Plant Molecular Biology Reporter

, Volume 36, Issue 3, pp 406–417 | Cite as

The Novel Rose MYB Transcription Factor RhMYB96 Enhances Salt Tolerance in Transgenic Arabidopsis

  • Xinqiang Jiang
  • Shaocui Li
  • Aiqin Ding
  • Zhujun Zhang
  • Qing Hao
  • Kuiling Wang
  • Qingchao Liu
  • Qinghua Liu
Original Paper


MYB transcription factors play diverse roles in plant development and responses to abiotic stresses. However, the biological roles of MYB family members in rose (Rosa hybrida) are still unknown. Here, we reported the isolation and functional characterization of a novel rose RhMYB96 gene. RhMYB96 have a close relationship to Arabidopsis AtMYB96, including the presence of typical R2- and R3-domains at the N-terminal. Salt, dehydration, or ethylene signaling induce the expression of RhMYB96. RhMYB96 localized in the nucleus when expressed in Arabidopsis thaliana. We generated three independent transgenic Arabidopsis overexpressing RhMYB96 to explore the function of RhMYB96 in salt tolerance. Overexpression of RhMYB96 in Arabidopsis resulted in NaCl insensitivity during germination. Furthermore, RhMYB96-overexpressing seedlings under salt stress had longer primary root length and increased biomass. Specifically, the RhMYB96-overexpressed Arabidopsis plants displayed higher capability of scavenging the reactive oxygen levels H2O2 and O2 under salt stress. In addition, overexpressing RhMYB96 improved abscisic acid (ABA) sensitivity during germination. Expression of abiotic stresses and ABA-related genes was stronger in RhMYB96-overexpressing plants. These findings suggest that the RhMYB96 plays and regulates salt stress tolerance modulating an ABA-mediated pathway. Main Conclusion The novel rose RhMYB96 regulates salt stress through the modulation of an ABA-mediated pathway in Arabidopsis.


Rose RhMYB96 Regulator Salt ABA 



abscisic acid




hydrogen peroxide




Murashige and Skoog


nitroblue tetrazolium


open reading frame


superoxide anion


quantitative reverse transcription PCR


transcription factors


wild type


Funding Information

This work was supported by the National Natural Science Foundation of China (Grant No. 31501798) and Promotive Research Fund for Excellent Young and Middle-aged Scientists of Shandong Province (No. BS2014SW032).

