Advertisement

Planta

, Volume 249, Issue 5, pp 1627–1643 | Cite as

Apple AP2/EREBP transcription factor MdSHINE2 confers drought resistance by regulating wax biosynthesis

  • Ya-Li Zhang
  • Chun-Ling Zhang
  • Gui-Luan Wang
  • Yong-Xu Wang
  • Chen-Hui Qi
  • Chun-Xiang You
  • Yuan-Yuan LiEmail author
  • Yu-Jin HaoEmail author
Original Article

Abstract

Main conclusion

This study showed that AP2/EREBP transcription factor MdSHINE2 functioned in mediating cuticular permeability, sensitivity to abscisic acid (ABA), and drought resistance by regulating wax biosynthesis.

Plant cuticular wax plays crucial roles in protecting plants from environmental stresses, particularly drought stress. Many enzymes and transcription factors involved in wax biosynthesis have been identified in plant species. In this study, we identified an AP2/EREBP transcription factor, MdSHINE2 from apple, which is a homolog of AtSHINE2 in Arabidopsis. MdSHINE2 was constitutively expressed at different levels in various apple tissues, and the transcription level of MdSHINE2 was induced substantially by abiotic stress and hormone treatments. MdSHINE2-overexpressing Arabidopsis exhibited great change in cuticular wax crystal numbers and morphology and wax composition of leaves and stems. Moreover, MdSHINE2 heavily influenced cuticular permeability, sensitivity to abscisic acid, and drought resistance.

Keywords

Apple AP2/EREBP ABA sensitivity Cuticular permeability Crystal morphology Drought resistance Wax load 

Abbreviations

AP2/ERF

APETALA2/ETHYLENE-RESPONSIVE FACTOR

CER

ECERIFERUM

KCS

KETOACYLCOA SYNTHASE

MDA

Malondialdehyde

SHN1

WAX INDUCER1 (WIN1)/SHINE1

Notes

Acknowledgements

We would like to thank Prof. Takaya Moriguchi of the National Institute of Fruit Tree Science, Japan, for ‘Orin’ apple calli. We would also like to thank EditorBar Language Editing Company for providing linguistic assistance during the preparation of this manuscript. This study was financially supported by the National Natural Science Foundation of China (31772275) and the Natural Science Fund for Excellent Young Scholars of Shandong Province (ZR2018JL014).

Supplementary material

425_2019_3115_MOESM1_ESM.jpg (6.4 mb)
Supplementary material 1 (JPEG 6553 kb)
425_2019_3115_MOESM2_ESM.jpg (9.2 mb)
Supplementary material 2 (JPEG 9461 kb)
425_2019_3115_MOESM3_ESM.jpg (6.9 mb)
Supplementary material 3 (JPEG 7064 kb)
425_2019_3115_MOESM4_ESM.docx (18 kb)
Supplementary material 4 (DOCX 18 kb)
425_2019_3115_MOESM5_ESM.docx (19 kb)
Supplementary material 5 (DOCX 19 kb)
425_2019_3115_MOESM6_ESM.docx (17 kb)
Supplementary material 6 (DOCX 17 kb)
425_2019_3115_MOESM7_ESM.docx (18 kb)
Supplementary material 7 (DOCX 18 kb)

