biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 59:253-265, 2015 | DOI: 10.1007/s10535-015-0498-x

Genome-wide identification and characterization of the DREB transcription factor gene family in mulberry

X. Q. Liu1, J. J. Zhu1, C. J. Wei1, Q. Guo1, C. K. Bian1, Z. H. Xiang1, A. C. Zhao1,*
1 State Key Laboratory of Silkworm Genome Biology, Key Laboratory for Sericulture Functional Genomics and Biotechnology of Agricultural Ministry, Southwest University, Chongqing, P.R. China

The dehydration responsive element binding (DREB) transcription factor (TF) family comprises unique and important proteins involved in abiotic stress responses and tolerance in plants. Although DREB TFs have been well identified and characterized in a few model plants, there is no detailed information available for mulberry. In this study, 110 AP2/ERF family genes were identified based on a genome-wide analysis of the Morus genome database. Among them, 30 Morus notabilis DREB family genes (MnDREBs) were identified. A comparative analysis with DREB gene families from other plants suggests that MnDREBs could be divided into six subgroups (A-1 to A-6) and could have similar functions in response to abiotic stresses since they have similar conserved domains/motifs within each subgroup. The expression patterns of MnDREBs were analyzed using transcriptome data of different organs from M. notabilis and the quantitative real-time polymerase chain reaction. The expression of most MnDREBs was detected in different organs and induced by various abiotic stresses, which suggest their vital roles in abiotic stress tolerance.

Keywords: abiotic stress; cold; expression profile; heat; Morus notabilis; salinity; water stress
Subjects: DREB transcription factor; gene expression; temperature - low; temperature - high; salinity; water stress; phylogenetic tree; mulberry

Received: June 9, 2014; Revised: October 27, 2014; Accepted: October 29, 2014; Published: June 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Liu, X.Q., Zhu, J.J., Wei, C.J., Guo, Q., Bian, C.K., Xiang, Z.H., & Zhao, A.C. (2015). Genome-wide identification and characterization of the DREB transcription factor gene family in mulberry. Biologia plantarum, 59(2), 253-265. doi: 10.1007/s10535-015-0498-x
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201502-0007_S1.pdf

