Skip to main content
Log in

Expression profiling of the BpIAA gene family and the determination of IAA levels in Betula platyphylla tetraploids

  • Review Article
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Betula platyphylla Sukaczev tetraploids have significantly larger leaf, fruit and stoma (gigantic phenotype) than diploids of the same species; however, the mechanism underlying this difference remains unclear. Tetraploid B. platyphylla transcriptome data have indicated that the expression of genes related to indole-3-acetic acid (IAA) biosynthesis and signal transduction was altered after genome duplication. IAA exerts pleiotropic effects on growth and development by inducing the expression of Aux/IAA. We identified 20 Aux/IAA genes (BpIAA1BpIAA20) in B. platyphylla distributed across 10 chromosomes. Multiple alignment and motif analyses revealed that nine BpIAA proteins shared all four conserved domains. Phylogenetic analysis indicated that Aux/IAA families were divided into four subfamilies and that there were two pairs of BpIAA sister genes. The BpIAAs were differentially expressed in diploids and tetraploids. Moreover, the expression levels of the nine BpIAA genes were specifically up-regulated in tetraploids from June to September compared with May (except August 5th) in tetraploids, while they were down-regulated in diploids. IAA levels were more than twofold higher in tetraploids than diploids during the vegetative season. These results indicate that genome duplication of B. platyphylla caused the up-regulated of genes involved in IAA synthesis, and the increased concentration of IAA may induce the constitutive expression of 20 BpIAA genes. Therefore, the significant changes in the expression patterns of the BpIAAs contributed to the gigantic phenotype of tetraploids to some extent. Our research sheds light on the phenotypic variations observed in B. platyphylla tetraploids.

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
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

Aux/IAA:

Auxin/indole-3-acetic acid protein

ARF:

Auxin response factor

IAA:

Indole-3-acetic acid

KEGG:

Kyoto Encyclopedia of Genes and Genomes

AUX1 :

Auxin influx transporter 1

GH3 :

Gretchen hagen 3

SRUR :

Small auxin-up RNA

DEUs:

Differentially expressed unigenes

NCBI:

National Center for Biotechnology Information

pI:

Isoelectric point

MEGA6:

Molecular Evolutionary Genetics Analysis

MEME:

Multiple Expectation Maximization for Motif Elicitation

CTAB:

Hexadecyltrimethylammonium bromide

qRT PCR:

Quantitative real-time reversed transcription PCR

NR:

Non-redundant

NLS:

Nuclear localization sequence

kDa:

The unit of protein molecular mass

References

  • Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012) Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant Cell Physiol 53:1583–1595

    Article  CAS  PubMed  Google Scholar 

  • Buggs RJ, Doust AN, Tate JA, Koh J, Soltis K, Feltus FA, Paterson AH, Soltis PS, Soltis DE (2009) Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 103:73–81

    Article  CAS  PubMed  Google Scholar 

  • Chang SPJ, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, Soltis PS, Carlson JE, Arumuganathan K, Barakat A, Albert VA, Ma H, dePamphilis CW (2006) Widespread genome duplications throughout the history of flowering plants. Genome Res 16:738–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devoghalaere et al (2012) A genomics approach to understanding the role of auxin in apple (Malus x domestica) fruit size control. BMC Plant Biol 12:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168

    Article  CAS  PubMed  Google Scholar 

  • Gao J, Cao X, Shi S, Ma Y, Wang K, Liu S, Chen D, Chen Q, Ma H (2016) Genome-wide survey of Aux/IAA gene family members in potato (Solanum tuberosum): identification, expression analysis, and evaluation of their roles in tuber development. Biochem Biophys Res Commun 471:320–327

    Article  CAS  PubMed  Google Scholar 

  • Guilfoyle TJ (2015) The PB1 domain in auxin response factor and Aux/IAA proteins: a versatile protein interaction module in the auxin response. Plant Cell 27:33–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guilfoyle TJ, Hagen G, Ulmasov T, Murfett J (1998) How does auxin turn on genes? Plant Physiol 118:341–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Korasick DA, Westfall CS, Lee SG, Nanao MH, Dumas R, Hagen G, Guilfoyle TJ, Jez JM, Strader LC (2014) Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression. Proc Natl Acad Sci USA 111:5427–5432

    Article  CAS  PubMed  Google Scholar 

  • Ku S-J, Park JY, Ha S-B, Kim J (2009) Overexpression of IAA1 with domain II mutation impairs cell elongation and cell division in inflorescences and leaves of Arabidopsis. J Plant Physiol 166:548–553

    Article  CAS  PubMed  Google Scholar 

  • Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, Kirchsteiger K, Estelle M (2016) Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife. https://doi.org/10.7554/eLife.13325

    Article  PubMed  PubMed Central  Google Scholar 

  • Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    Article  CAS  PubMed  Google Scholar 

  • Li H, Tiwari SB, Hagen G, Guilfoyle TJ (2011) Identical amino acid substitutions in the repression domain of auxin/indole-3-acetic acid proteins have contrasting effects on auxin signaling. Plant Physiol 155:1252–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Löve Á (1944) A new triploid Betula verrucosa. Svensk Bot Tidskr 38:381–393

