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A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members

Plant Molecular Biology volume 66, pages 87–103 (2008)Cite this article

Abstract

The homeodomain leucine zipper (HD-Zip) genes encode transcription factors that have diverse functions in plant development and have often been implicated in stress adaptation. The HD-Zip genes are the most abundant group of homeobox (HB) genes in plants and do not occur in other eukaryotes. This paper describes the complete annotation of the HD-Zip families I, II and III from rice and compares these gene families with Arabidopsis in a phylogeny reconstruction. Orthologous pairs of rice and Arabidopsis HD-Zip genes were predicted based on neighbour joining and maximum parsimony (MP) trees with support of conserved intron–exon organization. Additionally, a number of HD-Zip genes appeared to be unique to rice. Searching of EST and cDNA databases and expression analysis using RT-PCR showed that 30 out of 31 predicted rice HD-Zip genes are expressed. Most HD-Zip genes were broadly expressed in mature plants and seedlings, but others showed more organ specific patterns. Like in Arabidopsis and other dicots, a subset of the rice HD-Zip I and II genes was found to be regulated by drought stress. We identified both drought-induced and drought-repressed HD-Zip genes and demonstrate that these genes are differentially regulated in drought-sensitive versus drought-tolerant rice cultivars. The drought-repressed HD-Zip family I gene, Oshox4, was selected for promoter-GUS analysis, showing that drought-responsiveness of Oshox4 is controlled by the promoter and that Oshox4 expression is predominantly vascular-specific. Loss-of-function analysis of Oshox4 revealed no specific phenotype, but overexpression analysis suggested a role for Oshox4 in elongation and maturation processes.

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Abbreviations

Athb:

Arabidopsis thaliana homeobox

CNA:

CORONA

DAF:

Days after flowering

EST:

Expressed sequence tag

HB:

Homeobox

HD:

Homeodomain

HD-Zip:

Homeodomain-leucine zipper

MP:

Maximum parsimony

NJ:

Neighbour-joining

Oshox:

Oryza sativa homeobox gene

PCR:

Polymerase chain reaction

PHB:

PHABULOSA

PHV:

PHAVOLUTA

REV:

REVOLUTA

RT:

Reverse transcription

RWC:

Relative water content

Zip:

Leucine zipper

References

  • Abe M, Katsumata H, Komeda Y, Takahashi T (2003) Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130:635–643

    PubMed  Article  CAS  Google Scholar 

  • Aoyama T, Dong C, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua N (1995) Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell 7:1773–1785

    PubMed  Article  CAS  Google Scholar 

  • Araus JL, Slafer GA, Reynolds MP, Royo C (2002) Plant breeding and drought in C3 cereals: what should we breed for? Ann Bot 89:925–940

    PubMed  Article  Google Scholar 

  • Aso K, Kato M, Banks JA, Hasebe M (1999) Characterization of homeodomain-leucine zipper genes in the fern Ceratopteris richardii and the evolution of the homeodomain-leucine zipper gene family in vascular plants. Mol Biol Evol 16:544–552

    PubMed  CAS  Google Scholar 

  • Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121:4171–4182

    PubMed  CAS  Google Scholar 

  • Byrne ME (2006) Shoot meristem function and leaf polarity: the role of class III HD-ZIP genes. Plos Genet 2:785–790

    Article  CAS  Google Scholar 

  • Carabelli M, Sessa G, Baima S, Ruberti I (1993) The Arabidopsis Athb-2 and -4 genes are strongly regulated by far-red-rich light. Plant J 4:469–479

    PubMed  Article  CAS  Google Scholar 

  • Carabelli M, Morelli G, Whitelam G, Ruberti I (1996) Twilight-zone and canopy shade induction of the ATHB-2 homeobox gene in green plants. Proc Natl Acad Sci USA 93:3530–3535

    PubMed  Article  CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant response to drought: from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Deng X, Phillips J, Meijer AH, Salamini F, Bartels D (2002) Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. Plant Mol Biol 49:601–610

    PubMed  Article  CAS  Google Scholar 

  • Deng X, Phillips J, Bräutigam A, Engström P, Johannesson H, Meijer AH, Ouwerkerk PBF, Ruberti I, Salinas J, Vera P, Iannacone R, Bartels D (2006) A homeodomain leucine zipper gene from Craterostigma plantagineum regulates abscisic acid responsive gene expression and physiological responses. Plant Mol Biol 61:469–489

    PubMed  Article  CAS  Google Scholar 

  • Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14:429–440

    PubMed  Article  CAS  Google Scholar 

  • Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10:393–402

    PubMed  Article  CAS  Google Scholar 

  • Frank W, Phillips J, Salamini F, Bartels D (1998) Two dehydrationinducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J 15:413–421