    File size: 355.31 kB

    References

    1. Agarwal, P., Agarwal, P.K., Nair, S., Sopory, S.K., Reddy, M.K.: Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. - Mol. Genet. Genomics 277: 189-198, 2007. Go to original source...
    2. Agarwal, P.K., Agarwal, P., Reddy, M.K., Sopory, S.K.: Role of DREB transcription factors in abiotic and biotic stress tolerance in plant. - Plant Cell Rep. 25: 1263-1274, 2006. Go to original source...
    3. Agarwal, P.K., Jha, B.: Transcription factors in plants and ABA dependent and independent abiotic stress signaling. - Biol. Plant. 54: 201-212, 2010. Go to original source...
    4. Akhtar, M., Jaiswal, A., Taj, G., Jaiswal, J.P., Qureshi, M.I., Singh, N.K.: DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. - J. Genet. 91: 385-395, 2012. Go to original source...
    5. Bouaziz, D., Pirrello, J., Ben Amor, H., Hammami, A., Charfeddine, M., Dhieb, A., Bouzayen, M., Gargouri-Bouzid, R.: Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. - Plant Physiol. Biochem. 60: 98-108, 2012. Go to original source...
    6. Boyer, J.S.: Plant Productivity and Environment. - Science 218: 443-448, 1982. Go to original source...
    7. Checker, V.G., Khurana, P.: Molecular and functional characterization of mulberry EST encoding remorin (MiREM) involved in abiotic stress. - Plant Cell Rep. 32: 1729-1741, 2013. Go to original source...
    8. Chen, M., Wang, Q.Y., Cheng, X.G., Xu, Z.S., Li, L.C., Ye, X.G., Xia, L.Q., Ma, Y.Z.: GmDREB2, a soybean DREbinding transcription factor, conferred drought and high-salt tolerance in transgenic plants. - Biochem. biophys. Res. Commun. 353: 299-305, 2007. Go to original source...
    9. Chen, Y., Yang. J., Wang, Z., Zhang, H., Mao, X., Li, C.: Gene structures, classification, and expression models of the DREB transcription factor subfamily in Populus trichocarpa. - Sci. World J. doi.org/10.1155/2013/954640, 2013. Go to original source...
    10. Cui, M., Zhang, W., Zhang, Q., Xu, Z., Zhu, Z., Duan, F., Wu, R.: Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. - Plant Physiol. Biochem. 49: 1384-1391, 2011. Go to original source...
    11. Dong, C.J., Liu, J.Y.: The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. - BMC Plant Biol. 10: 47, 2010. Go to original source...
    12. Dubouzet, J.G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E.G., Miura, S., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K.: OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought, high salt and cold responsive gene expression. - Plant J. 33: 751-763, 2003. Go to original source...
    13. Egawa, C., Kobayashi, F., Ishibashi M., Nakamura, T., Nakamura, C., Takumi, S.: Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. - Genes. Genet. Syst. 81: 77-91, 2006. Go to original source...
    14. Guo, A.Y., Zhu, Q.H., Chen, X., Luo, J.C.: GSDS: a gene structure display server. - Yi Chuan 29: 1023-1026, 2007. Go to original source...
    15. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J.: Plant cellular and molecular responses to high salinity. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 463-499, 2000. Go to original source...
    16. He, N., Zhang, C., Qi, X., Zhao, S., Tao, Y., Yang, G., Lee, T.H., Wang, X., Cai, L., Li, D., Lu, M., Liao, S., Luo, G., He, R., Tan, H., Xu, Y., Li, T., Zhao, A., Jia, L., Fu, Q., Zeng, Q., Gao, C., Ma, B., Liang, J., Wang, X., Shang, J., Song, P., Wu, H., Fan, L., Wang, Q., Shuai, Q., Zhu, J., Wei, C., Zhu-Salzman, K., Jin, D., Wang, J., Liu, T., Yu, M., Tang, C., Wang, Z., Dai, F., Chen, J., Liu, Y., Zhao, S., Lin, T., Zhang, S., Wang, J., Wang, J., Yang, H., Yang, G., Wang, J., Paterson, A.H., Xia, Q., Ji, D.: Draft genome sequence of the mulberry tree Morus notabilis. - Nat. Commun. 4: 2445, 2013. Go to original source...
    17. Huang, G.T., Ma, S.L., Bai, L.P., Zhang, L., Ma, H., Jia, P., Liu, J., Zhong, M., Guo, Z.F.: Signal transduction during cold, salt, and drought stresses in plants. - Mol. Biol. Rep. 39: 969-987, 2012. Go to original source...
