Abstract
Alcohol acyltransferase (AAT) plays an important role in ester biogenesis in ripening fruit. In apple, MdAAT2 is up-regulated in response to treatment with defense-related hormones. We cloned a novel MdAAT2 promoter via thermal asymmetric interlaced PCR (TAIL-PCR). Sequence analysis indicated the presence of salicylic acid (SA)- and methyl jasmonate (MeJA)-responsive elements in the promoter region. To examine further the operational mechanism for transcription factors (TFs) in regulating expression of the MdAAT2 promoter, we isolated and investigated six potential stress-induced TFs — MdMYB1, MdMYB2, MdMYB6, MdERF1, MdERF2, and WRKY. These were monitored during various stages of fruit development as well as under several hormonal treatments. Reverse transcription-polymerase chain reaction (RT-PCR) analysis showed that all of these TF genes, as well as MdAAT2, were detectable in the stigmas. Levels of expression by MdMYB1, MdMYB2, and MdERF1 were significantly correlated with that by MdAAT2 during fruit ontogeny. Moreover, transcription of three TFs (MdMYB1, MdMYB6, and MdERF1) was significantly correlated with that of MdAAT2 upon exposure to ethephon, SA, or MeJA. Sequence analysis demonstrated that CAAT, CCAAT elements, and several MYB transcription factor binding sites (CNGTTmotif, AACCA, and CTAACCA elements) existed in the MdAAT2 promoter region. Using that analysis, we performed modeling of MdMYB1 and MdMYB6 based on PROTEINDNA complex1 and complex3 (PDB Accession Numbers 1H88 and 1H8A). There, similarities were found with the protein complex of CAAT or CCAAT consensus sequences. Thus, we propose that two TFs — MdMYB1 and MdMYB6 — are directly or indirectly involved in the activation of MdAAT2 expression in apple fruit.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aharoni A, Keizer LC, Bouwmeester HJ, Sun Z, Alvarez-Huerta M, Verhoeven HA, Blaas J, van Houwelingen AM, De Vos RC, van der Voet H, Jansen RC, Guis M, Mol J, Davis RW, Schena M, van Tunen AJ, O’Connell AP (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12:647–662
Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen FW, Bouwmeester HJ, Aharoni A (2004) Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiol 135:1865–1878
Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132:1020–1032
Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Reptr 11:113–116
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574
Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5:e1000440
Defilippi BG, Dandekar AM, Kader AA (2005a) Relationship of ethylene biosynthesis to volatile production, related enzymes, and precursor availability in apple peel and flesh tissues. J Agric Food Chem 53:3133–3141
Defilippi BG, Kader AA, Dandekar AM (2005b) Apple aroma: alcohol acyltransferase, a rate limiting step for ester biosynthesis, is regulated by ethylene. Plant Sci 168:1199–1210
Dixon J, W Hewett E (2000) Factors affecting apple aroma/flavour volatile concentration:a review. New Zealand Journal of Crop and Horticultural Science 28:155–173
Echeverría G, Graell J, López ML, Feldbrugge M, Sprenger M, Hahlbrock K, Weisshaar B (1997) PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J 11:1079–1093
Fellman JK, Miller TW, Mattinson DS (2000) Factors that influence biosynthesis of volatile flavor compounds in apple fruits. Hort Science 35:1026–1033
Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404
Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49
Hong JK, Hwang BK (2006) Promoter activation of pepper class II basic chitinase gene, CAChi2, and enhanced bacterial disease resistance and osmotic stress tolerance in the CAChi2-overexpressing Arabidopsis. Planta 223:433–448
Kim CY, Ahn YO, Kim SH, Kim YH, Lee HS, Catanach AS, Jacobs JM, Conner AJ, Kwak SS (2010) The sweet potato IbMYB1 gene as a potential visible marker for sweet potato intragenic vector system. Physiol Plant
Li D, Shen J, Wu T, Xu Y, Zong X, Li D, Shu H (2008) Overexpression of the apple alcohol acyltransferase gene alters the profile of volatile blends in transgenic tobacco leaves. Physiol Plant 134:394–402
Li D, Xu Y, Xu G, Gu L, Li D, Shu H (2006a) Molecular cloning and expression of a gene encoding alcohol acyltransferase (MdAAT2) from apple (cv. Golden Delicious). Phytochemistry 67:658–667
Li DP, Xu YF, Sun LP, Liu LX, Hu XL, Li DQ, Shu HR (2006b) Salicylic acid, ethephon, and methyl jasmonate enhance ester regeneration in 1-MCP-treated apple fruit after long-term cold storage. J Agric Food Chem 54:3887–3895
Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylatemediated signals in plant defense. Plant Cell 16:319–331
Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15:165–178
Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiol 149:851–862
Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46:984–1008
Memelink J (2009) Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560–1570
Olıas R, Perez AG, Sanz C (2002) Catalytic properties of alcohol acyltransferase in different strawberry species and cultivars. J Agric Food Chem 50:4031–4036
Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003a) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754
Patzlaff A, Newman LJ, Dubos C, Whetten RW, Smith C, McInnis S, Bevan MW, Sederoff RR, Campbell MM (2003b) Characterisation of Pt MYB1, an R2R3-MYB from pine xylem. Plant Mol Biol 53:597–608
Qin X, Zheng X, Shao C, Gao J, Jiang L, Zhu X, Yan F, Tang L, Xu Y, Chen F (2009) Stress-induced curcin-L promoter in leaves of Jatropha curcas L. and characterization in transgenic tobacco. Planta 230:387–395
Ren CM, Zhu Q, Gao BD, Ke SY, Yu WC, Xie DX, Peng W (2008) Transcription factor WRKY70 displays important but no indispensable roles in jasmonate and salicylic acid signaling. J Integr Plant Biol 50:630–637
Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523
Shalit M, Guterman I, Volpin H, Bar E, Tamari T, Menda N, Adam Z, Zamir D, Vainstein A, Weiss D, Pichersky E, Lewinsohn E (2003) Volatile ester formation in roses. Identification of an acetylcoenzyme A. Geraniol/Citronellol acetyltransferase in developing rose petals. Plant Physiol 131:1868–1876
St-Pierre B, DeLuca V (2000) Evolution of acyltransferase genes: origin and diversification of the BAHD superfamily of acyltransferases involved in secondary metabolism. Elsevier Science Ltd., Oxford, UK (34):285–315
Takos AM, Jaffe FW, Jacob SR, Bogs J, Robinson SP, Walker AR (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol 142:1216–1232
Ulker B, Shahid Mukhtar M, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226:125–137
Wang A, Tan D, Takahashi A, Li TZ, Harada T (2007) MdERFs, two ethylene-response factors involved in apple fruit ripening. J Exp Bot 58:3743–3748
Wyllie SG, Fellman JK (2000) Formation of volatile branched chain esters in bananas (Musa sapientum L.). J Agric Food Chem 48:3493–3496
Yang XY, Li JG, Pei M, Gu H, Chen ZL, Qu LJ (2007) Over-expression of a flower-specific transcription factor gene AtMYB24 causes aberrant anther development. Plant Cell Rep 26:219–228
Yang Y, Klessig DF (1996) Isolation and characterization of a tobacco mosaic virus-inducible myb oncogene homolog from tobacco. Proc Natl Acad Sci USA 93:14972–14977
Rights and permissions
About this article
Cite this article
Li, Q., Shen, J., Li, P. et al. Correlations among six hormone-induced transcription factors and the alcohol acyltransferase gene in apple. J. Plant Biol. 55, 290–297 (2012). https://doi.org/10.1007/s12374-011-0261-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-011-0261-6