Skip to main content
Log in

Apple RING finger E3 ubiquitin ligase MdMIEL1 negatively regulates salt and oxidative stresses tolerance

Journal of Plant Biology Aims and scope Submit manuscript

Abstract

RING-finger-containing E3 ubiquitin ligases play important roles in plant response to biotic and abiotoc stresses. In this study, through homology analysis, a Malus× domestica MYB30-Interacting E3 Ligase 1 gene, MdMIEL1, was identified and subsequently cloned from apple ‘Gala’ (Malus×domestica). MdMIEL1 contained a zinc finger domain close to N-terminus and a RING finger domain close to Cterminus. Expression of MdMIEL1 was significantly induced by NaCl and H2O2 treatments. Further study demonstrated that the MdMIEL1-overexpressing Arabidopsis and apple calli were less tolerance to salt stress than wild-type control. In addition, transgenic plants had higher levels of reactive oxygen species (ROS) (H2O2 and O2 ). And transgenic Arabidopsis and apple calli exhibited more sensitive phenotype to H2O2 treatment, which was associated with increased levels of ROS. These findings indicate MdMIEL1 is an important regulator involved in plant response to salt and oxidative stresses tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

References

  • Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plantarum 54:201–212

    Article  CAS  Google Scholar 

  • An XH, Tian Y, Chen KQ, Wang XF, Hao YJ (2012) The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. J Plant Physiol 169(7):710–717

    Article  CAS  PubMed  Google Scholar 

  • Berrocal-Lobo M, Stone S, Yang X, Antico J, Callis J, Ramonell KM, Somerville S (2010) ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin-and NADPH oxidase-mediated defense responses. Plos One 5(12):e14426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai G, Wang G, Wang L, Liu Y, Pan J, Li D (2014) A maize mitogenactivated protein kinase kinase, ZmMKK1, positively regulated the salt and drought tolerance in transgenic Arabidopsis. J Plant Physiol 171(12):1003–1016

    Article  CAS  PubMed  Google Scholar 

  • Chawla S, Jain S, Jain V (2013) Salinity induced oxidative stress and antioxidant system in salt-tolerant and salt-sensitive cultivars of rice (Oryza sativa L.). J Plant Biochem Biot 22(1):27–34

    Article  CAS  Google Scholar 

  • Cheng MC, Hsieh EJ, Chen JH, Chen HY, Lin TP (2012) Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol 158(1):363–375

    Article  CAS  PubMed  Google Scholar 

  • Clough S, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Biochemistry-US 78(1):399

    Article  CAS  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. P Natl Acad Sci USA 103(21):8281–8286

    Article  CAS  Google Scholar 

  • Fang H, Meng Q, Xu J, Tang H, Tang S, Zhang H, Huang J (2015) Knock-down of stress inducible OsSRFP1 encoding an E3 ubiquitin ligase with transcriptional activation activity confers abiotic stress tolerance through enhancing antioxidant protection in rice. Plant Mol Biol 87(4-5):441–458

    Article  CAS  PubMed  Google Scholar 

  • Guo L, Nezames CD, Sheng L, Deng X, Wei N (2013) Cullin-RING ubiquitin ligase family in plant abiotic stress pathways. J Integr Plant Biol 55:21–30

    Article  CAS  PubMed  Google Scholar 

  • Hahn A, Kilian J, Mohrholz A, Ladwig F, Peschke F, Dautel R, Harter K, Berendzen KW, Wanke D (2013) Plant core environmental stress response genes are systemically coordinated during abiotic stresses. Int J Mol Sci 14:7617–7641

    Article  PubMed  PubMed Central  Google Scholar 

  • Hellmann H, Estelle M (2002) Plant development: regulation by protein degradation. Science 297:793–797

    Article  CAS  PubMed  Google Scholar 

  • Hernandez JA, Olmos E, Corpas FJ, Sevilla F, Del Rio LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105(2):151–167

    Article  CAS  Google Scholar 

  • Huang Y, Li CY, Pattison DL, Gray WM, Park S, Gibson SI (2010) SUGAR-INSENSITIVE3, a RING E3 ligase, is a new player in plant sugar response. Plant Physiol 152(4):1889–1900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang XS, Wang W, Zhang Q, Liu JH (2013) A basic helix-loophelix transcription factor, PtrbHLH, of poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol 162(2):1178–1194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SJ, Kim WT (2013) Suppression of Arabidopsis RING E3 ubiquitin ligase AtATL78 increases tolerance to cold stress and decreases tolerance to drought stress. FEBS Lett 587(16): 2584–2590