    PubMed  Article  CAS  Google Scholar 

  • Gago GM, Almoguera C, Jordano J, Gonzales DH, Chan RL (2002) Hahb-4, a homeobox-leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower. Plant Cell Environ 25:633–640

    Article  CAS  Google Scholar 

  • Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun WL, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L ssp japonica). Science 296:79–92

    Article  Google Scholar 

  • Green KA, Prigge MJ, Katzman RB, Clark SE (2005) CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17:691–704

    PubMed  Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harrison CJ, Langdale JA (2006) A step by step guide to phylogeny reconstruction. Plant J 45:561–572

    PubMed  Article  CAS  Google Scholar 

  • Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139:509–518

    PubMed  Article  CAS  Google Scholar 

  • Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E (2002) Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J 21:3029–3038

    PubMed  Article  CAS  Google Scholar 

  • Hjellström M, Olsson ASB, Engström P, Söderman EM (2003) Constitutive expression of the water deficit-inducible homeobox gene ATHB7 in transgenic Arabidopsis causes a suppression of stem elongation growth. Plant Cell Environ 26:1127–1136

    Article  Google Scholar 

  • Hülskamp M, Misa S, Jurgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566

    PubMed  Article  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  CAS  Google Scholar 

  • Ito M, Sentoku N, Nishimura A, Hong SK, Sato Y, Matsuoka M (2002) Position dependent expression of GL2-type homeobox gene, Roc1: significance for protoderm differentiation and radial pattern formation in early rice embryogenesis. Plant J 29:497–507

    PubMed  Article  CAS  Google Scholar 

  • Jantasuriyarat C, Gowda M, Haller K, Hatfield J, Lu G, Stahlberg E, Zhou B, Li H, Kim H, Yu Y, Dean RA, Wing RA, Soderlund C, Wang GL (2005) Large-scale identification of expressed sequence tags involved in rice and rice blast fungus interaction. Plant Physiol 138:105–115

    PubMed  Article  Google Scholar 

  • Johannesson H, Wang Y, Engström P (2001) DNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. Plant Mol Biol 45:63–73

    PubMed  Article  CAS  Google Scholar 

  • Kawahara R, Komamine A, Fukuda H (1995) Isolation and characterization of homeobox-containing genes of carrot. Plant Mol Biol 27:155–164

    PubMed  Article  CAS  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–906

    PubMed  Article  CAS  Google Scholar 

  • Kikuchi S et al (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379

    PubMed  Article  Google Scholar 

  • Khaled AS, Vernoud V, Ingram GC, Perez P, Sarda X, Rogowsky PM (2005) Engrailed-ZmOCL1 fusions cause a transient reduction of kernel size in maize. Plant Mol Biol 58:123–139

    PubMed  Article  CAS  Google Scholar 

  • Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Masahiro YM (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci USA 104:1424–1429

    PubMed  Article  CAS  Google Scholar 

  • Lee YH, Chun JY (1998) A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol Biol 37:377–384

    PubMed  Article  CAS  Google Scholar 

  • Lee YH, Oh HS, Cheon CI, Hwang IT, Kim YJ, Chun JY (2001) Structure and expression of the Arabidopsis thaliana homeobox gene Athb-12. Biochem Biophys Res Commun 284:133–141

    PubMed  Article  CAS  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    PubMed  Article  CAS  Google Scholar 

  • Levitt J (1972) Responses of plants to environmental stresses. Academic Press, New York

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the \( {\text{2}}^{{ - \Updelta \Updelta {\text{C}}_{{\text{T}}} }} \) method. Methods 25:402–408

    PubMed  Article  CAS  Google Scholar 

  • Lu P, Porat R, Nadeau JA, O’Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8:2155–2168

    PubMed  Article  CAS  Google Scholar 

  • Manavella PA, Arce AL, Dezar CA, Bitton F, Renou FP, Crespi M, Chan RL (2006) Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor. Plant J 48:125–137

    PubMed  Article  CAS  Google Scholar 

  • Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW (1996) The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122:1253–1260

    PubMed  CAS  Google Scholar 

  • Mattsson J, Soderman E, Svenson M., Borkird C, Engstrom P (1992) A new homeobox-leucine zipper gene from Arabidopsis thaliana. Plant Mol Biol 18:1019–1022

    PubMed  Article  CAS  Google Scholar 

  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    PubMed  Article  CAS  Google Scholar 

