Review

HY5, an integrator of light and temperature signals in the regulation of anthocyanins biosynthesis in Arabidopsis

  • Received: 15 February 2020 Accepted: 24 April 2020 Published: 27 April 2020
  • Anthocyanins are well-known plant specialized metabolites and this group can be classified into the phenolic compound class based on their chemical structure characterizing by a C6-C3-C6 carbon framework. Anthocyanins have been identified to play various functions in plants, for example, pigmentation of floral organs, UV protection, and defense system. In addition to their functions in plant growth and development, anthocyanins are also considered as a good natural antioxidant which can be used for human. Because of important functions, the biosynthesis of anthocyanins is precisely regulated by a number of endogenous and exogenous factors. In the plant, light and temperature are critical environmental factors contributing to various developmental processes. From the first identification, ELONGATED HYPOCOTYL 5 (HY5) has been documented to play as an important transcription factor that is involved in a number of signal transduction ways including light and temperature pathways. The purpose of this review is to provide a precise overview of current research progress on the regulation of anthocyanins biosynthesis under the control of HY5 transcription factor.

    Citation: Nguyen Hoai Nguyen. HY5, an integrator of light and temperature signals in the regulation of anthocyanins biosynthesis in Arabidopsis[J]. AIMS Molecular Science, 2020, 7(2): 70-81. doi: 10.3934/molsci.2020005

    Related Papers:

  • Anthocyanins are well-known plant specialized metabolites and this group can be classified into the phenolic compound class based on their chemical structure characterizing by a C6-C3-C6 carbon framework. Anthocyanins have been identified to play various functions in plants, for example, pigmentation of floral organs, UV protection, and defense system. In addition to their functions in plant growth and development, anthocyanins are also considered as a good natural antioxidant which can be used for human. Because of important functions, the biosynthesis of anthocyanins is precisely regulated by a number of endogenous and exogenous factors. In the plant, light and temperature are critical environmental factors contributing to various developmental processes. From the first identification, ELONGATED HYPOCOTYL 5 (HY5) has been documented to play as an important transcription factor that is involved in a number of signal transduction ways including light and temperature pathways. The purpose of this review is to provide a precise overview of current research progress on the regulation of anthocyanins biosynthesis under the control of HY5 transcription factor.


    加载中

    Acknowledgments



    This work was supported by a grant from Ho Chi Minh City Open University (to Nguyen Hoai Nguyen, 2020).

    Conflict of interest



    The author declares there is no conflict of interest.