Supplementary material

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  1. Aasland R, Stewart AF, Gibson TJ (1996) The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. Trends Biochem Sci 21:87–88PubMedGoogle Scholar
  2. Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud J (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 51:1975–1987CrossRefPubMedGoogle Scholar
  3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol 160:379–395CrossRefPubMedPubMedCentralGoogle Scholar
  5. Carnavale Bottino M, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L, Hemerly AS, Ferreira PC (2013) High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8:e59423CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chen S, Polle A (2010) Salinity tolerance of Populus. Plant Biol 12:317–333CrossRefPubMedGoogle Scholar
  7. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  8. Dai F, Zhang C, Jiang X, Kang M, Yin X, Lu P, Zhang X, Zheng Y, Gao J (2012) RhNAC2 and RhEXPA4 are involved in the regulation of dehydration tolerance during the expansion of rose petals. Plant Physiol 160:2064–2082CrossRefPubMedPubMedCentralGoogle Scholar
  9. Ding ZJ, Yan JY, Li CX, Li GX, Wu YR, Zheng SJ (2015) Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J 84:56–69CrossRefPubMedGoogle Scholar
  10. Espley RV, Hellens RP, Putterill J, Stevenson DE, Kutty-Amma S, Allan AC (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. Plant J 49:414–427CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fang Q, Jiang T, Xu L, Liu H, Mao H, Wang X, Jiao B, Duan Y, Wang Q, Dong Q, Yang L, Tian G, Zhang C, Zhou Y, Liu X, Wang H, Fan D, Wang B, Luo K (2017) A salt-stress-regulator from the Poplar R2R3 MYB family integrates the regulation of lateral root emergence and ABA signaling to mediate salt stress tolerance in Arabidopsis. Plant Physiol Bioch 114:100–110Google Scholar
  12. Feng K, Xu Z, Que F, Liu J, Wang F, Xiong A (2018) An R2R3-MYB transcription factor, OjMYB1, functions in anthocyanin biosynthesis in Oenanthe javanica. Planta 247:301–315CrossRefPubMedGoogle Scholar
  13. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohmetakagi M, Tran LS, Yamaguchi- Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876CrossRefPubMedGoogle Scholar
  14. Gates D, Olson B, Clemente T, Smith S (2018) A novel R3 MYB transcriptional repressor associated with the loss of floral pigmentation in Iochroma. New Phytol 217:1346–1356CrossRefPubMedGoogle Scholar
  15. Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1909CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gruber V, Blanchet S, Diet A, Zahaf O, Boualem A, Kakar K, Alunni B, Udvardi MK, Frugier F, Crespi M (2009) Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula. Mol Gen Genomics 281:55–66CrossRefGoogle Scholar
  17. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411CrossRefPubMedPubMedCentralGoogle Scholar
  18. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular response to high salinity. Annu Rev Plant Bio 51:463–499CrossRefGoogle Scholar
  19. Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci 7:4CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 39:1029–1048CrossRefPubMedGoogle Scholar
  21. Ito M, Araki S, Matsunaga S, Itoh T, Nishihama R, Machida Y, Doonan JH, Watanabe A (2001) G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13:1891–1905CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jiang X, Zhang C, Lv P, Jiang G, Liu X, Dai F, Gao J (2014) RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. Plant Biotechnol J 12:38–48CrossRefPubMedGoogle Scholar
  23. Johnson SM, Cummins I, Lim FL, Slabas AR, Knight MR (2015) Transcriptomic analysis comparing stay-green and senescent Sorghum bicolor lines identifies a role for proline biosynthesis in the stay-green trait. J Exp Bot 66:7061–7073CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong J (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146:623–635CrossRefPubMedPubMedCentralGoogle Scholar
  25. Koca H, Bor M, Özdemir F, Türkan İ (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351CrossRefGoogle Scholar
  26. Kotchoni SO, Kuhns C, Ditzer A, Kirch H-H, Bartels D (2006) Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 29:1033–1048CrossRefPubMedGoogle Scholar
  27. Kurkela S, Borg-Franck M (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant Mol Biol 19:689–692CrossRefPubMedGoogle Scholar
  28. Lang V, Palva ET (1992) The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20:951–962CrossRefPubMedGoogle Scholar
  29. Li C, Ng CKY, Fan LM (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91CrossRefGoogle Scholar
  30. Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206CrossRefPubMedGoogle Scholar
  31. Lippold F, Sanchez DH, Musialak M, Schlereth A, Scheible W, Hincha DK, Udvardi MK (2009) AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiol 149:1761–1772CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ma N, Tan H, Liu X, Xue J, Li Y, Gao J (2006) Transcriptional regulation of ethylene receptor and CTR genes involved in ethylene-induced flower opening in cut rose (Rosa hybrida) cv. Samantha. J Exp Bot 57:2763–2773CrossRefPubMedGoogle Scholar