  • Meijer AH, Scarpella E, van Dijk EL, Qin L, Taal AJ, Rueb S, Harrington SE, McCouch SR, Schilperoort RA, Hoge JHC (1997) Transcriptional repression by Oshox1, a novel homeodomain leucine zipper protein from rice. Plant J 11:263–276

    PubMed  Article  CAS  Google Scholar 

  • Meijer AH, de Kam RJ, d’Erfurth I, Shen W, Hoge JHC (2000) HD-Zip proteins of families I and II from rice: interactions and functional properties. Mol Gen Genet 263:12–21

    PubMed  Article  CAS  Google Scholar 

  • Memelink J, Swords KMM, Staehelin LA, Hoge JHC (1994) Southern, Northern and Western blot analysis In: Gelvin SB, Schilperoort RA (eds) Plant molecular biology manual. Kluwer Academic Publishers, Dordrecht, pp F1–F23

    Google Scholar 

  • Morelli G, Ruberti I (2002) Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci 7:399–404

    PubMed  Article  CAS  Google Scholar 

  • Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T (2006) Characterization of the class IV homeodomain-leucine zipper gene family in Arabidopsis. Plant Physiol 141:1363–1375

    PubMed  Article  CAS  Google Scholar 

  • Ohashi Y, Oka A, Ruberti I, Morelli G, Aoyama T (2002) Entopically additive expression of GLABRA2 alters the frequency and spacing of trichome initiation. Plant J 29:359–369

    PubMed  Article  CAS  Google Scholar 

  • Ohgishi OM, Oka A, Morelli G, Ruberti I, Aoyama T (2001) Negative autoregulation of the Arabidopsis homeobox gene ATHB-2. Plant J 25:389–398

    PubMed  Article  CAS  Google Scholar 

  • Olsson ASB, Engström P, Söderman E (2004) The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 55:663–677

    PubMed  Article  CAS  Google Scholar 

  • Ponting CP, Aravind L (1999) START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem Sci 24:130–132

    PubMed  Article  CAS  Google Scholar 

  • Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clarka SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61–76

    PubMed  Article  CAS  Google Scholar 

  • Ratcliffe OJ, Riechmann JL, Zhang JZ (2000) INTERFASCICULAR FIBERLESS1 is the same gene as REVOLUTA. Plant Cell 12:315–317

    PubMed  Article  CAS  Google Scholar 

  • Reddy AR, Ramakrishna W, Sekhar AC, Ithal N, Babu PR, Bonaldo MF, Soares MB, Bennetzen JL (2002) Novel genes are enriched in normalized cDNA libraries from drought-stressed seedlings of rice (Oryza sativa L. subsp. indica cv. Nagina 22). Genome 45:204–211

    PubMed  Article  CAS  Google Scholar 

  • Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399

    PubMed  Article  CAS  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    PubMed  Article  CAS  Google Scholar 

  • Ruberti I, Sessa G, Lucchetti S, Morelli G (1991) A novel class of plant proteins containing a homeodomain with a closely linked leucine zipper motif. EMBO J 10:1787–1791

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sakakibara K, Nishiyama T, Kato M, Hasebe M (2001) Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Mol Biol Evol 18:491–502

    PubMed  CAS  Google Scholar 

  • Sawa S, Ohgishi M, Goda H, Higuchi K, Shimada Y, Yoshida S, Koshiba T (2002) The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin inducible gene by DNA microarray screening, affects auxin response in Arabidopsis. Plant J 32:1011–1022

    PubMed  Article  CAS  Google Scholar 

  • Scarpella E, Rueb S, Boot KJM, Hoge JHC, Meijer AH (2000) A role for the rice homeobox gene Oshox1 in provascular cell fate commitment. Development 127:3655–3669

    PubMed  CAS  Google Scholar 

  • Scarpella E, Boot KJM, Rueb S, Meijer AH (2002) The procambium specification gene Oshox1 promotes polar auxin transport capacity and reduces its sensitivity towards inhibition. Plant Physiol 130:1349–1360

    PubMed  Article  CAS  Google Scholar 

  • Scarpella E, Rueb S, Meijer AH (2003) The RADICLELESS1 gene is required for vascular pattern formation in rice. Development 130:645–658

    PubMed  Article  CAS  Google Scholar 

  • Schena M, Davis RW (1992) HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89:3894–3898

    PubMed  Article  CAS  Google Scholar 

  • Schena M, Davis RW (1994) Structure of homeobox-leucine zipper genes suggests a model for the evolution of gene families. Proc Natl Acad Sci USA 91:8393–8397

