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The auxin-responsive GH3 gene family in rice (Oryza sativa)

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Abstract

Auxin regulates plant growth and development by altering the expression of diverse genes. Among these, the genes of Aux/IAA, SAUR, and GH3 classes have been extensively studied in dicots, but little information is available on monocots. We have identified 12 members of GH3 gene family in rice using sequences of full-length cDNA clones available from KOME and analysis of the whole genome sequence of rice. The genomic organization as well as chromosomal location of all the OsGH3 genes is reported. The rice GH3 proteins can be classified in two groups (groups I and II) on the basis of their phylogenetic relationship with Arabidopsis GH3 proteins. Based upon the sequences available in the database, not a single group III GH3 protein could be identified in rice. An extensive survey of EST sequences of other monocots led to the conclusion that although GH3 gene family is highly conserved in both dicots and monocots but the group III is conspicuous by its absence in monocots. The in silico analysis has been complemented with experimental data to quantify transcript levels of all GH3 gene family members. Using real-time polymerase chain reaction, the organ-specific expression of individual OsGH3 genes in light- and dark-grown seedlings/plants has been examined. The transcript abundance of nearly all OsGH3 genes is enhanced on auxin treatment, with the effect more pronounced on OsGH3-1, -2, and -4. The functional validation of these genes in transgenics or analysis of gene-specific insertional mutants will help in elucidating their precise role in auxin signal transduction.

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References

  • Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducilbe mRNAs in Arabidopsis thaliana. J Mol Biol 251:533–549

    Article  PubMed  CAS  Google Scholar 

  • Adams MD, Kerlavage AR, Fleischmann RD, Fuldner RA, Bult CJ, Lee NH, Kirkness EF, Weinstock KG, Gocayne JD, White O et al (1995) Initial assessment of human gene diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature 377:3–17

    PubMed  CAS  Google Scholar 

  • Ainley WM, Walker JC, Nagao RT, Key JL (1988) Sequence and characterization of two auxin-regulated genes from soybean. J Biol Chem 263:10658–10666

    PubMed  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Conner TW, Goekjian VH, LaFayette PR, Key JL (1990) Structure and expression of two auxin-inducible genes from Arabidopsis. Plant Mol Biol 15:623–632

    Article  PubMed  CAS  Google Scholar 

  • Franco AR, Gee MA, Guilfoyle TJ (1990) Induction and superinduction of auxin-responsive mRNAs with auxin and protein synthesis inhibitors. J Biol Chem 265:15845–15849

    PubMed  CAS  Google Scholar 

  • Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, Mundodi S, Reiser L, Rhee SY, Scholl R, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2:239–253

    Article  PubMed  CAS  Google Scholar 

  • Gil P, Liu Y, Orbovic V, Verkamp E, Poff KL, Green PJ (1994) Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol 104:777–784

    Article  PubMed  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 (O. sativa L. ssp. japonica). Science 296:92–100

    Article  PubMed  CAS  Google Scholar 

  • Guilfoyle TJ (1999) Auxin-regulated genes and promoters. In: Hooykaas PJJ, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. Elsevier, Amsterdam, The Netherlands

    Google Scholar 

  • Guilfoyle TJ, Hagen G, Li Y, Ulmasov T, Liu Z, Strabala T, Gee MA (1993) Auxin-regulated transcription. Aust J Plant Physiol 20:489–502

    Article  CAS  Google Scholar 

  • Hagen G, Guilfoyle TJ (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  PubMed  CAS  Google Scholar 

  • Hagen G, Kleinschmidt AJ, Guilfoyle TJ (1984) Auxin-regulated gene expression in intact soybean hypocotyls and excised hypocotyls sections. Planta 16:147–153

    Article  Google Scholar 

  • Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17:567–579

    Article  PubMed  CAS  Google Scholar 

  • Hsieh HL, Okamoto H, Wang M, Ang LH, Matsui M, Goodman H, Deng XW (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14:1958–1970

    PubMed  CAS  Google Scholar 

  • Jain M, Tyagi SB, Thakur JK, Tyagi AK, Khurana JP (2004) Molecular characterization of a light-responsive gene, breast basic conserved protein 1 (OsiBBC1), encoding nuclear-localized protein homologous to ribosomal protein L13 from Oryza sativa indica. Biochim Biophys Acta 1676:182–192