  33. Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signaling pathway. Plant J 25:295–303CrossRefPubMedGoogle Scholar
  34. Msanne J, Lin J, Stone JM, Awada T (2011) Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta 234:97–107CrossRefPubMedGoogle Scholar
  35. Nakashima K, Tran LP, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630CrossRefPubMedGoogle Scholar
  36. Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95CrossRefPubMedPubMedCentralGoogle Scholar
  37. Parcy F, Giraudat J (1997) Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J 11:693–702Google Scholar
  38. Qiu Q, Guo Y, Dietrich MA, Schumaker KS, Zhu J (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci U S A 99:8436–8441CrossRefPubMedPubMedCentralGoogle Scholar
  39. Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo J, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431CrossRefPubMedPubMedCentralGoogle Scholar
  40. Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151:275–289CrossRefPubMedPubMedCentralGoogle Scholar
  41. Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152CrossRefPubMedPubMedCentralGoogle Scholar
  42. Shan H, Chen S, Jiang J, Chen F, Chen Y, Gu C, Li P, Song A, Zhu X, Gao H, Zhou G, Li T, Yang X (2012) Heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Mol Biotechnol 51:160–173CrossRefPubMedGoogle Scholar
  43. Shekhawat UKS, Ganapathi TR (2013) Transgenic banana plants overexpressing MusabZIP53 display severe growth retardation with enhanced sucrose and polyphenol oxidase activity. Plant Cell Tiss Org 116:387–402CrossRefGoogle Scholar
  44. Shen X, Guo X, Guo X, Zhao D, Zhao W, Chen J, Li T (2017) PacMYBA, a sweet cherry R2R3-MYB transcription factor, is a positive regulator of salt stress tolerance and pathogen resistance. Plant Physiol Bioch 112:302–311CrossRefGoogle Scholar
  45. Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30:914–922CrossRefPubMedGoogle Scholar
  46. Shin D, Moon SJ, Han S, Kim BG, Park SR, Lee SK, Yoon HJ, Lee HE, Kwon HB, Baek D, Yi BY, Byun MO (2011) Expression of StMYB1R-1, a novel potato single MYB-like domain transcription factor, increases drought tolerance. Plant Physiol 155:421–432CrossRefPubMedGoogle Scholar
  47. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Bio Evol 28:2731–2739CrossRefGoogle Scholar
  48. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wan B, Lin Y, Mou T (2007) Expression of rice Ca2+-dependent protein kinases (CDPKs) genes under different environmental stresses. FEBS Lett 581:1179–1189CrossRefPubMedGoogle Scholar
  50. Wang Z, Tang J, Hu R, Wu P, Hou XL, Song XM, Xiong AS (2015) Genome-wide analysis of the R2R3-MYB transcription factor genes in Chinese cabbage (Brassica rapa ssp. Pekinensis) reveals their stress and hormone responsive patterns. BMC Genomics 16:17CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wang K, Zhong M, Wu Y, Bai Z, Liang Q, Liu Q, Pan Y, Zhang L, Jiang B, Jia Y, Liu G (2017) Overexpression of a chrysanthemum transcription factor gene DgNAC1 improves the salinity tolerance in chrysanthemum. Plant Cell Rep 36:571–578CrossRefPubMedGoogle Scholar
  52. Xie CG, Lin H, Deng XW, Guo Y (2009) Roles of SCaBP8 in salt stress response. Plant Signal Behav 4:956–958CrossRefPubMedPubMedCentralGoogle Scholar
  53. Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xiong H, Li J, Liu P, Duan J, Zhao Y, Guo X, Li Y, Zhang H, Ali J, Li Z (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS One 9:e92913CrossRefPubMedPubMedCentralGoogle Scholar
  55. Xu F, Ning Y, Zhang W, Liao Y, Li L, Cheng H, Cheng S (2014) An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Funct Integr Genomics 14:177–189CrossRefPubMedGoogle Scholar
  56. Yan J, Wang B, Zhong Y, Yao L, Cheng L, Wu T (2015) The soybean R2R3 MYB transcription factor GmMYB100 negatively regulates plant flavonoid biosynthesis. Plant Mol Biol 89:35–48CrossRefPubMedGoogle Scholar
  57. Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556CrossRefPubMedPubMedCentralGoogle Scholar
  58. Yoshiba Y, Nanjo T, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem Biophys Res Commun 261:766–772CrossRefPubMedGoogle Scholar
  59. Yuan Y, Qi L, Yang J, Wu C, Liu Y, Huang L (2014) A Scutellaria baicalensis R2R3-MYB gene, SbMYB8, regulates flavonoid biosynthesis and improves drought stress tolerance in transgenic tobacco. Plant Cell Tiss Org 120:961–972CrossRefGoogle Scholar
  60. Zhang L, Liu G, Zhao G, Xia C, Jia J, Liu X, Kong X (2014) Characterization of a wheat R2R3-MYB transcription factor gene, TaMYB19, involved in enhanced abiotic stresses in Arabidopsis. Plant Cell Physiol 55:1802–1812CrossRefPubMedGoogle Scholar
  61. Zhou H, Peng Q, Zhao J, Owiti A, Ren F, Liao L, Wang L, Deng X, Jiang Q, Han Y (2016) Multiple R2R3-MYB transcription factors involved in the regulation of anthocyanin accumulation in peach flower. Front Plant Sci 7:1557PubMedPubMedCentralGoogle Scholar
  62. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Xinqiang Jiang
    • 1
  • Shaocui Li
    • 1
  • Aiqin Ding
    • 1
  • Zhujun Zhang
    • 1
  • Qing Hao
    • 1
  • Kuiling Wang
    • 1
  • Qingchao Liu
    • 1
  • Qinghua Liu
    • 1
  1. 1.College of Landscape Architecture and ForestryQingdao Agricultural UniversityQingdaoChina

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