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Apple MdMYC2 reduces aluminum stress tolerance by directly regulating MdERF3 gene

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Abstract

Background and aims

Jasmonate (JA) and ethylene are involved in the regulation of the aluminum (Al)-induced growth inhibition. Although it has been reported that JA enhances Al-induced root-growth inhibition, its role in the regulation of growth interplaying with ethylene is still not well understood. In this study, we investigated the mechanism underlying the effect of apple MdMYC2 transcription factor on Al stress.

Methods

Overexpression lines were used for functional analysis. Real-time quantitative RT-PCR was used to examine the expression level of ethylene responsive genes. ChIP-PCR, EMSA, and Y1H assays were used to test whether MdMYC2-GST fusion protein could directly bind to MdERF3 promoter. Transient transactivation assays in tobacco leave were conducted to confirm whether MdMYC2 positively regulated the expression of MdERF3.

Results

MdMYC2 negatively regulated Al tolerance with up-regulating the expression of ethylene responsive genes. Moreover, MdMYC2 was observed to bind to the promoter of MdERF3, a positive regulator of ethylene biosynthesis, and directly activated its transcription. And applying the antagonist of ethylene biosynthesis, AVG, alleviated MdMYC2-modulated growth inhibition in Al stress.

Conclusions

We consider that MdMYC2 protein directly interacts and promotes the transcript of MdERF3 to affect ethylene biosynthesis, thereby regulating the Al-mediated stress response. Our findings provide a deeper understanding of the crosstalk between JA and ethylene as well as JA-mediated growth inhibition in apple.

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Abbreviations

Al:

Aluminum

ABA:

Abscisic acid

JA:

Jasmonate

SA:

Salicylic acid

ACSs:

ACC synthases

ACOs:

ACC oxidases

COI 1:

CORONATINE INSENSITIVE 1

PIN2:

PIN-FORMED 2

EIN3:

ETHYLENE INSENSITIVE 3

MS:

Murashige and Skoog

IAA:

Indole-3-acetic acid

6-BA:

6-benzylaminopurine

Col-0:

Arabidopsis ecotype Columbia

ORF:

Open reading frame

EMSA:

Electrophoretic mobility shift assay

ChIP-PCR:

Chromatin immunoprecipitation-PCR

References

  • Adams E, Turner J (2010) COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp bot 61:4373–4386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An XH, Tian Y, Chen KQ, Liu XJ, Liu DD, Xie XB, Hao YJ (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant Cell Physiol 56:650–662

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Li X (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, 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 

  • Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environ Exp bot 115:49–57

    Article  CAS  Google Scholar 

  • Daszkowska-Golec A, Szarejko I (2013) Open or close the gate stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916

    Article  CAS  PubMed  Google Scholar 

  • Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Kazan K (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doncheva S, Amenos M, Poschenrieder C, Barcelo J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp bot 56:1213–1220

    Article  CAS  PubMed  Google Scholar 

  • Dong L, Cheng Y, Wu J, Cheng Q, Li W, Fan S, Xu P (2015) Overexpression of GmERF5, a new member of the soybean EAR motif-containing ERF transcription factor, enhances resistance to Phytophthora sojae in soybean. J Exp bot 66:2635–2647

    Article  CAS  PubMed  Google Scholar 

  • Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397

    Article  PubMed  PubMed Central  Google Scholar 

  • Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plan 19:959–987

    Article  CAS  Google Scholar 

  • Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218

    Article  CAS  PubMed  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression–c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jayakannan M, Bose J, Babourina O, Shabala S, Massart A, Poschenrieder C, Rengel Z (2015) The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J Exp bot 66:1865–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant Cell Environ 29:1309–1318

    Article  CAS  PubMed  Google Scholar 

  • Kazan K (2015) Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:219–229

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu rev Plant Biol 46:237–260

    Article  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu rev Plant Biol 55:459–493

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Pineros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu rev of Plant Biol 66:571–598

    Article  CAS  Google Scholar 

  • Kopittke PM, Moore KL, Lombi E, Gianoncelli A, Ferguson BJ, Blamey FPC, Gresshoff PM (2015) Identification of the primary lesion of toxic aluminum in plant roots. Plant Physiol 167:1402–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehotai N, Kolbert Z, Pető A, Feigl G, Ördög A, Kumar D, Erdei L (2012) Selenite-induced hormonal and signalling mechanisms during root growth of Arabidopsis thaliana L. J Exp bot 63:5677–5687

    Article  CAS  PubMed  Google Scholar 

  • Li T, Jiang Z, Zhang L, Tan D, Wei Y, Yuan H, Wang A (2016) Apple (Malus domestica) MdERF2 negatively affects ethylene biosynthesis during fruit ripening by suppressing MdACS1 transcription. Plant J 88:735–748

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int rev Cytol 200:1–46

    Article  CAS  PubMed  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Bba-Biomembranes 1819:86–96

    CAS  PubMed  Google Scholar 

  • Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotox Environ Safe 104:202–208

