Plant Molecular Biology

, Volume 93, Issue 3, pp 299–311 | Cite as

Two MYB-related transcription factors play opposite roles in sugar signaling in Arabidopsis

  • Yi-Shih Chen
  • Yi-Chi Chao
  • Tzu-Wei Tseng
  • Chun-Kai Huang
  • Pei-Ching Lo
  • Chung-An Lu


Key message

Sugar regulation of gene expression has profound effects at all stages of the plant life cycle. Although regulation at the transcriptional level is one of the most prominent mechanisms by which gene expression is regulated, only a few transcription factors have been identified and demonstrated to be involved in the regulation of sugar-regulated gene expression. OsMYBS1, an R1/2-type MYB transcription factor, has been demonstrated to be involved in sugar- and hormone-regulated α-amylase gene expression in rice. Arabidopsis contains two OsMYBS1 homologs. In the present study, we investigate MYBS1 and MYBS2 in sugar signaling in Arabidopsis. Our results indicate that MYBS1 and MYBS2 play opposite roles in regulating glucose and ABA signaling in Arabidopsis during seed germination and early seedling development.


MYB proteins have been classified into four subfamilies: R2R3-MYB, R1/2-MYB, 3R-MYB, and 4R-MYB. An R1/2-type MYB transcription factor, OsMYBS1, has been demonstrated to be involved in sugar- and hormone-regulated α-amylase genes expression in rice. In this study, two genes homologous to OsMYBS1, MYBS1 and MYBS2, were investigated in Arabidopsis. Subcellular localization analysis showed that MYBS1 and MYBS2 were localized in the nucleus. Rice embryo transient expression assays indicated that both MYBS1 and MYBS2 could recognize the sugar response element, TA-box, in the promoter and induced promoter activity. mybs1 mutant exhibited hypersensitivity to glucose, whereas mybs2 seedlings were hyposensitive to it. MYBS1 and MYBS2 are involved in the control of glucose-responsive gene expression, as the mybs1 mutant displayed increased expression of a hexokinase gene (HXK1), chlorophyll a/b-binding protein gene (CAB1), ADP-glucose pyrophosphorylase gene (APL3), and chalcone synthase gene (CHS), whereas the mybs2 mutant exhibited decreased expression of these genes. mybs1 also showed an enhanced response to abscisic acid (ABA) in the seed germination and seedling growth stages, while mybs2 showed reduced responses. The ABA biosynthesis inhibitor fluridone rescued the mybs1 glucose-hypersensitive phenotype. Moreover, the mRNA levels of three ABA biosynthesis genes, ABA1, NCED9, and AAO3, and three ABA signaling genes, ABI3, ABI4, and ABI5, were increased upon glucose treatment of mybs1 seedlings, but were decreased in mybs2 seedlings. These results indicate that MYBS1 and MYBS2 play opposite roles in regulating glucose and ABA signaling in Arabidopsis during seed germination and early seedling development.


MYB transcription factor Sugar signaling ABA Arabidopsis 



This work was supported by grants (104-2321-B-008-001 and 105-2321-B-008-001) from the Ministry of Science and Technology of the Republic of China, Taiwan.

Authors’ contributions

YC, YC, and CL participated in the design of the study. YC, YC, and TT carried out the gene cloning, real-time RT-PCR, and subcellular localization. PL and CH carried out the GUS activity assay. TT, and CH carried out the bioinformatics analysis. YC, and CL carried out data analysis, and wrote manuscript. All authors read and approved the final manuscript.

Supplementary material

11103_2016_562_MOESM1_ESM.pptx (8 mb)
Supplementary material 1 (PPTX 8226 KB)
11103_2016_562_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 KB)


