Up-Regulation of OsBIHD1, a Rice Gene Encoding BELL Homeodomain Transcriptional Factor, in Disease Resistance Responses

H. Luo; F. Song; R. M. Goodman; Z. Zheng

doi:10.1055/s-2005-865851

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2005; 7(5): 459-468
DOI: 10.1055/s-2005-865851

Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Up-Regulation of OsBIHD1, a Rice Gene Encoding BELL Homeodomain Transcriptional Factor, in Disease Resistance Responses

H. Luo¹ ^, ² ^, ⁵ , F. Song¹ ^, ² ^, ³ , R. M. Goodman⁴ , Z. Zheng¹ ^, ²

¹Institute of Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310029, P.R. China
²Department of Plant Protection, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310029, P.R. China
³State Key Laboratory of Rice Biology, Zhejiang University, Hangzhou, Zhejiang 310029, P.R. China
⁴Department of Botany and Plant Pathology, Gaylord Nelson Institute for Environmental Studies, University of Wisconsin, Madison, WI 53706, USA
⁵Present address: Institute of Biotechnology, Hainan University, Haikou, Hainan 570000, P.R. China

Abstract

In the present study, we cloned and identified a full-length cDNA of a rice gene, OsBIHD1, encoding a homeodomain type transcriptional factor. OsBIHD1 is predicted to encode a 642 amino acid protein and the deduced protein sequence of OsBIHD1 contains all conserved domains, a homeodomain, a BELL domain, a SKY box, and a VSLTLGL box, which are characteristics of the BELL type homedomain proteins. The recombinant OsBIHD1 protein expressed in Escherichia coli bound to the TGTCA motif that is the characteristic cis-element DNA sequence of the homeodomain transcriptional factors. Subcellular localization analysis revealed that the OsBIHD1 protein localized in the nucleus of the plant cells. The OsBIHD1 gene was mapped to chromosome 3 of the rice genome and is a single-copy gene with four exons and three introns. Northern blot analysis showed that expression of OsBIHD1 was activated upon treatment with benzothiadiazole (BTH), which is capable of inducing disease resistance. Expression of OsBIHD1 was also up-regulated rapidly during the first 6 h after inoculation with Magnaporthe grisea in BTH-treated rice seedlings and during the incompatible interaction between M. grisea and a resistant genotype. These results suggest that OsBIHD1 is a BELL type of homeodomain transcription factor present in the nucleus, whose induction is associated with resistance response in rice.

Key words

Benzothiadiazole (BTH) - rice (Oryza sativa L.) - homeodomain; disease resistance response - OsBIHD1 - Magnaporthe grisea.

