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Biochemistry & Molecular Biology

A genome-wide survey of homeodomain-leucine zipper genes and analysis of cold-responsive HD-Zip I members’ expression in tomato

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Pages 1337-1349 | Received 28 Nov 2013, Accepted 20 Mar 2014, Published online: 18 Jun 2014

References

  • Mukherjee K, Brocchieri L, Burglin TR. A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol. Biol. Evol. 2009;26:2775–2794.10.1093/molbev/msp201
  • Ariel FD, Manavella PA, Dezar CA, Chan RL. The true story of the HD-Zip family. Trends Plant Sci. 2007;12:419–426.10.1016/j.tplants.2007.08.003
  • Ruberti I, Sessa G, Lucchetti S, Morelli G. A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J. 1991;10:1787–1791.
  • Tron AE, Bertoncini CW, Palena CM, Chan RL, Gonzalez DH. Combinatorial interactions of two amino acids with a single base pair define target site specificity in plant dimeric homeodomain proteins. Nucleic Acids Res. 2001;29:4866–4872.10.1093/nar/29.23.4866
  • Sessa G, Morelli G, Ruberti I. The Athb-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. EMBO J. 1993;12:3507–3517.
  • Chan RL, Gago GM, Palena CM, Gonzalez DH. Homeoboxes in plant development. Biochim. Biophys. Acta. 1998;1442:1–19.10.1016/S0167-4781(98)00119-5
  • Schrick K, Nguyen D, Karlowski WM, Mayer KF. START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 2004;5:R41.10.1186/gb-2004-5-6-r41
  • Ponting CP, Aravind L. START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 1999;24:130–132.10.1016/S0968-0004(99)01362-6
  • Mukherjee K, Bürglin TR. MEKHLA, a novel domain with similarity to PAS domains, is fused to plant homeodomain-leucine zipper III proteins. Plant Physiol. 2006;140:1142–1150.10.1104/pp.105.073833
  • Arce AL, Raineri J, Capella M, Cabello JV, Chan RL. Uncharacterized conserved motifs outside the HD-Zip domain in HD-Zip subfamily I transcription factors; a potential source of functional diversity. BMC Plant Biol. 2011;11:42.10.1186/1471-2229-11-42
  • Hu R, Chi X, Chai G, Kong Y, He G, Wang X, Shi D, Zhang D, Zhou G. Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One. 2012;7:e31149.10.1371/journal.pone.0031149
  • Soderman E, Mattsson J, Engstrom P. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J. 1996;10:375–381.10.1046/j.1365-313X.1996.10020375.x
  • Wang Y, Henriksson E, Söderman E, Henriksson KN, Sundberg E, Engström P. The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev. Biol. 2003;264:228–239.10.1016/j.ydbio.2003.07.017
  • Aoyama T, Dong CH, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua NH. Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell. 1995;7:1773–1785.10.1105/tpc.7.11.1773
  • Hanson J, Johannesson H, Engstro¨m P. Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol. Biol. 2001;45:247–262.10.1023/A:1006464907710
  • Mattsson J, Ckurshumova W, Berleth T. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol. 2003;131:1327–1339.10.1104/pp.013623
  • Barrero JM, Millar AA, Griffiths J, Czechowski T, Scheible WR, Udvardi M, Reid JB, Ross JJ, Jacobsen JV, Gubler F. Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant J. 2010;61:611–622.10.1111/tpj.2010.61.issue-4
  • Johannesson H, Wang Y, Hanson J, Engström P. The arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol. 2003;51:719–729.10.1023/A:1022567625228
  • Himmelbach A, Hoffmann T, Leube M, Höhener B, Grill E. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J. 2002;21:3029–3038.10.1093/emboj/cdf316
  • Valdés AE, Övernäs E, Johansson H, Rada-Iglesias A, Engström P. The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities. Plant Mol. Biol. 2012;80:405–418.10.1007/s11103-012-9956-4
  • Deng X, Phillips J, Bräutigam A, Engström P, Johannesson H, Ouwerkerk PB, Ruberti I, Salinas J, Vera P, Iannacone R, Meijer AH, Bartels D. A homeodomain leucine zipper gene from Craterostigma plantagineum regulates abscisic acid responsive gene expression and physiological responses. Plant Mol. Biol. 2006;61:469–489.10.1007/s11103-006-0023-x
  • Zúñiga-Mayo VM, Marsch-Martínez N, de Folter S. The class II HD-ZIP JAIBA gene is involved in meristematic activity and important for gynoecium and fruit development in Arabidopsis. Plant Signal. Behav. 2012;7:1501–1503.10.4161/psb