    [1] Crozier A, Jaganath IB, Clifford MN (2006) Phenols, polyphenols and tannins: an overview. Plant Secondary Metabolites: Occurrence, Structure and Role in the Human Diet Oxford, UK: Blackwell Publishing Ltd, 1-24.
    [2] Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55: 481-504. doi: 10.1016/S0031-9422(00)00235-1
    [3] Wang LS, Stoner GD (2008) Anthocyanins and their role in cancer prevention. Cancer Lett 269: 281-290. doi: 10.1016/j.canlet.2008.05.020
    [4] Romagnolo DF, Selmin OI (2012) Flavonoids and cancer prevention: a review of the evidence. J Nutr Gerontol Geriatr 31: 206-238. doi: 10.1080/21551197.2012.702534
    [5] Chen AY, Chen YC (2013) A review of the dietary flavonoid, kaempferol on human health and cancer chemoprevention. Food Chem 138: 2099-2107. doi: 10.1016/j.foodchem.2012.11.139
    [6] Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12: 556-563. doi: 10.1016/j.tplants.2007.10.003
    [7] Cotelle N (2001) Role of flavonoids in oxidative stress. Curr Top Med Chem 1: 569-590. doi: 10.2174/1568026013394750
    [8] Howard LR, Pandjaitan N, Morelock T, et al. (2002) Antioxidant capacity and phenolic content of spinach as affected by genetics and growing season. J Agric Food Chem 50: 5891-5896. doi: 10.1021/jf020507o
    [9] Oh JE, Kim YH, Kim JH, et al. (2011) Enhanced level of anthocyanin leads to increased salt tolerance in Arabidopsis PAP1-D plants upon sucrose treatment. J Korean Soc Appl Bi 54: 79-88.
    [10] Di Ferdinando M, Brunetti C, Fini A, et al. (2012) Flavonoids as antioxidants in plants under abiotic stresses. Abiotic stress responses in plants: metabolism productivity and sustainability New York: Springer, 159-179. doi: 10.1007/978-1-4614-0634-1_9
    [11] Nakabayashi R, Yonekura-Sakakibara K, Urano K, et al. (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77: 367-379. doi: 10.1111/tpj.12388
    [12] Nguyen NH, Kim JH, Kwon J, et al. (2016) Characterization of Arabidopsis thaliana FLAVONOL SYNTHASE 1 (FLS1)-overexpression plants in response to abiotic stress. Plant Physiol Biochem 103: 133-142. doi: 10.1016/j.plaphy.2016.03.010
    [13] Kuhn BM, Geisler M, Bigler L, et al. (2011) Flavonols accumulate asymmetrically and affect auxin transport in Arabidopsis. Plant Physiol 156: 585-595. doi: 10.1104/pp.111.175976
    [14] Petrussa E, Braidot E, Zancani M, et al. (2013) Plant flavonoids-biosynthesis, transport and involvement in stress responses. Int J Mol S 14: 14950-14973. doi: 10.3390/ijms140714950
    [15] Saslowsky DE, Ware U, Winkel BSJ (2005) Nuclear localization of flavonoid enzymes in Arabidopsis. J Bio Chem 280: 23735-23740. doi: 10.1074/jbc.M413506200
    [16] Tian L, Wan SB, Pan QH, et al. (2008) A novel plastid localization of chalcone synthase in developing grape berry. Plant Sci 175: 431-436. doi: 10.1016/j.plantsci.2008.03.012
    [17] Wang HL, Wang W, Zhang P, et al. (2010) Gene transcript accumulation, tissue and subcellular localization of anthocyanidin synthase (ANS) in developing grape berries. Plant Sci 179: 103-113. doi: 10.1016/j.plantsci.2010.04.002
    [18] Toda K, Kuroiwa H, Senthil K, et al. (2012) The soybean F3′H protein is localized to the tonoplast in the seed coat hilum. Planta 236: 79-89. doi: 10.1007/s00425-012-1590-5
    [19] Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5: 218-223. doi: 10.1016/S1369-5266(02)00256-X
    [20] Fini A, Brunetti C, Di Ferdinando M, et al. (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6: 709-711. doi: 10.4161/psb.6.5.15069
    [21] Nguyen NH, Jeong CY, Kang GH, et al. (2015) MYBD employed by HY5 increases anthocyanin accumulation via repression of MYBL2 in Arabidopsis. Plant J 84: 1192-1205. doi: 10.1111/tpj.13077
    [22] Wang Y, Wang Y, Song Z, et al. (2016) Repression of MYBL2 by both microRNA858a and HY5 leads to the activation of anthocyanin biosynthetic pathway in Arabidopsis. Mol Plant 9: 1395-1405. doi: 10.1016/j.molp.2016.07.003
    [23] Kim S, Hwang G, Lee S, et al. (2017) High ambient temperature represses anthocyanin biosynthesis through degradation of HY5. Front Plant Sci 8: 1787. doi: 10.3389/fpls.2017.01787
    [24] Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3: 2-20. doi: 10.1093/mp/ssp106
    [25] Holton TA, Cornish EC (1995) Genetics and Biochemistry of Anthocyanin Biosynthesis. Plant Cell 7: 1071-1083. doi: 10.2307/3870058
    [26] Tanaka Y, Sasaki N, Ohmiya A (2008) Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54: 733-749. doi: 10.1111/j.1365-313X.2008.03447.x
