective for studying the molecular mechanism of flower spots formation in plants.

Key words: flower spots formation, flavonoid, molecular mechanism

QI Fang-ting, HUANG He. Research Advance in the Regulation Mechanism of Flower Spots Formation in Ornamental Plant[J]. Biotechnology Bulletin, 2023, 39(10): 17-28.

Figures/Tables 2

Fig. 1 Regular and irregular flower spots a: A. majus showing venosa phenotype[10]; b: blotch pattern in the P. rockii[11]; c: Lilium spp. present spots in the petals[12]; d: S. cruentus ‘Jester’ having bicolor flower[13]; e: picotee type flower in P. hybrida[14]; f: star type flower in P. hybrida[14]; g: G. diffusa showing a unique “eye” pattern in ray florets[15]; h: C. orchid presenting a differential coloration in nectar guide[16]; i: variational coloration type in D. variabilis[17]; j: P. persica showing two-color and variegated flowers in one single plant[18]; k: flower in P. suffruticosa ‘Er Qiao’ presenting various coloration type[11]; m: S. ionantha showing pink-purple flower[19]

Fig. 2 Multiple regulation mechanisms of the flower spots formation

References 107

[14]	Morita Y, Saito R, Ban Y, et al. Tandemly arranged chalcone synthase A genes contribute to the spatially regulated expression of siRNA and the natural bicolor floral phenotype in Petunia hybrida[J]. Plant J, 2012, 70(5): 739-749. doi: 10.1111/tpj.2012.70.issue-5 URL
[15]	Thomas MM, Rudall PJ, Ellis AG, et al. Development of a complex floral trait: the pollinator-attracting petal spots of the beetle daisy Gorteria diffusa(Asteraceae)[J]. Am J Bot, 2009, 96(12): 2184-2196. doi: 10.3732/ajb.0900079 URL
[16]	Wang L, Albert NW, Zhang HB, et al. Temporal and spatial regulation of anthocyanin biosynthesis provide diverse flower colour intensities and patterning in Cymbidium orchid[J]. Planta, 2014, 240(5): 983-1002. doi: 10.1007/s00425-014-2152-9 pmid: 25183255
[17]	Ohno S, Hosokawa M, Hoshino A, et al. A bHLH transcription factor, DvIVS, is involved in regulation of anthocyanin synthesis in dahlia(Dahlia variabilis)[J]. J Exp Bot, 2011, 62(14): 5105-5116. doi: 10.1093/jxb/err216 pmid: 21765172
[18]	陈丽, 薛良交, 李淑娴. 跳枝碧桃花色性状的全基因组关联分析[J]. 园艺学报, 2021, 48(3): 553-565. doi: 10.16420/j.issn.0513-353x.2020-0465
	Chen L, Xue LJ, Li SX. Genome-wide association study of flower color trait in Prunus persica f. versicolor[J]. Acta Hortic Sin, 2021, 48(3): 553-565.
