Abstract
Key message
Nuclear-localized Arabidopsis MYB3 functions as a transcriptional repressor for regulation of lignin and anthocyanin biosynthesis under high salt conditions.
Abstract
Salinity stress is a major factor which reduces plant growth and crop yield worldwide. To improve growth of crops in high salinity environments, plant responses to salinity stress must be tightly controlled. Here, to further understand the regulation of plant responses under high salinity conditions, the function of the MYB3 transcription factor was studied as a repressor to control accumulation of lignin and anthocyanin under salt stress conditions. Nuclear-localized MYB3 forms a homodimer. It is ubiquitously expressed, especially in vascular tissues, with expression highly induced by NaCl in tissues such as roots, leaves, stems, and flowers. myb3 mutant plants exhibited longer root growth in high NaCl conditions than wild-type plants. However, several NaCl responsive genes were not significantly altered in myb3 compared to wild-type. Interestingly, high accumulation of lignin and anthocyanin occurred in myb3 under NaCl treatment, as well as increased expression of genes involved in lignin and anthocyanin biosynthesis, such as phenylalanine ammonia lyase 1 (PAL1), cinnamate 4-hydroxylase (C4H), catechol-O-methyltransferase (COMT), 4-coumaric acid-CoA ligase (4CL3), dihydroflavonol reductase (DFR), and leucoanthocyanidin dioxygenase (LDOX). According to yeast two-hybrid screenings, various transcription factors, including anthocyanin regulators Transparent Testa 8 (TT8) and Enhancer of Glabra 3 (EGL3), were isolated as MYB3 interacting proteins. MYB3 was characterized as a transcriptional repressor, with its repressor domain located in the C-terminus. Overall, these results suggest that nuclear-localized MYB3 functions as a transcriptional repressor to control lignin and anthocyanin accumulation under salinity stress conditions.
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References
Abrahams S, Lee E, Walker AR et al (2003) The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development. Plant J 35:624–636. https://doi.org/10.1046/j.1365-313x.2003.01834.x
Ambawat S, Sharma P, Yadav NR, Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants 19:307–321. https://doi.org/10.1007/s12298-013-0179-1
Bang WY, Kim SW, Jeong IS et al (2008) The C-terminal region (640–967) of Arabidopsis CPL1 interacts with the abiotic stress- and ABA-responsive transcription factors. Biochem Biophys Res Commun 372:907–912. https://doi.org/10.1016/j.bbrc.2008.05.161
Biała W, Jasiński M (2018) The phenylpropanoid case—it is transport that matters. Front Plant Sci 9:1–8
Brinkmann K, Blaschke L, Polle A (2002) Comparison of different methods for lignin determination as a basis for calibration of near-infrared reflectance spectroscopy and implications of lignoproteins. J Chem Ecol 28:2483–2501. https://doi.org/10.1023/a:1021484002582
Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29. https://doi.org/10.1104/pp.108.117887
Chen K, Guo Y, Song M et al (2020) Dual role of MdSND1 in the biosynthesis of lignin and in signal transduction in response to salt and osmotic stress in apple. Hortic Res 7:1–13. https://doi.org/10.1038/s41438-020-00433-7
Cominelli E, Galbiati M, Vavasseur A et al (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200. https://doi.org/10.1016/j.cub.2005.05.048
Cone KC, Burr FA, Burr B (1986) Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci USA 83:9631–9635. https://doi.org/10.1073/pnas.83.24.9631
de Vetten N, Quattrocchio F, Mol J, Koes R (1997) The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev 11:1422–1434. https://doi.org/10.1101/gad.11.11.1422
Dubos C, Stracke R, Grotewold E et al (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581. https://doi.org/10.1016/j.tplants.2010.06.005
Eryılmaz F (2006) The relationships between salt stress and anthocyanin content in higher plants. Biotechnol Biotechnol Equip 20:47–52. https://doi.org/10.1080/13102818.2006.10817303
Fraser CM, Chapple C (2011) The phenylpropanoid pathway in Arabidopsis. Arabidopsis Book 9:e0152. https://doi.org/10.1199/tab.0152
Goff SA, Cone KC, Chandler VL (1992) Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev 6:864–875. https://doi.org/10.1101/gad.6.5.864
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
Holton TA, Cornish EC (1995) Genetics and biochemistry of anthocyanin biosynthesis. Plant Cell 7:1071–1083. https://doi.org/10.1105/tpc.7.7.1071
Hwang SM, Kim DW, Woo MS et al (2014) Functional characterization of Arabidopsis HsfA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant Cell Environ 37:1202–1222. https://doi.org/10.1111/pce.12228