    [27] Rosinski JA, Atchley WR (1998) Molecular evolution of the Myb family of transcription factors: Evidence for polyphyletic origin. J Mol Evol 46: 74-83. doi: 10.1007/PL00006285
    [28] Jin HL, Martin C (1999) Multi-functionality and diversity within the plant MYB-gene family. Plant Mol Biol 41: 577-585. doi: 10.1023/A:1006319732410
    [29] Dubos C, Stracke R, Grotewold E, et al. (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573-581. doi: 10.1016/j.tplants.2010.06.005
    [30] Ogata K, Morikawa S, Nakamura H, et al. (1994) Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 79: 639-648. doi: 10.1016/0092-8674(94)90549-5
    [31] Dias AP, Braun EL, McMullen MD, et al. (2003) Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol 131: 610-620. doi: 10.1104/pp.012047
    [32] Matus JT, Aquea F, Arce-Johnson P (2008) Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol 8: 83. doi: 10.1186/1471-2229-8-83
    [33] Nguyen NH, Cheong JJ (2018) AtMYB44 interacts with TOPLESS-RELATED corepressors to suppress Protein Phosphatase 2C gene transcription. Biochem Biophys Res Commun 499: 437-442. doi: 10.1016/j.bbrc.2018.11.057
    [34] Stracke R, Ishihara H, Barsch GHA, et al. (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50: 660-677. doi: 10.1111/j.1365-313X.2007.03078.x
    [35] Koornneef M (1990) Mutations affecting the testa color in Arabidopsis. Arabid Inf Serv 27: 1-4.
    [36] Meyerowitz EM, Bowman JL, Chang C, et al. (1990) RFLP map of Arabidopsis thalianaCold Spring Harbor New York: Cold Spring Harbor Laboratory Press, 98-99.
    [37] Shirley BW, Hanley S, Goodman HM (1992) Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. Plant Cell 4: 333-347.
    [38] Focks N, Sagasser M, Weisshaar B, et al. (1999) Characterization of tt15, a novel transparent testa mutant of Arabidopsis thaliana (L.) Heynh. Planta 208: 352-357. doi: 10.1007/s004250050569
    [39] Fuglevand G, Jackson JA, Jenkins GI (1996) UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell 8: 2347-2357.
    [40] Wade HK, Bibikova TN, Valentine WJ, et al. (2001) Interaction within a network of phytochrome, cryptochrome and UV-B phototransduction pathways regulate chalcone synthase gene expression in Arabidopsis leaf tissue. Plant J 25: 675-685. doi: 10.1046/j.1365-313x.2001.01001.x
    [41] Mehrtens F, Kranz H, Bednarek P, et al. (2005) The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138: 1083-1096. doi: 10.1104/pp.104.058032
    [42] Borevitz JO, Xia YJ, Blount J, et al. (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12: 2383-2393. doi: 10.1105/tpc.12.12.2383
    [43] Nguyen H, Kim JH, Hyun WY, et al. (2013) TTG1-mediated flavonols biosynthesis alleviates root growth inhibition in response to ABA. Plant Cell Rep 32: 503-514. doi: 10.1007/s00299-012-1382-1
    [44] Li C, Zhang B, Chen B, et al. (2018b) Site-specific phosphorylation of TRANSPARENT TESTA GLABRA1 mediates carbon partitioning in Arabidopsis seeds. Nat Commun 9: 571. doi: 10.1038/s41467-018-03013-5
    [45] Baudry A, Heim MA, Dubreucq B, et al. (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39: 366-380. doi: 10.1111/j.1365-313X.2004.02138.x
    [46] Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20: 176-185. doi: 10.1016/j.tplants.2014.12.001
    [47] Dubos C, Le Gourrierec J, Baudry A, et al. (2008) MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thalianaPlant J 55: 940-953. doi: 10.1111/j.1365-313X.2008.03564.x
    [48] Matsui K, Umemura Y, Ohme-Takagi M (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55: 954-967. doi: 10.1111/j.1365-313X.2008.03565.x
    [49] Gou JY, Felippes FF, Liu CJ, et al. (2011) Negative regulation of anthocyanin biosynthesis in arabidopsis by a miR156-Targeted SPL transcription factor. Plant Cell 23: 1512-1522. doi: 10.1105/tpc.111.084525
    [50] Shin J, Park E, Choi G (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 50: 933. doi: 10.1111/j.1365-313X.2007.03178.x
    [51] Vandenbussche F, Habricot Y, Condiff AS, et al. (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49: 428-441. doi: 10.1111/j.1365-313X.2006.02973.x
    [52] Shin DH, Choi M, Kim K, et al. (2013) HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett 587: 1543-1547. doi: 10.1016/j.febslet.2013.03.037
    [53] Pietta PG (2000) Flavonoids as antioxidants. J Nat Prod 63: 1035-1042. doi: 10.1021/np9904509
    [54] Potapovich AI, Kostyuk VA (2003) Comparative study of antioxidant properties and cytoprotective activity of flavonoids. Biochemistry (Mosc) 68: 514-519. doi: 10.1023/A:1023947424341