[19]	Yang SJ, Ohno S, Deguchi A, et al. The histological study in sympetalous corolla development of pinwheel-type flowers of Saintpaulia[J]. Sci Hortic, 2017, 223: 10-18. doi: 10.1016/j.scienta.2017.04.036 URL
[20]	Erpelding JE. Genetic characterisation of the petal spot phenotype for Gossypium arboreum accession PI 408798[J]. Czech J Genet Plant Breed, 2020, 56(2): 79-83. doi: 10.17221/88/2019-CJGPB URL
[21]	Yuan YW, Rebocho AB, Sagawa JM, et al. Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species[J]. Proc Natl Acad Sci USA, 2016, 113(9): 2448-2453. doi: 10.1073/pnas.1515294113 URL
[22]	Niki T, Sasaki K, Shikata M, et al. Conversion of abaxial to adaxial petal in a Torenia(Torenia fournieri Lind. ex fourn.)mutant appeared in selfed progeny of the mutable line ‘flecked’[J]. Hortic J, 2016, 85(4): 351-359. doi: 10.2503/hortj.MI-129 URL
[1]	Davies KM, Albert NW, Schwinn KE. From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning[J]. Funct Plant Biol, 2012, 39(8): 619-638. doi: 10.1071/FP12195 pmid: 32480814
[2]	Leonard AS, Papaj DR. ‘X’ marks the spot: the possible benefits of nectar guides to bees and plants[J]. Funct Ecol, 2011, 25(6): 1293-1301. doi: 10.1111/fec.2011.25.issue-6 URL
[3]	van der Kooi CJ, Dyer AG, Kevan PG, et al. Functional significance of the optical properties of flowers for visual signalling[J]. Ann Bot, 2019, 123(2): 263-276. doi: 10.1093/aob/mcy119 URL
[4]	Dinkel T, Lunau K. How drone flies(Eristalis tenax L., Syrphidae, Diptera)use floral guides to locate food sources[J]. J Insect Physiol, 2001, 47(10): 1111-1118. pmid: 12770188
[5]	Goodale E, Kim E, Nabors A, et al. The innate responses of bumble bees to flower patterns: separating the nectar guide from the nectary changes bee movements and search time[J]. Naturwissenschaften, 2014, 101(6): 523-526. doi: 10.1007/s00114-014-1188-9 pmid: 24879351
[6]	Simonds V, Plowright CMS. How do bumblebees first find flowers? Unlearned approach responses and habituation[J]. Animal Behav, 2004, 67(3): 379-386. doi: 10.1016/j.anbehav.2003.03.020 URL
[7]	Gronquist M, Bezzerides A, Attygalle A, et al. Attractive and defensive functions of the ultraviolet pigments of a flower(Hypericum calycinum)[J]. Proc Natl Acad Sci USA, 2004, 98(24): 13745-13750. doi: 10.1073/pnas.231471698 URL
[8]	Koski MH, MacQueen D, Ashman TL. Floral pigmentation has responded rapidly to global change in ozone and temperature[J]. Curr Biol, 2020, 30(22): 4425-4431. doi: 10.1016/j.cub.2020.08.077 URL
[9]	Cooley AM, Willis JH. Genetic divergence causes parallel evolution of flower color in Chilean Mimulus[J]. New Phytol, 2009, 183(3): 729-739. doi: 10.1111/nph.2009.183.issue-3 URL
[10]	Shang YJ, Venail J, Mackay S, et al. The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum[J]. New Phytol, 2011, 189(2): 602-615. doi: 10.1111/nph.2010.189.issue-2 URL
[23]	Kondo M, Tanikawa N, Nishijima T. Mutation of CYCLOIDEA expands variation of dorsal-ventral flower asymmetry expressed as a pigmentation pattern in Torenia fournieri cultivars[J]. Hortic J, 2020, 89(4): 481-487. doi: 10.2503/hortj.UTD-174 URL
[24]	Martins TR, Berg JJ, Blinka S, et al. Precise spatio-temporal regulation of the anthocyanin biosynthetic pathway leads to petal spot formation in Clarkia gracilis(Onagraceae)[J]. New Phytol, 2013, 197(3): 958-969. doi: 10.1111/nph.2013.197.issue-3 URL
[25]	Zhang YZ, Cheng YW, Xu SZ, et al. Tree peony variegated flowers show a small insertion in the F3'H gene of the acyanic flower parts[J]. BMC Plant Biol, 2020, 20(1): 211. doi: 10.1186/s12870-020-02428-x
[26]	Cheng J, Liao L, Zhou H, et al. A small indel mutation in an anthocyanin transporter causes variegated colouration of peach flowers[J]. J Exp Bot, 2015, 66(22): 7227-7239. doi: 10.1093/jxb/erv419 pmid: 26357885
[27]	Koseki M, Goto K, Masuta C, et al. The star-type color pattern in Petunia hybrida ‘red Star’ flowers is induced by sequence-specific degradation of chalcone synthase RNA[J]. Plant and Cell Physiol, 2005, 46(11): 1879-1883. doi: 10.1093/pcp/pci192 URL
[28]	McMillan RT, Palmateer A, Vendrame WA. Survey for Cymbidium mosaic and odontoglossum ring spot viruses in domestic and international orchids[J]. Phytopathology, 2006, 96(6): S76-S76.