  • Bou-Torrent J, Salla-Martret M, Brandt R, Musielak T, Palauqui JC, Martínez-García JF, Wenkel S. ATHB4 and HAT3, two class II HD-ZIP transcription factors, control leaf development in Arabidopsis. Plant Signal. Behav. 2012;7:1382–1387.10.4161/psb
  • Steindler C, Carabelli M, Borello U, Morelli G, Ruberti I. Phytochrome A, phytochrome B and other phytochrome(s) regulate ATHB-2 gene expression in etiolated and green Arabidopsis plants. Plant, Cell Environ. 1997;20:759–763.10.1046/j.1365-3040.1997.d01-123.x
  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature. 2001;411:709–713.10.1038/35079635
  • Green KA, Prigge MJ, Katzman RB, Clark SE. CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell. 2005;17:691–704.10.1105/tpc.104.026179
  • Ohashi-Ito K, Kubo M, Demura T, Fukuda H. Class III homeodomain leucine-zipper proteins regulate xylem cell differentiation. Plant Cell Physiol. 2005;46:1646–1656.10.1093/pcp/pci180
  • Zhong R, Ye ZH. Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol. 2004;45:369–385.10.1093/pcp/pch051
  • Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G. The arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol. 2001;126:643–655.10.1104/pp.126.2.643
  • Abe M, Katsumata H, Komeda Y, Takahashi T. Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development. 2003;130:635–643.10.1242/dev.00292
  • Vernoud V, Laigle G, Rozier F, Meeley RB, Perez P, Rogowsky PM. The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J. 2009;59:883–894.10.1111/tpj.2009.59.issue-6
  • Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell. 1999;11:1217–1226.10.1105/tpc.11.7.1217
  • Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C, Li J, Wang T, Zhang Y, Lu Y, Ye Z. A regulatory gene induces trichome formation and embryo lethality in tomato. Proc. Nat. Acad. Sci. USA. 2012;108:11836–11841.
  • Tomato Genome Consortium. Nature. 2012;485:635–641.
  • Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. Protein identification and analysis tools in the ExPASy server. Methods Mol. Biol. 1999;112:531–552.
  • Yu CS, Lin CJ, Hwang JK. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 2004;13:1402–1406.10.1110/(ISSN)1469-896X
  • 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. 2001;28:2731–2739.
  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–W208.10.1093/nar/gkp335
  • Guo AY, Zhu QH, Chen X, Luo JC. GSDS: a gene structure display server. Hereditas. 2007;29:1023–1026.10.1360/yc-007-1023
  • Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999;27:297–300.10.1093/nar/27.1.297
  • Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E. Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol. 2005;139:509–518.10.1104/pp.105.063461
  • Agalou A, Purwantomo S, Overnäs E, Johannesson H, Zhu X, Estiati A, de Kam RJ, Engström P, Slamet-Loedin IH, Zhu Z, Wang M, Xiong L, Meijer AH, Ouwerkerk PB. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol. Biol. 2008;66:87–103.10.1007/s11103-007-9255-7
  • Zhao Y, Zhou Y, Jiang H, Li X, Gan D, Peng X, Zhu S, Cheng B. Systematic analysis of sequences and expression patterns of drought-responsive members of the HD-Zip gene family in maize. PLoS One. 2011;6:e28488.10.1371/journal.pone.0028488
  • Ciarbelli AR, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, Fruscalzo A, Sessa G, Morelli G, Ruberti I. The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol. Biol. 2008;68:465–478.10.1007/s11103-008-9383-8
  • Mayda E, Tornero P, Conejero V, Vera P. A tomato homeobox gene (HD-zip) is involved in limiting the spread of programmed cell death. Plant J. 1999;20:591–600.10.1046/j.1365-313X.1999.00633.x
  • Bartley GE, Ishida BK. Ethylene-sensitive and insensitive regulation of transcription factor expression during in vitro tomato sepal ripening. J. Exp. Bot. 2007;58:2043–2051.10.1093/jxb/erm075
  • Lin ZF, Hong Y, Yin M, Li C, Zhang K, Grierson D. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant J. 2008;55:301–310.10.1111/tpj.2008.55.issue-2
  • Turchi L, Carabelli M, Ruzza V, Possenti M, Sassi M, Peñalosa A, Sessa G, Salvi S, Forte V, Morelli G, Ruberti I. Arabidopsis HD-Zip II transcription factors control apical embryo development and meristem function. Development. 2013;140:2118–2129.10.1242/dev.092833
  • Meissner R, Theres K. Isolation and characterization of the tomato homeobox gene THOM1. Planta. 1995;195:541–547.