Jacob P, Brisou G, Dalmais M et al (2021) The seed development factors TT2 and MYB5 regulate heat stress response in Arabidopsis. Genes (basel) 12:746. https://doi.org/10.3390/genes12050746
Jin H, Cominelli E, Bailey P et al (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19:6150–6161. https://doi.org/10.1093/emboj/19.22.6150
Katiyar A, Smita S, Lenka SK et al (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genom 13:544. https://doi.org/10.1186/1471-2164-13-544
Kim DW, Jeon SJ, Hwang SM et al (2016) The C3H-type zinc finger protein GDS1/C3H42 is a nuclear-speckle-localized protein that is essential for normal growth and development in Arabidopsis. Plant Sci 250:141–153. https://doi.org/10.1016/j.plantsci.2016.06.010
Kranz HD, Denekamp M, Greco R et al (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J 16:263–276. https://doi.org/10.1046/j.1365-313x.1998.00278.x
Mahmood K, Xu Z, El-Kereamy A et al (2016) The Arabidopsis transcription factor ANAC032 represses anthocyanin biosynthesis in response to high sucrose and oxidative and abiotic stresses. Front Plant Sci 7
Mancinelli AL (1984) Photoregulation of anthocyanin synthesis 1: VIII. Effect of light pretreatments. Plant Physiol 75:447–453. https://doi.org/10.1104/pp.75.2.447
Naing AH, Kim CK (2021) Abiotic stress-induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiol Plant 172:1711–1723. https://doi.org/10.1111/ppl.13373
Nesi N, Debeaujon I, Jond C et al (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12:1863–1878. https://doi.org/10.1105/tpc.12.10.1863
Preston J, Wheeler J, Heazlewood J et al (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995. https://doi.org/10.1111/j.1365-313X.2004.02280.x
Schwinn K, Venail J, Shang Y et al (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
Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol (stuttg) 11:90–96. https://doi.org/10.1111/j.1438-8677.2008.00162.x
Seo PJ, Park C-M (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483. https://doi.org/10.1111/j.1469-8137.2010.03183.x
Shimada S, Otsuki H, Sakuta M (2007) Transcriptional control of anthocyanin biosynthetic genes in the Caryophyllales. J Exp Bot 58:957–967. https://doi.org/10.1093/jxb/erl256
Shirley BW, Kubasek WL, Storz G et al (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659–671. https://doi.org/10.1046/j.1365-313x.1995.08050659.x
Sompornpailin K, Makita Y, Yamazaki M, Saito K (2002) A WD-repeat-containing putative regulatory protein in anthocyanin biosynthesis in Perilla frutescens. Plant Mol Biol 50:485–495. https://doi.org/10.1023/a:1019850921627
Spitz F, Furlong EEM (2012) Transcription factors: from enhancer binding to developmental control. Nat Rev Genet 13:613–626. https://doi.org/10.1038/nrg3207
Stracke R, Ishihara H, Huep G 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. https://doi.org/10.1111/j.1365-313X.2007.03078.x
Tamagnone L, Merida A, Parr A et al (1998) The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–154. https://doi.org/10.1105/tpc.10.2.135
Van der Ent S, Verhagen BWM, Van Doorn R et al (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304. https://doi.org/10.1104/pp.107.113829
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3:2–20. https://doi.org/10.1093/mp/ssp106
Wang X-C, Wu J, Guan M-L et al (2020) Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis. Plant J 101:637–652. https://doi.org/10.1111/tpj.14570
Xu W, Grain D, Bobet S et al (2014) Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed. New Phytol 202:132–144. https://doi.org/10.1111/nph.12620
Zhou M, Zhang K, Sun Z et al (2017) LNK1 and LNK2 corepressors interact with the MYB3 transcription factor in phenylpropanoid biosynthesis. Plant Physiol 174:1348–1358. https://doi.org/10.1104/pp.17.00160
Funding
This research was supported by grants from the National Research Foundation (NRF) of Korea funded by the Korean government (MSIT) (2020R1A2C1004560) and the Korea Research Institute of Bioscience and Biotechnology (KRIBB) Research Initiative Program (KGM5372221).
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DK, SJJ and SK designed and mainly performed the experiments. The manuscript was written primarily by D. Kim and revised by SY, HSK and SK supervised the study and edited the manuscript. All authors discussed the results and commented on the manuscript.
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Kim, D., Jeon, S.J., Yanders, S. et al. MYB3 plays an important role in lignin and anthocyanin biosynthesis under salt stress condition in Arabidopsis. Plant Cell Rep 41, 1549–1560 (2022). https://doi.org/10.1007/s00299-022-02878-7
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DOI: https://doi.org/10.1007/s00299-022-02878-7