[29]	Deguchi A, Tatsuzawa F, Hosokawa M, et al. Tobacco streak virus(strain dahlia)suppresses post-transcriptional gene silencing of flavone synthase II in black dahlia cultivars and causes a drastic flower color change[J]. Planta, 2015, 242(3): 663-675. doi: 10.1007/s00425-015-2365-6 pmid: 26186968
[30]	Kay QON, Daoud HS, Stirton CH. Pigment distribution, light reflection and cell structure in petals[J]. Bot J Linn Soc, 1981, 83: 57-84. doi: 10.1111/j.1095-8339.1981.tb00129.x URL
[31]	Zhang R, Lu Y. Molecular mechanisms and natural selection of flower color variation[J]. Bota Res, 2016, 5(6): 186-209.
[32]	Grotewold E. The genetics and biochemistry of floral pigments[J]. Ann Rev Plant Biol, 2006, 57: 761-780. doi: 10.1146/arplant.2006.57.issue-1 URL
[33]	Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids[J]. Plant J, 2008, 54(4): 733-749. doi: 10.1111/tpj.2008.54.issue-4 URL
[34]	Todesco M, Bercovich N, Kim A, et al. Genetic basis and dual adaptive role of floral pigmentation in sunflowers[J]. eLife, 2022, 11: e72072. doi: 10.7554/eLife.72072 URL
[35]	Schwinn K, Venail J, Shang YJ, et al. A Small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum[J]. Plant Cell, 2006, 18(4): 831-851. doi: 10.1105/tpc.105.039255 pmid: 16531495
[36]	Li J, Wang ZH. Integrative metabolomic and transcriptome analysis reveal the differential mechanisms of spot color in the lips of Dendrobium chrysotoxum[J]. J Plant Biol, 2022: 1-13.
[37]	Yuan Y, Li X, Yao X, et al. Mechanisms underlying the formation of complex color patterns on Nigella orientalis(Ranunculaceae)petals[J]. New Phytol, 2023, 237(6): 2450-2466. doi: 10.1111/nph.v237.6 URL
[38]	Morita Y, Hoshino A. Recent advances in flower color variation and patterning of Japanese morning glory and petunia[J]. Breed Sci, 2018, 68(1): 128-138. doi: 10.1270/jsbbs.17107 URL
[39]	Huyen DTT, Van DT, Huang KL, et al. Distribution and composition of flavonols in the flowers of Rhododendron oldhamii maxim[J]. J Fac Agric Kyushu Univ, 2016, 61(1): 37-40.