References

  1. Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127.  https://doi.org/10.1105/tpc.7.12.2115 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16(9):2463–2480.  https://doi.org/10.1105/tpc.104.022897 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  4. An JP, Li HH, Song LQ, Su L, Liu X, You CX, Hao YJ (2016) The molecular cloning and functional characterization of MdMYC2, a bHLH transcription factor in apple. Plant Physiol Bioch 108:24–31.  https://doi.org/10.1016/j.plaphy.2016.06.032 CrossRefGoogle Scholar
  5. Beisson F, Li-Beisson Y, Pollard M (2012) Solving the puzzles of cutinand suberin polymer biosynthesis. Plant Biol 15:329–337.  https://doi.org/10.1016/j.pbi.2012.03.003 CrossRefGoogle Scholar
  6. Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Progin Lipid Res 52(1):110–129.  https://doi.org/10.1016/j.plipres.2012.10.002 CrossRefGoogle Scholar
  7. Blee E, Schuber F (1993) Biosynthesis of cutin monomers: involvement of a lipoxygenase/peroxygenase pathway. Plant J 4:113–123.  https://doi.org/10.1046/j.1365-313X.1993.04010113.x CrossRefGoogle Scholar
  8. Borisjuk N, Hrmova M, Lopato S (2014) Transcriptional regulation of cuticle biosynthesis. Biotechnol Adv 32:526–540.  https://doi.org/10.1016/j.biotechadv.2014.01.005 CrossRefGoogle Scholar
  9. Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101:4706–4711.  https://doi.org/10.1073/pnas.0305574101 CrossRefGoogle Scholar
  10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743.  https://doi.org/10.1046/j.1365-313x.1998.00343.x CrossRefGoogle Scholar
  11. Gao G, Zou J, Zhou X, Liu A, Wei B, Chen X (2010) Tissue speciality and stress responses in expression of three WAX2 homologous genes in rice. Acta Agronomica Sinica 36(8):1336–1341.  https://doi.org/10.3724/SP.J.1006.2010.01336 CrossRefGoogle Scholar
  12. Go YS, Kim H, Kim HJ, Suh MC (2014) Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. Plant Cell 26(4):1666–1680.  https://doi.org/10.1105/tpc.114.123307 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Haslam TM, Haslam R, Thoraval D, Pascal S, Delude C, Domergue F, Kunst L, Fernández AM, Beaudoin F, Napier JA, Joubès J (2015) ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiol 167(3):682–692.  https://doi.org/10.1104/pp.114.253195 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hooker TS, Millar AA, Kunst L (2002) Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol 129(4):1568–1580.  https://doi.org/10.1104/pp.003707 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jeffree CE (1996) Structure and ontogeny of plant cuticle. BIOS Scientific Publishers, Oxford, pp 33–83Google Scholar
  16. Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G, Höfte H, Pauly M, Riechmann JL, Broun P (2007) The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19(4):1278–1294.  https://doi.org/10.1105/tpc.106.047076 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kunst L, Samuels L (2009) Plant cuticles shine: advances in wax biosynthesis and export. Curr Opin Plant Biol 12:721–727.  https://doi.org/10.1016/j.pbi.2009.09.009 CrossRefGoogle Scholar
  18. Lam P, Zhao L, McFarlane HE, Aiga M, Lam V, Hooker TS (2012) RDR1 and SGS3 components of RNA-mediated gene silencing are required for regulation of cuticular wax biosynthesis in developing stems of Arabidopsis. Plant Physiol 159:1385–1395.  https://doi.org/10.1104/pp.112.199646 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Lee SB, Suh MC (2014) Cuticular wax biosynthesis is up-regulated by the MYB94 transcription factor in Arabidopsis. Plant Cell Physiol 56(1):48–60.  https://doi.org/10.1093/pcp/pcu142 CrossRefGoogle Scholar
  20. Lee SB, Go YS, Bae HJ, Park JH, Cho SH, Cho HJ, Suh MC (2009) Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol 150(1):42–54.  https://doi.org/10.1104/pp.109.137745 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lee SB, Kim H, Kim RJ, Suh MC (2014) Overexpression of Arabidopsis MYB96 confers drought resistance in Camelina sativa via cuticular wax accumulation. Plant Cell Rep 33:1535–1546.  https://doi.org/10.1007/s00299-014-1636-1 CrossRefGoogle Scholar
  22. Li Y, Yang S, Wang X, Hu J, Cui L, Huang X, Jiang W (2016) Leaf wax n-alkane distributions in Chinese loess since the Last Glacial Maximum and implications for paleoclimate. Quatern Int 399:190–197.  https://doi.org/10.1016/j.quaint.2015.04.029 CrossRefGoogle Scholar
