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

  • Mukesh Jain
  • Navneet Kaur
  • Akhilesh K. Tyagi
  • Jitendra P. Khurana
Original Paper


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.


Auxin GH3 gene family Phylogenetic analysis Rice 



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.

Supplementary material

10142_2005_142_MOESM1_ESM.pdf (345 kb)
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  1. Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducilbe mRNAs in Arabidopsis thaliana. J Mol Biol 251:533–549CrossRefPubMedGoogle Scholar
  2. 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 377:3–17PubMedGoogle Scholar
  3. Ainley WM, Walker JC, Nagao RT, Key JL (1988) Sequence and characterization of two auxin-regulated genes from soybean. J Biol Chem 263:10658–10666PubMedGoogle Scholar
  4. 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 25:3389–3402CrossRefPubMedGoogle Scholar
  5. Conner TW, Goekjian VH, LaFayette PR, Key JL (1990) Structure and expression of two auxin-inducible genes from Arabidopsis. Plant Mol Biol 15:623–632CrossRefPubMedGoogle Scholar
  6. Franco AR, Gee MA, Guilfoyle TJ (1990) Induction and superinduction of auxin-responsive mRNAs with auxin and protein synthesis inhibitors. J Biol Chem 265:15845–15849PubMedGoogle Scholar
  7. 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 2:239–253CrossRefPubMedGoogle Scholar
  8. 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 104:777–784CrossRefPubMedGoogle Scholar
  9. 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 296:92–100CrossRefPubMedGoogle Scholar
  10. 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 NetherlandsGoogle Scholar
  11. Guilfoyle TJ, Hagen G, Li Y, Ulmasov T, Liu Z, Strabala T, Gee MA (1993) Auxin-regulated transcription. Aust J Plant Physiol 20:489–502CrossRefGoogle Scholar
  12. Hagen G, Guilfoyle TJ (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385CrossRefPubMedGoogle Scholar
  13. Hagen G, Kleinschmidt AJ, Guilfoyle TJ (1984) Auxin-regulated gene expression in intact soybean hypocotyls and excised hypocotyls sections. Planta 16:147–153CrossRefGoogle Scholar
  14. Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17:567–579CrossRefPubMedGoogle Scholar
  15. 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 14:1958–1970PubMedGoogle Scholar
  16. 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 1676:182–192PubMedGoogle Scholar
  17. 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 301:376–379PubMedCrossRefGoogle Scholar
  18. Kim J, Harter K, Theologis A (1997) Protein–protein interactions among the Aux/IAA proteins. Proc Natl Acad Sci U S A 94:11786–11791CrossRefPubMedGoogle Scholar
  19. Kolkman JA, Stemmer WPC (2001) Directed evolution of proteins by exon shuffling. Nat Biotechnol 19:423–428CrossRefPubMedGoogle Scholar
  20. Li Y, Liu ZB, Shi X, Hagen G, Guilfoyle TJ (1994) An auxin-inducible element in soybean SAUR promoters. Plant Physiol 106:37–43CrossRefPubMedGoogle Scholar
  21. Liu ZB, Ulmasov T, Shi X, Hagen G, Guilfoyle TJ (1994) Soybean GH3 promoter contains multiple auxin-inducible elements. Plant Cell 6:645–657CrossRefPubMedGoogle Scholar
  22. 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 15:1771–1780CrossRefPubMedGoogle Scholar
  23. 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 25:213–221CrossRefPubMedGoogle Scholar
  24. 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 101:9903–9908CrossRefPubMedGoogle Scholar
  25. Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369CrossRefPubMedGoogle Scholar
  26. 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 419:131–136CrossRefPubMedGoogle Scholar
  27. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  28. 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 14:1405–1415CrossRefPubMedGoogle Scholar
  29. 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 17:616–627CrossRefPubMedGoogle Scholar
  30. 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 44:1071–1080CrossRefPubMedGoogle Scholar
  31. 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 37:471–483CrossRefPubMedGoogle Scholar
  32. 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 43:281–289CrossRefPubMedGoogle Scholar
  33. 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 98:9437–9442CrossRefPubMedGoogle Scholar
  34. 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 8:193–203PubMedCrossRefGoogle Scholar
  35. Theologis A, Huynh TV, Davis RW (1985) Rapid induction of specific mRNAs by auxin in pea epicotyl tissue. J Mol Biol 183:53–68CrossRefPubMedGoogle Scholar
  36. 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 25:4876–4882CrossRefPubMedGoogle Scholar
  37. Tiwari SB, Hagen G, Guilfoyle TJ (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543CrossRefPubMedGoogle Scholar
  38. Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ (1995) Composite structure of auxin response elements. Plant Cell 7:1611–1623CrossRefPubMedGoogle Scholar
  39. 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 9:1963–1971CrossRefPubMedGoogle Scholar
  40. 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 79:7185–7189PubMedCrossRefGoogle Scholar
  41. 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 33:93–97Google Scholar
  42. 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 296:79–92CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Mukesh Jain
    • 1
  • Navneet Kaur
    • 1
  • Akhilesh K. Tyagi
    • 1
  • Jitendra P. Khurana
    • 1
  1. 1.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia

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