[40]	Shoji K, Miki N, Nakajima N, et al. Perianth bottom-specific blue color development in Tulip cv. Murasakizuisho requires ferric ions[J]. Plant Cell Physiol, 2007, 48(2): 243-251. pmid: 17179184
[41]	Yoshida K, Oniduka T, Oyama KI, et al. Blue flower coloration of Corydalis ambigua requires ferric ion and kaempferol glycoside[J]. Biosci Biotechnol Biochem, 2021, 85(1): 61-68. doi: 10.1093/bbb/zbaa022 URL
[42]	Li Y, Kong F, Liu Z, et al. PhUGT78A22, a novel glycosyltransferase in Paeonia ‘He Xie’, can catalyze the transfer of glucose to glucosylated anthocyanins during petal blotch formation[J]. BMC Plant Biol, 2022, 22(1): 405. doi: 10.1186/s12870-022-03777-5
[43]	Zhang S, Chen J, Jiang T, et al. Genetic mapping, transcriptomic sequencing and metabolic profiling indicated a glutathione S-transferase is responsible for the red-spot-petals in Gossypium arboreum[J]. Theor Appl Gene, 2022, 135(10): 3443-3454. doi: 10.1007/s00122-022-04191-z
[44]	Yamagishi M. How genes paint lily flowers: regulation of colouration and pigmentation patterning[J]. Sci Hortic, 2013, 163: 27-36. doi: 10.1016/j.scienta.2013.07.024 URL
[45]	Wang X, Yamagishi M. Mechanisms suppressing carotenoid accumulation in flowers differ depending on the hybrid groups of lilies(Lilium spp.)[J]. Sci Hortic, 2019, 243: 159-168. doi: 10.1016/j.scienta.2018.08.025 URL
[46]	Inagaki Y, Hisatomi Y, Suzuki T, et al. Isolation of a suppressor-mutator/enhancer-like transposable element, Tpnl, from Japanese morning glory bearing variegated flowers[J]. Plant Cell, 1994, 6(3): 375-383. pmid: 8180498
[47]	Morita Y, Takagi K, Fukuchi-Mizutani M, et al. A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation[J]. Plant J, 2014, 78(2): 294-304. doi: 10.1111/tpj.2014.78.issue-2 URL
[48]	Morita Y, Ishiguro K, Tanaka Y, et al. Spontaneous mutations of the UDP-glucose: flavonoid 3-O-glucosyltransferase gene confers pale- and dull-colored flowers in the Japanese and common morning glories[J]. Planta, 2015, 242(3): 575-587. doi: 10.1007/s00425-015-2321-5 URL
[49]	Itoh Y, Higeta D, Suzuki A, et al. Excision of transposable elements from the chalcone isomerase and dihydroflavonol 4-reductase genes may contribute to the variegation of the yellow-flowered carnation(Dianthus caryophyllus)[J]. Plant Cell Physiol, 2002, 43(5): 578-585. doi: 10.1093/pcp/pcf065 URL
[50]	Wong DCJ, Perkins J, Peakall R. Anthocyanin and flavonol glycoside metabolic pathways underpin floral color mimicry and contrast in a sexually deceptive orchid[J]. Front Plant Sci, 2022, 13: 860997. doi: 10.3389/fpls.2022.860997 URL
[51]	Li Q, Wang J, Sun HY, et al. Flower color patterning in pansy(Viola×wittrockiana Gams.) is caused by the differential expression of three genes from the anthocyanin pathway in acyanic and cyanic flower areas[J]. Plant Physiol Biochem, 2014, 84: 134-141. doi: 10.1016/j.plaphy.2014.09.012 URL
[52]	Dubos C, Stracke R, Grotewold E, et al. MYB transcription factors in Arabidopsis[J]. Trends Plant Sci, 2010, 15(10): 573-581. doi: 10.1016/j.tplants.2010.06.005 URL