    18. Hussain, S.S., Kayani, M.A., Amjad, M.: Transcription factors as tools to engineer enhanced drought stress tolerance in plants. - Biotechnol. Progr. 27: 297-306, 2011. Go to original source...
    19. Hwang, J.E., Lim, C.J., Chen, H., Je, J., Song, C., Lim, C.O.: Overexpression of Arabidopsis dehydration-responsive element-binding protein 2C confers tolerance to oxidative stress. - Mol. Cells 33: 135-140, 2012. Go to original source...
    20. Islam, M.S., Wang, M.H.: Expression of dehydration responsive element-binding protein-3 (DREB3) under different abiotic stresses in tomato. - BMB Rep. 42: 611-616, 2009. Go to original source...
    21. Jaillon, O., Aury, J.M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C., Vezzi, A., Legeai, F., Hugueney, P., Dasilva, C., Horner, D., Mica, E., Jublot, D., Poulain, J., Bruyère, C., Billault, A., Segurens, B., Gouyvenoux, M., Ugarte, E., Cattonaro, F., Anthouard, V., Vico, V., Fabbro, C.D., Alaux, M., Gaspero, G.D., Dumas, V., Felice, N., Paillard, S., Juman, I., Moroldo, M., Scalabrin, S., Canaguier, A., Clainche, I.L., Malacrida, G., Durand, E., Pesole, G., Laucou, V., Chatelet, P., Merdinoglu, D., Delledonne, M., Pezzotti, M., Lecharny, A., Scarpelli, C., Artiguenave, F., Pè, M.E., Valle, G., Morgante, M., Caboche, M., Adam-Blondon, A.F., Weissenbach, J., Quétier, F., Wincker, P.: The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. - Nature 449: 463-467, 2007. Go to original source...
    22. Jofuku, K.D., Den Boer, B.G., Van Montagu, M., Okamuro, J.K.: Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. - Plant Cell 6: 1211-1225, 1994. Go to original source...
    23. Kizis, D., Pages, M.: Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought responsive element in an ABA-dependent pathway. - Plant J. 30: 679-689, 2002. Go to original source...
    24. Lata, C., Prasad, M.: Role of DREBs in regulation of abiotic stress responses in plants. - J. exp. Bot. 62: 4731-4748, 2011. Go to original source...
    25. Lee, S.J., Kang, J.Y., Park, H.J., Kim, H.D., Bae, M.S., Choi, Choi, H.I., Kim, S.Y.: DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsivegene expression, and its overexpression affects abscisic acid sensitivity. - Plant Physiol. 153: 716-727, 2010. Go to original source...
    26. Li, M., Li, Y., Li, H., Wu, G.: Improvement of paper mulberry tolerance to abiotic stresses by ectopic expression of tall fescue FaDREB1. - Tree Physiol. 32: 104-113, 2011a. Go to original source...
    27. Li, M.R., Li, Y., Li, H.Q., Wu, G.J.: Ectopic expression of FaDREB2 enhances osmotic tolerance in paper mulberry. - J. Integr. Plant Biol. 53: 951-960, 2011b. Go to original source...
    28. Lucas, S., Durmaz, E., Akpinar, B.A., Budak, H.: The drought response displayed by a DRE-binding protein from Triticum dicoccoides. - Plant Physiol. Biochem. 49, 346-351, 2011. Go to original source...
    29. Marcolino-Gomes, J., Rodrigues, F.A., Oliveira, M.C., Farias, J.R., Neumaier, N., Abdelnoor, R.V., Marcelino-Guimarães, F.C., Nepomuceno, A.L.: Expression patterns of GmAP2/EREB-like transcription factors involved in soybean responses to water deficit. - PLOS ONE. 8: e62294, 2013. Go to original source...
    30. Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., Shinozaki, K., Yamaguchi-Shinozaki, K.: Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. - Mol. Genet. Genomics 283: 185-196, 2010. Go to original source...
    31. Mayer, K., White, O., Bevan, M., Lemcke, K., Creasy, T.H., Bielke, C., Haas, B., Haase, D., Maiti, R., Rudd, S., Peterson, J., Schoof, H., Frishman, D., Morgenstern, B., Zaccaria, P., Ermolaeva, M., Pertea, M., Quackenbush, J., Volfovsky, N., Wu, D., Lowe, T.M., Salzberg, S.L., Mewes, H.W.: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. - Nature 408: 796-815, 2000. Go to original source...
    32. Nakano, T., Suzuki, K., Fujimura, T., Shinshi, H.: Genomewide analysis of the ERF gene family in Arabidopsis and rice. - Plant Physiol. 140: 411-432, 2006. Go to original source...
    33. Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L.S., Shinozaki, K., Yamaguchi-Shinozaki, K.: Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. - Plant J. 50: 54-69, 2007. Go to original source...
