Skip to main content
Log in

Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Auxin is one of the most important phytohormones and exerts pleiotropic effects on plant growth and development. Aux/IAA and auxin response factor (ARF) are two important protein families that are well recognized for their roles in auxin-mediated responses. Aux/IAA proteins are short-lived transcriptional regulators that mediate auxin responses through interaction with ARF transcription factors. Here, we systematically compared the genomic organization of the two families in rice. The expression profiles of both families were compared to show possible association of the two gene families at expression level, which would help reveal their synergistic relationships and functions. The expression profile analysis of Aux/IAA and ARF genes in 30 organs/tissues (collected from an entire life cycle of rice) suggested that Aux/IAA and ARF genes are expressed in very diverse patterns. In general, the genes showing similar expression patterns tended to be in the same phylogenetic subgroup even though their expression patterns were not always the same. Hierarchical cluster analysis revealed that there are eight pairs of IAA and ARF genes, with each pair showing highly correlated expression. The expression levels of the IAA gene family were also checked under various hormone treatments including abscisic acid, kinetin, gibberellin, jasmonic acid, auxin and brassinolide. The results indicated that most of the IAA genes respond to at least one of the treatments. Furthermore, DNA chip and real-time PCR results show that many genes in these families were responsive to various abiotic stresses, indicating an interaction between plant growth and abiotic stress. The effect of abiotic stress on plant growth and auxin distribution was further confirmed with the root growth of DR5-GUS transgenic rice under mannitol treatment, in which a close association between mannitol-induced changes of auxin distribution and root growth was observed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

Aux/IAA:

Auxin/indoleacetic acid

ARF:

Auxin response factor

BR:

Brassinosteroid

DR5:

Synthetic auxin response element

24-epiBL:

24-Epibrassinolide

GA:

Gibberellin

HLE (LLE, MLE):

High expression pattern (low, middle)

IAA:

Indole-3-acetic acid

JA:

Jasmonic acid

TSE:

Tissue- and organ-specific expression pattern

References

  • Berleth T, Krogan NT, Scarpella E (2004) Auxin signals—turning genes on and turning cells around. Curr Opin Plant Biol 7:553–563

    Article  PubMed  CAS  Google Scholar 

  • Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852

    Article  PubMed  CAS  Google Scholar 

  • Choi G, Yi H, Lee J, Kwon YK, Soh MS, Shin B, Luka Z, Hahn TR, Song PS (1999) Phytochrome signalling is mediated through nucleoside diphosphate kinase 2. Nature 401:610–613

    Article  PubMed  CAS  Google Scholar 

  • Coenen C, Lomax TL (1997) Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends Plant Sci 2:351–356

    Article  PubMed  CAS  Google Scholar 

  • Colon-Carmona A, Chen DL, Yeh KC, Abel S (2000) Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol 124:1728–1738

    Article  PubMed  CAS  Google Scholar 

  • Dowd C, Wilson IW, McFadden H (2004) Gene expression profile changes in cotton root and hypocotyl tissues in response to infection with Fusarium oxysporum f. sp. vasinfectum. Mol Plant Microbe Interact 17:654–667

    Article  PubMed  CAS  Google Scholar 

  • Dreher KA, Brown J, Saw RE, Callis J (2006) The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18:699–714

    Article  PubMed  CAS  Google Scholar 

  • Eklof S, Astot C, Sitbon F, Moritz T, Olsson O, Sandberg G (2000) Transgenic tobacco plants co-expressing Agrobacterium iaa and ipt genes have wild-type hormone levels but display both auxin- and cytokinin-overproducing phenotypes. Plant J 23:279–284

    Article  PubMed  CAS  Google Scholar 

  • Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  PubMed  CAS  Google Scholar 

  • Gazarian IG, Lagrimini LM, Mellon FA, Naldrett MJ, Ashby GA, Thorneley RN (1998) Identification of skatolyl hydroperoxide and its role in the peroxidase-catalysed oxidation of indol-3-yl acetic acid. Biochem J 333:223–232

    PubMed  CAS  Google Scholar 

  • Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T (2004) Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 131:1089–1100

    Article  PubMed  CAS  Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    Article  PubMed  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739

    Article  PubMed  CAS  Google Scholar 

  • Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  PubMed  CAS  Google Scholar 

  • Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59

    Article  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2004) Auxin-induced SCFTIR1-Aux/IAA interaction involves stable modification of the SCFTIR1 complex. Proc Natl Acad Sci USA 101:12381–12386