[53]	LaFountain AM, Yuan YW. Repressors of anthocyanin biosynthesis[J]. New Phytol, 2021, 231(3): 933-949. doi: 10.1111/nph.17397 pmid: 33864686
[54]	Abid MA, Wei Y, Meng Z, et al. Increasing floral visitation and hybrid seed production mediated by beauty mark in Gossypium hirsutum[J]. Plant Biotechnol J, 2022, 20(7): 1274-1284. doi: 10.1111/pbi.v20.7 URL
[55]	Nishijima T, Morita Y, Sasaki K, et al. A Torenia(Torenia fournieri Lind. ex fourn.)novel mutant ‘Flecked’ produces variegated flowers by insertion of a DNA transposon into an R2R3-MYB gene[J]. J Japan Soc Hort Sci, 2013, 82(1): 39-50. doi: 10.2503/jjshs1.82.39 URL
[56]	Hsu CC, Su CJ, Jeng MF, et al. A HORT1 retrotransposon insertion in the PeMYB11promoter causes harlequin/black flowers in Phalaenopsis orchids[J]. Plant Physiol, 2019, 180(3): 1535-1548. doi: 10.1104/pp.19.00205 URL
[57]	Suzuki K, Suzuki T, Nakatsuka T, et al. RNA-seq-based evaluation of bicolor tepal pigmentation in Asiatic hybrid lilies(Lilium spp.)[J]. BMC Genomics, 2016, 17(1): 611. doi: 10.1186/s12864-016-2995-5 URL
[58]	Yamagishi M. MYB19LONG is involved in brushmark pattern development in Asiatic hybrid lily(Lilium spp.) flowers[J]. Sci Hortic, 2020, 272: 109570. doi: 10.1016/j.scienta.2020.109570 URL
[59]	Yamagishi M. Isolation and identification of MYB transcription factors(MYB19Long and MYB19Short)involved in raised spot anthocyanin pigmentation in lilies(Lilium spp.)[J]. J Plant Physiol, 2020, 250: 153164. doi: 10.1016/j.jplph.2020.153164 URL
[60]	Yamagishi M, Ihara H, Arakawa K, et al. The origin of the LhMYB12 gene, which regulates anthocyanin pigmentation of tepals, in Oriental and Asiatic hybrid lilies(Lilium spp.)[J]. Sci Hortic, 2014, 174: 119-125. doi: 10.1016/j.scienta.2014.05.017 URL
[61]	Yamagishi M. A novel R2R3-MYB transcription factor regulates light-mediated floral and vegetative anthocyanin pigmentation patterns in Lilium regale[J]. Mol Breeding, 2016, 36(1): 3. doi: 10.1007/s11032-015-0426-y URL
[62]	Luan Y, Tang Y, Wang X, et al. Tree peony R2R3-MYB transcription factor PsMYB30 promotes petal blotch formation by activating the transcription of the anthocyanin synthase gene[J]. Plant Cell Physiol, 2022, 63(8): 1101-1116. doi: 10.1093/pcp/pcac085 pmid: 35713501
[11]	Zhang YZ, Cheng YW, Ya HY, et al. Transcriptome sequencing of purple petal spot region in tree peony reveals differentially expressed anthocyanin structural genes[J]. Front Plant Sci, 2015, 6: 964. doi: 10.3389/fpls.2015.00964 pmid: 26583029
[12]	Yamagishi M, Toda S, Tasaki K. The novel allele of the LhMYB12 gene is involved in splatter-type spot formation on the flower tepals of Asiatic hybrid lilies(Lilium spp.)[J]. New Phytol, 2014, 201(3): 1009-1020. doi: 10.1111/nph.12572 pmid: 24180488
[13]	Qi FT, Liu YT, Luo YL, et al. Functional analysis of the ScAG and ScAGL11 MADS-box transcription factors for anthocyanin biosynthesis and bicolour pattern formation in Senecio cruentus ray florets[J]. Hortic Res, 2022, 9: uhac071. doi: 10.1093/hr/uhac071 URL
