A novel transcription factor CmMYB012 inhibits flavone and anthocyanin biosynthesis in response to high temperatures in chrysanthemum

Li-Jie Zhou , Zhiqiang Geng , Yuxi Wang , Yiguang Wang , Shenhui Liu , Chuwen Chen , Aiping Song , Jiafu Jiang , Sumei Chen , Fadi Chen

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 248

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :248 DOI: 10.1038/s41438-021-00675-z
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A novel transcription factor CmMYB012 inhibits flavone and anthocyanin biosynthesis in response to high temperatures in chrysanthemum
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Abstract

Flavones are among the major colorless pigments synthesized through branches of the flavonoid pathway in plants. However, due to the absence of a gene encoding flavone synthase (FNS) in the model plant Arabidopsis thaliana species, the regulatory mechanism of FNS-catalyzed flavone biosynthesis has rarely been studied in plants. Here, it was found that flavones play a predominant role in the elimination of excess reactive oxygen species (ROS) at high temperatures in colorless plant organs. A novel atypical subgroup 7 (SG7) R2R3-MYB transcription factor, CmMYB012, was found to be induced in response to prolonged high temperatures and to inhibit flavone biosynthesis by directly regulating CmFNS. Moreover, CmMYB012 was also found to inhibit anthocyanin biosynthesis by suppressing the expression of CmCHS, CmDFR, CmANS, and CmUFGT. CmMYB012 overexpression exerted a negative influence on plant fitness and pink flower color formation, while CmMYB012 suppression had the opposite effect in response to high temperatures. Our findings provide new insights into the mechanisms by which high temperatures regulate the metabolism of flavones and anthocyanins to affect plant fitness and flower color formation.

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Li-Jie Zhou, Zhiqiang Geng, Yuxi Wang, Yiguang Wang, Shenhui Liu, Chuwen Chen, Aiping Song, Jiafu Jiang, Sumei Chen, Fadi Chen. A novel transcription factor CmMYB012 inhibits flavone and anthocyanin biosynthesis in response to high temperatures in chrysanthemum. Horticulture Research, 2021, 8 (1) : 248 DOI:10.1038/s41438-021-00675-z

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References

[1]

Li, P. et al. The Arabidopsis UDP-glycosyltransferases UGT79B2 and UGT79B3, contribute to cold, salt and drought stress tolerance via modulating anthocyanin accumulation. Plant J. 89, 85-103 (2017).

[2]

Miller, R., Owens, S. J. & Rørslett, B. Plants and colour: flowers and pollination. Opt. Laser Technol. 43, 282-294 (2011).

[3]

Steyn, W. J., Wand, S., Holcroft, D. & Jacobs, G. Anthocyanins in vegetative tissues: a proposed unified function in photoprotection. N. Phytologist 155, 349-361 (2002).

[4]

Agati, G., Azzarello, E., Pollastri, S. & Tattini, M. Flavonoids as antioxidants in plants: location and functional significance. Plant Sci. 196, 67-76 (2012).

[5]

Jiang, N., Doseff, A. I. & Grotewold, E. Flavones: from biosynthesis to health benefits. Plants 5, 27 (2016).

[6]

Brunetti, C., Fini, A., Sebastiani, F., Gori, A. & Tattini, M. Modulation of phytohormone signaling: a primary function of flavonoids in plant-environment interactions. Front. Plant Sci. 9, 1042 (2018).

[7]

Winkel-Shirley, B. Biosynthesis of flavonoids and effects of stress. Curr. Opin. Plant Biol. 5, 218-223 (2002).

[8]

Martens, S. & Mithöfer, A. Flavones and flavone synthases. Phytochemistry 66, 2399-2407 (2005).

[9]

Ferreyra, M. L., Emiliani, J., Rodriguez, E. J., Campos-Bermudez, V. A., Grotewold, E. & Casati, P. The Identification of Maize and Arabidopsis Type I FLAVONE SYNTHASEs Links Flavones with Hormones and Biotic Interactions. Plant Physiology 169, 1090-1107, https://doi.org/10.1104/pp.15.00515 (2015).

[10]

Petroni, K. & Tonelli, C. Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci. 181, 219-229 (2011).

[11]

Gonzalez, A., Zhao, M., Leavitt, J. M. & Lloyd, A. M. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814-827 (2008).

[12]

Walker, A. R. et al. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11, 1337-1349 (1999).

[13]

Borevitz, J. O., Xia, Y., Blount, J., Dixon, R. A. & Lamb, C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12, 2383-2393 (2000).

[14]

Albert, N. W. et al. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26, 962-980 (2014).

[15]

Matsui, K., Umemura, Y. & Ohme-Takagi, M. AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J. 55, 954-967 (2008).

[16]

Xiang, L. L. et al. A novel bHLH transcription factor involved in regulating anthocyanin biosynthesis in Chrysanthemums (Chrysanthemum morifolium Ramat.) . PLoS ONE 10, e0143892 (2015).

[17]

Mehrtens, F., Kranz, H., Bednarek, P. & Weisshaar, B. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol. 138, 1083-1096 (2005).

[18]

Stracke, R. et al. 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 (2007).

[19]

Zhang, X. et al. Identification of two novel R2R3-MYB transcription factors, PsMYB114L and PsMYB12L, related to anthocyanin biosynthesis in Paeonia suffruticosa . Int. J. Mol. Sci. 20, 1055 (2019).