  23. Lim C, Baek W, Jung J, Kim JH, Lee S (2015) Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 16(7):15251–15270.  https://doi.org/10.3390/ijms160715251 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter WD, Pruitt RE (1997) Developmental Regulation of Cell Interactions in the Arabidopsis fiddlehead-1Mutant: A Role for the Epidermal Cell Wall and Cuticle. Dev Biol 189(2):311–321.  https://doi.org/10.1006/dbio.1997.8671 CrossRefGoogle Scholar
  25. Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59(4):553–564.  https://doi.org/10.1111/j.1365-313X.2009.03892.x CrossRefGoogle Scholar
  26. Millar AA, Kunst L (1997) Very-long-chain fatty acid biosynthesis is controlled through the expression and specificity of the condensing enzyme. Plant J 12:121–131.  https://doi.org/10.1046/j.1365-313X.1997.12010121.x CrossRefGoogle Scholar
  27. Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatt acid condensing enzyme. Plant Cell 11:825–838.  https://doi.org/10.1105/tpc.11.5.825 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mishra MK (1997) Stomatal characteristics at different ploidy levels in Coffea L. Ann Bot 80:689–692.  https://doi.org/10.1006/anbo.1997.0491 CrossRefGoogle Scholar
  29. Nawrath C (2002) The biopolymers cutin and suberin. The Arabidopsis book/American Society of Plant Biologists 1: e0021.  https://doi.org/10.1199/tab.0021 CrossRefGoogle Scholar
  30. Oshima Y, Shikata M, Koyama T, Ohtsubo N, Mitsuda N, Ohme-Takagi M (2013) MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri.  Plant Cell 25(5):1609–1624.  https://doi.org/10.1105/tpc.113.110783 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Park CS, Go YS, Suh MC (2016) Cuticular wax biosynthesis is positively regulated by WRINKLED 4, an AP 2/ERF-type transcription factor. Arabidopsis stems. Plant J 88(2):257–270.  https://doi.org/10.1111/tpj.13248 CrossRefGoogle Scholar
  32. Pil JS, Saet BL, Mi CS, Mi-Jeong P, Young SG, Chung-Mo P (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23:1138–1152.  https://doi.org/10.1105/tpc.111.083485 CrossRefGoogle Scholar
  33. Qi CH, Zhao XY, Jiang H, Zheng PF, Liu HT, Li YY,  Hao YJ (2018) Isolation and functional identification of an apple MdCER1 gene. Plant Cell Tiss Org 1–13.  https://doi.org/10.1007/s11240-018-1504-8 CrossRefGoogle Scholar
  34. Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, Huard C, Blée E, Mongrand S, Domergue F, Roby D (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20:752–767.  https://doi.org/10.1105/tpc.107.054858 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142:866–877.  https://doi.org/10.1104/pp.106.086785 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rowland O, Lee R, Franke R, Schreiber L, Kunst L (2007) The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett 581:3538–3554.  https://doi.org/10.1016/j.febslet.2007.06.065 CrossRefGoogle Scholar
  37. Sajeevan RS, Nataraja KN, Shivashankara KS, Pallavi N, Gurumurthy DS, Shivanna MB (2017) Expression of Arabidopsis SHN1 in Indian mulberry (Morus indica L.) increases leaf surface wax content and reduces post-harvest water loss. Front Plant Sci 8:418.  https://doi.org/10.3389/fpls.2017.00418 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Comm 290:998–1009.  https://doi.org/10.1006/bbrc.2001.6299 CrossRefGoogle Scholar
  39. Seo PJ, Park CM (2011) Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signal Behav 6(7):1043–1045.  https://doi.org/10.4161/psb.6.7.15606 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Shen H, Zhu L, Castillon A, Majee M, Downie B, Huq E (2008) Light-induced phosphorylation and degradation of the negative regulator PHYTOCHROME-INTERACTING FACTOR1 from Arabidopsis depend upon its direct physical interactions with photoactivated phytochromes. Plant Cell 20(6):1586–1602.  https://doi.org/10.1105/tpc.108.060020 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Shi JX, Malitsky S, De Oliveira S, Branigan C, Franke RB, Schreiber L, Aharoni A (2011) SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 7(5):e1001388.  https://doi.org/10.1371/journal.pgen.1001388 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sieber H, Hoffmann C, Kaindl A, Greil P (2000) Biomorphic cellular ceramics. Adv Eng Mater 2(3):105–109. https://doi.org/10.1002/(SICI)1527-2648(200003)2:3<105::AID-ADEM105>3.0.CO;2-PCrossRefGoogle Scholar