[63]	Shi Q, Yuan M, Wang S, et al. PrMYB5 activates anthocyanin biosynthetic PrDFR to promote the distinct pigmentation pattern in the petal of Paeonia rockii[J]. Front Plant Sci, 2022, 13: 955590. doi: 10.3389/fpls.2022.955590 URL
[64]	Li CX, Yu WJ, Xu JR, et al. Anthocyanin biosynthesis induced by MYB transcription factors in plants[J]. Int J Mol Sci, 2022, 23(19): 11701. doi: 10.3390/ijms231911701 URL
[65]	Albert NW, Griffiths AG, Cousins GR, et al. Anthocyanin leaf markings are regulated by a family of R2R3-MYB genes in the genus Trifolium[J]. New Phytol, 2015, 205(2): 882-893. doi: 10.1111/nph.13100 pmid: 25329638
[66]	Yamagishi M, Shimoyamada Y, Nakatsuka T, et al. Two R2R3-MYB genes, homologs of petunia AN2, regulate anthocyanin biosyntheses in flower tepals, tepal spots and leaves of Asiatic hybrid lily[J]. Plant Cell Physiol, 2010, 51(3): 463-474. doi: 10.1093/pcp/pcq011 pmid: 20118109
[67]	Yamagishi M. 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”[J]. Mol Breeding, 2018, 38(5): 60. doi: 10.1007/s11032-018-0806-1
[68]	Gu Z, Zhu J, Hao Q, et al. A novel R2R3-MYB transcription factor contributes to petal blotch formation by regulating organ-specific expression of PsCHS in tree peony(Paeonia suffruticosa)[J]. Plant Cell Physiol, 2019, 60(3): 599-611. doi: 10.1093/pcp/pcy232 URL
[69]	Albert NW, Lewis DH, Zhang H, et al. Members of an R2R3-MYB transcription factor family in Petunia are developmentally and environmentally regulated to control complex floral and vegetative pigmentation patterning[J]. Plant J, 2011, 65(5): 771-784. doi: 10.1111/tpj.2011.65.issue-5 URL
[70]	Hsu CC, Chen YY, Tsai WC, et al. Three R2R3-MYB transcription factors regulate distinct floral pigmentation patterning in Phalaenopsis spp[J]. Plant Physiol, 2015, 168(1): 175. doi: 10.1104/pp.114.254599 URL
[71]	Martins TR, Jiang P, Rausher MD. How petals change their spots: cis-regulatory re-wiring in Clarkia(Onagraceae)[J]. New Phytol, 2017, 216(2): 510-518. doi: 10.1111/nph.2017.216.issue-2 URL
[72]	Lin RC, Rausher MD. R2R3-MYB genes control petal pigmentation patterning in Clarkia gracilis ssp. sonomensis(Onagraceae)[J]. New Phytol, 2021, 229(2): 1147-1162. doi: 10.1111/nph.v229.2 URL
[73]	Lin RC, Rausher MD. Ancient gene duplications, rather than polyploidization, facilitate diversification of petal pigmentation patterns in Clarkia gracilis(Onagraceae)[J]. Mol Biol Evol, 2021, 38(12): 5528-5538. doi: 10.1093/molbev/msab242 URL
[74]	Ding B, Patterson EL, Holalu SV, et al. Two MYB proteins in a self-organizing activator-inhibitor system produce spotted pigmentation patterns[J]. Curr Biol, 2020, 30(5): 802-814. doi: S0960-9822(19)31700-2 pmid: 32155414
[75]	Zheng X, Om K, Stanton KA, et al. The regulatory network for petal anthocyanin pigmentation is shaped by the MYB5a/NEGAN transcription factor in Mimulus[J]. Genetics, 2021, 217(2): iyaa036. doi: 10.1093/genetics/iyaa036 URL
[76]	Zahn LM, Feng BM, Ma H. Beyond the ABC-model: regulation of floral homeotic genes[M]//Developmental Genetics of the Flower. Amsterdam: Elsevier, 2006, 44: 163-207.