Full Text

References

1 Abe M., Takahashi T., Komeda Y.. Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. The Plant Journal. (2001); 26 487-494
2 Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. (1997); 25 3389-3402
3 Aoyama T., Dong C. H., Wu Y., Carabelli M., Sessa G., Ruberti I., Morelli G., Chua N. H.. Ectopic expression of the Arabidopsis transcriptional activator Athb-1 alters leaf cell fate in tobacco. Plant Cell. (1995); 7 1773-1785
4 Bellaoui M., Pidkowich M. S., Samach A., Kushalappa K., Kohalmi S. E., Modrusan Z., Crosby W. L., Haughn T G. W.. The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell. (2001); 13 2455-2470
5 Bellmann R., Werr W.. Zmhox1a, the product of a novel maize homeobox gene, interacts with the Shrunken 26 bp feedback control element. The EMBO Journal. (1992); 11 3367-3374
6 Chan R. L., Gago G. M., Palena C. M., Gonzalez D. H.. Homeoboxes in plant development. Biochimica et Biophysica Acta. (1998); 1442 1-19
7 Chang C. P., Jacobs Y., Nakamura T., Jenkins N. A., Copeland N. G., Cleary M. L.. Meis proteins are major in vivo DNA binding partners for wild-type but not chimeric Pbx proteins. Molecular and Cellular Biology. (1997); 17 5679-5687
8 Chen H., Rosin F. M., Prat S., Hannapel D. J.. Interacting transcription factors from the three-amino acid loop extension superclass regulate tuber formation. Plant Physiology. (2003); 132 1391-1404
9 Chiu W. I., Niwa Y., Zeng W., Hirano T., Kobayashi H., Sheen J.. Engineered GFP as a vital reporter in plants. Current Biology. (1996); 6 325-330
10 Chomczynski P., Brar A. K., Frohman L. A.. Single-step method of RNA isolation by guanidium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry. (1987); 162 156-159
11 Damiani R. D. J., Wessler S. R.. An upstream open reading frame represses expression of Lc, a member of the R/B family of maize transcriptional activators. Proceedings of the National Academy of Sciences of the USA. (1993); 90 8244-8248
12 Deng X., Phillips J., Meijer A. H., Salamini F., Bartels D.. Characterization of five novel dehydration-responsive homeodomain leucine zipper genes from the resurrection plant Craterostigma plantagineum. . Plant Molecular Biology. (2002); 49 601-610
13 Desplan C., Theis J., O'Farrell P. H.. The sequence specificity of homeodomain-DNA interaction. Cell. (1988); 54 1081-1090
14 Dong Y. H., Yao J. L., Atkinson R. G., Putterill J. J., Morris B. A., Gardner R. C.. MDH1: an apple homeobox gene belonging to the BEL1 family. Plant Molecular Biology. (2000); 42 623-633
15 Frank W., Phillips J., Salamini F., Bartels D.. Two dehydration-inducible transcripts from the resurrection plant Craterostigma plantagineum encode interacting homeodomain-leucine zipper proteins. The Plant Journal. (1998); 15 413-421
16 Gago G. M., Almoguera C., Jordano J., Gonzalez D. H., Chan R. L.. Hahb-4, a homeobox-leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower. Plant, Cell and Environment. (2002); 25 633-640
17 Gehring W. J.. Homeoboxes in the study of development. Science. (1987); 236 1245-1252
18 Himmelbach A., Hoffmann T., Leube M., Hohener B., Grill E.. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. . The EMBO Journal. (2002); 21 3029-3038
19 Hung C. Y., Lin Y., Zhang M., Pollock S., Marks M. D., Schiefelbein J.. A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. . Plant Physiology. (1998); 117 73-84
20 Johannesson H., Wang Y., Engstrom P.. DNA-binding and dimerization preferences of Arabidopsis homeodomain-leucine zipper transcription factors in vitro. . Plant Molecular Biology. (2001); 45 63-73
21 Johannesson H., Wang Y., Hanson J., Engstrom P.. The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Molecular Biology. (2003); 51 719-729
22 Kerstetter R. A., Laudencia-Chingcuanco D., Smith L. G., Hake S.. Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development. (1997); 124 3045-3054
23 Korfhage U., Trezzini G. F., Meier I., Hahlbrock K., Somssich I. E.. Plant homeodomain protein involved on transcriptional regulation of a pathogen defense-related gene. Plant Cell. (1994); 6 695-708
24 Kusaba S., Kano-Murakami Y., Matsuoka M., Tamaoki M., Sakamoto T., Yamaguchi I., Fukumoto M.. Alteration of hormone levels in transgenic tobacco plants overexpressing the rice homeobox gene, OSH1. . Plant Physiology. (1998); 116 471-476
25 Lee Y. H., Chun J. Y.. A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Molecular Biology. (1998); 37 377-384
26 Lincoln C., Long J., Yamaguchi J., Serikawa K., Hake S.. A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell. (1994); 6 1859-1876