  43. Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436.  https://doi.org/10.1016/S1369-5266(02)00289-3 CrossRefGoogle Scholar
  44. Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1(4):2019.  https://doi.org/10.1038/nprot.2006.286 CrossRefGoogle Scholar
  45. Wang ZY, Tian X, Zhao Q, Liu Z, Li X, Ren Y, Bu Q (2018a) The E3 Ligase DROUGHT HYPERSENSITIVE negatively regulates cuticular wax biosynthesis by promoting the degradation of transcription factor ROC4 in rice. Plant Cell 30(1):228–244.  https://doi.org/10.1105/tpc.17.00823 CrossRefGoogle Scholar
  46. Wang TY, Xing JW, Liu X, Yao YY, Hu Z, Peng H, Ni Z (2018b) GCN5 contributes to stem cuticular wax biosynthesis by histone acetylation of CER3 in Arabidopsis. J Exp Bot 69(12):2911–2922.  https://doi.org/10.1093/jxb/ery077 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wang XF, An JP, Liu X, Su L, You CX, Hao YJ (2018c) The nitrate-responsive protein MdBT2 regulates anthocyanin biosynthesis by interacting with the MdMYB1 transcription factor. Plant Physiol 178(2):890–906.  https://doi.org/10.1104/pp.18.00244 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wang T, Xing J, Liu X, Yao Y, Hu Z, Peng H, Xin M, Zhou Y, Ni Z (2018d) GCN5 contributes to stem cuticular wax biosynthesis by histone acetylation of CER3 in Arabidopsis. J Exp Bot 69(12):2911–2922.  https://doi.org/10.1093/jxb/ery077 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang Z, Gurule EE, Brennan TP, Gerold JM, Kwon KJ, Hosmane NN, Kumar MR, Beg SA, Capoferri AA, Ray SC, Ho YC, Hill AL, Siliciano JD, Siliciano RF (2018e) Expanded cellular clones carrying replication-competent HIV-1 persist, wax, and wane. Proc Natl Acad Sci USA 115(11):E2575–E2584.  https://doi.org/10.1073/pnas.1720665115 CrossRefGoogle Scholar
  50. Weng H, Moilina I, Shockey J, Browse J (2010) Organ fusion and defective cuticle function in a lacs1 lacs2 double mutant of Arabidopsis. Planta 231:1089–1100.  https://doi.org/10.1007/s00425-010-1110-4 CrossRefGoogle Scholar
  51. Xu Y, Wu H, Zhao M, Wu W, Xu Y, Gu D (2016) Overexpression of the transcription factors GmSHN1 and GmSHN9 differentially regulates wax and cutin biosynthesis, alters cuticle properties, and changes leaf phenotypes in Arabidopsis. Int J Mol Sci 17(4):587.  https://doi.org/10.3390/ijms17040587 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Yang XP, Zhao HY, Kosma DK, Tomasi P, Dyer JM, Li RJ, Liu XL, Wang ZY, Parsons EP, Jenks MA, Lü S (2017) The acyl desaturase CER17 is involved in producing wax unsaturated primary alcohols and cutin monomers. Plant Physiol 173(2):1109–1124.  https://doi.org/10.1104/pp.16.01956 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689-707.  https://doi.org/10.1111/j.1365-313X.2005.02405.x CrossRefGoogle Scholar
  54. Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646CrossRefGoogle Scholar
  55. Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64:265–278.  https://doi.org/10.1007/s11103-007-9150-2 CrossRefGoogle Scholar
  56. Zhang CL, Mao K, Zhou LJ, Wang GL, Zhang YL, Li YY, Hao YJ (2018) Genome-wide identification and characterization of apple long-chain acyl-CoA synthetases and expression analysis under different stresses. Plant Physiol Biochem 132:320–332.  https://doi.org/10.1016/j.plaphy.2018.09.004 CrossRefGoogle Scholar
  57. Zheng Y, Schumaker KS, Guo Y (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc Natl Acad Sci USA 109(31):12822–12827.  https://doi.org/10.1073/pnas.1202630109 CrossRefGoogle Scholar
  58. Zheng HQ, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17:1467–1481.  https://doi.org/10.1105/tpc.104.030155 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Zhao SJ, Xu CC, Zou Q, Meng QW (1994) Improvements of method for measurement of malondialdehyde in plant tissues. Plant Physiol Commun 30(3):207–210Google Scholar
  60. Zhou LJ, Mao K, Qiao Y, Jiang H, Li YY, Hao YJ (2017) Functional identification of MdPIF1 as a phytochrome interacting factor in apple. Plant Physiol Biochem 119:178–188.  https://doi.org/10.1016/j.plaphy.2017.08.027 CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.National Key Laboratory of Crop Biology, College of Horticulture Science and EngineeringShandong Agricultural UniversityTai-anChina

Personalised recommendations