    Article  CAS  Google Scholar 

  • Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116:409–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo YJ, Park JB, Cho YJ, Jung C, Seo HS, Park SK, Song JT (2010) Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol Cells 30:271–277

    Article  CAS  PubMed  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Zhang XF (2010) The mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen X, Wang Z, Song X, Xu J, Jiang C, Zhao Y, Zhang H (2014) Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Mole Biol 86:303–317

    Article  CAS  Google Scholar 

  • Shi Y, Tian S, Hou L, Huang X, Zhang X, Guo H, Yang S (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-a ARR genes in Arabidopsis. Plant Cell 24:2578–2595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song S, Huang H, Gao H, Wang J, Wu D, Liu X, Xie D (2014) Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell 26:263–279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun P, Tian QY, Zhao MG, Dai XY, Huang JH, Li LH, Zhang WH (2007) Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol 48:1229–1335

    Article  CAS  PubMed  Google Scholar 

  • Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp bot 61:347–356

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Palme K (2011) Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 191:360–375

    Article  CAS  PubMed  Google Scholar 

  • Thao NP, Khan MIR, Thu NBA, Hoang XLT, Asgher M, Khan NA, Tran LS (2015) Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiol 169(1):73–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang F, Cui X, Sun Y, Dong CH (2013) Ethylene signaling and regulation in plant growth and stress responses. Plant Cell rep 32:1099–1109

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Chen X, Ren H, Zhang Z, Zhang H, Wang J, Wang XC, Huang R (2007) ERF protein JERF1 that transcriptionally modulates the expression of abscisic acid biosynthesis-related gene enhances the tolerance under salinity and cold in tobacco. Planta 226:815–825

    Article  CAS  PubMed  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2008) Functions of the ERF transcription factor family in plants. Botany 86:969–977

    Article  CAS  Google Scholar 

  • Yang ZB, He C, Ma Y, Herde M, Ding Z (2016) Jasmonic acid enhances al-induced root-growth inhibition. Plant Physiol. doi:10.1104/pp.16.01756

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp bot 60:3781–3796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Z (2014) Molecular basis for jasmonate and ethylene signal interactions in Arabidopsis. J Exp bot 65:5743–5748

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from Natural Science Foundation of China (31601742), the Ministry of Education of China (IRT15R42), Shandong Province Government (SDAIT-06-03),and Ministry of Agriculture of China (CARS-28).

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Authors and Affiliations

  1. National Key Laboratory of Crop Biology, Tai-An, Shandong, 271018, China

    Jian-Ping An, Ji-Fang Yao, Yi-Ran Ren, Chun-Xiang You, Xiao -Fei Wang & Yu-Jin Hao

  2. MOA Key Laboratory of Horticultural Crop Biology and Germplasm Innovation, Tai-An, Shandong, 271018, China

    Jian-Ping An, Ji-Fang Yao, Yi-Ran Ren, Chun-Xiang You, Xiao -Fei Wang & Yu-Jin Hao

  3. College of Horticulture Science and Engineering, Shandong Agricultural University, Tai-An, Shandong, 271018, China

    Jian-Ping An, Ji-Fang Yao, Yi-Ran Ren, Chun-Xiang You, Xiao -Fei Wang & Yu-Jin Hao

  4. College of Life Science, Shandong Agricultural University, Tai-An, Shandong, 271018, China

    Xiao-Na Wang

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  1. Jian-Ping An
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Correspondence to Xiao -Fei Wang or Yu-Jin Hao.

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Responsible Editor: Juan Barcelo.

Key message

Apple MdMYC2 protein directly binds to the promoter of MdERF3 and activates its transcript to affect ethylene biosynthesis, thereby regulating the Al-mediated stress response.

Electronic supplementary material

Fig. S1

Vector construction and generation of transgenic apple calli (A) Schematic diagram of the 35S promoter: MdMYC2 construct. qRT-PCR analysis of the expression levels of MdMYC2 in transgenic apple calli (B) and transgenic Arabidopsis. (TIFF 239 kb)

High Resolution Image (JPEG 91 kb)

Fig. S2

Effect of various stresses on expression of MdMYC2 and root inhibition assays of MdMYC2-transgenic Arabidopsis (A) qRT-PCR analysis of MdMYC2 expression in response to various stresses such as acid solution (pH 6.0, 5.0, 4.0), LaCl3, CdCl2, and CuCl2 treatments (0, 25, 50 uM) for 6 h. (B) The root-growth phenotypes and (C) primary root lengths in Col-0 and MdMYC2-transgenic Arabidopsis in response to La (2 uM LaCl3) and acid (pH = 4) stresses. The indicated genotypes seedlings were exposed to LaCl3 and acid medium for 7 days. The pH of the control was 6.0. Bar = 1 cm. (TIFF 3379 kb)

High Resolution Image (JPEG 144 kb)

Table S1

Primers used in this paper (DOCX 17 kb)

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An, JP., Wang, XN., Yao, JF. et al. Apple MdMYC2 reduces aluminum stress tolerance by directly regulating MdERF3 gene. Plant Soil 418, 255–266 (2017). https://doi.org/10.1007/s11104-017-3297-7

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