Banana MaBZR1/2 associate with MaMPK14 to modulate cell wall modifying genes during fruit ripening

  • Wei Shan
  • Yu-Fan Guo
  • Wei Wei
  • Jian-Ye Chen
  • Wang-Jin Lu
  • De-Bao Yuan
  • Xin-Guo SuEmail author
  • Jian-Fei KuangEmail author
Original Article


Key message

Banana MaBZR1/2 interact with MaMPK14 to enhance the transcriptional inhibition of cell wall modifying genes including MaEXP2, MaPL2 and MaXET5.


Fruit ripening and softening, the major attributes to perishability in fleshy fruits, are modulated by various plant hormones and gene expression. Banana MaBZR1/2, the central transcription factors of brassinosteroid (BR) signaling, mediate fruit ripening through regulation of ethylene biosynthesis, but their possible roles in fruit softening as well as the underlying mechanisms remain to be determined. In this work, we found that MaBZR1/2 directly bound to and repressed the promoters of several cell wall modifying genes such as MaEXP2, MaPL2 and MaXET5, whose transcripts were elevated concomitant with fruit ripening. Moreover, yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays indicated that MaBZR1/2 physically interacted with a mitogen-activated protein kinase MaMPK14, and this interaction strengthened the MaBZR1/2-mediated transcriptional inhibitory abilities. Collectively, our study provides insight into the mechanism of MaBZR1/2 contributing to fruit ripening and softening, which may have potential for banana molecular improvement.


Banana fruit BZR Cell wall modification Protein–protein interaction Transcriptional regulation 





BRI1-associated receptor kinase 1


Brassinosteroid Insensitive 1-EMS-Suppressor 1


Bimolecular fluorescence complementation


Brassinosteroid insensitive 2




Brassinosteroid insensitive 1


Brassinazole resistant 1


Electrophoretic mobility shift assay




Mitogen-activated protein kinase


Mitogen-activated protein kinase kinase


Mitogen-activated protein kinase kinase kinase


Polymerase chain reaction


Pectate lyase


Transcription factor


Xyloglucan endotransglycosylase


Yeast two-hybrid



This work was funded by the National Natural Science Foundation of China (Grant no. 31401922, 31772021), Guangdong Special Support Program (Grant no. 2017TQ04N512), China Agriculture Research System (Grant no. CARS-31-11), and Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams.

Author contribution statement

JK and XS conceived and designed the research. WS and YG carried out most of the experiments. WW performed some of the experiments. JC, WL, and DY analyzed the data. JK, XS, JC and WL wrote the manuscript. All the authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Supplementary material

299_2019_2471_MOESM1_ESM.doc (44 kb)
Supplementary material 1 (DOC 44 kb)