  • Takada S, Takada N, Yoshida A. Induction of epidermal cell fate in Arabidopsis shoots. Plant Signal. Behav. 2013;8:e26236.10.4161/psb
  • Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol. 2009;50:1019–1031.10.1093/pcp/pcp068
  • Takada S, Takada N, Yoshida A. ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development. 2013;140:1919–1923.10.1242/dev.094417
  • Peterson KM, Shyu C, Burr CA, Horst RJ, Kanaoka MM, Omae M, Sato Y, Torii KU. Arabidopsis homeodomain-leucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis. Development. 2013;140:1924–1935.10.1242/dev.090209
  • Nadakuduti SS, Pollard M, Kosma DK, Allen C Jr, Ohlrogge JB, Barry CS. Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiol. 2012;159:945–960.10.1104/pp.112.198374
  • Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J. 2003;33:259–270.10.1046/j.1365-313X.2003.01624.x
  • Stålberg K, Ellerstöm M, Ezcurra I, Ablov S, Rask L. Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta. 1996;199:515–519.
  • Kaplan B, Davydov O, Knight H, Galon Y, Knight MR, Fluhr R, Fromm H. Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis. Plant Cell. 2006;18:2733–2748.10.1105/tpc.106.042713
  • Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK. Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol. 2005;138:341–351.10.1104/pp.104.059147
  • Dunn MA, White AJ, Vural S, Hughes MA. Identification of promoter elements in a low-temperature-responsive gene (blt4.9) from barley (Hordeum vulgare L.). Plant Mol. Biol. 1998;38:551–564.10.1023/A:1006098132352
  • Kim HJ, Kim YK, Park JY, Kim J. Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C-repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J. 2002;29:693–704.10.1046/j.1365-313X.2002.01249.x
  • Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell. 1993;5:1529–1539.10.1105/tpc.5.11.1529
  • Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell. 1997;9:1859–1868.
  • Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, Kim MC, Park CY, Jeong JC, Moon BC, Lee JH, Yoon HW, Lee SH, Chung WS, Lim CO, Lee SY, Hong JC, Cho MJ. Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol. 2004;135:2150–2161.10.1104/pp.104.041442
  • Lijavetzky D, Carbonero P, Vicente-Carbajosa J. Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol. Biol. 2003;3:17.10.1186/1471-2148-3-17
  • Liu Y, Jiang HY, Chen WJ, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z. Genome-wide analysis of the auxin response factor (ARF) gene family in maize (Zea mays). Plant Growth Regul. 2003;63:225–234.
  • Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol. Genet. Genomics. 2012;287:495–513.10.1007/s00438-012-0696-6
  • Van der Hoeven RC, Ronning J Giovannoni, Martin G, Tanksley S. Deductions about the number organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell. 2002;14:1441–1456.10.1105/tpc.010478
  • Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC. Mining EST databases to resolve evolutionary events in major crop species. Genome. 2004;47:868–876.10.1139/g04-047
  • Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell. 2005;17:61–76.10.1105/tpc.104.026161
  • Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T. Characterization of the class IV homeodomain-Leucine zipper gene family in Arabidopsis. Plant Physiol. 2006;141:1363–1375.10.1104/pp.106.077388
  • Jain M, Tyagi AK, Khurana JP. Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J. 2008;275:2845–2861.10.1111/j.1742-4658.2008.06424.x
  • Koonin EV. Orthologs, paralogs, and evolutionary genomics. Annu. Rev. Genet. 2005;39:309–338.10.1146/annurev.genet.39.073003.114725
  • Li WH, Yang J, Gu X. Expression divergence between duplicate genes. Trends Genet. 2005;21:602–607.10.1016/j.tig.2005.08.006
  • Ku HM, Vision T, Liu J, Tanksley SD. Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny. Proc. Nat. Acad. Sci. USA. 2000;97:9121–9126.10.1073/pnas.160271297
  • Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y. Modeling gene and genome duplications in eukaryotes. Proc. Nat. Acad. Sci. USA. 2005;102:5454–5459.10.1073/pnas.0501102102
  • Blanc G, Hokamp K, Wolfe KH. A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res. 2003;13:137–144.10.1101/gr.751803

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