  1. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14:2085–2096PubMedPubMedCentralGoogle Scholar
  2. Baena-Gonzalez E (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3:300–313CrossRefPubMedGoogle Scholar
  3. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942CrossRefPubMedGoogle Scholar
  4. Carvalho RF, Carvalho SD, Duque P (2010) The plant-specific SR45 protein negatively regulates glucose and ABA signaling during early seedling development in Arabidopsis. Plant Physiol 154:772–783CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chan MT, Yu SM (1998a) The 3’ untranslated region of a rice alpha-amylase gene functions as a sugar-dependent mRNA stability determinant. Proc Natl Acad Sci USA 95:6543–6547CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chan MT, Yu SM (1998b) The 3’ untranslated region of a rice alpha-amylase gene mediates sugar-dependent abundance of mRNA. Plant J 15:685–695CrossRefPubMedGoogle Scholar
  7. Chen PW, Lu CA, Yu TS, Tseng TH, Wang CS, Yu SM (2002) Rice alpha-amylase transcriptional enhancers direct multiple mode regulation of promoters in transgenic rice. J Biol Chem 277:13641–13649CrossRefPubMedGoogle Scholar
  8. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ciereszkoa I, Kleczkowskib LA (2002) Glucose and mannose regulate the expression of a major sucrose synthase gene in Arabidopsis via hexokinase-dependent mechanisms. Plant Physiol Biochem 40:907–911CrossRefGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  11. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469CrossRefPubMedPubMedCentralGoogle Scholar
  12. Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63:3367–3377CrossRefPubMedGoogle Scholar
  13. Finkelstein RR, Lynch TJ (2000) Abscisic acid inhibition of radicle emergence but not seedling growth is suppressed by sugars. Plant Physiol 122:1179–1186CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gibson SI, Laby RJ, Kim D (2001) The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 280:196–203CrossRefPubMedGoogle Scholar
  15. Huang CK, Lo PC, Huang LF, Wu SJ, Yeh CH, Lu CA (2015) A single-repeat MYB transcription repressor, MYBH, participates in regulation of leaf senescence in Arabidopsis. Plant Mol Biol 88:269–286CrossRefPubMedGoogle Scholar
  16. Huijser C, Kortstee A, Pego J, Weisbeek P, Wisman E, Smeekens S (2000) The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: involvement of abscisic acid in sugar responses. Plant J 23:577–585CrossRefPubMedGoogle Scholar
  17. Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kang SG, Price J, Lin PC, Hong JC, Jang JC (2010) The Arabidopsis bZIP1 transcription factor is involved in sugar signaling, protein networking, and DNA binding. Mol Plant 3:361–373CrossRefPubMedGoogle Scholar
  19. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246CrossRefPubMedGoogle Scholar
  20. Koch KE, Wu Y, Xu J (1996) Sugar and metabolic regulation of genes for sucrose metabolism: potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing. J Exp Bot 47:1179–1185CrossRefPubMedGoogle Scholar
  21. Laby RJ, Kincaid MS, Kim D, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23:587–596CrossRefPubMedGoogle Scholar
  22. Lu CA, Lim EK, Yu SM (1998) Sugar response sequence in the promoter of a rice alpha-amylase gene serves as a transcriptional enhancer. J Biol Chem 273:10120–10131CrossRefPubMedGoogle Scholar
  23. Lu CA, Ho TH, Ho SL, Yu SM (2002) Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression. Plant Cell 14:1963–1980CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lu CA, Lin CC, Lee KW, Chen JL, Huang LF, Ho SL, Liu HJ, Hsing YI, Yu SM (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499CrossRefPubMedPubMedCentralGoogle Scholar
  25. Mita S, Suzuki-Fujii K, Nakamura K (1995) Sugar-inducible expression of a gene for beta-amylase in Arabidopsis thaliana. Plant Physiol 107:895–904CrossRefPubMedPubMedCentralGoogle Scholar
  26. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336CrossRefPubMedGoogle Scholar
  27. Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143:156–171CrossRefPubMedPubMedCentralGoogle Scholar
  28. Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rolland F, Sheen J (2005) Sugar sensing and signaling networks in plants. Biochem Soc Trans 33:269–271CrossRefPubMedGoogle Scholar
  30. Rolland F, Moore B, Sheen J. (2002) Sugar sensing and signaling in plants. Plant Cell 14(Suppl 1):S185–S205PubMedPubMedCentralGoogle Scholar
  31. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709CrossRefPubMedGoogle Scholar
  32. Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling. Plant J 26:421–433CrossRefPubMedGoogle Scholar
  33. Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434CrossRefPubMedGoogle Scholar
  34. Rubio-Somoza I, Martinez M, Diaz I, Carbonero P (2006) HvMCB1, a R1MYB transcription factor from barley with antagonistic regulatory functions during seed development and germination. Plant J 45:17–30CrossRefPubMedGoogle Scholar
  35. Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sheu JJ, Jan SP, Lee HT, Yu SM (1994) Control of transcription and messenger-RNA turnover as mechanisms of metabolic repression of alpha-amylase gene-expression. Plant J 5:655–664CrossRefGoogle Scholar
  37. Sun C, Palmqvist S, Olsson H, Boren M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092CrossRefPubMedPubMedCentralGoogle Scholar
  38. Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461CrossRefPubMedGoogle Scholar
  39. Xiong Y, Sheen J (2013) Moving beyond translation: glucose-TOR signaling in the transcriptional control of cell cycle. Cell Cycle 12:1989–1990CrossRefPubMedPubMedCentralGoogle Scholar
  40. Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124CrossRefPubMedGoogle Scholar
  41. Yuan K, Wysocka-Diller J (2006) Phytohormone signalling pathways interact with sugars during seed germination and seedling development. J Exp Bot 57:3359–3367CrossRefPubMedGoogle Scholar
  42. Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS (2011) The R-R-Type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol 52:138–148CrossRefPubMedGoogle Scholar
  43. Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci U S A 95:10294–10299CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Yi-Shih Chen
    • 1
  • Yi-Chi Chao
    • 1
  • Tzu-Wei Tseng
    • 1
  • Chun-Kai Huang
    • 1
  • Pei-Ching Lo
    • 1
  • Chung-An Lu
    • 1
  1. 1.Department of Life SciencesNational Central UniversityTaoyuan CityTaiwan

Personalised recommendations