    34. Ramachandra Reddy, A., Chaitanya, K.V., Jutur, P.P., Sumithra, K.: Differential antioxidative responses to water stress among five mulberry (Morus alba L.) cultivars. - Environ. exp. Bot. 52: 33-42, 2004. Go to original source...
    35. Saitou, N., Nei, M.: The neighbor-joining method: a new method for reconstructing phylogenetic trees. - Mol. Biol. Evol. 4: 406-425, 1987.
    36. Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., Yamaguchi-Shinozaki, K.: DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydrationand cold-inducible gene expression. - Biochem. biophys. Res. Commun. 290: 998-1009, 2002. Go to original source...
    37. Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., Shinozaki, K.: Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. - Plant Cell 13: 61-72, 2001. Go to original source...
    38. Sharma, M.K., Kumar, R., Solanke, A.U., Sharma, R., Tyagi, A.K., Sharma, A.K.: Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. - Mol. Genet. Genomics 284: 455-475, 2010. Go to original source...
    39. Sharoni, A.M.1., Nuruzzaman, M., Satoh, K., Shimizu, T., Kondoh, H., Sasaya, T., Choi, I.R., Omura, T., Kikuchi, S.: Gene structures, classification and expression models of the AP2/ERFBP transcripttion factor family in rice. - Plant Cell Physiol. 52: 344-360, 2011. Go to original source...
    40. Shen, Y.G., Zhang, W.K., He, S.J., Zhang, J.S., Liu, Q., Chen, S.Y.: An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. - Theor. appl. Genet. 106: 923-930, 2003. Go to original source...
    41. Singhal, B.K., Khan, M.A., Dhar, A., Baqual, F.M., Bindroo, B.B.: Approaches to industrial exploitation of mulberry (Mulberry sp.) fruits. - J. Fruit Ornam. Plant Res. 18: 83-99, 2010.
    42. Stockinger, E.J., Gilmour, S.J., Thomashow, M.F.: Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. - Proc. nat. Acad. Sci. USA 94: 1035-104, 1997. Go to original source...
    43. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S.: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. - Mol. Biol. Evol. 28: 2731-2739, 2011. Go to original source...
    44. Tang, M., Liu, X., Deng, H., Shen, S.: Over-expression of JcDREB, a putative AP2/EREBP domain-containing transcription factor gene in woody biodiesel plant Jatropha curcas, enhances salt and freezing tolerance in transgenic Arabidopsis thaliana. - Plant Sci. 181: 623-631, 2011. Go to original source...
    45. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G.: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. - Nucl. Acids Res. 25: 4876-4882, 1997. Go to original source...
    46. Tuskan, G.A., Difazio, S., Jansson, S., Bohlmann, J., Grigorive, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, G.L., Cooper, D., Coutinho, P. M., Couturier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Déjardin, A., De Pamphilis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehlting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Hamberger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjärvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leplé, J.C., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montanini, B., Napoli, C., Nelson, D. R., Nelson, C., Nieminen, K., Nilsson, O., Pereda, V., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouzé, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, C.J., Uberbacher, E., Unneberg, P., Vahala, J., Wall, K., Wessler, S., Yang, G., Yin, T., Douglas, C., Marra, M., Sandberg, G., Van de Peer, Y., Rokhsar, D.: The Genome of black cottonwood, Populus trichocarpa (Torr. & Gray). - Science 313: 1596-1604, 2006. Go to original source...