27 Lu P., Porat R., Nadeau J. A., O'Neill S. D.. 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. (1996); 8 2155-2168
28 Masucci J. D., Schiefelbein J. W.. Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell. (1996); 8 1505-1517
29 Mayda E., Tornero P., Conejero V., Vera P.. A tomato homeobox gene (HD-zip) is involved in limiting the spread of programmed cell death. The Plant Journal. (1999); 20 591-600
30 Meissner R., Theres K.. Isolation and characterization of the tomato homeobox gene THOM1. . Planta. (1995); 195 541-547
31 Muller J., Wang Y., Franzen R., Santi L., Salamini F., Rohde W.. In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. The Plant Journal. (2001); 27 13-23
32 Murray M. G., Thompson W. F.. Rapid isolation of high-molecular weight plant DNA. Nucleic Acids Research. (1980); 8 4321-4325
33 Mussig C., Kauschmann A., Clouse S. D., Altmann T.. The Arabidopsis PHD-finger protein SHL is required for proper development and fertility. Molecular and General Genetics. (2000); 264 363-370
34 Nagasaki H., Sakamoto T., Sato Y., Matsuoka M.. Functional analysis of the conserved domain of KNOX homeodomain protein, OSH15. Plant Cell. (2001); 13 2085-2098
35 Niwa Y., Hirano T., Yoshimoto K., Shimizu M., Kobayashi H.. Non-invasive quantitative detection and applications of non-toxic, S65T-type green fluorescent protein in living plants. The Plant Journal. (1999); 8 455-463
36 Ohashi Y., Oka A., Rodrigues-Pousada R., Possenti M., Ruberti I., Morelli G., Aoyama T.. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science. (2003); 300 1427-1430
37 Otting G., Qian Y. Q., Billeter M., Muller M., Affolter M., Gehring W. J., Wuthrich K.. Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. The EMBO Journal. (1990); 9 3085-3092
38 Quaedvlieg N., Dockx J., Rook F., Weisbeek P., Smeekens S.. The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. . Plant Cell. (1995); 7 117-129
39 Reiser L., Modrusan Z., Margossian L., Samach A., Ohad N., Haughn G. W., Fisher R. K.. The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell. (1995); 83 735-742
40 Sakamoto T., Kamiya N., Ueguchi-Tanaka M., Iwahori S., Matsuoka M.. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes and Development. (2001); 15 581-590
41 Sawa S., Ohgishi M., Goda H., Higuchi K., Shimada Y., Yoshida S., Koshiba T.. 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. . The Plant Journal. (2002); 32 1011-1022
42 Sentoku N., Sato Y., Matsuoka M.. Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Developmental Biology. (2000); 220 358-364
43 Smith H. M., Boschke I., Hake S.. Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proceedings of the National Academy of Sciences of the USA. (2002); 99 9579-9584
44 Soderman E., Mattsson J., Engstrom P.. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. The Plant Journal. (1996); 10 375-381
45 Soderman E., Hjellstrom M., Fahleson J., Engstrom P.. The HD-Zip gene ATHB6 in Arabidopsis is expressed in developing leaves, roots and carpels and up-regulated by water deficit conditions. Plant Molecular Biology. (1999); 40 1073-1083
46 Song F., Goodman R. M.. OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta. (2002 a); 215 997-1005
47 Song F., Goodman R. M.. Molecular cloning and characterization of a rice phosphoinositide-specific phospholipase C gene, OsPI-PLC1 that is activated in systemic acquired resistance. Physiological and Molecular Plant Pathology. (2002 b); 61 31-40
48 Takeuchi Y., Dotson M., Keen N. T.. Plant transformation: a simple particle bombardment device based on flowing helium. Plant Molecular Biology. (1992); 18 835-839
49 Tamaoki M., Kusaba S., Kano-Murakami Y., Matsuoka M.. Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant and Cell Physiology. (1997); 38 917-927
50 Tang Z., Sadka A., Morishige D. T., Mullet J. E.. Homeodomain leucine zipper proteins bind to the phosphate response domain of the soybean VspB tripartite promoter. Plant Physiology. (2001); 125 797-809
51 Thompson J. D., Higgins D. G., Gibson T. J.. CLUSTALw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Research. (1994); 22 4673-4680
52 Western T. L., Haughn G. W.. BELL1 and AGAMOUS genes promote ovule identity in Arabidopsis thaliana. . The Plant Journal. (1999); 18 329-336

F. Song

Department of Plant Protection
College of Agriculture and Biotechnology
Zhejiang University - Huajiachi Campus

Hangzhou

Zhejiang 310029

P.R. China

Email: fmsong@zju.edu.cn

Editor: C. M. J. Pieterse