[20]

Nakatsuka, T. et al. Isolation and characterization of GtMYBP3 and GtMYBP4, orthologues of R2R3-MYB transcription factors that regulate early flavonoid biosynthesis, in gentian flowers. J. Exp. Bot. 63, 6505-6517 (2012).

[21]

Zhang, P. et al. A maize QTL for silk maysin levels contains duplicated Myb-homologous genes which jointly regulate flavone biosynthesis. Plant Mol. Biol. 52, 1-15 (2003).

[22]

Li, S. et al. MYB75 phosphorylation by MPK4 is required for light-induced anthocyanin accumulation in Arabidopsis. Plant Cell 28, 2866-2883 (2016).

[23]

An, J. P. et al. The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant J. 101, 573-589 (2020).

[24]

Zhou, L. J. et al. The small ubiquitin-like modifier E3 ligase MdSIZ1 promotes anthocyanin accumulation by sumoylating MdMYB1 under low-temperature conditions in apple. Plant Cell Environ. 40, 2068-2080 (2017).

[25]

Fang, H. et al. The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell Environ. 42, 2090-2104 (2019).

[26]

Gould, K., McKelvie, J. & Markham, K. Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury . Plant Cell Environ. 25, 1261-1269 (2002).

[27]

Song, Z. P. et al. NtMYB12 positively regulates flavonol biosynthesis and enhances tolerance to low Pi stress in Nicotiana tabacum . Front. Plant Sci. 10, 1683 (2019).

[28]

Muhlemann, J. K., Younts, T. L. & Muday, G. K. Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. Proc. Natl Acad. Sci. 115, e11188-e11197 (2018).

[29]

Lin-Wang, K. et al. High temperature reduces apple fruit colour via modulation of the anthocyanin regulatory complex. Plant Cell Environ. 34, 1176-1190 (2011).

[30]

Mori, K., Sugaya, S. & Gemma, H. Decreased anthocyanin biosynthesis in grape berries grown under elevated night temperature condition. Sci. Horticulturae 105, 319-330 (2005).

[31]

Fang, H. et al. MdCOL4 interaction mediates crosstalk between UV-B and high temperature to control fruit coloration in apple. Plant Cell Physiol. 60, 1055-1066 (2019b).

[32]

Gill, S. S. & Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem 48, 909-930, https://doi.org/10.1016/j.plaphy.2010.08.016 (2010).

[33]

Wang, B. et al. Structural insights into target DNA recognition by R2R3-MYB transcription factors. Nucleic Acids Res. 48, 460-471 (2020a).

[34]

Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616-620 (2011).

[35]

Lee, G. J. & Vierling, E. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol. 122, 189-198 (2000).

[36]

Liu, Y. et al. StMYB44 negatively regulates anthocyanin biosynthesis at high temperatures in tuber flesh of potato. J. Exp. Botany 7, 3809-3824, https://doi.org/10.1093/jxb/erz194 (2019).

[37]

Shin, J., Park, E. & Choi, G. PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J. 49, 981-994 (2007).

[38]

Kim, S. et al. High ambient temperature represses anthocyanin biosynthesis through degradation of HY5. Front. Plant Sci. 8, 1787 (2017).

[39]

Liu, X. F. et al. The identification of a MYB transcription factor controlling anthocyanin biosynthesis regulation in Chrysanthemum flowers. Sci. Horticulturae 194, 278-285 (2015).

[40]

Zhou, H. et al. Activator-type R2R3-MYB genes induce a repressor-type R2R3-MYB gene to balance anthocyanin and proanthocyanidin accumulation. N. Phytologist 221, 1919-1934 (2019).

[41]

Zimmermann, I. M., Heim, M. A., Weisshaar, B. & Uhrig, J. F. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40, 22-34 (2004).

[42]

Kagale, S. & Rozwadowski, K. EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6, 141-146 (2011).

[43]

Kazan, K. Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci. 11, 109-112 (2006).

[44]

Gill, S. S. & Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930 (2010).

[45]

Mekawy, A. M. M., Abdelaziz, M. N. & Ueda, A. Apigenin pretreatment enhances growth and salinity tolerance of rice seedlings. Plant Physiol. Biochem. 130, 94-104 (2018).

[46]

Wang, L. et al. CmBBX8 accelerates flowering by targeting CmFTL1 directly in summer chrysanthemum. Plant Biotechnol. J. 18, 1562 (2020).

[47]

Simmons, C. W., VanderGheynst, J. S. & Upadhyaya, S. K. A model of Agrobacterium tumefaciens vacuum infiltration into harvested leaf tissue and subsequent in planta transgene transient expression. Biotechnol. Bioeng. 102, 965-970 (2009).

[48]

An, J. P. et al. EIN3-LIKE1, MYB1, and ETHYLENE RESPONSE FACTOR3 act in a regulatory loop that synergistically modulates ethylene biosynthesis and anthocyanin accumulation. Plant Physiol. 178, 808-823 (2018).

[49]

Gay, C. & Gebicki, J. M. A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal. Biochem. 284, 217-220 (2000).

[50]

Shen, G., Niu, J. & Deng, Z. Abscisic acid treatment alleviates cadmium toxicity in purple flowering stalk (Brassica campestris L. ssp. chinensis var. purpurea Hort.) seedlings . Plant Physiol. Biochem. 118, 471-478 (2017).

[51]

Zheng, T. et al. Regulation of anthocyanin accumulation via MYB75/HAT1/TPL-mediated transcriptional repression. PLoS Genet. 15, e1007993 (2019).

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