    PubMed  Article  CAS  Google Scholar 

  • Schena M, Lloyd AM, Davis RW (1993) The HAT4 gene of Arabidopsis encodes a developmental regulator. Genes Dev 7:367–379

    PubMed  Article  CAS  Google Scholar 

  • Schrick K, Nguyen D, Karlowski WM, Mayer KF (2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol 5:R41

    PubMed  Article  Google Scholar 

  • Sessa G, Morelli G, Ruberti I (1993) The Athb-1 and -2 HD-Zip domains homodimerize, forming complexes of different DNA binding specifcities. EMBO J 12:3507–3517

    PubMed  CAS  Google Scholar 

  • Sessa G, Carabelli M, Ruberti I (1994) Identification of distinct families of HD-Zip proteins in Arabidopsis thaliana. In: Coruzzi GP (ed) Plant molecular biology. Springer-Verlag, Berlin, pp 412–426

    Google Scholar 

  • Sessa G, Steindler C, Morell G, Ruberti I (1998) The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609–622

    PubMed  Article  CAS  Google Scholar 

  • Söderman E, Mattsson J, Svenson M, Borkird C, Engström P (1994) Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana. Plant Mol Biol 26:145–154

    PubMed  Article  Google Scholar 

  • Söderman E, Mattsson J, Engström P (1996) The Arabidopsis homeobox gene Athb-7 is induced by water deficit and by abscisic acid. Plant J 10:375–381

    PubMed  Article  Google Scholar 

  • Söderman E, Hjellström M, Fahleson J, Engström P (1999) The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Mol Biol 40:1073–1083

    PubMed  Article  Google Scholar 

  • Steindler C, Matteucci A, Sessa G, Weimar T, Ohgishi M, Aoyama T, Morelli G, Ruberti I (1999) Shade avoidance responses are mediated by the ATHB-2 HD-Zip protein, a negative regulator of gene expression. Development 126:4235–4245

    PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (*and other methods). Version 4 Sinauer Associates, Sunderland

  • Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    PubMed  Article  CAS  Google Scholar 

  • Turner NC (1986) Crop water deficits: a decade of progress. Adv Agron 39:1–51

    Article  Google Scholar 

  • Wang Y, Henriksson E, Söderman E, Henriksson NK, Sundberg E, Engström P (2003) The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev Biol 264:228–239

    PubMed  Article  CAS  Google Scholar 

  • Wesley SV, Helliwell CA, Smith NA, Wan MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high throughput gene silencing in plants. Plant J 27:581–590

    PubMed  Article  CAS  Google Scholar 

  • Wu J, Maehara T, Shimokawa T, Yamamoto S, Harada C, Takazaki Y, Ono N, Mukai Y, Koike K, Yazaki J, Fujii F, Shomura A, Ando T, Kono I, Waki K, Yamamoto K, Yano M, Matsumoto T, Sasaki T (2002) A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14:525–535

    PubMed  Article  CAS  Google Scholar 

  • Yamamoto K, Sasaki T (1997) Large-scale EST sequencing in rice. Plant Mol Biol 35:135–144

    PubMed  Article  CAS  Google Scholar 

  • Yang J-Y, Chung M-C, Tu C-Y, Leu W-M (2002) OSTF1: A HD-GL2 family homeobox gene is developmentally regulated during early embryogenesis in rice. Plant Cell Physiol 43:628–638

    PubMed  Article  CAS  Google Scholar 

  • Yu J, Hu S, Wang J, Wong GK, Li S, Li 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, Zen 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 (2002) A draft sequence of the rice genome (Oryza sativa L ssp indica). Science 296:79–92

    PubMed  Article  CAS  Google Scholar 

  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, Zhang J, Zhang Y, Li J, Xu Z, Li S, Li X, Zheng H, Cong L, Lin L, Yin J, Geng J, Li G, Shi J, Liu J, Lv H, Li J, Wang J, Deng Y, Ran L, Shi X, Wang X , Wu Q, Li C, Ren X, Wang J, Wang X, Li D, Liu D, Zhang X, Ji Z, Zhao W, Sun Y, Zhang Z, Bao J, Han Y, Dong L, Ji J, Chen P, Wu S, Liu J, Xiao Y, Bu D, Tan J, Yang L, Ye C, Zhang J, Xu J, Zhou Y, Yu Y, Zhang B, Zhuang S, Wei H, Liu B, Lei M, Yu H, Li Y, Xu H, Wei S, He X, Fang L, Zhang Z, Zhang Y, Huang X, Su Z, Tong W, Li J, Tong Z, Li S, Ye J, Wang L, Fang L, Lei T, Chen C, Chen H, Xu Z, Li H, Huang H, Zhang F, Xu H, Li N, Zhao C, Li S, Dong L, Huang Y, Li L, Xi Y, Qi Q, Li W, Zhang B, Hu W, Zhang Y, Tian X, Jiao Y, Liang X, Jin J, Gao L, Zheng W, Hao B, Liu S, Wang W, Yuan L, Cao M, McDermott J, Samudrala R, Wang J, Wong GKS, Yang H (2005) The genomes of Oryza sativa: a history of duplications. Plos Biol 3:266–281

    Article  CAS  Google Scholar 

  • Yue B, Xue W, Xiong L, Yu X, Luo L, Cui K, Jin D, Xing Y, Zhang Q (2006) Genetic basis of drought resistance at reproductive stage in rice: separation of drought tolerance from drought avoidance. Genetics 172:1213–1228

    PubMed  Article  Google Scholar 

  • Zhong R, Ye ZH (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139–2152

    PubMed  Article  CAS  Google Scholar 

  • Zhou Y, Tang J, Walker MG, Zhang X, Wang J, Hu S, Xu H, Deng Y, Dong J, Ye L, Lin L, Li J, Wang X, Xu H, Pan Y, Lin W, Tian W, Liu J, Wei L, Liu S, Yang H, Yu J, Wang J (2003) Gene identification and expression analysis of 86,136 expressed sequence tags (EST) from the rice genome. Genomics Proteomics Bioinformatics 1:26–42

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Elly Schrijnemakers for plant care and NIAS DNA Bank in Japan for sending EST clones. This work was supported by the EU FP5 project TF-STRESS (QLK3-2000-00328) for HJ, PE and AHM, by the SPIN-BIORIN Programme (99-BT-01) of the Royal Netherlands Academy of Arts and Sciences (KNAW) for SP and AE, by the Programme Scientific Alliance (04-PSA-BD-04) of KNAW for AA, MW and ZZ, by the EU FP6 INCO-MPC2 project CEDROME (INCO-CT-2005-015468) for XZ, LX and PBFO and by the Indonesian International Joint Research Program (RUTI) for IHS and SP.

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Author notes

  1. Adamantia Agalou

    Present address: Laboratory of Cellular Signaling and Molecular Pharmacology, Institute of Biology, National Center for Scientific Research “Demokritos”, Ag. Paraskevi, 15310, Athens, Greece

Affiliations

  1. Institute of Biology, Clusius Laboratory, Leiden University, P.O. Box 9505, 2300 RA, Leiden, The Netherlands

    Adamantia Agalou, Sigit Purwantomo, Amy Estiati, Rolf J. de Kam, Mei Wang, Annemarie H. Meijer & Pieter B. F. Ouwerkerk

  2. Research Center for Biotechnology, Indonesian Institute of Sciences (LIPI), Jl. Raya Bogor Km. 46, Cibinong, 16911, Indonesia

    Sigit Purwantomo, Amy Estiati & Inez H. Slamet-Loedin

  3. Department of Physiological Botany, EBC, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    Elin Övernäs, Henrik Johannesson & Peter Engström

  4. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Shi-Zhi-Shan Street, No. 1, 430070, Wuhan, China

    Xiaoyi Zhu & Lizhong Xiong

  5. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, 917 Building, Datun Road, Deshenmenwai, Beijing, 100101, China

    Zhen Zhu

  6. TNO Quality of Life, Zernikedreef 9, P.O. Box 2215, 2301 CE, Leiden, The Netherlands

    Mei Wang

Authors
  1. Adamantia Agalou
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  2. Sigit Purwantomo
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  3. Elin Övernäs
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  4. Henrik Johannesson
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  5. Xiaoyi Zhu
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  6. Amy Estiati
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  7. Rolf J. de Kam
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  8. Peter Engström
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  9. Inez H. Slamet-Loedin
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  10. Zhen Zhu
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  11. Mei Wang
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  12. Lizhong Xiong
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  13. Annemarie H. Meijer
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  14. Pieter B. F. Ouwerkerk
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Corresponding author

Correspondence to Pieter B. F. Ouwerkerk.

Additional information

Adamantia Agalou and Sigit Purwantomo contributed equally to this work.

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Agalou, A., Purwantomo, S., Övernäs, E. et al. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol 66, 87–103 (2008). https://doi.org/10.1007/s11103-007-9255-7

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  • DOI: https://doi.org/10.1007/s11103-007-9255-7

Keywords

  • Homeodomain-leucine zipper
  • Homeobox
  • Rice
  • Arabidopsis
  • Drought