[77]	Saedler H, Becker A, Winter KU, et al. MADS-box genes are involved in floral development and evolution[J]. Acta Biochim Pol, 2001, 48(2): 351-358. pmid: 11732606
[78]	Li BJ, Zheng BQ, Wang YJ, et al. New insight into the molecular mechanism of colour differentiation among floral segments in orchids[J]. Commun Biol, 2020, 3(1): 89. doi: 10.1038/s42003-020-0821-8
[79]	Otani M, Aoyagi K, Nakano M. Suppression of B function by chimeric repressor gene-silencing technology(CRES-T)reduces the petaloid tepal identity in transgenic Lilium sp.[J]. PLoS One, 2020, 15(8): e0237176. doi: 10.1371/journal.pone.0237176 URL
[80]	Noor SH, Ushijima K, Murata A, et al. Double flower formation induced by silencing of C-class MADS-box genes and its variation among petunia cultivars[J]. Sci Hortic, 2014, 178: 1-7. doi: 10.1016/j.scienta.2014.07.029 URL
[81]	Hsu HF, Chen WH, Shen YH, et al. Multifunctional evolution of B and AGL6 MADS box genes in orchids[J]. Nat Commun, 2021, 12(1): 902. doi: 10.1038/s41467-021-21229-w
[82]	Su S, Xiao W, Guo W, et al. The CYCLOIDEA-RADIALIS module regulates petal shape and pigmentation, leading to bilateral corolla symmetry in Torenia fournieri(Linderniaceae)[J]. New Phytol, 2017, 215(4): 1582-1593. doi: 10.1111/nph.2017.215.issue-4 URL
[83]	Zheng X, Lan J, Yu H, et al. Arabidopsis transcription factor TCP4 represses chlorophyll biosynthesis to prevent petal greening[J]. Plant Commun, 2022, 3(4): 100309. doi: 10.1016/j.xplc.2022.100309 URL
[84]	Romanowski A, Yanovsky MJ. Circadian rhythms and post-transcriptional regulation in higher plants[J]. Front Plant Sci, 2015, 6: 437. doi: 10.3389/fpls.2015.00437 pmid: 26124767
[85]	Chang YF, Imam JS, Wilkinson MF. The nonsense-mediated decay RNA surveillance pathway[J]. Ann Rev Biochem, 2007, 76: 51-74. doi: 10.1146/biochem.2007.76.issue-1 URL
[86]	Yin P, Zhen Y, Li SX. Identification and functional classification of differentially expressed proteins and insight into regulatory mechanism about flower color variegation in peach[J]. Acta Physiol Plant, 2019, 41(6): 95. doi: 10.1007/s11738-019-2886-x
[87]	St Laurent G, Wahlestedt C, Kapranov P. The landscape of long noncoding RNA classification[J]. Trends Genet, 2015, 31(5): 239-251. doi: 10.1016/j.tig.2015.03.007 pmid: 25869999
[88]	Ohta Y, Atsumi G, Yoshida C, et al. Posttranscriptional gene silencing of the chalcone synthase gene CHS causes corolla lobe-specific whiting of Japanese gentian[J]. Planta, 2022, 225(1): 29.
[89]	Ohno S, Makishima R, Doi M. Post-transcriptional gene silencing of CYP76AD controls betalain biosynthesis in bracts of bougainvillea[J]. J Exp Bot, 2021, 72(20): 6949- 6962. doi: 10.1093/jxb/erab340 pmid: 34279632
[90]	Sunkar R, Zhu JK. Micro RNAs and short-interfering RNAs in plants[J]. J Intergr Plant Biol, 2007, 49(6): 817-826.
[91]	Bradley D, Xu P, Mohorianu II, et al. Evolution of flower color pattern through selection on regulatory small RNAs[J]. Science, 2017, 358(6365): 925-928. doi: 10.1126/science.aao3526 pmid: 29146812
[92]	Liang M, Chen W, LaFountain AM, et al. Taxon-specific, phased siRNAs underlie a speciation locus in monkeyflowers[J]. Science, 2023, 379(6632): 576-582. doi: 10.1126/science.adf1323 pmid: 36758083
[93]	Yang K, Han H, Li Y, et al. Significance of miRNA in enhancement of flavonoid biosynthesis[J]. Plant Biol, 2022, 24(2): 217-226. doi: 10.1111/plb.v24.2 URL
[94]	Gou JY, Felippes FF, Liu CJ, et al. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor[J]. Plant Cell, 2011, 23(4): 1512-1522. doi: 10.1105/tpc.111.084525 URL
[95]	Zhao DQ, Xia X, Wei MR, et al. Overexpression of herbaceous peony miR156e-3p improves anthocyanin accumulation in transgenic Arabidopsis thaliana lateral branches[J]. 3 Biotech, 2017, 7(6): 379. doi: 10.1007/s13205-017-1011-3 URL
[96]	Zhao A, Cui Z, Li T, et al. mRNA and miRNA expression analysis reveal the regulation for flower spot patterning in Phalaenopsis ‘Panda’[J]. Int J Mol Sci, 2019, 20(17): E4250.