    PubMed  CAS  Google Scholar 

  • Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, Hotta I, Kojima K, Namiki T, Ohneda E, Yahagi W, Suzuki K, Li CJ, Ohtsuki K, Shishiki T, Otomo Y, Murakami K, Iida Y, Sugano S, Fujimura T, Suzuki Y, Tsunoda Y, Kurosaki T, Kodama T, Masuda H, Kobayashi M, Xie Q, Lu M, Narikawa R, Sugiyama A, Mizuno K, Yokomizo S, Niikura J, Ikeda R, Ishibiki J, Kawamata M, Yoshimura A, Miura J, Kusumegi T, Oka M, Ryu R, Ueda M, Matsubara K, Kawai J, Carninci P, Adachi J, Aizawa K, Arakawa T, Fukuda S, Hara A, Hashizume W, Hayatsu N, Imotani K, Ishii Y, Itoh M, Kagawa I, Kondo S, Konno H, Miyazaki A, Osato N, Ota Y, Saito R, Sasaki D, Sato K, Shibata K, Shinagawa A, Shiraki T, Yoshino M, Hayashizaki Y, Yasunishi A (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301:376–379

    Article  PubMed  Google Scholar 

  • Kim J, Harter K, Theologis A (1997) Protein–protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci U S A 94:11786–11791

    Article  PubMed  CAS  Google Scholar 

  • Kolkman JA, Stemmer WPC (2001) Directed evolution of proteins by exon shuffling. Nat Biotechnol 19:423–428

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Liu ZB, Shi X, Hagen G, Guilfoyle TJ (1994) An auxin-inducible element in soybean SAUR promoters. Plant Physiol 106:37–43

    Article  PubMed  CAS  Google Scholar 

  • Liu ZB, Ulmasov T, Shi X, Hagen G, Guilfoyle TJ (1994) Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6:645–657

    Article  PubMed  CAS  Google Scholar 

  • Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15:1771–1780

    Article  PubMed  Google Scholar 

  • Nakazawa M, Yabe N, Ichikawa T, Yamamoto YY, Yoshizumi T, Hasunuma K, Matsui M (2001) DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J 25:213–221

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A 101:9903–9908

    Article  PubMed  CAS  Google Scholar 

  • Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369

    Article  PubMed  CAS  Google Scholar 

  • Roux C, Perrot-Rechenmann C (1997) Isolation by differential display and characterization of a tobacco auxin-responsive cDNA Nt-gh3, related to GH3. FEBS Lett 419:131–136

    Article  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 

  • Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415

    Article  PubMed  CAS  Google Scholar 

  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627

    Article  PubMed  CAS  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Manabe K, Matsui M (2003) DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation. Plant Cell Physiol 44:1071–1080

    Article  PubMed  CAS  Google Scholar 

  • Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M (2004) ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37:471–483

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Mochizuki N, Nagatani A (2002) Expression of the AtGH3a gene, an Arabidopsis homologue of the soybean GH3 gene, is regulated by phytochrome B. Plant Cell Physiol 43:281–289

    Article  PubMed  CAS  Google Scholar 

  • Tepperman JM, Zhu T, Chang HS, Wang X, Quail PH (2001) Multiple transcription-factor genes are early targets of phytochrome a signaling. Proc Natl Acad Sci U S A 98:9437–9442

    Article  PubMed  CAS  Google Scholar 

  • Thakur JK, Tyagi AK, Khurana JP (2001) OsIAA1, an Aux/IAA cDNA from rice, and changes in its expression as influenced by auxin and light. DNA Res 8:193–203

    Article  PubMed  CAS  Google Scholar 

  • Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183:53–68

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle TJ (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • Walker JC, Key JL (1982) Isolation of cloned cDNAs to auxin-responsive poly(A) RNAs of elongating soybean hypocotyls. Proc Natl Acad Sci U S A 79:7185–7189

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto KT, Mori H, Imaseki H (1992) cDNA cloning of indole-3-acetic acid regulated genes: Aux22 and SAUR from mung bean (Vigna radiata) hypocotyls tissue. Plant Cell Physiol 33:93–97

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

MJ acknowledges the award of Senior Research Fellowship from the Council of Scientific and Industrial Research, New Delhi. This research work was financially supported by the Department of Biotechnology, Government of India, and the University Grants Commission, New Delhi. We gratefully acknowledge KOME, TAIR, TIGR, and IRGSP database resources for availability of detailed sequence information on rice and Arabidopsis.

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  1. Department of Plant Molecular Biology, University of Delhi South Campus, Benito Juarez Road, New Delhi, 110021, India

    Mukesh Jain, Navneet Kaur, Akhilesh K. Tyagi & Jitendra P. Khurana

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  1. Mukesh Jain
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  2. Navneet Kaur
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  3. Akhilesh K. Tyagi
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  4. Jitendra P. Khurana
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Correspondence to Jitendra P. Khurana.

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Jain, M., Kaur, N., Tyagi, A.K. et al. The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genomics 6, 36–46 (2006). https://doi.org/10.1007/s10142-005-0142-5

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