    47. Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S.K., Troggio, M., Pruss, D., Salvi, S., Pindo, M., Baldi, P., Castelletti, S., Cavaiuolo, M., Coppola, G., Costa, F., Cova, V., Ri, A.D., Goremykin, V., Komjanc, M., Longhi, S., Magnago, P., Malacarne, G., Malnoy, M., Micheletti, D., Moretto, M., Perazzolli, M., Si-Ammour, A., Vezzulli, S., Zini, E., Eldredge, G., Fitzgerald, L.M., Gutin, N., Lanchbury, J., Macalma, T., Mitchell, J.T., Reid, J., Wardell, B., Kodira, C., Chen, Z., Desany, B., Niazi, F., Palmer, M., Koepke, T., Jiwan, D., Schaeffer, S., Krishnan, V., Wu, C., Chu, V.T., King, S.T., Vick, J., Tao, Q., Mraz, A., Stormo, A., Stormo, K., Bogden, R., Ederle, D., Stella, A., Vecchietti, A., Kater, M.M., Masiero, S., Lasserre, P., Lespinasse, Y., Allan, A.C., Bus, V., Chagné, D., Crowhurst, R.N., Gleave, A.P., Lavezzo, E., Fawcett, J.A., Proost, S., Rouzé, P., Sterck, L., Toppo, S., Lazzari, B., Hellens, R.P., Durel, C.E., Gutin, A., Bumgarner, R.E., Gardiner, S.E., Skolnick, M., Egholm, M., Van de Peer, Y., Salamini, F., Viola, R.: The genome of the domesticated apple (Malus × domestica Borkh.). - Nat. Genet. 42: 833-839, 2010. Go to original source...
    48. Wei, C., Liu, X., Long, D., Guo, Q., Fang, Y., Bian, C., Zhang, D., Zeng, Q., Xiang, Z., Zhao, A.: Molecular cloning and expression analysis of mulberry MAPK gene family. - Plant Physiol. Biochem. 77C: 108-116, 2014. Go to original source...
    49. Xue, G.P., Loveridge, C.W.: HvDRF1 is involved in abscisic acid mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. - Plant J. 37: 326-339, 2004. Go to original source...
    50. Xue, Y., Wang, Y.Y., Peng, R.H., Zhen, J.L., Zhu, B., Gao, J.J., Zhao, W., Han, H.J., Yao, Q.H.: Transcription factor MdCBF1 gene increases freezing stress tolerance in transgenic Arabidopsis thaliana. - Biol. Plant. 58: 499-506, 2014. Go to original source...
    51. Yu, J., Hu, S., Wang, J., Wong, G.K., Li, S., Liu, B., Deng, Y., Dai, L., Zhou, Y., Zhang, X., Cao, M., Liu, J., Sun, J., Tang, J., Chen, Y., Huang, X., Lin, W., Ye, C., Tong, W., Cong, L., Geng, J., Han, Y., Li, L., Li, W., Hu, G., Huang, X., Li, W., Li, J., Liu, Z., Li, L., Liu, J., Qi, Q., Liu, J., Li, L., Li, T., Wang, X., Lu, H., Wu, T., Zhu, M., Ni, P., Han, H., Dong, W., Ren, X., Feng, X., Cui, P., Li, X., Wang, H., Xu, X., Zhai, W., Xu, Z., Zhang, J., He, S., Zhang, J., Xu, J., Zhang, K., Zheng, X., Dong, J., Zeng, W., Tao, L., Ye, J., Tan, J., Ren, X., Chen, X., He, J., Liu, D., Tian, W., Tian, C., Xia, H., Bao, Q., Li, G., Gao, H., Cao, T., Wang, J., Zhao, W., Li, P., Chen, W., Wang, X., Zhang, Y., Hu, J., Wang, J., Liu, S., Yang, J., Zhang, G., Xiong, Y., Li, Z., Mao, L., Zhou, C., Zhu, Z., Chen, R., Hao, B., Zheng, W., Chen, S., Guo, W., Li, G., Liu, S., Tao, M., Wang, J., Zhu, L., Yuan, L., Yang, H.: A draft sequence of the rice genome (Oryza sativa L. ssp.indica). - Science 296: 79-92, 2002. Go to original source...
    52. Zhao, T., Liang, D., Wang, P., Liu, J., Ma, F.: Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. - Mol. Genet. Genomics 287: 423-436, 2012. Go to original source...
    53. Zhao, T., Xia, H., Liu, G., Ma, F.: The gene family of dehydration responsive element-binding transcription factors in grape (Vitis vinifera): genome-wide identification and analysis, expression profiles, and involvement in abiotic stress resistance. - Mol. Biol. Rep. 41: 1577-1590, 2014. Go to original source...
    54. Zhou, M.L., Ma, J.T., Zhao, Y.M., Wei, Y.H., Tang, Y.X., Wu, Y.M.: Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica. - Gene 506: 10-17, 2012. Go to original source...
    55. Zhu, T., Budworth, P., Han, B., Brown, D., Chang, H.S., Zou, G.Z., Wang, X.: Toward elucidating the global expression patterns of developing Arabidopsis: parallel analysis of 8 300 genes by a high-density oligonucleotide probe array. - Plant Physiol. Biochem. 39: 221-242, 2001. Go to original source...
    56. Zhuang, J., Cai, B., Peng, R.H., Zhu, B., Jin, X.F., Xue, Y., Gao, F., Fu, X.Y., Tian, Y.S., Zhao, W., Qiao, Y.S., Zhang, Z., Xiong, A.S., Yao, Q.H.: Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. - Biochem. biophys. Res. Commun. 371: 468-474, 2008. Go to original source...
    57. Zhuang, J., Peng, R.H., Cheng, Z.M., Zhang, J., Cai, B., Zhang, Z., Gao, F., Zhu, B., Fu, X.Y., Jin, X.F., Chen, J.M., Qiao, Y.S., Xiong, A.S., Yao, Q.H.: Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. - Scientia Hort. 123: 73-81, 2009. Go to original source...

    Return to the content