Formation Mechanism of Blue Flowers in Ornamental Plants

doi:10.3969/j.issn.1009-7791.2021.02.013

Subtropical Plant Science ›› 2021, Vol. 50 ›› Issue (02): 155-162.DOI: 10.3969/j.issn.1009-7791.2021.02.013

Formation Mechanism of Blue Flowers in Ornamental Plants

LI Han-chun^1*, ZHANG Da-sheng^1*, LIU Qing-qing¹, LIU Feng-luan¹, LIU Zhuo-xing^1,2, XIONG Lei^1,2, AN Xiang-jie¹, TIAN Dai-ke^1**

(1.Shanghai Key Laboratory for Plant Functional Genomics and Resources / Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences / Shanghai Chenshan Botanical Garden, Shanghai 201602, China; 2.College of Life Science, Shanghai Normal University, Shanghai 200234, China)

Received:2020-10-22 Revised:2021-01-07 Online:2021-04-30 Published:2021-04-30
Contact: TIAN Dai-ke

观赏植物蓝色花形成的机制

李瀚纯^1*，张大生^1*，刘青青¹，刘凤栾¹，刘卓星^1,,2，熊磊^1,2，安向婕¹，田代科^1**

(1.上海市资源植物功能基因组学重点实验室 / 中国科学院上海辰山植物科学研究中心 / 上海辰山植物园，上海 201602；2.上海师范大学生命科学学院，上海 200234)

通讯作者: 田代科
基金资助:
国家自然科学基金面上项目(31572158、32072620)；上海市绿化和市容管理局科技攻关项目(G152422、G192415、G202405)；上海市资源植物功能基因组学重点实验室开放课题(PFGR201801)

Abstract

Abstract: Blue color is not common in flowers of ornamental plants and it is also a breeding goal for flower breeders. In this paper, the influencing factors related to biosynthesis of anthocyanins, types of anthocyanins, transfer and accumulation of anthocyanins in vacuoles, covalent modification of anthocyanins, inter molecular copigmentation, metal ions and vacuolar pH were discussed.

Key words: blue-petaled flower, anthocyanin biosynthesis, copigmentation, vacuolar pH, genetic engineering

摘要： 在观赏植物中，蓝色系的花卉属于较为罕见的种类，也是花卉育种一直以来的目标。本文对蓝色花卉的花青素代谢途径，影响蓝色花卉形成的核心色素种类，花青素转运方式，花青素在液泡中的积累，花青素的共价修饰，分子间辅色作用，金属离子和液泡pH等影响因素进行系统地介绍和讨论，以期为培育新的蓝色花卉提供参考。

关键词: 蓝色花, 花青素代谢, 辅助显色, 液泡pH, 基因工程

CLC Number:

S688

LI Han-chun, ZHANG Da-sheng, LIU Qing-qing, LIU Feng-luan, LIU Zhuo-xing, XIONG Lei, AN Xiang-jie, TIAN Dai-ke. Formation Mechanism of Blue Flowers in Ornamental Plants[J]. Subtropical Plant Science, 2021, 50(02): 155-162.

李瀚纯，张大生，刘青青，刘凤栾，刘卓星，熊磊，安向婕，田代科. 观赏植物蓝色花形成的机制[J]. 亚热带植物科学, 2021, 50(02): 155-162.