    Google Scholar 

  • Mu H, Liu Z, Lin L, Li H, Jiang J, Liu G (2012) Transcriptomic analysis of phenotypic changes in birch (Betula platyphylla) autotetraploids. Int J Mol Sci 13:13012–13029

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Osborn TC, Pires JC, Birchler JA, Auger DL et al (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19(3):141–147

    Article  CAS  Google Scholar 

  • Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17

    Article  CAS  Google Scholar 

  • Paul P, Dhandapani V, Rameneni JJ, Li X, Sivanandhan G, Choi SR, Pang W, Im S, Lim YP (2016) Genome-wide analysis and characterization of Aux/IAA family genes in Brassica rapa. PLoS ONE 11:e0151522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petit M, Guidat C, Daniel J et al (2010) Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol 186:135–147

    Article  CAS  PubMed  Google Scholar 

  • Pieninkeroinen K, Valanne T (1989) Old colchicine-induced polyploid materials of Betula pendula Roth and Betula pubescens Ehrh. Ann Sci For 46:264s–266s

    Article  Google Scholar 

  • Qiao LY, Zhang XJ, Han X, Zhang L, Li X et al (2015) A genome-wide analysis of the auxin/indole-3-acetic acid gene family in hexaploid bread wheat (Triticum aestivum L.). Frontiers. Plant Sci 6:770

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  Google Scholar 

  • Schranz ME, Osborn TC (2004) De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). Am J Bot 91:174–183

    Article  PubMed  Google Scholar 

  • Shen C, Yue R, Yang Y, Zhang L, Sun T, Xu L, Tie S, Wang H (2014) Genome-wide identification and expression profiling analysis of the Aux/IAA gene family in Medicago truncatula during the early phase of Sinorhizobium meliloti infection. PLoS ONE 9:e107495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh VK, Jain M (2015) Genome-wide survey and comprehensive expression profiling of Aux/IAA gene family in chickpea and soybean. Front Plant Sci. 6:918

    PubMed  PubMed Central  Google Scholar 

  • Soltis PS (2005) Ancient and recent polyploidy in angiosperms. New Phytol 166:5–8

    Article  PubMed  Google Scholar 

  • Song Y, Wang L, Xiong L (2009) Comprehensive expression profiling analysis of OsIAA gene family in developmental processes and in response to phytohormone and stress treatments. Planta 229:577–591

    Article  CAS  Google Scholar 

  • Su L, Bassa C, Audran C, Mila I, Cheniclet C, Chevalier C, Bouzayen M, Roustan JP, Chervin C (2014) The auxin SlIAA17 transcriptional repressor controls fruit size via the regulation of endoreduplication-related cell expansion. Plant Cell Physiol 55:1969–1976

    Article  CAS  PubMed  Google Scholar 

  • Su LY, Audran C, Bouzayen M, Roustan JP, Chervin C (2015) The Aux/IAA, Sl-IAA17 regulates quality parameters over tomato fruit development. Plant Signal Behav 10:e1071001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sumimoto H, Kamakura S, Ito T (2007) Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci Signal. https://doi.org/10.1126/stke.4012007re6

    Article  Google Scholar 

  • Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721

    CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Zhao H, Jiang J, Liu G, Yang C (2015) Analysis of three types of triterpenoids in tetraploid white birches (Betula platyphylla Suk.) and selection of plus trees. J For Res 26:623–633

    Article  Google Scholar 

  • Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Peng Z, Liu S, He Y, Cheng L, Kong F, Wang J, Lu G (2012) Genome-wide analysis of Aux/IAA gene family in Solanaceae species using tomato as a model. Mol Genet Genomics 287:295–311

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Liu Y, Wang Y, Li H, Liu J, Tan J, He J, Bai J, Ma H (2017) Evolution analysis of the Aux/IAA gene family in plants shows dual origins and variable nuclear localization signals. Int J Mol Sci. https://doi.org/10.3390/ijms18102107

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie R, Pang S, Ma Y, Deng L, He S, Yi S, Lv Q, Zheng Y (2015) The ARF, AUX/IAA and GH3 gene families in citrus: genome-wide identification and expression analysis during fruitlet drop from abscission zone A. Mol Genet Genomics 290:2089–2105

    Article  CAS  PubMed  Google Scholar 

  • Yang et al (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1. Plant J 40:772–782

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Chen S, Wang S, Liu G, Li H, Huang H, Jiang J (2015) BpGH3.5, an early auxin-response gene, regulates root elongation in Betula platyphylla × Betula pendula. Plant Cell, Tissue Organ Cult 120:239–250

    Article  CAS  Google Scholar 

  • Yuan H, Zhao K, Lei H, Shen X, Liu Y, Liao X, Li T (2013) Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genomics 14:297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guifeng Liu.

Additional information

Project funding: This work was supported by the National Natural Science Foundation of China (Grant Nos. 31370660 and 31670673), and the 111 Project (B16010).

The online version is available at http://www.springerlink.com

Corresponding editor: Yu Lei.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, W., Chen, S., Jiang, J. et al. Expression profiling of the BpIAA gene family and the determination of IAA levels in Betula platyphylla tetraploids. J. For. Res. 30, 855–867 (2019). https://doi.org/10.1007/s11676-018-0670-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-018-0670-1

Keywords

Navigation