    [55] Maier A, Schrader A, Kokkelink L, et al. (2013) Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74: 638-651. doi: 10.1111/tpj.12153
    [56] Das PK, Geul B, Choi SB, et al. (2011) Photosynthesis-dependent anthocyanin pigmentation in Arabidopsis. Plant Signal Behav 6: 23-25. doi: 10.4161/psb.6.1.14082
    [57] Zoratti L, Karppinen K, Escobar AL, et al. (2014) Light-controlled flavonoid biosynthesis in fruits. Front Plant Sci 5: 534. doi: 10.3389/fpls.2014.00534
    [58] Saure MC (1990) External control of anthocyanin formation in apple. Sci Hortic 42: 181-218. doi: 10.1016/0304-4238(90)90082-P
    [59] Chen DQ, Li ZY, Pan RC, et al. (2006) Anthocyanin accumulation mediated by blue light and cytokinin in Arabidopsis seedlings. J Integr Plant Biol 48: 420-425. doi: 10.1111/j.1744-7909.2006.00234.x
    [60] Cao SF, Hu ZC, Zheng YH, et al. (2010) Effect of BTH on anthocyanin content and activities of related enzymes in strawberry after harvest. J Agric Food Chem 58: 5801-5805. doi: 10.1021/jf100742v
    [61] Kadomura-Ishikawa Y, Miyawaki K, Noji S, et al. (2013) Phototropin 2 is involved in blue light-induced anthocyanin accumulation in Fragaria x ananassa fruits. J Plant Res 126: 847-857. doi: 10.1007/s10265-013-0582-2
    [62] Xu F, Cao SF, Shi LY, et al. (2014) Blue light irradiation affects anthocyanin content and enzyme activities involved in postharvest strawberry fruit. J Agric Food Chem 62: 4778-4783. doi: 10.1021/jf501120u
    [63] Catala R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci USA 108: 16475-16480. doi: 10.1073/pnas.1107161108
    [64] Mori K, Sugaya S, Gemma H (2005) Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci Hortic-Amsterdam 105: 319-330. doi: 10.1016/j.scienta.2005.01.032
    [65] Yamane T, Jeong ST, Goto-Yamamoto N, et al. (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Viticult 57: 54-59.
    [66] Koornneef M, Rolff E, Spruit CJP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L) Heynh. Zeitschrift für Pflanzenphysiologie 100: 147-160. doi: 10.1016/S0044-328X(80)80208-X
    [67] Gangappa SN, Botto JF (2016) The multifaceted roles of HY5 in plant growth and development. Mol Plant 9: 1353-1365. doi: 10.1016/j.molp.2016.07.002
    [68] Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11: 2983-2995. doi: 10.1101/gad.11.22.2983
    [69] Ang LH, Chattopadhyay S, Wei N, et al. (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1: 213-222. doi: 10.1016/S1097-2765(00)80022-2
    [70] Laubinger S, Fittinghoff K, Hoecker U (2004) The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell 16: 2293-2306. doi: 10.1105/tpc.104.024216
    [71] Lau OS, Deng XW (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17: 584-593. doi: 10.1016/j.tplants.2012.05.004
    [72] Podolec R, Ulm R (2018) Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase. Curr Opin Plant Biol 45: 18-25. doi: 10.1016/j.pbi.2018.04.018
    [73] Chattopadhyay S, Ang LH, Puente P, et al. (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10: 673-683. doi: 10.1105/tpc.10.5.673
    [74] Osterlund MT, Hardtke CS, Wei N, et al. (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466. doi: 10.1038/35013076
    [75] Li B, Gao K, Ren H, et al. (2018) Molecular mechanisms governing plant responses to high temperatures. J Integr Plant Biol 60: 757-779. doi: 10.1111/jipb.12701
    [76] Park YJ, Lee HJ, Ha JH, et al. (2017) COP1 conveys warm temperature information to hypocotyl thermomorphogenesis. New Phytol 215: 269-280. doi: 10.1111/nph.14581
    [77] Stracke R, Favory JJ, Gruber H, et al. (2010) The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. Plant Cell Environ 33: 88-103.
    [78] Zhang H, He H, Wang X, et al. (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-translational regulation. Plant J 65: 346-358. doi: 10.1111/j.1365-313X.2010.04426.x
    [79] Burko Y, Seluzicki A, Zander M, et al. (2020) Chimeric activators and repressors define HY5 activity and reveal a light-regulated feedback mechanism. Plant Cell 32: 967-983. doi: 10.1105/tpc.19.00772
    [80] Ram H, Priya P, Jain M, et al. (2014) Genome-wide DNA binding of GBF1 is modulated by its heterodimerizing protein partners, HY5 and HYH. Mol Plant 7: 448-451. doi: 10.1093/mp/sst143
  • Reader Comments
  • © 2020 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(5666) PDF downloads(624) Cited by(3)

Article outline

Figures and Tables

Figures(2)

Other Articles By Authors

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog