Abstract
The homeodomain-leucine zipper (HD-Zip) putative transcription factor genes are divided into 4 families. In this work, we studied the function of a rice HD-Zip I gene, H OME O BO X4 (Oshox4). Oshox4 transcripts were detected in leaf and floral organ primordia but excluded from the shoot apical meristem and the protein was nuclear localized. Over-expression of Oshox4 in rice induced a semi-dwarf phenotype that could not be complemented by applied GA3. The over-expression plants accumulated elevated levels of bioactive GA, while the GA catabolic gene GA2ox3 was upregulated in the transgenic plants. In addition, over-expression of Oshox4 blocked GA-dependent α-amylase production. However, down-regulation of Oshox4 in RNAi transgenic plants induced no phenotypic alteration. Interestingly, the expression of YAB1 that is involved in the negative feedback regulation of the GA biosynthesis was upregulated in the Oshox4 over-expressing plants. One-hybrid assays showed that Oshox4 could interact with YAB1 promoter in yeast. In addition, Oshox4 expression was upregulated by GA. These data together suggest that Oshox4 may be involved in the negative regulation of GA signalling and may play a role to fine tune GA responses in rice.
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References
Alabadi D, Gil J, Blazquez MA, Garcia-Martinez JL (2004) Gibberellins repress photomorphogenesis in darkness. Plant Physiol 134:1050–1057
Aoyama T, Dong CH, Wu Y, Carabelli M, Sessa G, Ruberti I, Morelli G, Chua NH (1995) Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell 7:1773–1785
Chan RL, Gago GM, Palena CM, Gonzalez DH (1998) Homeoboxes in plant development. Biochim Biophys Acta 1442:11–19
Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064
Dai M, Zhao Y, Ma Q, Hu Y, Hedden P, Zhang Q, Zhou DX (2007a) The rice YABBY1 gene is involved in the feedback regulation of gibberellin metabolism. Plant Physiol 144:121–133
Dai M, Hu Y, Zhao Y, Liu H, Zhou DX (2007b) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144:380–390
Dezar CA, Fedrigo GV, Chan RL (2005) The promoter of the sunflower HD-Zip protein gene Hahb4 directs tissue-specific expression and is inducible by water stress, high salt concentrations and ABA. Plant Sci 169:447–459
Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class III HD-Zip and KANADI genes. Curr Biol 13:1768–1774
Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85
Frank W, Phillips J, Salamini F, Bartels D (1998) Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. Plant J 15:413–421
Hanson J, Johannesson H, Engstrom P (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant Mol Biol 45:247–262
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004) MicroRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88
Johannesson H, Wang Y, Engstrom P (2001) DNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. Plant Mol Biol 45:63–73
Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2003) Where do gibberellin biosynthesis and gibberellin signalling occur in rice plants? Plant J 35:104–115
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
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
Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658
Manavella PA, Arce AL, Dezar CA, Bitton F, Renou JP, 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
Mason HS, Lam DM, Arntzen CJ (1992) Expression of hepatitis B surface antigen in transgenic plants. Proc Natl Acad Sci USA 89:11745–11749
Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339
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
Meijer AH, de Kam RJ, d′Erfurth I, Shen W, Hoge JH (2000) HD-Zip proteins of families I and II from rice: interactions and functional properties. Mol Gen Genet 263:12–21
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signalling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl):S61–S80
Peng J, Harberd NP (2002) The role of GA-mediated signalling in the control of seed germination. Curr Opin Plant Biol 5:376–381
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
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
Rueda EC, Dezar CA, Gonzalez DH, Chan RL (2005) Hahb-10, a sunflower homeobox-leucine zipper gene, is regulated by light quality and quantity, and promotes early flowering when expressed in Arabidopsis. Plant Cell Physiol 46:1954–1963
Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653
Schena M, Davis RW (1992) HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89:3894–3898
Sessa G, Morelli G, Ruberti I (1993) The Athb-1 and -2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. Embo J 12:3507–3517
Sessa G, Carabelli M, Ruberti I, Lucchetti S, Baima S, Morelli G (1994) Identification of distinct families of HD-Zip proteins in Arabidopsis thaliana. In: Puigdomenech P, Coruzzi G (eds) Molecular-genetic analysis of plant development and metabolism. Springer, Berlin, pp 411–426
Soderman E, Mattsson J, Engstrom P (1996) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10:375–381
Soderman E, Hjellstrom M, Fahleson J, Engstrom 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
Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019
Zhang J, Feng Q, Jin C, Qiu D, Zhang L, Xie K, Yuan D, Han B, Zhang Q, Wang S (2005) Features of the expressed sequences revealed by a large-scale analysis of ESTs from a normalized cDNA library of the elite indica rice cultivar Minghui 63. Plant J 42:772–780
Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456
Acknowledgements
We thank Dr. Xianhua Li for technical assistance, Professor Chaiguo Xu for rice field management and Dr. Peter Hedden for providing facilities ands advices for GA quantification. This research was supported by grants from The National Special Key Project of China on Functional Genomics of Major Plants and Animals, and the National Natural Science Foundation of China.
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Mingqiu Dai and Yongfeng Hu equally contributed to this work.
Sequence data from this article can be found in the GenBank/EMBL data libraries under the accession number: AF145728.
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Dai, M., Hu, Y., Ma, Q. et al. Functional analysis of rice HOMEOBOX4 (Oshox4) gene reveals a negative function in gibberellin responses. Plant Mol Biol 66, 289–301 (2008). https://doi.org/10.1007/s11103-007-9270-8
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DOI: https://doi.org/10.1007/s11103-007-9270-8