[97]	Yamagishi M. microRNA828/MYB12 module mediated bicolor flower development in Lilium dauricum[J]. Hortic J, 2022, 91(3): 399-407. doi: 10.2503/hortj.UTD-373 URL
[98]	Zhang XP, Jia JS, Zhao MY, et al. Identification and characterization of microRNAs involved in double-color formation in Paeonia suffruticosa ‘Shima Nishiki’ by high-throughput sequencing[J]. Hortic Environ Biotechnol, 2022, 63(1): 125-135. doi: 10.1007/s13580-021-00379-2
[99]	Peng JM, Schwartz D, Elias JE, et al. A proteomics approach to understanding protein ubiquitination[J]. Nat Biotechnol, 2003, 21(8): 921-926. doi: 10.1038/nbt849 pmid: 12872131
[100]	Gu Z, Men S, Zhu J, et al. Chalcone synthase is ubiquitinated and degraded via interactions with a RING-H2 protein in petals of Paeonia hybrid ‘He Xie’[J]. J Exp Bot, 2019, 70(18): 4749-4762. doi: 10.1093/jxb/erz245 URL
[101]	Jo YD, Ryu J, Kim YS, et al. Dramatic increase in content of diverse flavonoids accompanied with down-regulation of F-box genes in a Chrysanthemum(Chrysanthemum × morifolium(Ramat.) hemsl.)mutant cultivar producing dark-purple ray florets[J]. Genes, 2020, 11(8): E865.
[102]	夏晗, 刘美芹, 尹伟伦. 植物 DNA 甲基化调控因子研究进展[J]. 遗传, 2008, 30(4): 426-432.
	Xia H, Liu MQ, Yin WL, et al. DNA methylation regulating factors in plants[J]. Hereditas, 2008, 30(4): 426-432.
[103]	Liu XJ, Chuang YN, Chiou CY, et al. Methylation effect on chalcone synthase gene expression determines anthocyanin pigmentation in floral tissues of two Oncidium orchid cultivars[J]. Planta, 2012, 236(2): 401-409. doi: 10.1007/s00425-012-1616-z URL
[104]	Wang Y, Zhao M, Xu Z, et al. MSAP analysis of epigenetic changes reveals the mechanism of bicolor petal formation in Paeonia suffruticosa ‘Shima Nishiki’[J]. 3 Biotech, 2019, 9(8): 313. doi: 10.1007/s13205-019-1844-z pmid: 31406635
[105]	Wu XX, Zhou Y, Yao D, et al. DNA methylation of LDOX gene contributes to the floral colour variegation in peach[J]. J Plant Physiol, 2020, 246/247: 153116. doi: 10.1016/j.jplph.2020.153116 URL
[106]	Zhu J, Wang YZ, Wang QY, et al. The combination of DNA methylation and positive regulation of anthocyanin biosynthesis by MYB and bHLH transcription factors contributes to the petal blotch formation in Xibei tree peony[J]. Hortic Res, 2023, 10(6): uhad100. doi: 10.1093/hr/uhad100 URL
[107]	Ringham L, Owens A, Cieslak M, et al. Modeling flower pigmentation patterns[J]. ACM Trans Graph, 2022, 40(6): 233.