    Article  PubMed  CAS  Google Scholar 

  • Kim BC, Soh MC, Kang BJ, Furuya M, Nam HG (1996) Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J 9:441–456

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kim BC, Soh MS, Hong SH, Furuya M, Nam HG (1998) Photomorphogenic development of the Arabidopsis shy2–1D mutation and its interaction with phytochromes in darkness. Plant J 15:61–68

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Park PJ, Hwang HJ, Lee SY, Oh MH, Kim SG (2006) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci Biotechnol Biochem 70:768–773

    Article  PubMed  CAS  Google Scholar 

  • Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  PubMed  CAS  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed  CAS  Google Scholar 

  • Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–574

    Article  PubMed  CAS  Google Scholar 

  • Nakamura A, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S (2006a) Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type. Plant J 45:193–205

    Article  PubMed  CAS  Google Scholar 

  • Nakamura A, Umemura I, Gomi K, Hasegawa Y, Kitano H, Sazuka T, Matsuoka M (2006b) Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. Plant J 46:297–306

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:E258

    Article  PubMed  Google Scholar 

  • Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044

    Article  PubMed  Google Scholar 

  • Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841

    Article  PubMed  CAS  Google Scholar 

  • Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300

    Article  PubMed  CAS  Google Scholar 

  • Pasternak T, Potters G, Caubergs R, Jansen MA (2005) Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J Exp Bot 56:1991–2001

    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 USA 101:9903–9908

    Article  PubMed  CAS  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  PubMed  CAS  Google Scholar 

  • Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425

    Article  PubMed  CAS  Google Scholar 

  • Reed JW, Elumalai RP, Chory J (1998) Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation. Genetics 148:1295–1310

    PubMed  CAS  Google Scholar 

  • Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426:255–260

    Article  PubMed  CAS  Google Scholar 

  • Ross JJ, O’Neill DP, Smith JJ, Kerckhoffs LH, Elliott RC (2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. Plant J 21:547–552

    Article  PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Sato A, Yamamoto KT (2008) Overexpression of the noncanonical Aux/IAA genes causes auxin-related aberrant phenotypes in Arabidopsis. Physiol Plant 133:397–405

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Slama I, Ghnaya T, Messedi D, Hessini K, Labidi N, Savoure A, Abdelly C (2007) Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grown in mannitol-induced water stress. J Plant Res 120:291–299

    Article  PubMed  CAS  Google Scholar 

  • Stowe-Evans EL, Harper RM, Motchoulski AV, Liscum E (1998) NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. Plant Physiol 118:1265–1275

    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 

  • Thakur JK, Jain M, Tyagi AK, Khurana JP (2005) Exogenous auxin enhances the degradation of a light down-regulated and nuclear-localized OsiIAA1, an Aux/IAA protein from rice, via proteasome. Biochim Biophys Acta 1730:196–205

    PubMed  CAS  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997a) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    Article  PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997b) 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 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849

    Article  PubMed  CAS  Google Scholar 

  • Vogler H, Kuhlemeier C (2003) Simple hormones but complex signalling. Curr Opin Plant Biol 6:51–56

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24

    Article  PubMed  CAS  Google Scholar 

  • Watahiki MK, Yamamoto KT (1997) The massugu1 mutation of Arabidopsis identified with failure of auxin-induced growth curvature of hypocotyl confers auxin insensitivity to hypocotyl and leaf. Plant Physiol 115:419–426

    Article  PubMed  CAS  Google Scholar 

  • Wolbang CM, Chandler PM, Smith JJ, Ross JJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol 134:769–776

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto KT (1994) Further characterization of auxin-regulated mRNAs in hypocotyl sections of mung bean [Vigna radiata (L.) Wilczek]: sequence homology to genes for fatty-acid desaturases and atypical late-embryogenesis-abundant protein, and the mode of expression of the mRNAs. Planta 192:359–364

    Article  PubMed  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 R, 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 GK, Yang H (2005) The Genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  PubMed  Google Scholar 

  • Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, Wang J, Xiong L, Zhang Q, Fan L, Deng XW (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63:591–608

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grants from the National Program on the Development of Basic Research, the National Program on High Technology Development, the National Natural Science Foundation, and the Ministry of Education of China. We thank Dr. P.B.F. Ouwerkerk for providing the binary vector DR5-GUS and Yu Zhao for generating the transgenic rice of DR5-GUS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lizhong Xiong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2047 kb)

Supplementary material 2 (XLS 2047 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, Y., Wang, L. & Xiong, L. Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229, 577–591 (2009). https://doi.org/10.1007/s00425-008-0853-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-008-0853-7

Keywords

Navigation