References

[1] Zhao J, Dixon R A. The ‘ins’ and ‘outs’ of flavonoid transport[J]. Trends in Plant Science, 2010,15(2): 72–80. [2] Qi Y Y, Lou Q, Li H B, Yue J, Liu Y L, Wang Y J. Anatomical and biochemical studies of bicolored flower development in Muscari latifolium[J]. Protoplasma, 2013,250: 1273–1281. [3] Nishihara M, Nakatsuka T. Genetic engineering of flavonoid pigments to modify flower color in floricultural plants[J]. Biotechnology Letters, 2010,33: 433–441. [4] Tanaka Y, Brugliera F, Kalc G, Senior M, Dyson B, Nakamura N, Katsumoto Y, Chandler S. Flower color modification by engineering of the flavonoid biosynthetic pathway: Practical perspectives[J]. Bioscience, Biotechnology, and Biochemistry, 2010,74(9): 1760–1769. [5] Katsumoto Y, Fukuchi- Mizutani M, Fukui Y, Brugliera F, Holton T A, Karan M, Nakamura N, Yonekura-Sakakibara K, Togami J, Pigeaire A, Tao G Q, Nehra N S, Lu C Y, Dyson B K, Tsuda S, Ashikari T, Kusumi T, Mason J G, Tanaka Y. Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin[J]. Plant and Cell Physiology, 2007,48(11): 1589–1600. [6] Nakamura N, Katsumoto Y, Brugliera F, Demelis L, Nakajima D, Suzuki H, Tanaka Y. Flower color modification in Rosa hybrida by expressing the S-adenosylmethionine: Anthocyanin 3′,5′- O-methyltransferase gene from Torenia hybrida[J]. Plant Biotechnology, 2015,32: 109–117. [7] Noda N, Aida R, Kishimoto S, Ishiguro K, Fukuchi-Mizutani M, Tanaka Y, Ohmiya A. Genetic engineering of novel bluer-colored chrysanthemums produced by accumulation of delphinidin-based anthocyanins[J]. Plant and Cell Physiology, 2013,54(10): 1684–1695. [8] Noda N, Yoshioka S, Kishimoto S, Nakayama M, Douzono M, Tanaka Y, Aida R. Generation of blue chrysanthemums by anthocyanin B-ring hydroxylation and glucosylation and its coloration mechanism[J]. Science Advances, 2017,3: e1602785. [9] Shoji K, Momonoi K, Tsuji T. Alternative expression of vacuolar iron transporter and ferritin genes leads to blue/purple coloration of flowers in tulip cv. ‘Murasakizuisho’[J]. Plant and Cell Physiology, 2010,51(2): 215–224. [10] Verweij W, Spelt C, Di Sansebastiano G P, Vermeer J, Reale L, Ferranti F, Koes R, Quattrocchio F. An H+P-ATPase on the tonoplast determines vacuolar pH and flower colour[J]. Nature Cell Biology, 2008,10(12): 1456–1462. [11] Liang C Y, Rengasamy K P, Huang L M, Hsu C C, Jeng M F, Chen W H, Chen H H. Assessment of violet-blue color formation in Phalaenopsis orchids[J]. BMC Plant Biology, 2020,20(1): 212. [12] Fukui Y, Tanaka Y, Kusumi T, Iwashita T, Nomoto K. A rationale for the shift in colour towards blue in transgenic carnation flowers expressing the flavonoid 3′,5′-hydroxylase gene[J]. Phytochemistry, 2003,63(1): 15–23. [13] Shiono M, Matsugaki N, Takeda K. Structure of the blue cornflower pigment[J]. Nature, 2005,436(11): 791. [14] Okitsu N, Matsui K, Horikawa M, Sugahara K, Tanaka Y. Identification and characterization of novel Nemophila menziesii flavone glucosyltransferases that catalyze biosynthesis of flavone 7,4'-o-diglucoside, a key component of blue metalloanthocyanins[J]. Plant and Cell Physiology, 2018,59(10): 2075–2085. [15] Gómez C, Conéjéro G, Torregrosa L, Cheynier V, Terrier N, Ageorges A. In vivo grapevine anthocyanin transport involves vesicle-mediated trafficking and the contribution of ANTHOMATE transporters and GST[J]. The Plant Journal, 2011,67(6): 960–970. [16] Goodman C D, Casati P, Walbot V. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays[J]. The Plant Cell, 2004,16(7): 1812–1826. [17] Marrs K, Alfenito M, Lloyd A, Walbot V. A glutathione-S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2[J]. Nature, 1995,375: 397–400. [18] Mueller L, Goodman C, Silady R, Walbot V. AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein[J]. Plant Physiology, 2000,123: 1561–1570. [19] Yazaki K. ABC transporters involved in the transport of plant secondary metabolites[J]. FEBS Letters, 2006,580: 1183–1191. [20] Markham K, Gould K, Winefield C, Mitchell K, Bloor S, Boase M. Anthocyanic vacuolar inclusions—their nature and significance in flower colouration[J]. Phytochemistry, 2000,55: 327–336. [21] Grotewold E. The genetics and biochemistry of floral pigments[J]. Annual Review of Plant Biology, 2006,57: 761–780. [22] Figueiredo P, George F, Tatsuzawa F, Toki K, Saito N, Brouillard R. New features of intramolecular copigmentation by acylated anthocyanins[J]. Phytochemistry, 1999,51(1): 125–132. [23] Goto T, Kondo T. Structure and molecular stacking of anthocyanins—flower color variation[J]. Angewandte Chemie International Edition in English, 1991,30: 17–33. [24] Yoshida K, Mori M, Kondo T. Blue flower color development by anthocyanins: From chemical structure to cell physiology[J]. Natural Product Reports, 2009,26(7): 884–915. [25] Shoji K, Miki N, Nakajima N, Momonoi K, Kato C, Yoshida K. Perianth bottom-specific blue color development in tulip cv. Murasakizuisho requires ferric ions[J]. Plant and Cell Physioloy, 2007,48(2): 243–251. [26] Ishikawa T, Li Z S, Lu Y P, Rea P. The GS-X pump in plant, yeast, and animal cells: Structure, function, and gene expression[J]. Bioscience Reports, 1997,17(2): 189–207. [27] Honda T, Saito N. Recent progress in the chemistry of polyacylated anthocyanins as flower color pigments[J]. Heterocycles, 2002,56(1–2): 633–692. [28] Spelt C, Quattrocchio F, Mol J, Koes R. ANTHOCYANIN1 of petunia controls pigment synthesis, vacuolar pH, and seed coat development by genetically distinct mechanisms[J]. The Plant Cell, 2002,14(9): 2121–2135. [29] Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis of plant pigments: Anthocyanins, betalains and carotenoids[J]. The Plant Journal, 2008,54(4): 733–749. [30] Ishii I, Sakaguchi K, Fujita K, Ozeki Y, Miyahara T. A double knockout mutant of acyl-glucose-dependent anthocyanin glucosyltransferase genes in Delphinium grandiflorum[J]. Journal of Plant Physiology, 2017,216: 74–78. [31] Mori M, Miki N, Ito D, Kondo T, Yoshida K. Structure of tecophilin, a tri-caffeoylanthocyanin from the blue petals of Tecophilaea cyanocrocus, and the mechanism of blue color development[J]. Tetrahedron, 2014,70(45): 8657–8664. [32] Tasaki K, Higuchi A, Watanabe A, Sasaki N, Nishihara M. Effects of knocking out three anthocyanin modification genes on the blue pigmentation of gentian flowers[J]. Scientific Reports, 2019,9(1): 15831. [33] Forkmann G. Flavonoids as flower pigments: The formation of the natural spectrum and its extension by genetic engineering[J]. Plant Breeding, 2006,106: 1–26. [34] 孙建霞,张燕,胡小,吴继,廖小军. 花色苷的结构稳定性与降解机制研究进展[J]. 中国农业科学, 2009,42(3): 996–1008. [35] Asen S, Stewart R N, Norris K H. Co-pigmentation of anthocyanins in plant tissues and its effect on color[J]. Phytochemistry, 1972,11(2): 1139–1144. [36] Hondo T, Yoshida K, Nakagawa A, Kawai T, Tamura H, Goto T. Structural basis of blue-colour development in flower petals from Commelina communis[J]. Nature, 1992,358: 515–518. [37] Takeda K, Yanagisawa M, Kifune T, Kinoshita T, Timberlake C. A blue pigment complex in flowers of Salvia patens[J]. Phytochemistry, 1994,35: 1167–1169. [38] Kondo T, Ueda M, Isobe M, Goto T. A new molecular mechanism of blue color development with protocyanin, a supramolecular pigment from cornflower, Centaurea cyanus[J]. Tetrahedron Letters, 1998,39: 8307–8310. [39] Kondo T, Ueda