    Article  CAS  PubMed  Google Scholar 

  • Lee HK, Cho SK, Son O, Xu Z, Hwang I, Kim WT (2009) Drought stress-induced Rma1H1, a RING membrane-anchor E3 ubiquitin ligase homolog, regulates aquaporin levels via ubiquitination in transgenic Arabidopsis plants. Plant Cell 21(2):622–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Wu B, Yu Y, Yang G, Wu C, Zheng C (2011) Genome-wide analysis of the RING finger gene family in apple. Mol Genet Genomics 286(1):81–94

    Article  CAS  PubMed  Google Scholar 

  • Lim SD, Hwang JG, Jung CG, Hwang SG, Moon JC, Jang CS (2013a) Comprehensive analysis of the rice RING E3 ligase family reveals their functional diversity in response to abiotic stress. DNA Res 20:299–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim SD, Cho HY, Park YC, Ham DJ, Lee JK, Jang CS (2013b) The rice RING finger E3 ligase, OsHCI1, drives nuclear export of multiple substrate proteins and its heterogeneous overexpression enhances acquired thermotolerance. J Exp Bot ert 143

  • Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhang C, Wei C, Liu X, Wang M, Yu F, Tu J (2016) The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170(1):429–443

    Article  CAS  PubMed  Google Scholar 

  • Mafakheri A, Siosemardeh A, Bahramnejad B, Struik PC, Sohrabi Y (2010) Effect of drought stress on yield, proline and chlorophyll contents in three chickpea cultivars. Aust J Crop Sci 4(8):580

    CAS  Google Scholar 

  • Marino D, Froidure S, Canonne J, Khaled SB, Khafif M, Pouzet C, Rivas S (2013) Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nat Commun 4:1476

    Article  PubMed  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zincfinger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. P Natl Acad Sci USA 101:6309–6314

    Article  CAS  Google Scholar 

  • Nakashima K, Tran LS, 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 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Ning YS, Jantasuriyarat C, Zhao QZ, Zhang HW, Chen SB, Liu JL, Liu LJ, Tang SY, Park CH, Wang XJ, Liu XL, Dai LY, Xie Q, Wang GL (2011) The SINA E3 ligase OsDIS1 negatively regulates drought response in rice. Plant Physiol 157:242–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Li D (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235(4):661–676

    Article  CAS  PubMed  Google Scholar 

  • Qin F, Sakuma Y, Tran LSP, Maruyama K, Kidokoro S, Fujita Y, Tanokura M (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20(6):1693–1707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50(1):2–18

    Article  CAS  PubMed  Google Scholar 

  • Ryu MY, Cho SK, Kim WT (2010) The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress. Plant Physiol 154(4):1983–1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  PubMed  Google Scholar 

  • Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiologica mechanisms underlying OsNAC5-dependent tolerance of ric plants to abiotic stress. Planta 234:331–345

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, van Ooijen G (2014) Circadian redox signaling in plant immunity and abiotic stress. Antioxid Redox Sign 20:3024–3039

    Article  CAS  Google Scholar 

  • Stone SL, Callis J (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol 10(6):624–632

    Article  CAS  PubMed  Google Scholar 

  • Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Biol 61:2807–2818

    CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plantarum 126:45–51

    Article  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Salvi S (2010) The genome of the domesticated apple (Malus×domestica Borkh.). Nature Genetics 42(10):833–839

    Article  CAS  PubMed  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Bio 10:385–397

    Article  CAS  Google Scholar 

  • Yang L, Liu Q, Liu Z, Yang H, Wang J, Li X, Yang Y (2016) Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling. J Integr Plant Biol 58(1):67–80

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Qi Y, Liu M, Yang C (2013) SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana. J Integr Plant Biol 55:83–95

    Article  CAS  PubMed  Google Scholar 

  • Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of saltstressed cucumber (Cucumis sativus L.). Plant Sci 167(3):527–533

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xiao-Fei Wang or Yu-Jin Hao.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

An, JP., Liu, X., Song, LQ. et al. Apple RING finger E3 ubiquitin ligase MdMIEL1 negatively regulates salt and oxidative stresses tolerance. J. Plant Biol. 60, 137–145 (2017). https://doi.org/10.1007/s12374-016-0457-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0457-x

Keywords

Navigation