  1. Ba LJ, Shan W, Xiao YY et al (2014a) A ripening-induced transcription factor MaBSD1 interacts with promoters of MaEXP1/2 from banana fruit. Plant Cell Rep 33:1913–1920CrossRefGoogle Scholar
  2. Ba LJ, Shan W, Kuang JF et al (2014b) The banana MaLBD (LATERAL ORGAN BOUNDARIES DOMAIN) transcription factors regulate EXPANSIN expression and are involved in fruit ripening. Plant Mol Biol Rep 32:1103–1113CrossRefGoogle Scholar
  3. Chen L, Zhong HY, Kuang JF et al (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390CrossRefGoogle Scholar
  4. Chen J, Nolan TM, Ye H et al (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29:1425–1439CrossRefGoogle Scholar
  5. Costa F, Peace CP, Stella S et al (2010) QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus × domestica Borkh.). J Exp Bot 61:3029–3039CrossRefGoogle Scholar
  6. Cui XY, Gao Y, Guo J et al (2019) BES/BZR transcription factor TaBZR2 positively regulates drought responses by activation of TaGST1. Plant Physiol 180:605–620CrossRefGoogle Scholar
  7. Ding Y, Li H, Zhang X et al (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32:278–289CrossRefGoogle Scholar
  8. Dóczi R, Bögre L (2018) The quest for MAP kinase substrates: gaining momentum. Trends Plant Sci 23:918–932CrossRefGoogle Scholar
  9. Fan ZQ, Kuang JF, Fu CC et al (2016) The banana transcriptional repressor MaDEAR1 negatively regulates cell wall-modifying genes involved in fruit ripening. Front Plant Sci 7:1021Google Scholar
  10. Fan C, Guo G, Yan H et al (2018) Characterization of Brassinazole resistant (BZR) gene family and stress induced expression in Eucalyptus grandis. Physiol Mol Biol Plants 24:821–831CrossRefGoogle Scholar
  11. Fu CC, Han YC, Qi XY et al (2016) Papaya CpERF9 acts as a transcriptional repressor of cell-wall-modifying genes CpPME1/2 and CpPG5 involved in fruit ripening. Plant Cell Rep 35:2341–2352CrossRefGoogle Scholar
  12. Guo YF, Shan W, Liang SM et al (2019) MaBZR1/2 act as transcriptional repressors of ethylene biosynthetic genes in banana fruit. Physiol Plant 165:555–568CrossRefGoogle Scholar
  13. He JX, Gendron JM, Sun Y et al (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638CrossRefGoogle Scholar
  14. Jonak C, Okresz L, Bogre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424CrossRefGoogle Scholar
  15. Kang S, Yang F, Li L et al (2015) The Arabidopsis transcription factor BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 is a direct substrate of MITOGEN-ACTIVATED PROTEIN KINASE6 and regulates immunity. Plant Physiol 167:1076–1086CrossRefGoogle Scholar
  16. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704CrossRefGoogle Scholar
  17. Li X, Xu C, Korban SS, Chen K (2010) Regulatory mechanisms of textural changes in ripening fruits. Crit Rev Plant Sci 29:222–243CrossRefGoogle Scholar
  18. Li QF, Wang C, Jiang L et al (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5:ra72Google Scholar
  19. Li H, Ding Y, Shi Y et al (2017a) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642CrossRefGoogle Scholar
  20. Li H, Ye K, Shi Y et al (2017b) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10:545–559CrossRefGoogle Scholar
  21. Li QF, Lu J, Yu JW et al (2018) The brassinosteroid-regulated transcription factors BZR1/BES1 function as a coordinator in multisignal-regulated plant growth. BBA Gene Regul Mech 1861:561–571Google Scholar
  22. Liu L, Jia C, Zhang M et al (2014) Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signaling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol J 12:105–115CrossRefGoogle Scholar
  23. Manoli A, Trevisan S, Quaggiotti S, Varotto S (2018) Identification and characterization of the BZR transcription factor family and its expression in response to abiotic stresses in Zea mays L. Plant Growth Regul 84:423–436CrossRefGoogle Scholar
  24. Mbéguié-A-Mbéguié D, Hubert O, Baurens FC et al (2009) Expression patterns of cell wall modifying genes from banana during ripening in relationship with finger drop. J Exp Bot 60:2021–2034CrossRefGoogle Scholar
  25. Mohapatra D, Mishra S, Sutar N (2010) Banana post harvest practices: current status and future prospects. Agric Rev 31:56–62Google Scholar
  26. Moustafa K, AbuQamar S, Jarrar M et al (2014) MAPK cascades and major abiotic stresses. Plant Cell Rep 33:1217–1225CrossRefGoogle Scholar
  27. Pua EC, Ong CK, Liu P, Liu JZ (2001) Isolation and expression of two pectate lyase genes during fruit ripening of banana (Musa acuminata). Physiol Plant 113:92–99CrossRefGoogle Scholar
  28. Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649CrossRefGoogle Scholar
  29. Saha G, Park JI, Jung HJ et al (2015) Molecular characterization of BZR transcription factor family and abiotic stress induced expression profiling in Brassica rapa. Plant Physiol Biochem 92:92–104CrossRefGoogle Scholar
  30. Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682–693CrossRefGoogle Scholar
  31. Sane AVA, Sane AP, Nath P (2007) Multple forms of α-expansin genes are expressed during banana fruit ripening and development. Postharvest Biol Technol 45:184–192CrossRefGoogle Scholar
  32. Song CB, Shan W, Yang YY et al (2018) Heterodimerization of MaTCP proteins modulates the transcription of MaXTH10/11 genes during banana fruit ripening. BBA Gene Regul Mech 1861:613–622Google Scholar
  33. Song L, Chen W, Wang B et al (2019) GmBZL3 acts as a major BR signaling regulator through crosstalk with multiple pathways in Glycine max. BMC Plant Biol 19:86CrossRefGoogle Scholar
  34. Sun Y, Fan XY, Cao DM et al (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777CrossRefGoogle Scholar
  35. Tang W, Yuan M, Wang R et al (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13:124–131CrossRefGoogle Scholar
  36. Tucker G, Yin X, Zhang A et al (2017) Ethylene and fruit softening. Food Qual Saf 1:253–267CrossRefGoogle Scholar
  37. Ueno Y, Yoshida R, Kishi-Kaboshi M et al (2015) Abiotic stresses antagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLoS Pathog 11:e1005231CrossRefGoogle Scholar
  38. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12CrossRefGoogle Scholar
  39. Wang ZY, Nakano T, Gendron J et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513CrossRefGoogle Scholar
  40. Wang ZY, Bai MY, Oh E, Zhu JY (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46:701–724CrossRefGoogle Scholar
  41. Wang Y, Cao JJ, Wang KX et al (2019) BZR1 mediates brassinosteroid-induced autophagy and Nitrogen starvation in tomato. Plant Physiol 179:671–685CrossRefGoogle Scholar
  42. Wu C, Shan W, Liang S et al (2019) MaMPK2 enhances MabZIP93-mediated transcriptional activation of cell wall modifying genes during banana fruit ripening. Plant Mol Biol 101:113–127CrossRefGoogle Scholar
  43. Ye H, Liu S, Tang B et al (2017) RD26 mediates crosstalk between drought and brassinosteroid signaling pathways. Nat Commun 8:14573CrossRefGoogle Scholar
  44. Yu X, Li L, Zola J et al (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65:634–646CrossRefGoogle Scholar
  45. Yu H, Feng W, Sun F et al (2018) Cloning and characterization of BES1/BZR1 transcription factor genes in maize. Plant Growth Regul 86:235–249CrossRefGoogle Scholar
  46. Zhao C, Wang P, Si T et al (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43:618–629CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Guangdong Provincial Key Laboratory of Postharvest Science of Fruits and Vegetables/Engineering Research Center of Southern Horticultural Products Preservation, Ministry of Education, College of HorticultureSouth China Agricultural UniversityGuangzhouPeople’s Republic of China
  2. 2.Guangdong Food and Drug Vocational CollegeGuangzhouPeople’s Republic of China
  3. 3.Hainan Key Laboratory of Banana Genetic Improvement, Haikou Experimental StationChinese Academy of Tropical Agricultural SciencesHaikouPeople’s Republic of China

Personalised recommendations