M, Tamura H, Yoshida K, Isobe M, Goto T. Composition of protocyanin, a self-assembled supramolecular pigment from the blue cornflower, Centaurea cyanus[J]. Angewandte Chemie International Edition, 1994,33: 978–979. [40] Momonoi K, Yoshida K, Mano S, Takahashi H, Nakamori C, Shoji K, Nitta A, Nishimura M. A vacuolar iron transporter in tulip, Tgvit1, is responsible for blue coloration in petal cells through iron accumulation[J]. The Plant Journal, 2009,59(3): 437–447. [41] Ma J F, Ryan P R, Delhaize E. Aluminium tolerance in plants and the complexing role of organic acids[J]. Trends in Plant Science, 2001,6(6): 273–278. [42] Negishi T, Oshima K, Hattori M, Kanai M, Mano S, Nishimura M, Yoshida K. Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant[J]. PloS One, 2012,7(8): e43189. [43] Anaya-Covarrubias J Y, Larranaga N, Almaráz-Abarca N, Escoto-Delgadillo M, Rodríguez-Macías R, Torres-Morán M I. Hydrangea DNA methylation caused by pH substrate changes to modify sepal colour is detected by MSAP and ISSR markers[J]. Agronomy, 2019,9(12). [44] 龚仲幸,何勇,杨静,宋亚,叶真逍,朱祝军. 外源硫酸铝调节八仙花花青苷组成和含量变化的分子生物学机制[J]. 植物营养与肥料学报, 2017,23(3): 821–826. [45] Marty F. Plant vacuoles[J]. The Plant Cell, 1999,11: 587–599. [46] Torskangerpoll K, Andersen ? M. Colour stability of anthocyanins in aqueous solutions at various pH values[J]. Food Chemistry, 2005,89(3): 427–440. [47] Yoshida K, Kondo T, Okazaki Y, Katou K. Cause of blue petal colour[J]. Nature, 1995,373: 291. [48] Faraco M, Spelt C, Bliek M, Verweij W, Hoshino A, Espen L, Prinsi B, Jaarsma R, Tarhan E, de Boer Albertus H, Di Sansebastiano G P, Koes R, Quattrocchio Francesca M. Hyperacidification of vacuoles by the combined action of two different P-ATPases in the tonoplast determines flower color[J]. Cell Reports, 2014,6(1): 32–43. [49] Toshio Y, Fukada Tanaka S, Yoshishige I, Norio S, Yonekura Sakakibara K, Yoshikazu T, Takaaki K, Shigeru I. Genes encoding the vacuolar Na+/H+ exchanger and flower coloration[J]. Plant and Cell Physiology, 2001,(5): 5. [50] Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kondo T. The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal color during flower opening of morning glory, Ipomoea tricolor cv. Heavenly blue[J]. Plant and Cell Physiology, 2005,46(3): 407–415. [51] Li Y B, Provenzano S, Bliek M, Spelt C, Appelhagen I, Laura M D F, Verweij W, Schubert A, Sagasser M, Seidel T. Evolution of tonoplast P-ATPase transporters involved in vacuolar acidification[J]. New Phytologist, 2016,211(3): 1092–1107. [52] Sundaramoorthy J, Park G T, Lee J D, Kim J H, Seo H S, Song J T. A P3A-type ATPase and an R2R3-MYB transcription factor are involved in vacuolar acidification and flower coloration in soybean[J]. Frontiers in Plant Science, 2020,11: 580085. [53] Houwelingen A, Souer E, Mol J, Koes R. Epigenetic interactions among three dTph1 transposons in two homologous chromosomes activate a new excision-repair mechanism in petunia[J]. The Plant Cell, 1999,11: 1319–1336. [54] Vlaming P, Schram A, Wiering H. Genes affecting flower colour and pH of flower limb homogenates in Petunia hybrida[J]. Theoretical and Applied Genetics, 1983,66: 271–278. [55] Faraco M, Li Y, Li S, Spelt C, Di Sansebastiano G P, Reale L, Ferranti F, Verweij W, Koes R, Quattrocchio F M. A tonoplast P3B-ATPase mediates fusion of two types of vacuoles in petal cells[J]. Cell Reports, 2017,19(12): 2413–2422. [56] 翟宇慧,吕嘉琪,李想,罗小宁,李龙,史倩倩. 欧洲报春细胞液pH对花色形成的作用机理初探[J]. 园艺学报, 2020,47(3): 477–491.

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Formation Mechanism of Blue Flowers in Ornamental Plants

观赏植物蓝色花形成的机制

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